Epidemiology and control of gastrointestinal helminth ...

\NEPIDEMIOLOGY AND CONTROL OF GASTROINTESTINAL

HELMINTH INFECTIONS IN SHEEP IN A SEMI-ARID AREA

OF KAJIADO DISTRICT OF KENYA

By

jchege J. Ng'ang’a, BVM, MSc. (Nairobi)

Department of Veterinary Pathology, Microbiology and Parasitology

Faculty of Veterinary Medicine

University of Nairobi

P.O. Box 29053, Nairobi

KENYA

Na ir o b i

*A*ET£ UNivfr s/TY

A Thesis submitted to the University of Nairobi in partial fulfillment of the

requirements for the degree of D o c to r^ Philosophy (Ph.D)

December 2002

Urtvwnly d NAIROBI

■IS1 1 1

II

DECLARATION

1 hereby declare lliat this thesis is my original work except where acknowledged and

has not been presented for the award of a degree in any other University.

Chege J. Ng'ang’a (B.V.M.. MSc)

......

Dat cJ $ h 3 : L Q . 2 r

This thesis has been submitted for examination with our approval as University

Supervisors.

Prof. W.K. Munyua (B.V.Sc., MSc., Dip.A.IT, Ph.D.)

....Date.......

Prof. P W)N Kanyari (B.V.M., MSc., Ph.D.)

Date....

Dr. N .j^M aingi (B.V.M., MSc., Ph.D.)

........................

Date...

Department of Veterinary Pathology, Microbiology and Parasitology

Ill

ACKNOWLEDGEMENTS

I wish to express iny sincere gratitude to the University of Nairobi, Department of

Veterinary Pathology, Microbiology and Parasitology, Faculty of Veterinary Medicine

for according me the opportunity to carry out this research.

My sincere thanks go to Prof. W.K. Munyua, Prof. P.W. Kanyari and

Dr. N.E. Maingi who supervised and guided me during my research and tirelessly

read and commented on the various manuscripts leading to the final draft of this

thesis.

I am deeply indebted to the management of the Maasai Rural Training Centre Ranch

and the Kitengela Sheep and Goat Project Ranch for allowing me to use their animals

without restriction. I am particularly indebted to Jeremiah Ole Sein and David Sirere

for weighing and recording the birth weights of lambs. Without their assistance that

work would not have been possible. My sincere thanks go to Mr. E. H. Weda, R.O.

Otieno and A.K. Murathi for their technical assistance in the field and in the

laboratory.

My sincere thanks also go to relatives and friends for their moral support. Their

endless encouragement was an inspiration throughout the course.

This study was financed by FAO through FAO-TCP Helminth Control Project

(TCP/KEN/8822(A) and the Germany Academic Exchange Programme (DAAD).

IV

DEDICATION

This work is dedicated to my wife Beatrice Nyambura and our children Anne

Wanjiru, Diana Muthoni and Samuel Ng’ang'a.

V

Title................

Declaration............

Acknowledgements

D edication ............

Table of contents.

List of Figures.

TABLE OF CONTENTS

List of T a b le s .........................................

A b s t ra c t ..........................................

Chapter 1................................................

1.0 . Introduction and objectives .............................

1.1. Introduction...............................................

1.2. Objectives................................................

Chapter 2: Literature Review....................................

2 .1. Epidemiology............................................

2.1.1. Gastrointestinal nematode infections in sheep

2.1.2. Nematode life-cycle .............................

2.1.3. Factors influencing the levels of infection

2.1.3.1. Rate of infection..............................................

2.1.3.2. Development and survival of free-living stages

2.1.3.3. Migration of infective larvae..................................

2.1.3.4. Seasonal patterns of larval development and host infection

2.1.4. Host im m unity..........................................

2.1.4.1. Influence of host age...........................

. . . i

. . . ii

. . iii

. . iv

. . . v

. . . x

. . xvi

. xviii

. . . 1

. . . 1

. . . 1

. . 5

. . 6

. . 6

. . 6

. . 7

. . 9

. . 9

. . 9

. 11

. 12

. 13

. 13

2 .1 .4 .2 . Influence of host sex................................................................................ 14

2 .1 .4 .3 . H e re d i ty .................................................................................................... 14

2 .1 .4 .4 . Nutrition.........................................................................................................15

2 .1 .4 .5 . Pregnancy and lactation.............................................................................. 16 _

2.1.4.6. Self-cure......................................................................................................... 17

2.1.4.7. Hypobiosis ................................................................................................. 19

2.1.5. Systems of livestock production ....................................................................21

2.2. Principles of helminth control........................................................................ 22

2.2.1. Control by anthelmintic t re a tm e n t....................................................................23

2.2.1.1. Strategic treatments .................................................................................23

2.2.1.2. Tactical treatments...................................................................................... 25

2.2.1.3. Anthelmintic resistance.............................................................................. 25

2.2.2. Grazing management..............................................................................................26

2.2.3. Breeding for genetic re s is tan ce ......................................................................... 28

2.2.4. Other methods of control...................................................................................... 29

2.2.4.1. Helminth vaccines...................................................................................29

2.2.4.2. Biological control ................................................................................ 30

Chapter 3: Studies on the prevalence and intensity of infection with

gastrointestinal helminths in Dorper and Red Maasai sheep. . . . 32

3.1. Introduction.............................................................................................................32

3.2. Materials and m eth o d s....................................................................................... 33

3.2.1. Study area............................................................................................................... 33

3.2.2. Climatic d a ta ......................................................................................................... 35

3.2.3. Experimental animals and treatments ............................................................... 35

' vi

3.2.4. Faecal sampling and processing...........................................................................35

3.2.5. Statistical analysis...................................................................................................36

3.3. Results ................................................................................................................. 37

3.3.1. Rainfall distribution.............................................................................................. 37

3.3.2. Faecal egg c o u n ts ................................................................................................. 37

3.3.3. Salvage treatments..................................................................................................45

3.4. Discussion...............................................................................................................47

Chapter 4: Studies on the occurrence of peri-parturient rise in

trichostrongylid nematode egg output in breeding ewes and

the prevalence and intensity of infection in lambs .............................54

4.1. Introduction.............................................................................................................54

4.2. Materials and m eth o d s........................................................................................ 56

4.2.1. Climatic d a ta ......................................................................................................... 56

4.2.2. Experimental animals and anthelmintic treatments............................................ 56

4.2.2.1. Breeding ewes..........................................................................................58

4.2.2.2. Lambs....................................................................................................... 59

4.2.3. Statistical analysis...................................................................................................59

4.3. Results .................................................................................................................. 60

4.3.1. Rainfall distribution..............................................................................................60

4.3.2. Mating, lambing and weaning schedule............................................................. 60

4.3.3. Egg counts in ewes and yearlings....................................................................... 60

4.3.4. Egg counts in Iambs ...........................................................................................67

4.3.5. Salvage treatments..................................................................................................72

vii

4.4. Discussion 73

V1U

Chapter 5: Studies on the development, survival and availability of

infective larvae on pastures......................................................................80

5.1. Introduction.............................................................................................................80

5.2. Materials and m eth o d s........................................................................................ 81

5.2.1. Climatic d a ta ......................................................................................................... 81

5.2.2. Plot studies..............................................................................................................81

5.2.3. Studies on the availability of infective larvae on naturally

contaminated pastures ........................................................................................ 82

5.2.4. Statistical analysis.................................................................................................. 84

5.3. Results ..................................................................................................................84

5.3.1. Climatic d a ta ......................................................................................................... 84

5.3.2. Plot studies..............................................................................................................88

5.3.3. Availability of infective larvae from naturally contaminated

pasture ..................................................................................................................90

5.4. Discussion............................................................................................................... 93

Chapter 6 : Seasonal prevalence, spectrum and intensity of

gastrointestinal nematode infections in Doiper sheep:

A post-mortem study..................................................................................97

6.1. Introduction............................................................................................................ 97

6.2. Materials and m ethods........................................................................................ 99

6.2.1. Climatic d a ta ......................................................................................................... 99

6.2.2. Experimental animals............................................................................................ 99

6.2.3. Worm recovery and identification.......................................................................99

6.2.4. Statistical analysis............................................................................................ 100

IX

6.3. Results ........................................................................................................... 101

6.3.1. Rainfall distribution........................................................................................ 101

6.3.2. Worm counts and identification..................................................................... 101

6.3.3. The correlation between worm counts and faecal egg c o u n t s ............... 104

6.4. Discussion......................................................................................................... 108

Chapter 7: Evaluation of the strategic use of anthelmintics in the

control of gastrointestinal nematode infections in s h e e p ............. 113

7.1. Introduction....................................................................................................... 113

7.2. Materials and m eth o d s.................................................................................. 114

7.2.1. Climatic d a ta ................................................................................................... 114

7.2.2. Experimental animals....................................................................................... 114

7.2.2.1. Breeding ewes....................................................................................... 115

1.2.2.2. Lambs..................................................................................................... 115

7.2.2.3. Yearlings................................................................................................ 116

7.2.3. Statistical analysis........................................................................................... 116

7.3. Results ............................................................................................................ 117

7.3.1. Rainfall distribution........................................................................................ 117

7.3.2. Faecal egg counts and weight gains in ewes................................................. 117

7.3.3. Birth weights and weight gains in lambs at 6 weeks................................... 125

7.3.4. Faecal egg counts and weight gains in lambs ........................................... 125

7.3.5. Faecal egg counts and weight gains in yearlings........................................ 131

7.4. Discussion........................................................................................................ 136

Chapter 8: General discussion, conclusions and significance of the study . . . 141

8.1. General discussion and conclusions............................................................... 141

8.2. Significance of the s tudy ............................................................................... 147

9.0. References........................................................................................................ 150

X

LIST OF FIGURES

Figure 3.1: Map of Kenya showing the location of Kajiado District.............. 34

Figure 3.2: Total monthly rainfall (ram) recorded at the Maasai Rural

Training Centre Meteorological Station between May 1999

and May 2000 and the long-term mean monthly rainfall

(1969 - 1998)....................................................................................... 38

Figure 3.3: The arithmetic mean strongyle eggs per gram (EPG) of faeces

for Dorper lambs, yearlings and adult breeding ewes during

the period May 1999 to May 2000.................................................. 39.


for Red Maasai lambs, yearlings and adult breeding ewes

during the period May 1999 to May 2000 ...................................... 40

Figure 3.5: A Dorper yearling with bottle jaw. The photograph was taken

in October 1999 just before the onset of the short rains.................46

Figure 4.1: Pregnant Dorper ewes on natural unimproved pastures

(June 1999).................................................................................................57

Figure 4.2: Dorper ewes and unwearied lambs on natural unimproved

pastures (November 1 9 9 9 ) ................................................................. 57

Figure 4.3: Dorper weaned lambs and yearlings on natural unimproved

pastures (March 2000)........................................................................... 57

Figure 4.4: Total monthly rainfall (mm) recorded at the Maasai Rural

I raining Centre Meteorological Station between January

1999 and December 2001 and the long-term mean monthly

rainfall (1969 - 1998)............................................................................ 61

XI

Figure 4.5: The arithmetic mean strongyle eggs per gram (FPG) of faeces

for mated Dorper ewes and un-mated yearlings during the

period June 1999 to April 2000 ........................................................ 62



period June 2000 to April 2001 ........................................................ 63



period April 2001 to December 2001 ............................................... 64


for mated Dorper ewes during the period June 1999 to December

2001 ...................................................................................................... 65


for Dorper ewes from the time of mating to six weeks post-

weaning and for lambs from the age of six weeks to the age

of 6 months during the period June 1999 to April 2000................. 68


for Dorper ewes from the time of mating to six weeks post-

weatiing and for lambs from the age of six weeks to the age

of five months during the period June 2000 to April 2001 . . . . 69


for Dorper lambs during the period November 1999 to November

2001 ...................................................................................... 71

Figure 5.1: Grazing Paddocks (March 2000)......................................................... 83

Figure 5.3: Watering point (March 2000)............................................................... 83

Figure 5.4: Relative humidity, mean minimum and maximum

temperatures recorded at the Maasai Rural Training

Centre Meteorological Station between January 1999

and December 2001............................................................................... 85


Training Centre Meteorological Station between January


rainfall (1969 - 1998)............................................................................ 86

Figure 5.6: The number of rainy days per month recorded at the Maasai

Rural Training Centre Meteorological Station between January

1999 and December 2001 ................................................................... 87

Figure 5.7: The number of larvae recovered per Kg herbage from plots

serially contaminated with sheep faeces from November 2000

to June 2001 ........................................................................................ 89

Figure 5.8: The state of the pastures in the paddocks during the dry

season (A, September 2000), the short rains (B, November 2000)

and the long rains season (C, April 2001)........................................ 91

Figure 5.9: The number of larvae (LjKg-1) recovered from pasture

samples collected from the paddocks, around the night

pen and the watering point between May 1999 and

December 2001....................................................................................... 92


Training Centre Meteorological Station between September

2000 and July 2001 and the long-term mean monthly rainfall

(1969 - 1998)......................................................................................... 102

*

xii

Figure 5.2: Night pen (March 2000)........................................................................ 83

Figure 6.2:

Figure 6.3:

Figure 6.4:

Figure 7.1:

Figure 7.2:

Figure 7.3:

Figure 7.4:

The mean worm counts and the proportions of different genera

of nematode parasites encountered in 24 Dorper sheep

slaughtered serially between September 2000 and July 2001. . 105

The proportions of adult and immature Ilaemonchus

and Trichostrongylus species during the wet and the

dry seasons in 24 Dorper sheep slaughtered between

September 2000 and July 2001 ..................................................... 106

The correlation between the faecal egg output and the worm

burden in 24 Dorper sheep slaughtered during the wet and the

dry season between September 2000 and July 2001..................... 107

Total monthly rainfall (mm) recorded at the Maasai Rural

Training Centre Meteorological Station between January


rainfall (1969 - 1 9 9 8 ) ...................................................................... 118

The arithmetic mean strongyle eggs per gram (EPG) of faeces

for Dorper breeding ewes given strategic albendazole treatments

and the un-treated control group during the period May 1999

to April 2000....................................................................................... 119



and the un-treated control group during the period June 2000

and April 2001 .................................................................................. 120



and the un treated control group during the period April 2001

to December 2001 ............................................................................ 121

xiii

Figure 7.5: The cumulative weight gains for Dorper breeding ewes given

strategic albendazole treatments and the un-treated control

group during the period June 1999 to April 2000 ..................... 122


strategic albendazole treatments and the un-treated control

group during the period July 2000 to April 2001......................... 123


strategic albendazole treatments and the un treated control

group during the period May 2001 to December 2001................ 124

Figure 7.8: The mean birth weights, weights at 6 weeks and the

weight gains for groups of lambs born of treated and

the un treated Dorper ewes during the period October 1999

to November 2001.............................................................................. 126


for Dorper lambs given strategic albendazole treatments and

the un treated control group during the period January 2000

to December 2001 ............................................................................ 127


for Dorper lambs given strategic albendazole treatments and

the un-treated control group during the period February 2001

to December 2001 ............................................................................ 128

Figure 7.11: The cumulative weight gains for Dorper lambs given strategic

albendazole treatments and the un-treated control group during

the period February 2000 to December 2000 ............................. 129

xiv

XV

Figure 7.12:

Figure 7.13:

Figure 7.14:

Figure 7.15:

Figure 7.16:

The cumulative weight gains for Dorper lambs given strategic

albendazole treatments and the untreated control group during

the period March 2001 to December 2001.....................................


for a group of Dorper yearlings given strategic albendazole

treatments and the un-treated control group during the period

May 1999 to April 2000 ................................................................


for a group of Dorper yearlings given strategic albendazole

treatments and the un-treated control group during the period

the April 2000 to March 2001 ........................................................

The cumulative weight gains for a group of Dorper yearlings

given strategic albendazole treatments and the un-treated

control group during the period June 1999 to April 2000

I he cumulative weight gains for a group of Dorper yearlings

given strategic albendazole treatments and the untreated

control group during the period July 2000 to March 2001

130

132

133

134

135

XVI

LIST OF TABLES

Table 3.1: Comparison between the geometric mean faecal egg output for

Dorper and Red Maasai lambs, yearlings and adult breeding

ewes during the period June 1999 to May 2000 .......................... 41

Table 3.2: Comparison between the geometric mean faecal egg output for

Dorper and Red Maasai lambs, yearlings and adult breeding

ewes during the wet and the dry season between June 1999

and May 2000 .................................................................................... 42

Table 3.3: The prevalence percentage (12 months) of strongyle and

tapeworm eggs in faecal samples in relation to age and

breed of sheep during the dry and the wet seasons between

June 1999 and May 2000 ................................................................... 43

Table 3.4: The mean distribution of genera of gastrointestinal nematodes

in faecal cultures from the Dorper and the Red Maasai sheep

during the dry and the wet seasons between June 1999 and

May 2000 ............................................................................................. 44

Table 3.5: The number of Dorper sheep given salvage treatment based on

clinical manifestation of nematodosis and or egg counts

(over 7000 EPG) during the wet and the dry season between

June 1999 and May 2000 ................................................................... 45

Table 3.6: The number of Red Maasai sheep given salvage treatment based

on clinical manifestation of nematodosis and or egg counts

(over 7000 EPG) during the wet and the dry season between

June 1999 and May 2000 ................................................................... 46

XVII

Table 4.1: The mating, lambing and weaning schedule for Dorper sheep

at the Maasai Rural Training Centre Ranch during the period

June 1999 to December 2001 .......................................................... 58

Table 4.2: Comparison between the geometric mean strongyle egg counts

for Dorper mated ewes and the un-mated yearlings during the

pre-lambing and lambing and lactation periods of the ewes

between June 1999 and December 2001............................................ 66

Table 4.3: Comparison between the arithmetic mean faecal strongyle egg

counts for Dorper mated ewes and lambs during the period

November 1999 to April 2000 (Year 1) and January 2001 to

April 2001 (year 2 )............................................................................... 67

Table 4.4 Comparison between the geometric mean faecal strongyle egg

output for Dorper Iambs during the wet and the dry seasons

during the period November 1999 to November 2001 .................. 70

Table 4.5 The number of Dorper ewes given salvage treatments based on

clinical signs of helminthosis and or faecal strongyle egg

counts (Over 7000 epg) during the wet and the dry seasons

between June 1999 and December 2001............................................ 72

Table 4.6 The number of Dorper lambs given salvage treatments based on

clinical signs of helminthosis and or faecal strongyle egg

counts (over 7000 EPG) during the wet and the dry seasons

between November 1999 and November 2001................................. 73

Table 6.1: The mean worm burdens and percentage prevalence of 24

Dorper sheep slaughtered at Isinya in Kajiado District

during the dry and the wet seasons during the period

September 2000 to July 2001............................................................ 103

XVI11

ABSTRACT

Gastrointestinal helminth parasites impose severe economic constraints on sheep

production worldwide. For rational and sustainable control of these parasites,

comprehensive knowledge on the epidemiology of the parasite as it interacts with the

host in a specific climatic, management and production environment is crucial. The

helminth infections have primarily been controlled by use of anthelmintics due to their

ease of application and high efficiency. However, in developing countries, there are

poor or ineffective set plans of prophylactic control of gastrointestinal helminths and

the use of anthelmintics is mainly irregular and haphazard. No previous information

was available on the epidemiology and control strategies of gastrointestinal helminths

of sheep in the semi-arid area of Kajiado District. The main objective o f this thesis

was therefore to establish the epidemiology and control strategies of gastrointestinal

helminths in sheep in this area.

A survey on the prevalence and intensity of infection with gastrointestinal helminths

of sheep in relation to age, breed and weather factors was carried out during the

period May 1999 to May 2000. Faecal samples from Dorper and Red Maasai lambs,

yearlings and adult breeding ewes were examined for helminth egg output and species

composition. The results indicated that the prevalence and intensity of strongyles and

tapewonns infections were highest for lambs and lowest for the yearlings in both

breeds. The proportions of infected animals were higher during the wet season than

in the dry season. Mixed infections were detected in both breeds of sheep where

Trichostrongylus (53 %), Haemonchus (29.5 %), Cooperia (11.3 %) and

Oesopliagostomum (6.2 %) were the most frequently encountered species throughout

XIX

the study period. The prevalence of infection with gastrointestinal nematodes was

significantly higher (p < 0.05) for the Dorpers than the Red Maasai in all the age

groups. The findings indicated that the prevalence and intensities of infection with

gastrointestinal helminths in this area were influenced by the age of the host, the

breed and weather factors.

An investigation on the occurrence of peri-parturient rise in trichostrongylid nematode

egg output in breeding ewes was carried out for 3 breeding seasons during the period

June 1999 to December 2001. Each season, 20 ewes randomly selected from the

breeding stock and 20 others selected from the un-mated yearlings were examined.

A significant peri-parturient rise in faecal egg output occurred at around the time of

lambing and throughout the lactation period in the mated ewes, but not in the un

mated yearlings. Higher peri-parturient rise in faecal egg output occurred when

lambing coincided with the end of the dry season before the short rains, a time when

the resumption of development of hypobiotic larvae occurred. The occurrence of peri-

parturient rise in breeding ewes contributed to higher pasture contamination at a time

when the number of susceptible lambs were increasing. Control of gastrointestinal

nematode parasites in this area should therefore aim at reducing the effects of this

phenomenon through treatment of ewes just before lambing and during lactation.

A study on the prevalence and intensity of gastrointestinal nematode infections in

lambs in relation to seasonal effects was carried out over a period of 2 years between

November 1999 to November 2001. Each year a total of 20 Iambs were randomly

recruited at the age of 6 weeks and their faecal samples examined for strongyle eggs

XX

for a period of one year. The results obtained during this period indicated that

strongyle infections started building up in lambs as they began to rely heavily on

pastures at around the age of 9-12 weeks. High strongyle egg counts occurred

between the age of 12 weeks and 7 months, with peak counts at the time of weaning

(4-5 months) thus significantly contributing to pasture contamination. The declining

levels in faecal egg output at the age of 7 months and the ability to self-cure at the

age of 10-12 months was attributed to the development of acquired immunity. The

mean faecal strongyle egg counts in these lambs were significantly higher during the

dry season (geometric mean EPG 867) than in the wet season (geometric mean EPG

462) in the first year of study, but significantly higher during the wet season

(geometric mean EPG 1062) than in the dry season (geometric mean EPG 449) in the

second year of study. The lower counts during the wet season in the first year of

study were attributed to low amounts of rainfall during the long rains season in the

year 2000. During the study period, clinical signs of helminthosis were observed both

in the wet and the dry seasons. Helminth control programmes in lambs in the study

area should therefore aim at reducing the levels of infection during both seasons with

particular emphasis on the 9 weeks to 7 months old lambs.

A series o f plots were contaminated with sheep faeces every month and pasture

samples collected weekly for the recovery and identification of larvae. The studies

were carried out during the period July 2000 to June 2001 to determine the seasonal

patterns of development and survival of gastrointestinal nematodes. The results from

the examination of the pasture samples indicated that rainfall distribution was the

major factor governing the development and survival of the pre-parasitic stages. No

XXI

parasitic larvae were detected from the plots contaminated during the dry months

from July to October 2000, but development and translocation of infective larvae on

pastures occurred in plots contaminated during the rainy seasons and soon after when

a relatively high moisture content was present in the herbage. During this period,

peak larval counts occurred during the first and the second week post-contamination,

then declined to undetectable levels between week 3 and 15 post-contamination. The

lack of development of infective larvae during the dry season and the relatively rapid

decline of their population during the wet season presents an opportunity for the use

of pasture spelling as a means of helminth control in the study area.

The seasonal availability of infective larvae on naturally contaminated pastures from

the paddocks grazed by sheep, around the night pen and the watering point was

monitored by examination of herbage samples during the period May 1999 to

December 2001. The larval availability on the pastures closely followed the rainfall

distribution pattern. The overall trend in larval counts indicated increasing levels of

availability during the rainy season with peaks just at the onset of the dry season. The

larval availability levels then declined as the dry season advanced. Infective larvae

were consistently recovered around the watering point throughout the year. This then

can be an important source of infection for sheep especially during the dry season

when the other pastures are non-infective. Observations made from this study

therefore indicated that sheep infection with gastrointestinal nematodes in this area

could occur both during the dry and the wet seasons and control measures should aim

at reducing the levels of infection in both seasons.

xxn

The seasonal spectrum of gastrointestinal nematode infections and the relationship

between worm burdens and faecal egg counts in sheep were investigated during the

dry and the wet seasons from September 2000 to July 2001. Each season, 12 female

Dorper sheep (9-12 months old) permanently on pastures at the Maasai Rural Training

Centre Ranch were slaughtered, their guts examined for the total and differential

worm counts and the rectal faecal egg output estimated. Regression analysis was

performed to determine the relationship between the worm burdens and the faecal egg

counts. All sheep examined had mixed infections with Trichostrongylus y Haemonchus

and Oesophagostomum occurring in 91.7% and Cooperia in 83.3% of the animals

respectively. During the study period, Trichostrongylus and Haemonchus were the

most abundant genera encountered and constituted approximately 60.8% and 27.3%

of the total worm counts respectively. Relatively higher worm counts were recorded

during the wet season (mean 4766) than the dry season (mean 4216), but was not

significantly different. The adult and immature worm populations co-existed in

proportions that varied with seasons. The proportion of immature Haemonchus was

significantly higher during the dry season (75.6%) than in the wet season (38.1%).

This confirmed the occurrence of hypobiosis of this species in the study area. The

proportions of immature Trichostrongylus species did not change significantly from

the dry season (6 %) to the wet season (6.8 %). This indicated that this species

mainly survived the dry season as adult populations. The relationship between the

worm burdens and the faecal egg counts revealed positive correlations during both the

wet season (r = 0.75) and the dry season (r = 0.97). This suggested that the faecal

egg output could be used as an indicator of the levels of infection with gastrointestinal

nematode parasites during the wet and the dry seasons in the study area.

XXU1

An investigation was carried out to evaluate the effectiveness of the strategic use of

anthelmintics in controlling naturally acquired gastrointestinal nematode infections in

breeding ewes. Iambs and yearlings from May 1999 to December 2001. Albendazole

at the dose rate of 5 mg Kg ' body weight was used based on the rainfall distribution

pattern and the Maasai Rural Training Cenre ranch breeding programme. Faecal egg

output, weight gain and reproductive parameters were monitored. The results

indicated that strategic treatment of breeding ewes pre-mating, prc-lambing and in

mid-lactation resulted in significantly lower faecal egg counts and higher weight gains

or lower weight losses compared to the un treated controls throughout the study

period. The lambs born of the treated ewes had higher birth weights and weight gains

at 6 w-eeks. Strategic treatment of lambs at the age of 9-12 weeks and at the time of

weaning (4-5 months) resulted in higher weight gains, lower weight losses and

significantly lower faecal egg output compared to the un treated controls. Also the

strategic treatments of weaned lambs and yearlings three weeks into the rains, at the

onset of the dry season in January and in mid-dry season in July resulted in higher

weight gains, lower weight losses and significantly lower faecal egg output compared

to the un-treated controls. These strategic treatments were considered effective in

decreasing the levels of pasture contamination and improving the productivity of the

animals. They are therefore recommended for use in the study area.

1

CHAPTER 1

1.0 INTRODUCTION AND OBJECTIVES

1.1 Introduction

Sheep and goats are better adopted to the seini-arid areas than cattle due to their

feeding habits. They have a high reproductive capacity and rapid growth rale and are

thus a potentially important source of animal protein. The recent animal population

census in Kenya, estimates a national population of 19 million sheep and goats

(KARI, 1994). To meet the animal protein requirements for the ever increasing human

population, there is need not only to increase these numbers, but also productivity.

To achieve this there is need to improve on management and production - limiting

diseases.

Although the importance of animal health as a constraint to livestock production in

developing countries has been recognised, focus on control measures has always

aimed at the acute, often fatal viral, bacterial and protozoal diseases (Waller, 1997).

However, it is now more apparent that losses due to helminth infections play a

significant and in some instances, a greater role than the acute diseases (Anon.,

1991). This is largely due to the fact that most of the acute diseases are essentially

temporary in nature and surviving animals do not only recover rapidly, but are often

immune for live (Waller, 1997). On the other hand nearly all grazing animals are

infected with helminths and the pick-up from pastures is more or less continuous

(Blood, Radostits, Ilerderson, Arundel and Gay, 1997; Waller, 1997). Therefore,

helminth infections are mostly associated with sub-clinical production losses which

2

largely go unnoticed or are accepted as the norm by farmers. The profound impact

of such chronic disease conditions on the long-term animal productivity cannot be

overemphasised.

In Kenya, gastrointestinal nematode parasitism is one of the major animal health

problems facing the ruminant livestock production (Allonby and Urquhart, 1975;

Maingi, 1996; Nginyi, Duncan, Mellor, Stear, Wanyangu, Bain and Gatongi, 2001).

Production losses are mainly manifested as mortalities, reduction in live weight gains,

lower milk, meat and wool production and in organ condemnations. In addition, the

cost of obtaining anthelmintics, a primary tool in the control of gastrointestinal

nematodes is a burden on the foreign currency exchange. Economic estimates of

losses caused by gastrointestinal nematode parasites are not readily available. Preston

and Allonby (1978) estimated an annual loss of up to US$ 26 million due to

Haanonchus contortus infection in the sheep industry in Kenya.

Since the eradication of gastrointestinal nematodes in small ruminants is impractical

and undesirable (Brunsdon, 1980; Vlassoff, Leathwick and Heath, 2001), it is

important that they be controlled. For rational and sustainable control of these

parasites, comprehensive knowledge on the epidemiology of the parasite as it interacts

with the host in a specific climatic, management and production environment is

crucial (Barger, 1999; Vlassoff et al., 2001).

Due to the wide diversity of environmental conditions in various regions of Kenya,

epidemiological studies carried out on the gastrointestinal helminths of sheep in one

3

area may not apply in another. Most of these studies in this country have mainly been

conducted in the high rainfall areas (Mbaria, McDermott, Kyule, Gichanga and

Manyole, 1995; Maingi, 1996; Nginyi et al., 2001) and the only extensive studies in

the semi-arid areas were those carried out in Naivasha (Allonby and Urquhart, 1975;

Galongi, 1995). No previous studies have been carried out on the epidemiology of

gastrointestinal helminth infections in the two main breeds of sheep, the Dorper and

the Red Maasai kept in the semi-arid area of Kajiado District.

The peri-parturient rise in faecal egg output in ewes is an important phenomenon in

the epidemiology of gastrointestinal nematodes of sheep. The occurrence of the

phenomenon and the significance of the peri-parturient ewes as a source of infection

for lambs have been extensively studied in the temperate regions (Gibbs, 1968;

Brunsdon, 1970; Connan, 1976; Michel, 1976; Gibbs and Barger, 1986) and to a

lesser extent in some parts of the tropics (Van Geldorp and Schillhorn van Veen,

1976; Schillhorn van Veen and Ogunsusi, 1978, Agyei, Sapong and Probert, 1991;

Romjali, Dorney, Batubara, Pandey and Gatenby, 1997; Tembely, Lahlou-Kassi,

Rege, Mukasa-Mugerwa, Anindo, Sovani and Baker, 1998). However, information

concerning this phenomenon in Kenya is scanty and is mainly based on the work of

Ulvund, Maina and Mararo, (1984) in Embu. There is need therefore to verify the

occurrence and significance of the phenomenon in specific localities.

The major epidemiological variable influencing worm burdens of grazing animals is

the infection rate which is in turn influenced by the climatic requirement for the egg

hatching, larval development and survival (Barger, 1999; Vlassoff et al., 2001). The

4

relative ability of the pre-parasitic stages to survive on pastures at different times of

the year is therefore relevant to successful formulation of control programmes

(Barger, 1999). Also the estimates of the density of larvae on herbage provides

information essential to the understanding of the population dynamics of nematode

infections in ruminants (Couvillion, 1993). In many tropical areas, the numbers of

free-living stages of gastrointestinal nematode parasites in pastures follow seasonal

fluctuations (Dinnik and Dinnik, 1961; Ogunsusi, 1979a; Banks, Singh, Barger,

Pratap and Jambre, 1990; Waruiru, 1998; Tembely, 1998). Since weather

conditions vary from place to place, studies on the bionomics of the free-living stages

of nematode parasites are needed in the planing of locally applicable control strategies

(Okon and Enyenihi, 1977). No study on the development, survival and availability

of infective larvae of gastrointestinal nematodes of sheep has been carried out in the

semi-arid area of Kajiado District.

Helminth infections have primarily been controlled by extensive use of anthelmintics

and grazing management in developed countries where appropriate timings for

intervention have been established for specific regions (Brunsdon, 1980). In

developing countries, there are poor or ineffective set plans of prophylactic control

of gastrointestinal helminths. Treatment regimes are frequently based on extrapolation

of studies carried out elsewhere. These are often inappropriate due to differences in

ecological factors and management practices that exist between different areas (Kinoti,

Maingi and Coles, 1994; Mbaria et al., 1995; Nginyi et al., 2001). There is need

therefore to develop epidemiological data and evaluate the effectiveness of control

methods based on anthelmintic treatments and management practices for specific

localities.

5

1.2 Objectives

1. To determine the prevalence, spectrum and levels of infection with

gastrointestinal nematodes in sheep in relation to age, breed and

reproductive status of the host and seasonal variation in weather factors

in a semi-arid region of Kajiado District.

2. To determine the seasonal pattern of egg hatching, development

survival and availability of infective larval stages of gastrointestinal

nematodes of sheep on pastures in a semi-arid area of Kajiado District.

3. To evaluate the effects of strategic use of anthelmintics on birth

weights, weight gains and the level of infection with gastrointestinal

nematodes in breeding ewes, lambs and yearlings in a semi-arid zone

of Kajiado District.

6

CHAPTER 2

2.0 LITERATURE REVIEW

2.1 Epidemiology

There is no single requirement more crucial to the rational and sustainable control of

helminth parasites in grazing animals than a comprehensive knowledge of the

epidemiology of the parasite as it interacts with the host in a specific climatic,

management and production environment (Barger, 1999; Vlassoff et al., 2001).

Therefore, a detailed understanding of the sequential inter-relationship between the

various sources of pasture contamination, the availability of infective larvae and the

build-up and decline of the infections in the host is important (Brunsdon, 1980;

Barger, 1999).

2.1.1 Gastrointestinal nematode infections in sheep

Infections with gastrointestinal worms in sheep usually involve several different

genera and species of nematodes, which may have additive pathogenic effects on the

host. The genera include Haemonchus, Ostertagia, Trichostrongylus, Bunostomum,

Cooperia, Nematodints, Oesophagostomum, Strongyloides, Chabertia and Trichuris

(Fraser, Mays Asa, Amstrutz, Archibald, Armour, Blood, Newberne, and

Syoeyenbos, 1986; Stear, Bairden, Bishop, Getlinby, McKellar, Park, Strain and

Wallace, 1998).

Sheep are more consistently susceptible to the adverse effects of worms than other

livestock (Fraser et al., 1986; Kanyari, 1993) and clinical disease is common. Young

7

lambs are particularly susceptible to infection and to the pathogenic effects of

strongyles as they do not effectively develop immunity to the infections (Soulsby,

1985). Haemonchus is a major cause of lamb mortality (Soulsby, 1985; Gatongi,

1995). Breeding ewes are also susceptible to the effects of parasitism during

pregnancy and lactation (Thomas and Ali, 1983). There is usually a temporary loss

of acquired immunity to nematode parasites at around this time (Connan, 1968a;

Lloyd, 1983; Houdijk, Kyriazakis, Coop and Jackson, 2001). The loss of immunity

typically involves a peri-parturient rise in faecal egg output in lactaling animals and

is often accompanied by clinical signs of parasitic gastroenteritis. The peri-parturient

rise in egg output is also the main source of gastrointestinal nematode infection for

lambs (Boag and Thomas, 1971; Dorny, Symoens, Jalila, Vercruysse and Sani, 1995;

Tembely et al., 1998).

2.1.2 Nematode life-cycle

The life-cycles of most trichostrongylid nematodes such as Haemonchus,

Trichostrongylus, Cooperia, Nematodirus, Ostertagia, Oesophagostomum and

Bunostomum are similar and direct. Adult nematodes inhabit the gastrointestinal tract.

Adult females lay eggs which are passed out in faeces into the environment. The eggs

hatch and release the first-stage larvae (L,). These then moult to the second-stage

larvae (Lj), shedding their protective cuticle in the process. The moult into the

infective third stage larvae (L,) but retains the cuticle from the previous moult. Under

optimal conditions of humidity and temperature this development process takes about

7 to 10 days. The parasitic phase of the life cycle begins with the ingestion of L3 on

pastures by the host. The L3 penetrate the gastrointestinal mucosa (Haemonchus and

8

Trichostrongylus) or enter gastric glands (Ostertagia) and ex-sheath the extra cuticle

in the process. The exshealhed L3 then moult to the fourth stage larvae (L4) and

remain in the mucous membranes or gastric glands for 10 to 14 days. They then

emerge and moult into young adults (L5), mature and start egg production in about

3 weeks post-infection (Hansen and Perry, 1994; Vlassoff et al., 2001).

There are some exceptions to the general pattern described as in Nematodirus where

the development to the L, occurs entirely within the egg. These larvae then hatch and

become infective to the host. The parasitic part of the life cycle of Oesophagostomum

requires about 6 weeks to complete. The infective Lj penetrate the lamina propria of

the intestinal wall and the host responds by surrounding it in fibrous nodules. The

larvae emerge into the intestinal lumen after 2 weeks and mature in the next 4 weeks.

In hosts with previous infections, their stay in intestinal wall nodules may be

prolonged to 3-5 months. Eventually most of the larvae die and the nodules may

become calcified.

Host infection with Bunostomum is by ingestion or skin penetration of the Lv The

larvae that penetrate the skin are then carried in the venous blood to the lungs, enter

the alveoli, coughed up and then swallowed. Larvae entering through both routes then

pass to the small intestines, moult and mature 8-9 weeks post-infection. The infective

larval stage of Trichuris is contained within the egg and is released following

ingestion of the egg by the host. Infection by Strongyloides occurs through oral

ingestion of infective third-stage larvae, through milk or penetration through the skin.

Development into the adult stage occurs in the small intestines.

9

2.1.3 Factors influencing the levels of infection

The size of any gastrointestinal nematode infection in grazing animals depends on

several interacting factors. These factors include the number of infective larvae

ingested by the host, host immunity, livestock production systems and the control

methods used (Hansen and Perry, 1994; Barger, 1999).

2.1.3.1 Rale of Infection

The major epidemiological factor influencing the worm burdens of grazing animals

is the infection rate (Barger, 1999). Fluctuations in the number and availability of the

infective larvae on the pastures are in turn influenced by factors that affect

contamination of the environment with nematode eggs. Such factors include the

stocking density and the intrinsic multiplication rates of the nematode species present

and by the translation process of development, survival and dissemination of the free-

living stages (Armour, 1980; Ilansen and Perry, 1994; Barger, 1999).

2.1.3.2 Development and survival of free-living stages

The development of nematode eggs to the infective larval stage and the survival of

these larvae on pastures are influenced by several environmental factors and biological

agents. These include temperature, moisture, humidity, sunlight, oxygen supply, soil

structure, herbage growth and composition, size and consistency of faeces,

predaceous fungi in the soil and faecal pats, dung-burying beetles and earthworms

(Hay, Niezen, Miller, Bateson and Robertson, 1997; Larsen, 2000; Vlassoff et al.,

2001). However, the principle factors are temperature and moisture (Gordon, 1948;

Waller and Donald, 1970; Gibson and Everett, 1976) and vary in different parts of

10

the world. In most of tropical and sub-tropical areas, little variations in temperatures

occur and are permanently favourable for larval development in the environment

(Ikeme, Iskander and Chong, 1987; Hansen and Perry, 1994). Variation in rainfall

is the major factor governing the survival and development of the pre-parasitic stages

(Altaif and Yakoob,1987; Banks et al., 1990; Onyali, Onwuliri and Ajayi, 1990;

Nginyi et al., 2001). The ideal temperature and relative humidity for larval

development of many species in the microclimate of the tuft of grass or vegetation is

between 22°C and 26nC and 100% (minimum 85%) respectively. Development can

also occur at a slower rate at temperatures as low as 5°C and at over 30°C, but with

a high larval mortality (Hansen and Perry, 1994).

The survival of larvae in the environment depends upon adequate moisture and shade.

Desiccation from lack of rainfall kills eggs and larvae and is the most rapidly lethal

of all climatic factors. The larvae may be protected from desiccation for a time by

the crust of the faecal pats in which they lie or by migrating into the soil (Hansen and

Perry, 1994). The pre-parasitic stages of nematodes differ in their response to the

environmental conditions especially temperature, moisture and sunlight. Generally,

the L3 which have a protective sheath and embryonated eggs are the most resistant,

followed by the un-embryonated eggs, L, and Lj in that order (Soulsby, 1982).

Variations in the response to the above stimuli also occurs in nematode species. The

pre-parasitic stages of Nematodirus which develop within the egg until hatching are

more resistant to the adverse environmental effects than those of other

trichostrongylid nematodes (Soulsby, 1982). The embryonated eggs and the third

stage larvae of Trichostrongylus colubriformis are resistant to desiccation and some

11

degree of water deprivation may enhance their survival (Andersen and Levine, 1968)

while those of Haemonchus are very susceptible (Waller and Donald, 1970).

2.1.3.3 Migration of infective larvae

For the infective larvae to be ingested by the ruminant host, they have to migrate or

be transported from the faeces in which they were deposited to any nearby herbage.

Suitable conditions for this migration occur when rainfall or moisture disintegrates the

crust o f faecal material and the larvae washed onto the herbage or transported by

invertebrates such as the dung beetles and earthworms (Hansen and Perry, 1994; Hay

et al., 1997; Larsen, 2000; Hein, Shoemarker and Heath, 2001). However, excessive

moisture or sustained torrential rainfall adversely affects development of eggs and

pasture larval density through rapid disintegration of faeces and washing of eggs and

larvae (Ikeme et al., 1987).

Once on the herbage, infective larvae migrate up and down the blades of grass

according to the amount of moisture on the grass (Hansen and Perry, 1994). During

the rains and when dew is on the grass, the larvae migrate to the top of the herbage.

Following evaporation the larvae migrate to the base of the herbage and even down

into the soil (Rose, 1963; Michel, 1976; Hansen and Perry, 1994). The rate of

migration of the infective larvae also depends primarily on the microclimate in the

herbage and this in turn depends on the soil type (Michel, 1976).

12

2.1.3.4 Seasonal patterns of larval development and host infection

The development and survival patterns of infective larvae in the environment and host

infections differ according to the climate. The humid tropical climate provides a more

or less permanently favourable environment for the development and survival of

parasitic larvae. Therefore, several larval peaks and generations of parasites develop

in the pastures and animals all the year round (Ikeme et al., 1987; Romjali et al.,

1997).

The arid tropical climate is often unfavourable for parasitic larval survival. However,

short periods of rain or irrigation can rapidly transform the environment into a

favourable one. The host infection and transmission of parasites in such areas is

restricted to the wet season (Ogunsusi, 1979a; Charles, 1989). The only means of

carry-over o f infection from one rainy season to the other is through animals

harbouring adult worms and/or hypobiotic larvae (Chiejina, Fakae and Eze, 1988;

Macpherson, 1994).

The savannah-type tropical and subtropical climate has long dry seasons. As the dry

season progresses, the environment for the development and survival of larvae

changes from unfavourable to hostile. The population of surviving larvae declines

rapidly in the open pastures, but more slowly in the wooded areas. Host infections

during the dry season are therefore minimal. At the start of the rains, the environment

is rapidly transformed into a favourable one. During the rainy season, there is a

continuous cycle of infection between the host and the pastures. Worm populations

in the animals fluctuate considerably throughout the rainy season (Ogunsusi, 1979a).

13

Immunity to helminth infection is usually less efficient and more transient than that

due to micro-organisms. This is possibly because helminths do not reproduce in the

host as do the bacteria, viruses and protozoa (Blood et al., 1997). The main stimulus

in helminth immunity appears to be due to antigens derived from the adult worms

which subsequently act on new parasites entering the body (Quinnell and Keymer,

1990). The development of acquired resistance in the host is then influenced by the

species of parasites and host factors such as age, sex, heredity, nutrition and

physiological stress as occurs in pregnancy and lactation.

2.1.4.1 Influence of host age

Age influences the susceptibility and resilience of animals to helminths. Lambs are

more susceptible to infections with gastrointestinal nematode parasites than are adult

sheep (Watson, 1991; Stear, Mitchell, Strain, Bishop and McKellar, 2000). The

greater susceptibility of young animals is ascribed to their defective development of

protective acquired immune responses to worm infection when compared to adult

animals (Watson and Gill, 1991; Barger, 1993). Generally, their resistance to

parasitic infections increases with age during the first 12 months of life (Watson,

1991; Colditz, Watson, Gray and Eady, 1996). In adult animals, exposure to more

or less continuous re-infection leads to the development of acquired resistance to the

helminth parasites. The worm numbers are then limited by the relatively poor

establishment of newly-acquired larvae and by the early expulsion of developing and

adult worms. In addition there is suppression of the fecundity of female wonns

already present (Connan, 1976; Quinnell and Keymer, 1990; Coop and Kyriazakis,

1999).

2.1.4 Host immunity

14

2.1.4.2 Influence of host sex

Male sheep have been shown to be more susceptible than females to experimental

infections with Haemonchus contortus, Oesophagosiomum columbianum and

Trichostrongylus colubriformis when challenge infections were given around or after

puberty (Barger, 1993). It is also known that rams acquire larger Ilaemonchus

contortus infections than ewes sharing the same pastures (Colglazier, Lindahl,

Wilson, Whitmore and Wilson, 1968; Barger, 1993). The difference in susceptibility

between the sexes can be attributed to the differential effects of gonadal steroid

hormones on the immunity and to grazing management (Barger, 1993).

2 .1.4.3 Heredity

Most breeds of sheep develop some degree of resistance following a primary exposure

to trichostrongylid nematode infections (Gamble and Zajac, 1992). However,

considerable variations in resistance to primary and secondary infections exist within

and between breeds (Preston and Allonby, 1979a; Gamble and Zajac, 1992; Stear and

Murray, 1994) and this has been shown to be heritable (Stear and Murray, 1994). It

is also known that some breeds of sheep develop resistance against nematode

infections at an earlier age than others (Gamble and Zajac, 1992; Bahirathan, Miller,

Barras and Kearney, 1996; Stear et al., 2000). Examples of such genetic resistance

can be found among the Red Maasai, Florida and Louisiana Native, Barbados

blackbelly and the St. Croix breeds (Waller, 1997).

15

It is a well established principle that good nutritional status and freedom from specific

nutritional deficiencies increase the resistance of livestock to the effects of helminth

parasites and that poorly fed animals are more susceptible to the effects of these

parasites (Blood et al., 1997; Waller, 1997; Coop and Kyriazakis, 1999). Poorly fed

animals tend to carry heavy worm burdens because of their failure to throw off

infections quickly. However, optimal nutrition does not offer complete protection

against overwhelming numbers of some helminth infections. In general terms

trichostrongylosis achieves its greatest importance in sheep when nutrition is poor.

On the other hand haemonchosis causes most losses when nutrition is excellent but

the environmental conditions are such that massive infestations occur as well as in

poor nutrition (Blood et al., 1997).

Inadequate intake or lack of protein, minerals and vitamins leads to the lowering of

body resistance and specifically to impaired cellular immune responses to infection

(McGee and McMurray, 1988; Roberts and Adams, 1990; Coop, Bartley, Jackson,

Houdijk, Kyriazakis and Jackson, 2001). In helminth infections, this manifests as

increased establishment, survival and pathogenicity of the parasite and hence

production losses in the host (Abbott, Parkins and Holmes, 1985, 1988; Coop and

Kyriazakis, 1999).

The crude protein content of most native tropical grasses is adequate for only

moderate levels of animal production for a few months of the year when the grasses

are young (Reynolds and Adediran, 1987). Consequently, there is usually severe

2.1.4.4 Nutrition

16

seasonal shortage leading to wide spread malnutrition and sometimes heavy

parasitism, particularly in the semi-arid and savanna zones (Schillhorn van Veen,

1974; Charles, 1989).

The full extent of malnutrition and its impact on gastrointestinal nematode infection

in the tropical livestock is at present impossible to assess accurately. However, it is

reasonable to conclude, based on the wide spread occurrence of infections and

undernutrition in animals that host nutrition is a major contributory factor to the

incidence and production effects of helminthosis in ruminants in the tropics

(Schillhorn van Veen, 1974; Kaufmann and Pfister, 1990).

2.1.4.5 Pregnancy and lactation

Breeding ewes are particularly susceptible to the effects of parasitism during

pregnancy and lactation (Thomas and Ali, 1983). With regard to gastrointestinal

nematodes, the animals often show an increased faecal egg count beginning in late

pregnancy and rising to a peak in early lactation.

The peri-parturient rise in faecal egg output (PPR) has been attributed to poor

nutrition, lack of antigenic stimulation and hormonal suppression of immunity

(O’Sullivan and Donald, 1970; Rahman and Collins, 1992; Coop and Kyriazakis,

1999; Houdijk el al., 2001). The hormonal suppression of immunity as a cause of

peri-parturient rise in egg output is further supported by the fact that prolactin

secretion in ewes follows the pattern of increased susceptibility to infection (Soulsby,

1982; Barger, 1993).

17

The peri-parturient relaxation in immunity is manifested by the resumption of

development of arrested larvae within the host (Brunsdon, 1970). In addition, there

is an increased fecundity of the parasites present and increased susceptibility to newly

acquired nematode infections (Gibbs and Barger, 1986; Romjali et a l., 1997).

Whereas the increased burdens of parasites, particularly Haemonchus contortus in

lactating ewes may result in clinical or sub-clinical disease, its greatest significance

is it’s association with decreased milk production with resultant negative effect on the

growth of lambs (Connan, 1976; Thomas and Ali, 1983). The phenomenon also

ensures the contamination of pastures with infective stages and transmission of the

infection to the new generation of animals. In temperate regions, it is the main source

of gastrointestinal nematode infection for spring-born lambs (Boag and Thomas,

1971), but the phenomenon has not been investigated extensively in the tropics.

However, the few existing reports are suggestive of a significant epidemiological role

(Dorny et a l., 1995; Tembely et al., 1998).

2 .1 .4 .6 Self-cure

The self-cure reaction to nematode infections is probably one of the best known

phenomena of immunity to helminth infection in sheep (Soulsby, 1982). In this

reaction, there is a sudden evacuation of a heavy, adult parasite load apparently

because of a local hypersensitivity reaction in the abomasum and the intestines

provoked by a second larval infection (Soulsby and Stewart, 1960; Dargie and

Allonby, 1975). Following the reaction, faecal egg counts fall drastically to a few or

zero. The reaction is not entirely species specific since the effect of the in-coming

larvae of one nematode species on the existing infections depends upon their

18

respective location in the alimentary tract. The reaction to abomasal inhabiting species

tends to evacuate both the abomasal and the intestinal species but not the reverse

(Gordon, 1968).

In grazing animals, the phenomenon is commonly observed after the rains when the

intake of infective larvae provides the stimulus for the reaction and tends to occur

simultaneously in nearly all the sheep in a flock (Allonby and Urquhart, 1973).

However, the phenomenon may also occur in sheep on lush pastures in the absence

of re-infection. This might be attributable to an "anthelmintic substance" or an

allergic substance in freshly growing grass or to physiological alterations in the

abomasum (Allonby and Urquhart, 1973).

In a review on self-cure induced by Haemonchus contortus in sheep, Gordon, (1968)

classified the phenomenon into 4 categories: (1) Classical self-cure characterized by

the loss of existing infection and the establishment of a new infection, (2) Self-cure

and protection characterized by loss of existing infection and no establishment of a

new infection, (3) Ilyper-infection characterized by loss of existing infection and

establishment of new infections and (4) No loss of infection and no establishment of

new infections. Although the phenomenon is an important mechanism for terminating

natural gastrointestinal parasitism in sheep, self-cure and protection against infection

are not necessarily inter-related (Gordon, 1968; Luffau, Perry and Petit, 1981). Its

greatest practical importance is in the misleading effect it may have on the assessment

of control programmes (Blood et a l., 1997).

19

Hypobiosis, inhibited, arrested, retarded or suppressed development are synonymous

terms used to describe the cessation of growth at a precise point in the early parasitic

development. The phenomenon usually occurs in the early fourth, but sometimes in

the early third (Michel, 1974; Schad, 1977; Eysker, 1978, 1997) or the early fifth

stage as in the case of Dictyocaulus spp. (Taylor and Michel, 1952). In sheep, high

rates of inhibition have been demonstrated in the development of Ilaemonchus

contort us (Connan, 1968a, 1971; Waller and Thomas, 1975), Ostertagia spp (Connan,

1968a; Reid and Armour, 1972; Eysker, 1978), Nematodirus filicollis (Reid and

Armour, 1972) and Chabertia ovina (Connan, 1974). Inhibition of development also

occurs in other species, but is less marked (Eysker, 1978).

There are varied stimuli that serve to initiate inhibition or to condition the infective

larvae in such a way that their development in the host is arrested. The stimuli may

be associated with parasite-related, host or environmental factors. Parasite-related

factors primarily include worm interactions and genetically regulated propensities for

arrest that might exist in certain strains (Gibbs, 1986). Larval arrest seems to be

initiated at a time of the year when their intake tends to be maximal. Overcrowding

of larvae might act as a signal or stimuli for the initiation of the arrest of development

(Barger, Le Jambre, Georgi and Davies, 1985). It has also been suggested that

arrested development is genetically programmed and a normal part of the life - cycle

of some nematodes (Waller and Thomas, 1975). Nearly all nematode species have an

innate capacity to interrupt their development at an early parasitic stage by depressing

their metabolic activity to extend their survival (Michel, 1978). This suggests that the

2.1.4.7 Hypobiosis

20

propensity to arrest is already well established in parasitic nematodes and that

depending on the selection process, a variety of stimuli might serve to induce this

type of development.

Host immunity has been implicated as being instrumental in causing this phenomenon

(Ross, 1963; Eysker, 1978, 1980). However, there is a remarkable variation in the

degree to which individual nematode species respond to this stimulus (Donald,

Dincen, Turner and Wagland, 1964; Waller, Donald and Dobson, 1981).

Seasonal factors are the most important in the induction of arrested development in

some nematode species. The onset of inhibition generally occurs just prior to the

time when weather conditions become adverse for the free-living stages. The onset

of inhibition coincides with declining temperatures in the temperate regions (Gibbs,

1982; Eysker, 1993), while in the tropics it coincides with the beginning of the dry

season (Ogunsusi and Eysker, 1979; Vercruysse, 1985; Jacquiet, Colas, Cabaret, Dia,

Cheikh and Thiam, 1995).

The mechanism or factors regulating the resumption of development o f inhibited

larvae are not known. It is assumed that loss of host immunity will result in the

resumption of the development of the arrested larvae and has consequently been

associated with peri-parturient rise in egg out put in ewes (Brunsdon, 1964; Gibbs,

1968; Connan, 1968b). However, neither experimental immunosuppression (Gibbs,

1968) nor parturition during the dry season (Schillhorn van Veen and Ogunsusi, 1978)

induced maturation of inhibited larvae.

21

In seasonally induced arrested development, the duration of arrest may be a pre

determined length equivalent to the period of adverse conditions (Gibbs, 1968). The

maturation of these larvae is therefore likely to be triggered by some internal

mechanism within the arrested larvae themselves or some external stimulus either host

or environmental (Gibbs, 1968; Connan, 1978). This would culminate in a fairly

synchronized maturation of most of the arrested larvae at an appropriate time of the

year. However, continuous rather than synchronous maturation has been observed for

Ostertagia spp. (Michel, Lancaster and Hong, 1976; Gibbs, 1986).

Hypobiosis plays an important role in the epidemiology of gastrointestinal parasites

in ruminants. In the temperate regions of the world, it is known to be the primary

means of survival over winter for Haemonchus contortus (Gibbs, 1968; Blitz and

Gibbs, 1971; Eysker, 1993). In the tropics, reports on the occurrence and extent of

hypobiosis of Haemonchus are varied. These range from none (El-Azazy, 1990;

Agyei et al., 1991), low levels (Allonby and Urquhart, 1975; Chiejina, et al., 1988;

Fakae, 1990; Pandey, 1990; El-Azazy, 1995) to high levels of hypobiosis (Ogunsusi

and Eysker, 1979; Gatongi, Prichard, Ranjan, Gathuma, Munyua, Cheruiyot and

Scott, 1998). Where high levels of hypobiosis was reported, the resumption of larval

development was associated with acute haeinonchosis in sheep and goats immediately

after the onset of the long rains (Ogunsusi and Eysker, 1979; Gatongi et a l., 1998).

2.1.5 Systems of livestock production

Livestock production systems and managerial practices influence the accessibility and

transmission of infection to a susceptible host population by creating opportunities for

22

contact between hosts and parasites. The concentration of infective stages in the

environment is very low in those systems which utilise extensive grazing areas as they

are thinly spread over a large territory. On the other hand, increased stocking density

increases contamination of pastures thus increasing the likelihood of disease. In this

case, the decreased mass and height of herbage increases concentration and

accessibility of infective larvae since they have a short distance to travel. Also larvae

which are concentrated in pasture litter are taken in with roots and soil (Blood el al.,

1997). However, the reduced plant cover may alter the micro-environment and expose

the free-living stages to conditions less favourable for their development and survival

(Soulsby, 1982).

2.2 Principles of helminth control

The fundamental ecological concepts of helminth infections in grazing animals are that

every animal is infected and that the contamination of the environment is continuous

(Blood et a l., 1997). It is also accepted that there is sufficient potential in most

grazing animals to permit the development of a major outbreak of helminthosis

whenever the correct circumstances arise and that the appearance of clinical

helminthosis indicates that proportionate losses due to sub-clinical levels of infestation

also occur in the same group (Blood el al., 1997).

Since the eradication of most helminth infections is not practical, the term control

generally implies the suppression of parasite burdens in the host at levels above which

economic losses may occur (Brunsdon, 1980). There are three main approaches to

this objective, namely, control by anthelmintic treatment, grazing management and

23

utilization of induced or natural resistance. The most efficient control programme

requires an integration of all the three facets. To do this effectively, an intimate

knowledge on the epidemiology of the helminth infection is required (Brunsdon,

1980).

2.2.1 Control by anthelmintic treatment

In many parts of the world, gastrointestinal worm control has been based on the

extensive use of anthelmintics. Anthelmintic treatments may be empirical, curative

or preventive. Empirical treatment is not based on any strategy. Curative treatment

is often delayed until clinical signs or deaths occur and at this time pastures are

usually heavily contaminated (Herd, 1988). Considerable production losses are

incurred by the time clinical signs are manifested and re-infections are common unless

the animals are moved to uninfected pastures (Michel, 1976). Preventive treatment

is the most important in forestalling excessive contamination of the pasture and thus

minimising the exposure of susceptible hosts to nematode infections. Normally, two

classes of treatment programmes, the strategic and tactical treatments are used.

2.2.1.1 Strategic treatments

Strategic treatments are normally based on the knowledge of the seasonal changes of

infection and are carried out at the same time each year or at the same stage in the

management programme with the purpose of reducing worm burdens and pasture

contamination (McKellar, 1994; Blood et al., 1997). Strategic treatments often

consists of a series of drenches at the start of the worm season, when the worms

commence egg production and when conditions become favourable for the

24

development of free-living stages on pastures. Therefore, worms do not accumulate

excessively at the beginning of the season and are not a threat to susceptible animals.

Other forms of strategic treatment include offensive and suppressive treatments. In

offensive treatment, drenching is done when conditions are unfavourable for worm

development on pastures and at a time when the worms in the host are in the

hypobiotic state. Suppressive treatment is aimed at reducing levels of infection when

nematodosis is an immediate threat to the animals. They are commonly applied as

continuous low-level administration of the drugs in licks or by means o f slow-release

devices or as repeated drenchings at short intervals of 2-3 weeks. This form of

control can be very effective, but the intensive use of drugs considerably increases

chances of development of anthelmintic resistance (Prichard, 1994).

Due to the greater susceptibility of young animals to infections, the most important

strategic treatments are those planned to provide maximal protection until weaning

and at weaning when the young animals suffer their greatest nutritional stress (Blood

et al., 1997). In older animals, strategic treatments are usually given to eliminate

contamination at a time when the pastures will be cleansed by adverse weather

conditions such as in hot dry summers (Blood et al., 1997) or the dry seasons in the

tropics (Carles, 1983).

A special strategic treatment is required for breeding sheep in most regions to counter

the peri-parturient relaxation of immunity. The precise timing of such treatment will

vary between regions and for different parasitic species, but generally treatment

25

within the month before and after parturition is desirable. Treatment two weeks

before breeding can also be useful as part of the "flashing up" (Fraser el al., 1986;

Blood el a l., 1997).

2.2.1.2 Tactical treatments

Tactical treatments are based on prompt recognition of conditions likely to favour

development of parasitic diseases. They are normally used in periods of heavy

rainfall, when nutrition is poor or when animals from a worm-free environment are

introduced into contaminated pastures and is normally used to supplement strategic

treatments. For proper use of tactical treatments, the diagnosis of critical levels of

infestation at which drug use is warranted becomes an important procedure (Blood et

al., 1997).

2.2.1.3 Anthelmintic resistance

Anthelmintic treatments have been remarkably successful in the control of

gastrointestinal helminths infections in domestic animals. However, the usefulness of

the treatments is threatened by the evolution of drug resistance in the parasite

populations and by the increasing demand for reduced levels of drug residues in food

and in the environment (Jackson, 1993; Slear and Murray, 1994; Knox and Smith,

2001). In small ruminants, reported cases of anthelmintic resistance are mainly

confined to trichostrongylid species of nematodes, (Prichard, Hall, Kelly, Martin and

Donald, 1980; Donald, 1983; Waller, 1986) and involve all commercially available

anthelmintics (Donald, 1994; Prichard, 1994). The occurrence of anthelmintic

resistance is mainly attributed to frequent usage of anthelmintics from the same class,

26

under dosing, percentage of parasite under selection pressure and the management

practices (Waller, 1987). The economic importance of this phenomenon is mainly the

occurrence of clinical and sub-clinical cases despite treatment with the anthelmintic

in question and subsequent losses in production, (Waller, 1985).

In Kenya, the number of reports on anthelmintic resistance are on the increase

(Njanja, Wescott and Ruvuna, 1987; Maingi, 1991; Waruiru, 1994; Mwamachi,

Audho, Thorpe and Baker, 1995; Wanyangu, Bain, Rugutt, Nginyi and Mugambi,

1996) . Most reports are on Haemonchus contortus, Trichostrongylus species and

rarely Oesophagostomum (Waruiru, Ngotho and Mukiri, 1998). Resistance mainly

involve benzimidazoles and levamisoles with few cases of Haemonchus contortus

being resistant to ivermectin (Mwamachi el. al., 1995; Waruiru, Ngotho and Mukiri,

1997) and closantel (Mwamachi et. al., 1995).

2.2.2 G razing managements

Various grazing managements have been used to control helminth parasites based on

the epidemiology of infections. The role of such a system is to provide clean pastures

on which livestock may safely graze. This is usually but not always after a strategic

anthelmintic treatment (Barger, 1999). The methods include various regiments of

rotational grazing, alternate grazing, mixed grazing, zero grazing and pasture rotation

among others. Such methods are only applicable to specific areas where they have

been tested and their adoption in different areas may not only fail but actually further

the development of parasitosis (Blood et al., 1997).

27

Rotational grazing is a grazing management technique involving intensive subdivision

of a pasture in which each constituent paddock is grazed for a short time then spelled

for a relatively longer time (Barger, 1999). The grazing times and rotational lengths

for a given number of paddocks requires that a compromise be made between

agronomic, production objectives and parasite control. The major requirement for

parasite control is a long enough rotation length such that most infective larvae from

previous grazing have died off and for sufficient pasture re-growth to occur. The time

should also be short enough to prevent auto-infection within a single grazing session

(Barger, 1999). This method has proved useful in wet tropics where larval survival

times are short and can readily be incorporated within a practicable rotational length

(Barger, Siale, Banks, and Le Jambre, 1994; Sani, Chong, Halim, Chandrawalhani

and Rajamanickam, 1995).

Mixed grazing of sheep and cattle is a more commonly practiced procedure. The

benefits are mainly agronomic, with better pasture utilization and the maintenance of

pasture species composition rather than parasitological. However, there are reports

in the temperate region (Barger, 1997) and in the tropics (Aumont, Mahieu, Kojfer,

Pouillot and Barre, 1995) that better parasite control as a result of grazing of sheep

and cattle together can improve performance particularly of sheep.

Alternate grazing between sheep and cattle can be a very effective form of parasite

control for both livestock species, provided that the grazing alternations are linked

with seasonal troughs in the larval availability on pastures (Waller, 1997). In the

temperate regions, excellent control of parasites from both species of livestock can

28

occur from very infrequent pasture interchange (Barger and Soutlicott, 1978). If the

timing is epideiniologically precise, pasture changes need not be accompanied by

anthelmintic treatment (Donald, Morley, Axelsen, Donnelly and Waller, 1987).

However, the implementation and effectiveness of this method in the tropics and

subtropics require that ecological studies on the free-living stages of parasites in the

environment be conducted first (Waller, 1997).

In circumstances of very high risks as in the case of flood irrigated pastures and

heavily stocked with ewes and lambs, satisfactory control may be possible only by

regular anthelmintic treatments or in some cases by the use of zero grazing (Blood

et al., 1997).

2.2.3 Breeding for genetic resistance

There is evidence that genetic variation in resistance to nematode infections within

sheep breeds (Gray, Presson, Albers, Le Jambre, Piper and Baker, 1987) is as great

as that between breeds (Barger, 1989). Therefore enhancement of genetically based

resistance to infection in the host is a potential source of helminth control (Miller,

1996; Woolaston and Baker, 1996). Sheep have been successfully bred for enhanced

resistance to nematode infection using faecal egg counts in young animals as a

selection criterion (Woolaston, 1992). Several Merino selection lines have been

established with increased resistance to either Haemonchus contortus (Woolaston,

Barger and Piper, 1990), Trichostrongylus colubriformis (Windon, Dineen and

Wagland, 1987) or Ostertagia circumcincta (Cummins, Thompson, Young, Riffkin,

Goddard, Callinan and Saunders, 1991). Similar, divergent lines of Romneys have

29

been created by selecting on faecal egg counts following infections with mixed species

(Baker, Watson. Bisset, Vlassoff and Douch, 1991; Bisset, Vlassoff, Douch, Jonas,

West and Green, 1996). Increased resistance achieved by selection under artificial

challenge regimes appear to be equally effective under natural challenges (Woolaston

et al., 1990), but somewhat variably effective when challenge is by species other than

those directly targeted in the breeding programme (Windon et al., 1987; Woolaston

and Baker, 1996).

More dramatic differences in resistance have been shown between breeds of sheep.

Breeds with superior resistance include the Scottish Blackface (Abbott, Parkins and

Holmes, 1985), Red Maasai (Preston and Allonby, 1978, 1979b; Bain, Wanyangu,

Mugambi, Ihiga, Duncan and Stear, 1993), Barbados Blackbelly, St. Croix and

Florida native (Courtney, Parker, McClure and Herd, 1985; Gamble and Zajac, 1992;

Miller, Bahirathan, Lemarie, Hembry, Kearney and Barras, 1998; Amarante, Graig,

Ramsey, El-Sayed, Desouki and Bazar, 1999).

2.2.4 Other methods of control

Other helminth control methods used at a lower scale include the use of vaccines

(Emery, 1996; Knox and Smith, 2001) and biological control (Waller, 1993;

Thamsborg, Roepstorff and Larsen, 1999; Larsen, 2000; Hein et al., 2001).

2.2.4.1 Helminth vaccines

The development of helminth vaccines for livestock has proved to be a particularly

intractable problem. The only successful vaccine against parasitic nematodes in

30

ruminants is the radiation - attenuated larval vaccine against the bovine lungworm,

Dictyocaulus vivipanis and to a lesser extent, D. filciria of sheep (Peacock and

Poynter, 1980; Waller, 1997). Unfortunately, attempts to produce vaccines for other

important gastrointestinal nematodes of livestock using the same attenuation

procedures and lately, the molecular approach using antigenic fractions of parasitic

materials have failed to provide the basis for a viable commercial product (Waller,

1997).

Several candidate vaccine antigens have been isolated from llaemonchus contortus in

the last few years and are relatively protective (Smith and Smith, 1993; Newton,

1995; Newton and Munn, 1999; Kabagambe, Barras, Li, Pena, Smith and Miller,

2000; Knox and Smith, 2001). Most of these antigens are integral membrane proteins

isolated from the intestinal cells of the parasite. However, one factor that conspires

against the acceptance of worm vaccine approach to nematode parasite control is the

general view that they have to compete favourably with modern anthelmintics not only

in terms of cost but also with regard to efficacy (Waller, 1997).

2 .2 .4.2 Biological control

The biological control of parasitic nematodes in livestock aims at establishing a

situation where the grazing animals are exposed to a low level of infective larvae that

will secure the development of naturally acquired immunity in the same animals

(Thamsborg et al., 1999). Potential biological agents include bacteria, viruses,

protozoa and fungi (Waller, 1993).

31

Among the naturally occurring enemies of free-living nematodes, including pre-

parasilic larval stages on pasture, only predacious micro-fungi have been extensively

tested (Gronvold, Wolstrup, Nansen, Henriksen, Larsen and Bresciani, 1993;

Githigia, Thamsborg, Larsen, Kyvsgaard and Nansen, 1997; Larsen, Faedo, Waller

and llennessy, 1998; Faedo, Barnes, Dobson and Waller, 1998). These micro-fungi

are able to reduce populations o f pre-parasitic nematodes significantly, are relatively

easily cultured and can be released in the environment of the target organisms in a

controlled fashion (Thamsborg et al., 1999).

32

CHAPTER 3

3.0 STUDIES ON THE PREVALENCE AND INTENSITY OF INFECTION

WITH GASTROINTESTINAL HELMINTHS IN DORPER AND RED

MAASAI SHEEP.

3.1 INTRODUCTION

Gastrointestinal helminth parasitism is one of the major animal health problems facing

ruminant livestock production in Kenya (Allonby and Urquhart, 1975; Ulvund et a l.,

1984; Carles, 1993; Gatongi, 1996; Maingi, 1996). The production and economic

losses due to these parasites may be high due to both clinical and chronic sub-clinical

infections (Allonby and Urquhart, 1975; Carles, 1993). The control of these

infections is therefore necessary in order to improve on livestock production in the

country.

The development and establishment of cost-effective and sustainable control

programmes for gastrointestinal helminths depends on the reliable estimate of

production losses and an insight into their epidemiological patterns (Brunsdon, 1980;

Nansen, 1991). Due to the wide diversity of environmental conditions in various

regions of the country, breed difference and production systems, studies carried out

in one area may not apply in another. No previous studies on the epidemiology of

gastrointestinal helminth infections in the two main breeds of sheep, the Dorper and

the Red Maasai kept in the semi-arid area of Kajiado District have been carried out.

33

The objective of the present study was therefore to determine the prevalence and

intensity of infection with gastrointestinal helminths of sheep in the area in relation

to age and breed of host and weather factors.

3 2 MATERIALS AND METHODS

3.2.1 Study area

The study was carried out in Kajiado District in the Rift Valley Province of Kenya

(Figure 3.1). Two ranches, the Maasai Rural Training Centre Ranch and the

Kitengela Sheep and Goat Project Ranch in Isinya Division were used. The area lies

at an altitude of approximately 1500 m -1850 m above sea level and is situated in

agro-ecological zone 5, classified as semi-arid. The area receives an average annual

rainfall of 607.4 mm (Range 281.6 - 923.1 mm) with a bimodal distribution. The

long rains fall between March and May and the short rains between October and

December. The rains are usually erratic, unpredictable and when they occur they fall

in bursts of high intensity for short durations. The mean annual temperatures range

from 18°C to 20°C with a mean minimum of 12"C to 14°C and a mean maximum of

24nC to 26°C, with little variation between seasons. The relative humidity ranges from

50% to 80%. The natural vegetation is characterized by (1) open grasslands

dominated by Themeda triandra, Pennisetuni meziannim and Selaria spp. and

occasional dwarf Acacia drepanolobium, Aspilia mossambisensis and Balanites

eagyptiaca, (2) wooded grasslands which are dominated by Acacia xanthophoea,

Acacia tortilis, Acacia drepanolibium, Balanites aegytiaca and Grewia similis with

Themeda triandra, Pennisetuni mazianum and Setaria spp. forming the undergrowth.

34

Figure 3.1: Map o f Kenya showing the location o f Kajiado District.

5

0 U

A Lt

A

35

3.2.2 Climatic data

Mean monthly rainfall data collected at the Isinya station was obtained from the

Meteorological Department Headquarters in Nairobi.

3.2.3 Experimental animals and treatments

The study was carried out between May 1999 and May 2000. Three age groups of

Dorper and Red Maasai female sheep were randomly selected from the flocks at the

Isenya and Kitengela ranches respectively. The age groups were made up 20 animals

each, representing lambs (3 months - 1 year old), yearlings (1-2 years old) and adult

breeding ewes (over 2 years old). On both ranches, all the animals were weighed, ear

tagged and given a single dose of albendazole (ValbazenR, Novartis East Africa Ltd,

Nairobi) at a dosage rate of 5 mg Kg '' body weight in early May 1999. No further

anthelmintic treatment was given except for salvage treatments administered to

animals showing clinical signs of helminthosis and or those with over 7000 strongyle

eggs per gram of faeces. In January 2000, new Iambs were recruited and the previous

ones moved to the group of yearlings, but the breeding ewes remained unchanged.

3.2.4 Faecal sampling and processing

Faecal samples (3 - 5 gm) were collected directly from the rectum of individual

animals at three week intervals throughout the study period. The samples were placed

in labelled plastic pots and stored at 4"C until examined. The number o f nematode

eggs per gram of faeces (EPG) and the presence of tapeworm eggs were determined

for each sample using a modified McMaster technique (Whitlock, 1948) with a lower

limit of detection of 100 eggs. Saturated sodium chloride was used as the floatation

RAmoBi UNivFRsmr KABETE LlbRARY

36

solution. A sedimentation technique as described by Hansen and Perry (1994) was

used to detect the presence of Fasciola eggs in the faecal samples. The modified

Bearmann method as described by Hansen and Perry (1994) was used to search for

lungworm larvae. The search for both the Fasciola eggs and lungworm larvae was

discontinued after being negative for four consecutive sampling occasions during the

dry season (May to July 1999) and during the wet season (October to December

1999).

Faecal samples were then pooled for all age groups, incubated at 27°C for 10 days

and nematode larvae recovered and identified to genus level using the cuticular

morphology and size as described in the MAFF (1986) manual. At least 100 larvae

were identified from the cultures on each sampling occasion.

3.2.5 Statistical analysis

Strongyle egg counts were logarithmically transformed [log (x + 10)] to normalise

their distribution and analysis of variance (ANOVA) performed in Microsoft Excel

Programme (2001). Comparisons were made between age groups (lambs, yearlings

and breeding ewes), breeds (Dorpers and Red Maasai) and seasons (wet and dry). To

exclude the effects of treatment, all the data for May 1999 and data from all animals

given salvage treatment and those which died before the end of the experiment were

excluded from the analysis. The term prevalence was defined as the percentage of

samples found positive for helminth eggs (Margolis, Esch, Holmes, Kuris and Schad,

1982) on each sampling occasion.

37

3.3 RESULTS

3.3.1 Rainfall distribution

The long-term rainfall distribution pattern for the study area and the monthly total

rainfall recorded between May 1999 and May 2000 are shown in Figure 3.2. During

this period, a total of 292 nun of rainfall was recorded. This was lower than the long

term mean of 658 mm. The amount of rainfall recorded during the short rains of

October to December 1999 (227.9 mm) was higher than the long-term mean (175.9

mm), but the total during the long rains of March to May 2000 (52.1 mm) was far

below the long-term mean (285 mm) .

3.3.2 Faecal egg counts

The arithmetic mean strongyle faecal egg counts for the three age groups of sheep are

shown in Figure 3.3 for the Dorpers and Figure 3.4 for the Red Maasai. The faecal

egg output rose from the low post-treatment level in May 1999 resulting in three

major peaks in July and August 1999, October and November 1999 and from January

to April 2000 for both breeds. Also two major troughs in egg output occurred in

September and in November to December 1999 for both breeds and a third one in

February and March 2000 for the Red Maasai. Overall the counts were significantly

different (p < 0.05) between the three age groups and between the breeds during the

study period.

38

160

May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May

Months

■ Long term monthly mean rainfall (1969-1998) S3 Monthly total rainfall May 1999-May 2000

Figure 3.2: Total monthly rainfall (mm) recorded at the Maasai Rural Training

Centre Meteorological Station between May 1999 and May 2000 and

the long-term mean monthly rainfall (1969 - 1998).

Mea

n gr

oup

stro

ngyl

e E

pg

39

Figure 3.3: The arithmetic mean strongyle eggs per gram (EPG) of faeces for

Dorper lambs, yearlings and adult breeding ewes during the period

May 1999 to May 2000.

40

igure 3.4: The arithmetic mean strongyle eggs per gram (EPG) of faeces for Red

Maasai lambs, yearlings and adult breeding ewes during the period

May 1999 to May 2000.

41

The mean faecal egg output for the different age groups and breeds and results of

statistical comparisons are shown in Table 3.1. The counts were highest for the lambs

followed by the adult ewes and lowest for the yearlings in both breeds.

Table 3.1: Comparison between the geometric mean faecal egg output for Dorper

and Red Maasai lambs, yearlings and adult breeding ewes during the

period June 1999 to May 2000.

Age groups Dorpers Red Maasai p. value

Mean faecal egg Mean faecal egg(breed difference)

counts (12 months) counts (12 months)

Lambs 762 297 P < 0.001

Yearlings 394 94 p < 0.001

Adult ewes 472 123 p < 0.001

42

The mean faecal egg output during the wet season (March, April, May, October,

November and December) and the dry season (January, February, June, July, August

and September) for the different age groups and breeds are shown in Table 3.2. The

mean counts were higher during the dry season for lambs, but higher during the wet

season for the other age groups. The counts were significantly higher (p < 0.05)

during the wet season for Dorper adult ewes, but not significantly different for all the

other groups.

Table 3.2: Comparison between the geometric mean faecal egg outputs for Dorper

and Red Maasai lambs, yearlings and adult breeding ewes during the

wet and the dry seasons between June 1999 and May 2000.

Breeds Age groups Mean EPG counts p.value

Wet season Dry season

Dorpers Lambs 709 811 0.55706

Yearlings 418 375 0.59998

Adult ewes 559 381 0.02832*

Red Maasai Lambs 287 306 0.82211

Yearlings 96 93 0.90715

Adult ewes 155 101 0.09711

* Significantly different.

43

The proportions of faecal samples from the lambs, the yearlings and the adult ewes

that were found positive for strongyle and tapeworm eggs during the wet and the dry

seasons for both breeds of sheep are shown in Table 3.3. The prevalence of strongyle

and tapeworm eggs was higher during the wet seasons for all age groups and in both

breeds of sheep. The prevalence for both strongyle and tapeworms was highest for

the lambs followed by the adult ewes and was lowest for the yearlings in both breeds

of sheep. There was a significantly higher prevalence of strongyle eggs for the

Dorper than for the Red Maasai in all the age groups during both the wet and the dry

seasons.

Table 3.3: The prevalence percentage (12 months) of strongyle and tapeworm

eggs in faecal samples in relation to age and breed of sheep during the

dry and the wet seasons between June 1999 and May 2000.

Breed and age groups Seasons

Dry Wet

Strongyles Tapeworms Strongyles Tapeworms

% • % % %

Dorper lambs 90.3 48.4 92.3 65.2

yearlings 85.9 21.2 89.7 35.6

adults ewes 84.6 25.4 92.3 40.2

Red Maasai lambs 73.3 44.1 78.3 69.5

" " yearlings 60.7 25.6 65.8 39.1

" " adults ewes 64.4 29.2 72.5 42.4

44

The distribution of the genera of gastrointestinal nematodes from the faecal cultures

from the Dorpers and the Red Maasai sheep are shown in Table 3.4.

Trichostrongylus, Haemonchus, Cooperia and Oesophagostomum were recovered in

that order of abundance throughout the year. Strongyloides was occasionally

encountered during the wet season. There was a sudden increase in the proportion of

Haemonchus from 18 % in September to 40 % in October and a decrease in

Trichostrongylus species from 80 % to 45 % over the same period.

Table 3.4: The mean distribution of genera of gastrointestinal nematodes in faecal

cultures from the Dorper and the Red Maasai sheep during the dry and

the wet seasons between June 1999 and May 2000.

Nematode genera Dorper Red Maasai

Dry Wet Dry Wet

% % % %

Trichostrongylus 61 49 57 45

Haemonchus 24 32 26 36

Cooperia 12 9 12 12

Oesophagostomum 3 9 5 7

Strongyloides 0 1 0 0

45

3.3.3 Salvage treatments

The number of animals that received salvage treatment based on clinical signs of

helminthosis such as diarrhoea, submandibular oedema and unthriftines and on

strongyle egg counts exceeding 7000 per gram of faeces during the wet and the dry

seasons are shown in Table. 3.5 for the Dorpers and Table 3.6 for the Red Maasai.

A significantly higher number of Iambs were given salvage treatments compared to

the other age groups in both breeds. In all age groups most clinical cases such as

bottle jaw (Figure 3.5) and salvage treatments occurred between June and September

during the dry season and between October and December during the wet season.

More animals received the treatment during the wet season than in the dry season.

Table 3.5: The number of Dorper sheep given salvage treatments based on

clinical manifestation of nematodosis and or egg counts (over 7000

EPG) during the dry and the wet seasons between June 1999 and May

2000.

Dorper Wet season Dry season

Mar - May Oct - Dec Jun - Sep Jan - Feb

Lambs 4 3 3 2

Yearlings 1 2 1 1

Adult 1 3 1 0

ewes

Total 6 8 5 3

46

Table 3.6: The number of Red Maasai sheep given salvage treatments based on clinical

manifestation of nematodosis and or egg counts (over 7000 EPG) during

the dry and the wet seasons between June 1999 and May 2000.

Dorper Wet season Dry season


Lambs 2 3 1 1

Yearlings 0 1 1 0

Adult ewes 0 2 1 0

Total 2 6 3 1

Figure 3.5: A Dorper yearling with bottle jaw. The photograph was taken in October 1999 just before the onset o f the short rains.

47

3.4 D IS C U S S IO N

Age influences the susceptibility of animals to helminth infections (Barger, 1993).

Lambs are more susceptible to infections due to immunological hypo-responsiveness

(Watson and Gill, 1991; Colditz et al., 1996). As the animals grow older, immunity

develops which results in a decline in levels of infection in adults (Dobson, Waller

and Donald, 1990). The results of the present study are in agreement with the

forementioned observation in that the prevalence, the strongyle egg counts and the

number of animals that received salvage treatments were highest in lambs and lowest

in the yearlings. It is also well recognized that previously acquired immunity to

nematode infection tends to be lost in late pregnancy and in lactation in ewes (Barger,

1993). Most of the adult ewes used in this study were pregnant between June and

October 1999 and lactating between October 1999 and March 2000. The loss of

immunity in ewes during this period may have contributed to the higher prevalence,

higher egg counts and the larger number that received salvage treatment compared to

the yearlings.

Differences in the susceptibility of breeds of sheep to gastrointestinal nematode

infections have been demonstrated in different parts of the world (Abbott et al., 1985;

Courtney et al., 1985; Baker, 1995; Amarante et al., 1999). In Kenya, the Red

Maasai has been observed to be more resistant to infection with Haemonchus than the

exotic breeds (Preston and Allonby, 1979a; Bain et al., 1993; Baker, 1995). The

results of the present study are therefore in agreement with these findings as the

prevalence, the strongyle egg counts and the number of animals that received salvage

treatments were significantly lower (p < 0.05) for the Red Maasai than the Dorpers.

48

The prevalence and (he intensity of infection witli gastrointestinal nematodes is greatly

influenced by the weather pattern. In most of the tropics and the sub-tropics, variation

in rainfall is the major factor that influences the development and survival of the pre-

parasitic stages on pastures and therefore the infection rates (Altaif and Yakoob,

1987; Banks el al., 1990; Waruiru, 1998). In Kenya, reports on the prevalence and

intensity of infection with strongyles in small ruminants indicate that higher counts

were recorded during the wet than the dry seasons in Naivasha (Gatongi, 1995),

Nyandarua (Maingi, 1996) and in Makuyu (Githigia, 2000). Higher counts were

recorded during the dry than the wet seasons in Embu (Ulvund et al., 1984) and in

Muguga (VVamae and Ihiga, 1990). In the present study, the counts were significantly

higher (P < 0.05) during the wet than the dry seasons for the Dorper adult ewes, but

not significantly different for all the other groups.

Several factors may have contributed to the current observations. The long rains of

March to May 2000 were lower than expected for the study area and may have

resulted in lower pasture infectivity than is normal during this period. Self-cure

mechanisms may have been operating during both the dry and the wet seasons having

self-limiting effects thus the sudden drops in the prevalence and egg output during the

months of September, November to December 1999 in all breeds and in February to

March 2000 for the Red Maasai. Lambing and lactation in the adult breeding ewes

coincided with the short rains in October to December. As a result of the peri-

parturient laxity in immunity, the prevalence and counts of strongyle eggs were

relatively higher during the wet season than the dry season. Lastly the rise in faecal

egg output observed during the late dry season and soon after the onset of the short

rains (October to November 1999) resulted in higher prevalence and egg counts than

was expected during this period.

49

The results of the present study indicated the occurrence of peaks and troughs in

strongyle faecal egg output in sheep within the study area. The peak observed in July

to August might have resulted from infections by residual larval population that

survived in the pastures after the long rains and that in January was as a result of

infections by larvae that developed during the short rains. However, the peak that

occurred during the late dry season and soon after the onset of the short rains

(October) can not entirely be accounted for by fresh infections in the pastures, since

the availability of infective larvae at that time was very low (See Chapter 5). Similar

peaks in strongyle egg output during the late dry season and at the onset of the rains

were observed in sheep and goats in the semi-arid area of Naivasha where they were

accompanied by parasitic gastritis and mortalities (Gatongi, 1996) and in goats in the

marginal low potential areas of Thika District (Githigia, 2000). These peaks were

attributed to increased egg laying by adult parasites following maturation of

hypobiotic larvae of Haemonchus. The results of the present study therefore suggest

the occurrence of hypobiosis of trichostrongylid nematode parasites of sheep in the

study area.

Some nematode parasites are able to adapt to adverse conditions by arresting their

development inside the host and then resume their development whenever field

conditions improve (Gibbs, 1968). In the tropics, hypobiosis normally occurs during

the dry season and the resumption of development occurs towards the end of the dry

season or at the onset of the rains (Ogunsusi, 1979b; Jacquiet, et al., 1995; Gatongi,

1996). The results of the present study suggest that the resumption of development

in the study area is limed to coincide with the favourable environment created by the

50

short rains. This observation agrees with that of Githigia (2000) in the marginal low

potential area of Thika District where the resumption of development of hypobiotic

larvae in goats was targeted towards the short rains. The present finding was however

at variance with that of Gatongi (1996) who observed the resumption of development

of hypobiotic larvae in sheep and goats in a semi-arid area of Naivasha targeted

towards the long rains. The long-term rainfall distribution pattern for the study area

and the results of the study on the dynamics of free-living stages on pastures (Chapter

5) indicated that the most adverse environment for the development and survival of

the pre-parasitic stages occur during the long dry period between June and October

rather than the short dry period between January and March. For survival and

effective transmission of the nematode parasites in the study area, the levels of

hypobiosis should therefore be higher during the long dry season and resumption of

development be targeted towards the short rains.

The troughs in faecal egg output occurred in both the Dorper and the Red Maasai

breeds. A decrease of about 60 % in egg counts occurred over a period of 3 weeks

and was considered as self-cure. Similar observations were made in a semi-arid area

of Naivasha where up to 80 % reduction in faecal egg output occurred in Merino and

Red Maasai breeds (Preston and Allonby, 1979a). In grazing animals, self-cure is

commonly observed after rains when the intake of infective larvae provides the

stimulus for the reaction and tends to occur in nearly all the sheep in the flock

(Allonby and Urquhart, 1973). The phenomenon may also occur in sheep on lush

pastures in the absence of re infection. This may be as a result of an "anthelmintic

substance" or an allergic substance in freshly growing grass or due to physiological

alterations in the abomasum (Allonby and Urquhart, 1973).

51

The spectrum of the self-cure may range from merely the temporary suppression of

egg-laying to complete expulsion of the adult worm burden (Allonby and Urquhart,

1973; Adams, 1983). In the present study, the self-cure that occurred in November

to December may be attributed to re-infection by larvae and or the consumption of

lush pastures that resulted from the short rains. However, none of these factors could

directly be associated with the phenomenon in February and September as this were

a dry month and not conducive for pasture growth and development of the infective

larvae. Similar observations were made in Naivasha where the Red Maasai sheep self-

cured during the dry season in the absence of fresh pastures (Preston and Allonby,

1979a). The self-cure observed at this time might therefore have resulted from a

temporary cessation in egg production by the parasites.

The frequency of self-cure may be influenced by the breed of sheep among other

factors. In their study on the influence of breed on the susceptibility o f sheep to

Haemonchus contortus in Kenya, Preston and Allonby, (1979a,b) did not only observe

that the frequency of self-cure was higher for the Red Maasai than the Merino, but

was also influenced by the blood type. In the present study the Doipers were able to

self-cure two times and the Red Maasai three times during the study period. It was

also evident that the physiological status of the animals influenced the extent of the

self-cure since the lactating ewes were unable to effectively self-cure in November

and December as a result of the laxity in immunity. This was more evident in the

Dorpers than in the Red Maasai and is again suggestive of breed differences in

susceptibility to helminth infections.

52

Most clinical cases of helminlhosis and salvage treatments in this study occurred

between July and November and were attributed to two main reasons.

a) fhe pastures were mostly dry and of low nutritional value from July to October.

At this lime the animals were in poor body condition (See Chapter 7) and therefore

highly susceptible to the effects of helminth infections.

b) The resumption of development of hypobiotic larvae of Haemonclius towards the

end of the long dry season and at the onset of the short rains (October to November)

resulted in clinical haemonchosis in some animals (Figure 3.5) thus necessitating

salvage treatment. This observation is in agreement with that of Gatongi (1995) who

reported clinical haemonchosis in sheep towards the end of the dry season and at the

onset of the long rains in sheep and goals under the semi-arid environment of

Naivasha.

The results of the distribution of nematode genera from the faecal cultures clearly

showed that in the semi-arid area of Kajiado District, mixed infections occur.

Trichostrongylus, Haemonclius, Cooperia and Oesophagoslomum in descending order

of occurrence were recovered throughout the year. Trichostrongylus species were

found to be the most prevalent in the study area. This finding differed from those of

Gatongi (1995) and Maingi (1996) who reported a higher prevalence for Haemonclius

in sheep in the semi-arid area of Naivasha and the high rainfall area of Nyandarua

District respectively. The higher prevalence of Trichostrongylus species in the present

study may be attributed to the ability of T. colubriformis free-living stages in the

herbage to resist desiccation compared to Haemonclius and the other species (Banks

et al., 1990; Silva, Bevilaqua and Costa, 1998). At the beginning of this study in

53

early May 1999, all the animals were treated with albendazole. The re-infection that

followed occurred during the dry period and was therefore favourable to the more

resilient Trichostrongylus species. This dominance was further enhanced by the

inadequate long rains of March to May 2000.

The results of the present study therefore indicate that mixed infections occur in sheep

in the study area and that the prevalence and intensity of infection is influenced by

the age of the host, the breed and by weather factors and in particular rainfall.

Therefore, the control measures in this area should aim at reducing the impact of the

most important nematode species, Haemonchus and Trichostrongylus, in all age

groups and breeds. The lambs should be protected from the adverse effects of

infection till they acquire immunity and the control of infections in the other age

groups be targeted towards reduction of pasture contamination based on the rainfall

distribution pattern and the reproductive status of the adult ewes. Farmers in the area

should also be encouraged to keep the more resistant Red Maasai breed which is

indigenous to the area or their crosses rather than the more susceptible imported

breeds, especially where the cost of anthelmintic treatments are unaffordable. Where

treatment is affordable, the bigger and faster growing Dorper should be kept.

54

C H A P T E R 4

4.0 S T U D IE S O N T H E O C C U R R E N C E O F P E R I-P A R T U R IE N T R IS E IN

T R IC H O S T R O N G Y L ID N E M A T O D E E G G O U T P U T IN B R E E D IN G

EVVES AND T I IE P R E V A L E N C E A N D IN T E N S IT Y O F IN F E C T IO N IN

L A M B S .

4.1 INTRODUCTION

Breeding ewes are particularly susceptible to the effects of parasitism during

pregnancy and lactation (Thomas and Ali, 1983). During this period, the animals

often show a peri-parturient rise (PPR) in faecal egg counts which may be

accompanied by clinical signs of parasitism and in case of poor nutrition even low

worm burdens can have detrimental effects (Armour, 1980).

Studies on the PPR have either been complicated by the coincidence of lambing with

the resumption of development of arrested larvae of gastrointestinal nematodes in the

spring in temperate regions (Gibbs, 1968) or the onset of the rains in the tropical

regions (Van Geldorp and Schillhorn van Veen, 1976; Schillhorn van Veen and

Ogunsusi, 1978) leading to increased faecal egg output in ewes. The peri-parturient

rise in egg output is known to be the main source of gastrointestinal nematode

infections for the spring-born lambs in the temperate regions (Boag and Thomas,

1971). The occurrence and impact of the phenomenon on sheep production in the

tropics is not clear. However, the phenomenon has been reported in Nigeria (Van

Geldorp and Schillhorn van Veen, 1976; Schillhorn van Veen and Ogunsusi, 1978)

55

and in Ethiopia (Tembely et al., 1998) where hypobiosis was also reported to occur.

It has also been reported in Southern Ghana (Agyei et al., 1991) and in Indonesia

where hypobiosis has not been reported (Romjali et al., 1997). The PER in these

regions is thought to be an important source of pasture contamination and a source

of infection for the lambs.

It is also known that lambs are more susceptible to infections with gastrointestinal

nematode parasites and have a higher mortality than adult sheep (Watson, 1991;

Gatongi, 1995). Their greater susceptibility to infection is largely due to

immunological hypo-responsiveness (Watson and Gill, 1991; Colditz et al., 1996).

This susceptibility of Iambs and weaners to parasitic infections represents a

considerable problem for farmers. Currently, the problem is addressed only by a

combination of strategic treatments with effective anthelmintics and astute grazing

management (Dash, 1986).

To develop strategic preventive measures against helminthosis, it is necessary to have

a fairly precise knowledge of the seasonal epidemiology of helminth infections for the

target group in a specific area. No studies have previously been carried out in Kajiado

District to examine the occurrence of PPR in breeding ewes and the epidemiology of

infection in lambs. The objectives of the present study were:

1. To investigate the occurrence of the PPR in trichostrongylid nematode egg

output in breeding ewes in a semi-arid area of Kajiado District over the

lambing and lactating periods.

56

2. To establish the prevalence and intensity of gastrointestinal nematode

infections in Iambs in relation to seasonal effects in a semi-arid area of

Kajiado District.

4.2 MATERIALS AND METHODS

4.2.1 Climatic data

Mean monthly rainfall data collected at the Isinya station was obtained from the

Meteorological Department Headquarters in Nairobi.

4.2.2 Experimental animals and anthelmintic treatments

The PPR study was carried out on Dorper ewes and yearlings raised at the Maasai

Rural Training Centre Ranch in Kajiado District between June 1999 and December

2001. The prevalence and intensity of infections study was carried out in lambs

between the age of 6 weeks to 12 months from November 1999 to November 2001.

The animals grazed on natural un-improved pastures (Figure 4.1) and received

mineral supplementation in the form of MacIickR blocks (Coopers Kenya Ltd,

Nairobi) in the morning and evening. The ewes and the un-weaned lambs grazed in

one group (Figure 4.2). After weaning, the lambs grazed together with the yearlings

in another group (Figure 4.3). Both groups of sheep however, grazed separately but

on the same paddocks. With the exception of Iambs, all the animals used in the study

were treated with albendazole (VaIbazenR, Novartis East Africa Ltd, Nairobi) at a

dosage rate of 5 mg Kg 1 body weight in May 1999 (Year 1), April 2000 (Year 2)

and January 2001 (Year 3). No further anthelmintic treatments were given except for

salvage treatments administered to animals showing clinical signs of helminthosis and

or those with over 7000 strongyle eggs per gram of faeces.

57

Figure 4.2: Dorper ewes and unweaned lambs on natural unimproved pastures (November 1999).

Figure 4.3: Dorper weaned lambs and yearlings on natural unimproved pastures (March 2000).

58

4 .2 .2 .1 Breeding ewes

The study on ewes was carried out through three breeding seasons between June 1999

and December 2001. During each of the breeding seasons, twenty animals aged

between two and four years were randomly selected from the breeding stock and

constituted the mated group and another twenty animals were randomly selected from

the un-mated yearlings and constituted the control group. Rectal faecal samples (3-5

gm) were collected from individual animals at three week intervals from the onset of

the mating season and ended 6 weeks post weaning in the first and the second year

o f study and just after weaning in the third year. The number of strongyle eggs per

gram of faeces were determined using the modified McMaster technique (Whitlock,

1948) with a lower limit of detection of 100 eggs. Saturated sodium chloride solution

was used as the floatation fluid. The mating, lambing and weaning schedule during

the three breeding seasons is shown in Table 4.1.

Table 4.1: The mating, lambing and weaning schedule for Dorper sheep at the

Maasai Rural Training Centre Ranch during the period June 1999 to

December 2001.

Breeding season Time of mating, lambing and weaning

Mating lim bing Weaning

Year 1 Jun 1999 Oct / Nov 1999 Mar 2000

Year 2 Jul 2000 Nov / Dec 2000 Mar 2000

Year 3 Apr / May 2001 Sep / Oct 2001 Dec 2001

59

4.2.2.2 Lambs

The prevalence and intensity study was conducted through two breeding seasons

between November 1999 and November 2001. During this period, two crops of

female lambs were studied. Each year, a total of twenty ear tagged lambs were

randomly selected from the flock at the age of six weeks (November 1999 and

January 2001). Rectal faecal samples (3-5 gm) were collected from individual lambs

at three week intervals for a period of one year. The samples were placed in labelled

plastic pots and stored at 4°C until examined. The number of nematode eggs per gram

of faeces (EPG) were determined for each sample using a modified McMaster

technique.


Strongyle nematode egg counts were logarithmically transformed [log (x + 10)] to

normalise their distribution and analysis of variance (ANOVA) performed using a

Microsoft Excel program (2001). Comparisons were made between the mated ewes

and the un-mated yearlings, breeding seasons, between the strongyle egg counts for

the lambs and those of the mated ewes in the respective years, between year 1 and

2 for lambs and the rainfall distribution.

60

4.3 RESULTS

4.3.1 Kainrall distribution

The total monthly rainfall (mm) recorded in the study area between January 1999 and

December 2001 is shown in Figure 4.4. During this period, the long rains fell during

the months of March and April. The short rains fell during the period of October to

December, except for the year 2001 when they extended to January. All the other

months were considered dry months.

4.3.2 Mating, lambing and weaning schedule

The mating, lambing and weaning schedule during the study period is shown in Table

4.1. Lambing occurred between September and December. The lambs were weaned

in the months of March for the first and second years and in December 2001 during

the third year.

4.3.3: Egg counts in ewes and yearlings

The arithmetic mean strongyle faecal egg counts for the mated ewes and the un-mated

yearlings during the study period are shown in Figure 4.5 (June 1999 to April 2000),

Figure 4.6 (June 2000 to April 2001) and Figure 4.7 (April 2001 to December 2001).

For ease of comparison, the arithmetic mean strongyle eggs counts for the mated

ewes during the three years are also shown in Figure 4.8. Peri-parturient rise in

faecal strongylid egg output in the mated ewes occurred in October 1999 to March

2000 (Year 1), November 2000 to February 2001 (Year 2) and September 2001 to

December 2001 (Year 3).

Rai

nfal

l (m

m)

61

Months

■■M onth ly total rainfall (mm) 1999 ES3 Monthly total rainfall (mm) 2000 EZ2Monthly total rainfall (mm) 2001 —x - Long-term monthly mean rainfall (mm)

Figure 4.4: Total monthly rainfall (nun) recorded at the Maasai Rural Training

Centre Meteorological Station between January 1999 and December

2001 and the long-term mean monthly rainfall (1969 - 1998).

Mea

n gr

oup

stro

ngyl

e ep

g62

Figure 4.5: The arithmetic mean strongyle eggs per gram (EPG) o f faeces for

mated Dorper ewes and un-mated yearlings during the period June

1999 to April 2000.

Mea

n gr

oup

sti

ongy

le e

pg

63


mated Dorper ewes and un-mated yearlings during the period June

2000 to April 2001.

Mea

n gr

oup

stro

ngyl

e ep

g

64


mated Dorper ewes and un-mated yearlings during the period April

2001 to December 2001.

Mea

n gr

oup

stro

ngyl

e ep

g

65


mated Dorper ewes during the period June 1999 to December 2001.

66

The mean strongyle egg counts for the mated ewes were significantly higher (p <

0.05) during the lambing and lactation period than in the pre-lambing period in the

first and the third years of study. The highest mean strongyle egg counts in the

breeding ewes during the peri-parturient period were recorded in the third year of

study from September 2001 to December 2001 and lowest during the second year

from November 2000 to March 2001 (Figure 4.8). In the first and third years of

study, the counts were significantly higher (p < 0.05) for the mated ewes during the

lambing and lactation period than in the un-maled yearlings. There was no significant

difference between the mean counts during the pre-lambing and post-lambing periods

for the un-mated yearlings in all the years (Table 4.2). The egg counts were

significantly higher (p < 0.05) during the wet than the dry season for the mated

ewes, but not significantly different during the two seasons for the un-mated

yearlings.

Table 4.2: Comparison between the geometric mean strongyle egg counts for

Dorper mated ewes and un-mated yearlings during the pre-lambing and

lambing and lactation periods of the ewes between June 1999 and

December 2001.

BreedingSeason

Age group Mean faecal egg counts & breeding cycle P value

Pre-lambing Lambing & lactation

Year 1 Ewes 295 720 0.00013*

Yearlings 355 315 0.61391

Year 2 Ewes 445 561 0.21917

Yearlings 474 540 0.50334

Year 3 Ewes 481 1104 0.00001*

Yearlings 331 382 0.56058

* Significantly different.

67

4.3.4: Egg counts in iambs

The arithmetic mean strongyle faecal egg counts for the ewes and lambs during the

study period are shown in Figures 4.9 (June 1999 to April 2000) and Figure 4.10

(June 1999 to April 2001) for the first and second year respectively. The mean

strongyle egg counts for the ewes were higher than those of the lambs under 12

weeks of age, but the counts for the lambs 12 weeks old to weaning at the age of

about 21 to 27 weeks were higher than those of the ewes (Table 4.3).

Table 4.3: Comparison between the arithmetic mean faecal strongyle egg counts

for Dorper mated ewes and Iambs during the periods November 1999

to April 2000 (Year 1) and January 2001 to April 2001 (Year 2).

Weeks Mean strongyle egg counts and P values

post-lambingYear 1 Year 2

Ewes Lambs P values Ewes Lambs P values

6 1167 0 P<0.001 1265 0 p<0.001

9 1067 731 0.00308 1695 400 p<0.001

12 1689 2315 0.34421* 1160 3050 0.01364

15 1933 2415 0.18122* 600 1840 0.00357

18 1289 2446 0.02974 1155 3360 0.002778

21 1500 2608 0.01681 1255 2430 0.02892

24 900 3000 0.00188 N/A N/A N/A

27 922 2769 0.00072 N/A N/A N/A

* Not significantly different

68


Dorper ewes from the time of mating to six weeks post-weaning and

for lambs from the age of six weeks to six months during the period

June 1999 to April 2000.

Mea

n gr

oup

str

ongy

le e

pg

69


Dorper ewes from the time of mating to six weeks post-weaning and

for lambs from the age of six weeks to the age of five months during

the period June 2000 to April 2001.

70

The arithmetic mean slrongyle faecal egg counts for the lambs during the first and the

second year of study are shown in Figures 4.11. The mean counts rose sharply in

January 2000 and in February 2001 in the first and second years of study

respectively. During the study period, the highest faecal egg counts were recorded in

April shortly after weaning. In the first year of study, the counts for lambs were

significantly higher during the dry than wet seasons (Table 4.4). The counts were

significantly higher (p < 0.05) during the wet than the dry season in the second year

of study. There was no significant difference between the overall faecal output in

lambs in the two years. In contrast the ewes had significantly higher (p < 0.05)

counts during the wet than the dry seasons in all the three years.

Table 4.4: Comparison between the geometric mean faecal strongyle egg output

for Dorper lambs during the wet and the dry seasons during the period

November 1999 to November 2001.

Year of study Mean strongyle egg counts P values

Wet season Dry season

Year 1 462 867 0.00764

Year 2 1062 449 0.00106

NAIROBI U N IVFRSfry

KABETE l ib r a r y

Mea

n gr

oup

stro

ngyl

e ep

g

71


Dorper lambs during the period November 1999 to November 2001.

72

4.3.5 Salvage treatments

The number of animals that received salvage treatment based on clinical signs of

helminthosis and for strongyle egg counts exceeding 7000 per gram of faeces during

the wet and the dry seasons are shown in Table 4.5 for ewes and Table 4.6 for

lambs. More ewes and lambs received salvage treatments during the wet season than

in the dry season. In lambs, most clinical cases and salvage treatments occurred

between June and September during the dry season and between October and

December during the wet season.

Table 4.5: The number of Dorper ewes given salvage treatments based on clinical

signs of helminthosis and or faecal strongyle egg (over 7000 EPG)

during the wet and the dry seasons between June 1999 and December

2001.

Period Wet season Dry season


Jun 1999 - Apr 2000 1 (n = 16) 3 (n =19) 1 (n = 20) 0 (n =16)

Jun 2000 - Apr 2001 1 (n = 12) 2 (n = 17) 3 (n = 20) 3 (n = 15)

Apr 2001 - Dec 2001 0 (n = 20) 4 (n = 18) 2 (n = 20) N/A

73

Table 4.6: The number of Dorper lambs given salvage treatments based on

clinical signs of helminthosis and or faecal strongyle egg (over 7000

EPG) during the wet and the dry seasons between November 1999 and

November 2001.

Period Wet season Dry season


Nov 1999 - Oct 2000 4 (n = 18) 2 (n = 11) 3 (n = 14) 2 (n = 20)

Jan 2001 - Nov 2001 4 (n = 18) 3 (n = 12) 2 (n = 14) 2 (n = 20)

4 .4 D IS C U S S IO N

The results of the present study demonstrate the occurrence of a peri-parturient rise

(PPR) in faecal egg output in Dorper ewes in a semi-arid area of Kajiado District.

The findings are in agreement with those of other workers in the tropics (Van

Geldorp and Schillhorn van Veen, 1976; Sclnllhorn van Veen and Ogunsusi, 1978;

Agyei et a l., 1991; Romjali et al., 1997; Tembely et. al., 1998). In the present

study, there was a significant rise in the strongyle egg output in ewes lambing before

the onset o f the short rains (September and October) as well as those lambing during

the short rains (November and December).

74

Although the peri-parturient rise in faecal egg output in the ewes is a well-recognized

phenomenon, the underlying mechanisms are complex and still not fully understood.

I t’s cause has been variously ascribed to poor nutrition, stress, lack of antigenic

stimulation and hormonal suppression of immunity (O’Sullivan and Donald, 1970;

Barger, 1993). The relaxation in immunity is manifested by the resumption of

development of arrested larvae within the host, increased fecundity of the parasites

present and increased susceptibility to newly acquired nematode infections (Gibbs and

Barger, 1986).

In the present study, most of the gestation period and early lactation coincided with

the dry months from May to October. Late pregnancy and lactation impose a drastic

increase in the nutrient requirements in mammals. The break-down in immunity in

the peri-parturient ewes has therefore been attributed to the scarce supply of

metabolisable proteins at times of increased demands (Coop and Kyriazakis, 1999;

Iloudijk et al., 2001). During the dry season, most native tropical grasses have a low

nutritional value and may not meet the requirements of the animals (Reynolds and

Adediran, 1987). It is therefore possible that the low plane of nutrition in the peri-

parturient ewes may have contributed to the occurrence of the phenomenon observed

in this study.

The role played by hypobiotic larvae in the occurrence and magnitude of PPR in

sheep varies with the time of lambing. In Nigeria, Schillhorn van Veen and Ogunsusi

(1978) demonstrated that resumed development of Haemonchus contortus hypobiotic

larvae did not occur in ewes lambing in the middle of the dry season. A rise in faecal

75

egg output was observed in the whole flock at the end of the dry season, but it was

most pronounced in ewres in early lactation. Michel (1978) also favoured the view that

in sheep and cattle, arrested worms that participate in the peri-parturient rise resume

development at a particular time in the calendar year, and the events associated with

parturition or lactation affect only the subsequent fate and fecundity of the developing

worms. In the present study, high rise in faecal egg output occurred when lambing

coincided with the end of the dry season and the onset of the short rains (September

and October) in the first and the third years of study. The rise can be attributed

almost entirely to the resumption of development of arrested larvae and increased

fecundity of the parasites present since the level o f pasture infectivity was low at

around this time (Chapter 5). Maturation of inhibited larvae may also have occurred

in the un-mated yearlings as seen in the rise of the faecal egg counts at around the

same period. However, the rise was of a lower magnitude compared to that observed

among the mated ewes. It was also noted that when lambing occurred in November

and December (Year 2000) there was no significant difference in the magnitude of

the rise in faecal egg counts between the mated ewes and the un-mated yearlings in

September and October.

High peaks of egg output were observed between December 1999, 2000 and March

2000, 2001 after the short rains. These peaks could only be attributed to new

infections that occurred from pasture contamination and increased fecundity of

existing adult parasites. Similar peaks were observed in the un-mated yearlings, but

were of lower magnitudes. It was also clear that relatively high egg counts were

maintained during lactation and that the ewes were not capable of effective self-cure

76

compared to the un-maled yearlings. Similar observations have been made in other

parts of the tropics where ewes lambing during the wet seasons had higher faecal egg

output than the dry ewes and were attributed to the hormonal suppression of immunity

in lactaling ewes (Agyei et al., 1991; Romjali et a l., 1997; Tembely et al., 1998).

In the present study, the strongyle egg output was significantly higher during the wet

than the dry season for the mated ewes. This differed from the observation of Ulvund

et. al., (1984) in Enibu, where the counts were higher during the dry than in the wet

season. The higher strongyle egg output during the wet season in the present study

may be attributed to the fact that two thirds of the lactation period when the ewes

were most susceptible to the effects of nematode infections occurred during this

season. In the study area and generally in other parts of the world, the gestation

period in livestock are designed to coincide with that of inadequate pastures (Figure

4.1) and is geared to completion at a time when freshly growing pastures become

available for the progeny (Armour, 1980). Parturition and lactation therefore

coincides with the rainy seasons when pastures are green (Figure 4.2) which are

conducive for the development of infective nematode larval stages in the pastures.

The epidemiological significance of the peri-parturient rise in egg output observed

here is that it contributes to high pasture contamination when the number of

susceptible lambs is increasing. This observation is in agreement with those of other

workers in the tropics (Ulvund et al., 1984; Agyei et al., 1991; Romjali et al., 1997;

Tembely et al., 1998). In addition the pathological consequences of the impaired

immunity on the peri-parturient ewes and the resulting adverse effects on the growth

of the lambs, may be more important. It is therefore important that control measures

77

in the study area be targeted at reducing the levels of infection during gestation and

to reduce the high pasture contamination levels resulting from the peri-parturient rise

in egg output.

The results of the present study also confirm that lambs are more susceptible to

infection with gastrointestinal nematode parasites than the adult sheep and that their

resistance increases with age during the first 12 months of life. Generally, lambs do

not suffer from nematode infections before the age of 10-12 weeks as long as the

ewes have adequate milk to delay the intake of significant quantities o f contaminated

pasture and hence infective larvae (Carles, 1983; Blood et al., 1997). The results of

the present study confirm these observations in that the lambs had zero nematode egg

counts at the age of 6 weeks. These results also suggest that the strongyle infections

started to build up in the young Iambs as they began to rely heavily on pastures as

seen in the sudden rise in egg counts at the age of 12 weeks (3 months). The counts

remained high till the lambs attained the age of about 7 months and then declined

gradually as the lambs grew older. These lambs were able to self-cure at the age of

10-12 months. This phenomenon has been well established for the common nematode

parasites of sheep including Haemonchus contortus (Manton, Peacock, Poynter,

Silverman and Terry, 1962), Trichostrongylus colubriformis (Gibson and Parfitt,

1972) and Osiertagia circumcincta (Smith, Jackson, Jackson and Williams, 1985).

The greater susceptibility of young animals to infection is not simply a consequence

of their not having been exposed sufficiently to the nematodes, but is ascribed to their

defective development of protective acquired immune responses to worm infections

78

(Watson and Gill, 1991; Colditz et al., 1996). The development of acquired immunity

normally occurs at around the age of 6 to 7 months (Watson and Gill, 1991; Douch

and Morum, 1993; Colditz et al., 1996). The declining levels in faecal egg output in

the lambs at the age of 7 months and their ability to self-cure at the age of 10 to 12

months was therefore attributed to the development of acquired immunity.

In the present study, the most likely source of infection for the lambs was the peri-

parturient rise in nematode egg output in the ewes. The peri-parturient rise caused

high levels of pasture contamination resulting in increased availability of infective

larvae for the new-born lambs. The high egg output by the lambs after they attained

the age of 12 weeks further increased the levels of pasture contamination and

consequently the rate of re-infection for the same lambs. Control measures in the

study area should aim at reducing the effects of the peri-parturient rise in

trichostrongylid nematode egg output, by treating the ewes just before lambing. A

second treatment should be given to both the ewes and the lambs at around 12 weeks

post-lambing and preferably the animals be moved to clean pastures.

In the present study, it was also observed that the highest strongyle egg counts in

lambs were recorded in April soon after weaning. Weaning imposes considerable

stress to the lambs as well as the ewes. The stress is observable as emotional anxiety

and is accompanied by significant increases in adrenal responses (Watson, 1991). The

physiological responses associated with this weaning stress (especially elevation in

glucocorticoids) have been shown to contribute to delayed development of protective

immune responses to the gastrointestinal parasites Haemonchus contortus and

79

Trichostrongylus colubriformis (Watson and Gill, 1991). Helminth control measures

in lambs should also aim at reducing the levels of infection at around this time and

if possible the lambs be moved to cleaner pastures after treatment.

In the second year of study, the mean strongyle egg counts in lambs were

significantly higher during the wet (geometric mean EPG 1062) than the dry season

(geometric mean EPG 449). This was not the case in the first year of study where the

counts were higher during the dry (geometric mean EPG 867) than the wet season

(geometric mean EPG 462). This was attributed to the fact that the long rains of

March to May 2000 were lower than expected for the area and may have resulted in

lower pasture infectivity than is normal during this period. The earlier finding was

in agreement with the observations of Maingi (1996) who reported the highest level

o f infection and prevalence of strongyle eggs in sheep during the wet months in the

high rainfall area of Nyandarua District.

In the tropics, most clinical cases of helminth infections occur during the wet season

(Eysker and Ogunsusi, 1980). In the present study, the number of animals that

received salvage treatments as a result of clinical cases and high faecal egg counts

was higher during the wet season. However, the high levels of infection observed

during both the wet and the dry seasons in the present study suggest that control

measures in this area should aim at reducing the infection levels in both seasons.

80

CHAPTER 5

5 .0 STUDIES ON THE DEVELOPMENT, SURVIVAL AND AVAILABILITY

OF INFECTIVE LARVAE ON PASTURES.

5.1 INTRODUCTION

The major epidemiological variable influencing nematode burdens of grazing animals

is the infection rate, or the number of infective larvae ingested from pastures each

day (Barger, 1999). The size of the populations of infective larvae of ruminant

nematode parasites on the pastures are the result of the number of eggs spread with

faeces by the animals, their development rate into larvae, their survival and the

translation of these larvae into the grass (Barger, 1999).

In many parts of the tropics the number of free-living stages of parasitic nematodes

on the pastures follows seasonal fluctuations (Tembely, 1998). Investigations carried

out on nematode larvae ecology in parts of Sub-Sahara Africa (Dinnik and Dinnik,

1961; Onyali el al., 1990; Ndamukong and Ngone, 1996; Tembely, 1998) show that

the rate of development and the longevity of eggs and larvae vary with temperature,

rainfall and relative humidity in different geo-ecological regions. Knowledge of

seasonal larval availability, origin of larvae contributing to peaks and climatic

requirements for nematode egg hatching, larval development and survival is essential

in the formulation of sustainable parasite control programmes. No previous studies

have been carried out in Kajiado District.

81

The objective of the present study was therefore to determine the seasonal pattern of

development, survival and availability of infective larvae of sheep nematodes on

pastures.


5.2.1 Climatic data

Climatic data from the study area was obtained from the Department o f Meteorology

Headquarters and was limited to the maximum and minimum air temperatures,

relative humidity and rainfall.

5.2.2 Plot studies

An area of pasture approximately 50 m x 50 m at the Maasai Rural Training Centre

Ranch was fenced off in January 2000 to prevent the entry of animals. A series of 36

plots each 5 in x 2 m were demarcated. Trenches were dug between the plots to avoid

cross contamination between the plots during heavy rains. The herbage and soil larval

counts in the plots were monitored monthly as described by Hansen and Perry (1994)

from January to June 2000 when no further larvae from the previous grazing were

recovered for 4 consecutive samplings. The herbage on each plot was periodically

clipped to maintain a height and density similar to grazed paddocks next to the

experimental site. The clippings remained on the plot. Experimental contamination

of the plots with faeces commenced in July 2000.

At the beginning of each month from July 2000 to June 2001, 2 plots were selected

and each uniformly contaminated with approximately 600 g of pooled, fresh faeces

82

obtained from 30 naturally infected donor sheep maintained on the ranch. On the

same day, samples from each of the donor animals were analysed for eggs per gram

of faeces using the modified McMaster technique as described in the MAFF (1986)

manual. A third plot remained as uncontaminated control to detect any extraneous

infections.

All plots were sampled weekly after the day of contamination, by collecting 60

uniformly distributed plucks of herbage per plot, taken at the ground level. Sampling

was continued until no larvae were recovered from the herbage for 4 consecutive

occasions. Infective larvae were recovered from the pasture samples and identified

to genus level as described in the MAFF (1986) manual. The herbage was placed in

gauze bags, hanged in the sun and weighed when completely dry. The larval

abundance was expressed as L, per Kg of herbage dry matter (L, Kg' 1 DM).

5.2.3 Studies on the availability of infective larvae on naturally contaminated

pastures

The study was carried out at the Maasai Rural Training Centre Ranch between May

1999 and December 2001. Monthly herbage samples were collected around the

paddocks where the sheep were grazing (Figure 5.1), around the night pens (Figure

5.2) and the watering point (Figure 5.3) using the W-transect procedure (Hansen and

Perry, 1994); the number of larvae (L,) per Kg of dry herbage was then determined.

83

Figure 5.1: Grazing paddocks (March 2000).

Figure 5.2: Night pen (March 2000).

Figure 5.3: Watering point (March 2000).

84


The number of eggs deposited on the plots was corrected to 1 million eggs per plot

and the number of larvae per kg dry herbage on each sampling occasion calculated

using the formula:

L, counts x 109LjKg 1 dry herbage = ----------------------------------------------------------------------

Herbage dry weight (g) x EPG x Faecal weight (g)

The number of larvae per kilogram of dry herbage were logarithmically transformed

[log (x + 10)] to normalise their distribution and analysis of variance (ANOVA)

performed using a Microsoft Excel Program (2001). Comparisons were made between

sampling points (paddock, night pen and watering point) and seasons (Wet and Dry).

A value of P < 0.05 was considered significant.

5.3 RESULTS

5.3.1 Climatic data

The relative humidity, mean maximum and minimum temperatures are shown in

Figure 5.4. The rainfall pattern during the study period is shown in Figure 5.5 and

the number of wet days recorded for each month in Figure 5.6. Generally, the

weather conditions during the study period were about average for the area. However,

the rainfall recorded during the months of January 2001, March 1999, 2001,

November 1999, 2001 was much higher and that of March 2000, April 1999, 2000,

October 2000, 2001 and December 2001 much lower than the long-term average.

Tem

p (c

el)

Tem

p (c

el )

Te

mp

(ce

l)

85

Months

IR Humidity - a - M in Temp -« -M a x Temp

Figure 5 4 Relative humiditv. mean minimum and maximum temperatures recorded at the Maasai Rural I raining C entre Meteorological Station between Januan IW ) and December 2<M>1

Rai

nfal

l (m

m)

86

Months

■■M onthly total rainfall (mm) 1999 E23 Monthly total rainfall (mm) 2000 VTZft Monthly total rainfall (mm) 2001

Long-term monthly mean rainfall (mm)


Centre Meteorological Station between January 1999 and December


Num

ber

of r

ainy

c^y

s87

Jan Feb Mar Apr May Jun Jul Aug Sep Oct

Months□ Number of rainy days 1999 ■ Number of rainy day: E3 Number of rainy days 2001

Figure 5.6: The number of rainy days per month recorded at tht

Training Centre Meteorological Station between Jan

December 2001

88

5.3.2 Plot studies

Figure 5.7 shows the mean number of larvae recovered per Kg of dry herbage after

correction for the number of eggs deposited on the plots sequentially contaminated

from November 2000 to June 2001. All the plots which were left uncontaminated

remained free of parasitic larvae throughout the experiment. Likewise, no infective

larvae were detected from herbage samples collected from all plots contaminated

between July 2000 and October 2000.

As from November 2000 to June 2001, larvae of Trichostrongylus, Haemonchus,

Cooperia and Oesophagoslomum developed and translocated into the pastures. During

this period, the infective larvae were consistently recovered from the herbage samples

taken one week after contamination. Peak numbers were recovered during the first

and the second week post-contamination. The larval counts declined to below

detectable levels after three weeks in November 2000 and between week five and

fifteen during the other months.

The pattern of egg hatching, development to L3 and larval survival on pasture was

almost similar for Trichostrongylus, Haemonchus, Cooperia and Oesophagostomum.

Peak numbers of L, occurred from the first to the third week post contamination.

Generally, there were proportionately more Trichostrongylus larvae recovered than

the other nematode genera present.

89

4.? 800 ,

iA/ee*s aosi-contaminanon

700C - A APR 2001j 5000 .

3. 4000 11 M » -

- 1000 i2 n -

’ 2 3 4 5 6 7 8 9 10 11

’ 2 3 4 5 6 7 8/vee«s oosi-contammatior

F igurc ' I he number ol larvae recovered per kg ol jr> herbage from plois seriallv contaminated w ith sheep faeces from November NMMi to June 2 0 0 I l T ru h u \ir itn % \ /u .\ H H oem unchus. C t m pefto

and *) ( h‘S)>phtignsiomum.

90

5.3.3 Availability of infective larvae from naturally contaminated pastures

The state of the pastures in the paddocks during the dry season, the short and the long

rains are shown in Figure 5.8. The trends of the herbage larval counts for the

paddocks, around the night pens and the watering point during the study period are

shown in Figure 5.9. The overall pattern indicated rising larval counts during the wet

seasons. The counts peaked just after the rains and then declined as the dry season

progressed. Infective L, were recovered from the watering point throughout the year,

but were undetectable around the paddocks and the night pens during the dry season

in July 1999 to October 1999, June 2000 to October 2000 and August 2001 to

October 2001. The overall counts were highest around the watering point and lowest

in the paddocks. The counts were significantly higher (p < 0.05) during the wet than

the dry seasons at all the sites during the study period.

91

Figure 5 8: The state o f the pastures in the paddocks during the dry season (A,September 2000), the short rains season (B, November 2000) and the long rains season (C, April 2001).

92

4) 4000 '

May 1999 • April 2000

May Jun Jui Aug Sep Ocl Nov Dec Jan Fee Mar Apr

May 2000 April 2001

4000

May 2001 Decernoer 2001

Figure 5 9 The lumper of larvae L; Kg recovered from pasture samples collected from the paaoocKs around the mgnt pen ana the ca te rin g point Detween May and Decemper 2001

93

5 4 DISCUSSION

The meteorological data during the study period indicates that little variation in

temperature occurred in the study area. The temperatures were permanently

favourable for larval development in the environment (mean minimum 12nC to 14°C

and mean maximum 24°C to 26°C). However, variations in the total monthly rainfall

(range 0 mm to 284 mm) did occur over the study period and was the major factor

governing the development, survival and availability of the pre-parasitic stages. This

was in agreement with the findings of other workers in the tropics (Dinnik and

Dinnik, 1961; Altaif and Yakoob,1987; Banks et al., 1990; Tembely, 1998; Waruiru,

1998).

Extreme climatic conditions of either very high or very low temperatures or intense

drought can virtually sterilize a pasture in some environments through rapid

desiccation and deaths of eggs and larvae (Chiejina et al., 1989; Barger, 1999). In

plot studies, no parasitic larvae were detected in the herbage during the months of

July to October 2000. This could be attributed to the fact that there was little or no

rain during this period and the faecal pellets rapidly dried out. There were usually

lower yields of parasitic larvae during periods of scarce, erratic and non-soaking rains

(February, May and June).

It is evident from this study that more eggs completed their development and there

was mass translocation of larvae into pastures after contaminations during the rainy

season (November to January, March and April). However, heavy rains may wash

larvae off the herbage and even down into the soil (Hansen and Perry, 1994). This

94

was possibly the case in the months of January and March 2001 when the rains were

higher than normal for the area and the larval counts lower than expected.

The survival of larvae in the environment depends upon adequate moisture and shade

(Hansen and Perry, 1994). But generally, cool, dry weather prolongs larval survival

and hot wet weather shortens it. This is attributable to the fact that infective larvae

do not feed and must survive on stored energy. Low temperatures and dry conditions

prevent active movement by larvae thus minimising energy expenditure (Barger,

1999). In the present study, the shortest larval survival time (3 weeks) occurred after

the November 2000 contamination. At this time the herbage cover was low and the

w'eather hot and wet. Such an environment leads to increased larval movements and

higher energy utilisation and thus progressively reduce their longevity (Rose, 1963).

The longest survival time (15 weeks) occurred after the May 2001 contamination. At

this time the herbage cover was dense, the environment dry and cool due to the heavy

cloud cover that persisted to July 2001. Dense herbage canopy is known to reduce the

detrimental impact of the climate as it experiences diminished temperature fluctuations

and evaporation (Brady and Weil, 1996). This and the low larval activity caused by

the dry condition may have increased duration of larval survival in the herbage.

Similar observations have been made by others in the tropics (Dinnik and Dinnik,

1961; Banks et al., 1990; Waruiru, 1998).

Embryonated eggs and third stage larvae of Trichostrongylus colubriformis have been

found to be more resistant to desiccation than Haemonchus contortus and some degree

of water deprivation may enhance its survival (Andersen and Levine, 1968). In the

95

present study, larvae of Trichostrongylus were always recovered in larger numbers

than those of other nematode species present. This was especially evident after

contaminations during the drier months of February, May and June 2001 when the

rainfall was less than 12 mm. Banks et al., (1990) made similar observations in the

drier parts of Fiji where the recovery of Trichostrongylus colubriformis was higher

than that of Haemonchus contortus during the dry season.

The relative ability of infective larvae to survive on pasture at different times of the

year is relevant to successful formulation of a control programme. This determines

how long a pasture remains dangerous following high levels of larval contamination

(Barger, 1999). In the temperate regions, the practicality of rotational grazing as a

means o f controlling internal parasites in small ruminants has been doubted (Chiejina

et al., 1989; Banks et al., 1990; Barger, 1999). This is because the time of 3 to 9

months needed to ensure significant reduction in larval numbers is too long for

economic management of pastures. In the present study area, there was either no

development of parasitic larvae or their population declined very rapidly and

rotational grazing is practicable. Similar observations have been made in other

tropical areas (Chiejina et al., 1989; Banks et al., 1990; Waruiru, 1998).

Results from the study on the availability of infective larvae from naturally

contaminated pastures indicate that the number of infective L3 also followed closely

the patterns of rainfall distribution and egg output of the animals. This was in

agreement with the observations made by other workers in the tropics (Ikeme et al.,

1987; Onyali et al., 1990; Maingi, 1996; Nginyi et al., 2001). At the onset of the

96

rains, the levels of pasture contamination was relatively low. As the rainy seasons

progressed the environment became conducive for the development of infective larvae

and the cumulative effect on pasture contamination and host infections increased. The

higher larval counts just after the rainy season may therefore have resulted from these

cumulative contaminative effects and also from the fact that the wash down of the

larvae into the soil by the rain drops was eliminated. As the dry season progressed,

most of the larvae died from desiccation and their numbers eventually declined to

undetectable levels in the paddocks and around the night pens. There was adequate

moisture for the development and survival of infective larvae around the watering

point throughout the year. However, during the dry seasons, the herbage cover at this

point was very low as a result of overgrazing. The low herbage cover then exposed

the larvae to desiccation resulting in deaths or they possibly burrowed deeper into the

soil. These results therefore indicate that the watering point may be an important

source of infection most of the year and more so during the dry seasons when other

pastures are clean.

Observations made from this study therefore suggest that grazing animals are exposed

to high levels of infection during the rainy season. It was also observed that peak

larval counts occurred just after the rains. Infections resulting from this peak and

from the dry season larval residue may have detrimental effects on the host more so

due to the poor nutritional status of the animals during the dry seasons. It is therefore

important that control measures in the study area be aimed at reducing the levels of

infection during both the dry and the wet seasons.

97

CHAPTER 6

6 0 SEASONAL PREVALENCE, SPECTRUM AND INTENSITY OF

GASTROINTESTINAL NEMATODE INFECTIONS IN DORPER

SIIEEP: A POST-MORTEM STUDY

6.1 INTRODUCTION

Gastrointestinal nematode parasitism is a major animal health problem facing the

sheep and goat industry in Kenya (Carles, 1993). Infections with gastrointestinal

nematodes usually involve several different genera and species which may have

additive pathogenic effects on the host. It is also known that the size of any

gastrointestinal nematode infection in grazing animals depends on several interacting

factors, including the number of infective larvae ingested, host immunity, livestock

production systems and control methods used (Hansen and Perry, 1994; Barger,

1999).

The problems pertaining to the use of egg output as a reliable indicator of the

intensity of infections in humans and animals have been highlighted. The number of

eggs per gram (EPG) of faeces may be influenced by a number of factors including

the consistency of the faeces, the amount of faeces passed per day, the worm burden,

age of worms and the technique used in determining the EPG. The egg output has

therefore been described as a qualitative rather than a quantitative measure of worm

burdens (Anderson and Schad, 1985). Inspite of these constraints, high correlations

between faecal egg output and the worm burden in farm animals have been recorded

98

(McKenna, 1981, 1987; Roberts and Swan, 1982; Bryan and Kerr, 1989; Bisset et

al., 1996). However, positive correlation between faecal egg counts and worm

burdens may not be universal owing to the difference in genera of nematodes

occurring in different regions. In Kenya, reports on these relationships are variable.

Allonby and Urquhart (1975) indicated that faecal egg counts were not a reliable

index of assessing the burdens of Haemonchus contortus infection in ewes and lambs

at Naivasha. However, Gatongi (1995) demonstrated that faecal egg counts were a

good indicator of worm burdens in sheep and goats in the same area during the wet

season. Maingi (1996) reported a positive correlation between faecal egg counts and

worm burdens in male and female sheep in Nyandarua District during both the wet

and the dry season. No study has been carried out to establish the seasonal changes,

the prevalence and spectrum of gastrointestinal helminths and to assess the

relationship between the worm burdens and faecal egg output in Dorper sheep in the

seini-arid area of Kajiado District.

The objectives of the present study were therefore:

1. To determine the seasonal prevalence, spectrum and intensity of

gastrointestinal nematode infections in Dorper sheep in Isinya Division of

Kajiado District at slaughter.

2 . To assess the relationship between worm burdens and faecal egg counts for

Dorper sheep in Isinya Division of Kajiado District during the wet and the dry

seasons.

99


6.2.1 Climatic data

Rainfall data recorded at the Maasai Rural Training Centre Meteorological Station

was obtained from the Meteorological Department Headquarters in Nairobi.

6.2.2 Experimental animals

A total of 24 female Dorper sheep, aged between nine and twelve months,

permanently on pastures at the Maasai Rural Training Centre Ranch were randomly

selected and slaughtered for total and differential worm counts during the dry and the

wet seasons. The animals were allowed at least four months from the last treatment

before they were slaughtered. During each season, twelve animals were slaughtered

in three batches of four animals each. Slaughter was done towards the end of the dry

season (September 2000), after the short rains (February 2001) and after the long

rains (July 2001). Also the animals were slaughtered at the beginning of the short

rains (October 2000), in mid-short rains (December 2000) and during the long rains

(April 2001). For each of the animals, rectal faecal samples were taken at slaughter

and the strongyle egg counts estimated by the modified McMaster technique.

6.2.3 W orm recovery and identification

The worms from the gastrointestinal tract were recovered as described in the MAFF

(1986) manual and by Hansen and Perry (1994). The abomasum, the small intestines,

caecum and the colon were double ligated at their extreme ends and separated

immediately after slaughter. The abomasum was then opened through the greater

curvature and the contents released into a bucket. The mucosa was thoroughly washed

under running tap water and the washings collected in the same bucket. The bucket

100

contents were further cleaned through a fine mesh sieve (0.063 mm), put into labeled

containers and preserved in 10 % alcohol until recover)’ of worms was undertaken.

The mucosa of the abomasum was scraped off, digested in hydrochloric acid-pepsin

mixture as described in the MAFF (1986) manual. The material was examined for the

presence of larvae as soon as the digestion was complete. At the time of examination,

the abomasal contents were put in a calibrated bucket and water added to make 2

litres. After thorough stirring, a sub-sample of 200 ml was drawn, in which all

worms present were recovered under a dissecting microscope and preserved in 10%

alcohol. The worms were then counted, differentiated to species level and

developmental stages based on the morphological characteristics described in the

MAFF (1986) manual.

I he small intestines were slit longitudinally, the contents collected and processed as

described for the abomasum excluding the mucosal digestion. The large intestinal

contents were washed into a bucket then passed through a course meshed sieve (500

mm), all worms present recovered, counted and identified as described in the MAFF

(1986) manual.


Worm burdens for the strongyle nematodes and strongyle egg counts recorded from

gastrointestinal tracts from the slaughtered animals were log transformed and their

relationship examined by regression analysis. A value of P < 0.05 was considered

significant. The term prevalence was defined as the percentage of animals found

positive for nematodes (Margolis et al., 1982).

101

6 3 RESULTS

6.3.1 Kainfall distribution

The monthly total rainfall (mm) and the long-term mean monthly rainfall (mm)

recorded in the study area between September 2000 and July 2001 are shown in

Figure 6.1. The amount of rainfall recorded during the study period showed marked

changes from the long-term pattern. The highest amount of total monthly rainfall

recorded during this period (282.4 mm) occurred in January which is normally a dry

month. I'he amount recorded in March (245.8 mm) was also higher than the long

term monthly mean (85.2 mm).

6.3.2 Worm counts and identification

The mean prevalence and intensity of infection with gastrointestinal nematodes in the

24 sheep slaughtered during the dry and the wet seasons are shown in Table 6.1. All

the sheep examined were infected by more than one species of nematodes so that 91.7

% were infected with Tricliostrongylus, Haemonchus conlortus and Oesophagostomum

and 83.3 % with Cooperia. Trichosirongylus species (60.8 %) and Haemonchus

conlonus (27.3 %) were the most abundant nematode species encountered.

Rai

nfal

l (m

m)

102

300 n

Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul

Months

■ Long-term monthly mean rainfall (mm)□ Monthly total rainfall (mm) September to July 2001


Centre Ranch Meteorological Station between September 2000 and July


103

Table 6.1: The mean worm burdens and percentage prevalence of 24 Dorper

sheep slaughtered during the dry and the wet seasons at Isinya in

Kajiado District during the period September 2000 to July 2001.

Organ Genera Seasons

Dry Wet

Mean % Mean %

Abomasum Ilaemonclms 1239 29.4 1202 27.7

T. axei 884 21 471 10.8

Intestines Trichostrongylus 1639 38.9 2045 47.1

Cooperia 378 9 549 12.6

Oesophagostomum 75 1.8 74 1.7

Trichuris 1 0.02 0 0

Strongyloides 0 0 1 0.02

Total 4216 100 4342 100

The trends of the group mean total worm counts during the study period are shown

in Figure 6.2. The lowest group mean worm counts were recorded at the onset of the

short rains (October 2000) and the highest level during the long rains (April 2001).

The proportion of Haemonchus contortus increased from the lowest levels of 10.3%

104

of the total worm burden in September 2000 to reach the highest level of 35.6% in

July 2001. There was no significant difference between the wet (mean 4766) and the

dry (mean 4216) seasons worm counts.

The mean counts and the proportions of adults to the immature for Haemonchus and

the intestinal Trichostrongylus species during the dry and the wet seasons are shown

in Figure 6.3. The adult worm counts were significantly higher during the wet than

the dry season for both genera. The counts for the immature Haemonchus were

significantly higher during the dry than the wet season, while those of

Trichostrongylus were higher during the wet season. The population of adult

Haemonchus contortus constituted 61.9% of the total count for the species during the

wet season and was significantly higher than in the dry season (24.4%). There was

no significant change in the proportions of adult Trichostrongylus species during the

wet (93.2%) and the dry (94%) season.

6.3.3 The correlation between worm counts and faecal egg counts

The plots of the log strongyle egg counts and the worm burdens recorded for the 12

gastrointestinal tracts examined during the dry season and those for the wet season

are shown in Figure 6.4. Data from these sampling occasions indicated positive linear

correlation with r values of 0.97 and 0.75 for the dry and wet seasons respectively.

Me

an

wor

m c

oun

ts

105

8000

^000 -■

6000 -■

5000

Sep Oct Dec Feb Apr JulMonths

□ Total counts S Coopena

□ Tnchostrongylus □ Haemonchus

□ Oesophagostomum

Figure 6.2: The mean worm counts and the proportions of different genera of

nematode parasites encountered in 24 Dorper sheep slaughtered serially

between September 2000 and July 2001.

Me

an

wor

m c

oun

ts

106

Seasons

■ Adult Trichostrongylus □ Immature Trichostrongylus

□ Adult Haemonchus □ Immature Haemonchus

Figure 6.3: The proportions of adult and immature Haemonchus and

Trichostrongylus species during the wet and the dry season in 24

Dorper sheep slaughtered serially between September 2000 and July

2001.

Log

stro

ngyl

e eg

g co

unts

Lo

g st

rong

yle

egg

coun

ts107

Figure 6.4: The correlation between the faecal egg output and the worm burden in

24 Dorper sheep slaughtered during the wet and the dry seasons

between September 2000 and July 2001.

108

6 4 DISCUSSION

This study clearly shows that gastrointestinal nematode infections are prevalent in

sheep within the study area. These findings are in agreement with those of Ndarathi,

Waghela and Semenye (1989) and Gatongi (1995) in an environment similar to that

of Kajiado District and with those of Maingi (1996) in a high rainfall area of

Nyandarua District. This study also showed that mixed nematode infections in sheep

occurred within the study area with Trichostrongylus and Haemonchus contoitus being

the most prevalent and important species. It also confirms observations from faecal

cultures (Chapter 3) where Trichostrongylus species were the most abundant. Similar

observations were made by Nginyi et al., (2001) in Central Kenya where

Trichostrongylus was recovered in higher proportions than Haemonchus contortus in

locally grazed sheep and in New Zealand where the genus is generally the most

widespread and abundant nematode in lambs (Vlassoff and McKenna, 1994). These

observations indicate that Trichostrongylus species might play a more important role

in the occurrence of parasitic gastroenteritis of sheep in the study area than was

previously thought.

The results of this study also indicated that the rainfall pattern influenced the

prevalence and intensity of infection with gastrointestinal nematodes as the lowest

levels were recorded in sheep slaughtered at the onset of the short rains (October) and

the highest during the long rains (April). This finding agrees with those of other

workers in the tropics (Ogunsusi and Eysker, 1979; Pandey, Ndao and Kumar, 1994;

Gatongi, 1995; Maingi, 1996). The levels of infection in the present study increased

during the short rains and soon after to reach a peak during the long rains then

109

declined as the dry season advanced. Similar observations have been made in a study

involving sheep and goats in the Nigerian derived savanna (Fakae, 1990), in

communally grazed goats in Zimbabwe (Pandey et al., 1994) and in sheep on

smallholder farms in Central Kenya (Nginyi et al., 2001) where the total worm

burden was lowest at the end of the dry season and increased to peak at the end of

the rains. During the present study there was a relatively high amount of rainfall from

the end of October 2000 to January 2001 during the short rains and in March to April

2001 during the long rains. The rainy season provides a conducive environment for

the development of free-living stages and increased pasture infectivity. The high

amount of rainfall that occurred in January 2001 may have contributed to the higher

infections observed in February and to the lack of statistical difference between the

dry and the wet seasons worm counts. The results of this study therefore indicate that

control measures in this area should aim at reducing the nematode burdens during

both the dry and the wet seasons.

In the present study, the proportion of //. contort us worms increased from the low

levels o f 10.3% in September 2000 to 35.6% in July 2001. This may be attributed

to the relatively short generation interval and high fecundity that enables the parasite

to take rapid advantage of the favourable climatic conditions during the rainy seasons

(Grant, 1981). In the face of repeated reinfection, this parasite has a rapid population

turnover and a short life-span (Courtney, Parker, McCLure and Herd, 1983) whereas

during the dry season and in the absence of reinfection the population declines rapidly

due to mortalities of the ageing adult worms (Fakae, 1990). This may therefore

account for the low levels of the adult population of H contortus towards the end of

the dry season in September 2000.

110

The observations made in this study indicated that the adult and immature worm

populations co-existed in proportions that varied with seasons. This is in agreement

with the findings of other workers in the tropics (Ogunsusi, 1979b; Jacquiet el a l.,

1995; Gatongi, 1995). The high population of immature Haemonchus observed during

the dry season in the present study confirmed the occurrence of hypobiosis in the

study area. Hypobiosis is an adaptive characteristic of nematode species that facilitates

their survival during harsh environmental conditions and enables subsequent

transmission when the conditions become conducive. In the tropics, the levels of

hypobiosis vary with the rainfall distribution and mostly occurs during the dry season.

Resumption of development occurs towards the end of the dry season or at the onset

o f the rains (Ogunsusi, 1979b; Jacquiet et al., 1995; Gatongi, 1995). In the present

study, the highest proportion of the immature to the adult Haemonchus was recorded

in September (81.9%) and the lowest in October (11.9%). This change in proportions

was as a result of a sudden increase in the adult worm population in October. The

increase could not be attributed to new infections as the rains had just started, the

pasture infectivity at this time was low (Chapter 5) and the adult worm population of

the other species was decreasing. Thus, this change could only be attributed to the

resumption of the development of hypobiotic larvae in anticipation o f the coming

short rains.

The resumption of development of hypobiotic larvae is normally associated with

increased faecal egg output and may be accompanied by outbreaks of clinical

haemonchosis (Gatongi, 1995). The sudden increase in the adult worm population in

the present study can therefore be associated with the rise in egg output observed in

I l l

sheep within the study area at around this period (Chapter 3 and 4). Similar findings

were reported in goats in the marginal low potential areas of Thika where faecal egg

output increased just before the short rains (Githigia, 2000) and in sheep and goats

in a semi-arid area in Naivasha at the onset of the long rains (Gatongi, 1995). Control

measures in the study area should therefore aim at reducing the effects of this

phenomenon through the administration of drugs that can eliminate the hypobiotic

larvae such as ivermectin and benzimidazoles.

In the present study, relatively high numbers of adult Trichostrongylus were recovered

during both the wet and the dry seasons without a significant change in their

proportions. Apparently the turnover rate of the adult Trichostrongylus spp. was much

lower than that of adult //. contortus. Similar observations were made in Northern

Nigeria where high proportions of adult Trichostrongylus species were recovered in

sheep during the long dry season (Ogunsusi, 1979b). The results obtained here

therefore confirm that these parasites are capable of surviving unfavourable

environmental conditions as an adult population in the hosts. Since trichostrongylosis

achieves it’s greatest impact in sheep when the nutrition is poor (Blood el al., 1997)

helminth control measures in the study area should aim at reducing this effect through

treatments and or improved nutrition during the dry season.

The pathogenic effects of these nematode parasites may be clinical or sub-clinical

depending on the worm burdens and the nutritional status of the host. The mean total

worm counts in this study may be regarded as moderate (McKenna, 1987; Hansen

and Perry, 1994). Such infections are normally sub-clinical and are a potential

112

problem in the productivity of sheep in this area. This problem is further aggravated

by the frequent droughts in the semi-arid areas and may be a major constraint to

sheep production in this region. It is therefore necessary to establish cost-efficient and

sustainable control programmes for this region.

The results of the study on the relationship between worm burdens and faecal egg

counts in sheep in the study area revealed positive correlation during both the dry (r

= 0.97) and the wet (r = 0.75) seasons. This was in agreement with the observations

of Maingi (1996) who reported similar correlation in the high rainfall area of

Nyandarua District, but were at variance with those of Allonby and Urquhart (1975)

who indicated that the faecal egg counts were not a reliable index of assessing the

burdens of H. coniortus infections in ewes and lambs in a semi-arid area of Naivasha.

The observations made during the present study indicate that faecal egg output can

be used as an indicator of the levels of infection with gastrointestinal nematode

parasites during the wet and the dry seasons in the study area. However, due to the

small number of animals used in the study, this observation may not be conclusive,

but only provides a guideline while awaiting further experiments.

113

C H A P T E R 7

7.0 E V A L U A T IO N O F T H E S T R A T E G IC U SE O F A N T H E L M IN T IC S IN

T H E C O N T R O L O F G A S T R O IN T E S T IN A L N E M A T O D E IN F E C T IO N S

IN S H E E P .

7 .1 IN T R O D U C T IO N


production worldwide. The helminth infections have primarily been controlled by

extensive use of anthelmintics and grazing management. However, in developing

countries, there are poor or ineffective set plans of prophylactic control of

gastrointestinal helminths. In Kenya, the use o f anthelmintics has mainly been

confined to large commercial farms and small scale dairy enterprises (Kinoti, Maingi

and Coles, 1994). In other enterprises the use of anthelmintics is mainly irregular and

haphazard (Mbaria et al., 1995) and treatments are carried out when animals show

signs of helminthosis. Considerable production losses are thus incurred by the time

the clinical signs are manifested and additionally, reinfections are common.

Effective control strategies for helminths using anthelmintics are usually those based

on the epidemiology of the parasites and where treatments are designed to reduce

pasture contamination and host infections (Brunsdon, 1980; Nansen, 1991). As

observed in my study reported in Chapter 4 of this thesis a special strategic treatment

is required for breeding ewes to counter the effects of the peri-parturient rise in

nematode egg output caused by the relaxation of immunity at around the time of

lambing and lactation.

114

The objective of this study was therefore to evaluate the effectiveness of the strategic

use of anthelmintics in controlling naturally acquired gastrointestinal nematodes of

Dorper breeding ewes based on the reproductive cycle and in lambs and yearlings

based on the seasonal changes of infection.

7.2 M A T E R IA L S A ND M E T H O D S

7.2.1 Climatic data

Rainfall data recorded at the Maasai Rural Training Centre meteorological station was

obtained from the Meteorological Department Headquarters in Nairobi.

7.2.2 Experimental animals

The study was carried out on Dorper sheep raised at the Maasai Rural Training

Centre Ranch in Isinya Division of Kajiado District between May 1999 and December

2001. Three age groups of sheep, the adult breeding ewes (2-4 years), the lambs

(under 1 year) and the yearlings (1-2 years) were used. The animals grazed on natural

un improved pastures and received mineral supplementation in form of MaclickR

blocks (Coopers Kenya Ltd, Nairobi) in the morning and evening. The ewes and the

un-weaned lambs grazed in one group and the weaned Iambs and yearlings in another,

but both groups of sheep grazed in the same paddocks under different shepherds. All

the animals had been treated by the fanner in early May 1999. From then on, the

animals were treated with albendazole (VaIbazenR, Novartis East Africa Ltd, Nairobi)

at a dose rate of 5 mg Kg 1 body weight as per the experimental design. All the

animals in the control groups remained un treated except for salvage treatments given

to animals showing clinical signs of helminthosis and those with over 7000 eggs per

115

gram of faeces. Data from all salvaged cases was excluded from analysis. For each

of the animals, faecal egg counts and weight gains were monitored every 3 weeks

from May 1999 to the end of the experiment in December 2001.

7 .2 .2 .1 Breeding ewes

The study was conducted through three breeding seasons between May 1999 and

December 2001. In each of the breeding seasons, a total of forty ear tagged Dorper

ewes aged 2 - 4 years were randomly selected from the breeding stock. The animals

were allocated to 2 groups A and B of 20 animals each. All the animals in group A

were treated 2 weeks pre-mating (May 1999, June 2000 and April 2001) to reduce

the worm load during gestation. To reduce the worm burden and the effects of the

peri-parturient rise in faecal trichostrongylid egg output the ewes were treated 1 to

3 weeks from the expected time of lambing (October 1999, November 2000 and

September 2001) and in mid-lactation (January 2000, 2001 and December 2001).

Group B ewes remained as the un-treated controls. Birth weights were recorded as

they occurred. The lambs were weighed again at the age of 6 weeks to determine the

weight gains.

7 .2 .2 .2 Lambs

The study was conducted over a 2 year period starting from January 2000 to

December 2001. Each year, a total of 40 ear tagged female Dorper lambs were

randomly recruited at the age of 3 months (January 2000 and February 2001). They

were divided into 2 groups, A and B of 20 animals each. To reduce pasture

contamination and the detrimental effect of helminthosis all lambs in group A were

116

treated at the age of 3 months, at around the time of weaning (April 2000 and 2001),

in mid dry season (July 2000 and 2001) and 3 weeks into the short rains (November

2000 and 2001). Lambs in group B remained as the un treated controls.

7.2.2.3 Yearlings

The study was conducted over a 2 year period starting from May 1999 to March

2001. Each year, a total of 40 ear tagged female Dorper yearlings (1-2 years) were

randomly selected from the flock in May 1999 and April 2000. The animals were

allocated to 2 groups (A and B) each with 20 animals. AH animals in group A were

treated 3 weeks into the long rains, in mid-dry season (July 1999), 3 weeks into the

short rains (November 1999) and after the short rains in January, 2000. Animals in

group B remained as the un-treated controls.


I he number of eggs per gram (EPG) of faeces were logarithmically transformed [log

(x + 10)] to normalise their distribution. Analysis of variance (ANOVA) was

performed using a Microsoft Excel Program (2001) to compare the faecal egg output

and the weight gains between the treated and the un-treated groups where a value of

P < 0.05 was considered significant.

117

7.3 RESULTS

7.3.1 Rainfall distribution

The rainfall distribution pattern observed in the study area during the period January

1999 to December 2001 is shown in Figure 7.1. Generally, the distribution was

bimodal and similar to the long-term pattern with variations in the monthly and annual

totals. The long rains fell between March and May and the short rains between

October and December except in 2000 when they extended to January 2001. The total

rainfall received in the year 1999 (474.5 mm) and 2000 (224.3 mm) were lower than

the long-term annual mean (600.7 mm) but that of 2001 (923.8 mm) was higher.

7.3.2 Faecal egg counts and weight gains in ewes

The arithmetic mean strongyle faecal egg counts for the treated and the un treated

groups of ewes during the study period are shown in Figure 7.2 (May 1999 to April

2000) , Figure 7.3 (June 2000 to April 2001) and Figure 7.4 (April 2001 to December

2001) . Overall, the treated ewes had significantly lower egg counts than the un-treated

controls throughout the study period. Peak egg counts were observed during the

lactation period in all the years (October 1999 to March 2000, November 2000 to

March 2000 and September 2001 to December 2001). The trends in the cumulative

weight gains for the ewes during the study period are shown in Figure 7.5 (June 1999

to April 2000), Figure 7.6 (July 2000 to April 2001) and Figure 7.7 (April 2001 to

December 2001). The weight gains for the treated and control groups increased

during gestation period except for the year 2000 in which decrease in body weights

was observed. Drastic decrease in the weights were observed at around the time of

lambing followed by an increase during lactation. The treated ewes had significantly

higher (p < 0.05) weight gains or lower weight losses than the un-treated controls.

Rai

nfal

l (m

m)

118

Months

■■M onth ly total rainfall (mm) 1999 EH3 Monthly total rainfall (mm) 2000

Monthly total rainfall (mm) 2001 -x-Long-term monthly mean rainfall (mm)


Centre Ranch Meteorological Station between January 1999 and

December 2001 and the long-term mean monthly rainfall (1969 -

1998).

Mea

n g

roup

epg

cou

nts

119

Trt


Dorper breeding ewes given strategic albendazole treatments and the

un-treated control group during the period May 1999 to April 2000.

Mea

n gr

oup

epg

coun

ts

120



un-treated control group during the period June 2000 to April 2001.

•WmoBi UNivFn^rrr ^•ETe library

Mea

n gr

oup

epg

coun

ts

121



un-treated control group during the period April 2001 to December

2001.

C u

rn m

illa

tive

wei

ght

gain

s

122

«g

Months

Figure 7.5: The cumulative weight gains for Dorper breeding ewes given strategic

albendazole treatments and the un-treated control group during the

period June 1999 to April 2000.

Cum

mul

ativ

e w

eigh

t gai

ns123

*9



period July 2000 to April 2001.

Cum

mul

ativ

e w

eigh

t ga

ins

124



period May 2001 to December 2001.

125

7.3.3 Birth weights and weight gains in lambs at 6 weeks

The mean (±SD) birth weights and mean (±SD ) weight gains for the 6 week old

lambs during the study period are shown in Figure 7.8. The mean birth weights for

lambs from the treated ewes were higher than those from the un treated ewes but not

significantly different (p > 0.05). The weight gains at 6 weeks were significantly

higher for the lambs from the treated ewes than those from the un treated ewes.

7.3.4 Faecal egg counts and weight gains in lambs

The arithmetic mean strongyle faecal egg counts for the treated and the un treated

lambs during the study period are showrn in Figure 7.9 (January 2000 to December

2000) and Figure 7.10 (February 2001 to December 2001) and that of the cumulative

weight gains in Figures 7.11 (January 2000 to December 2000) and Figure 7.12

(March 2001 to December 2001). The egg counts for the treated groups were

significantly lower (p < 0.05) than those of the un-treated controls. The cumulative

weight gains were significantly higher (P < 0.05) for the treated than the un treated

controls. Generally, the trends in the cumulative weight gains increased from the start

at the age of 3 months in January 2000 and February, 2001 to peak in June and July,

then leveled off or dropped to low levels in November and increased again in

December.

126

14

YEAR1

12

10

a) 8c

4

2

0

YEAR 2 YEAR 3

□ Birtn *eignts ■ Weignts at 5 *ee«s □ Weignt gams at 8 *ee*s

Figure 7.8: The mean birth weights, weight at 6 weeks and the weight gains for

groups of lambs bom of treated and un-treated Dorper ewes during the

period October 1999 to November 2001.

Mea

n gr

oup

epg

coun

ts

127


Dorper lambs given strategic albendazole treatments and the un-treated

control group during the period January 2000 to December 2000.

Mea

n gr

oup

epg

coun

ts128


Dorper Iambs given strategic albendazole treatments and the un treated

control group during the period February 2001 to December 2001.

Cum

mul

ativ

e w

eigh

t gam

s

129

<9



period February 2000 to December 2000.

Cum

mul

ativ

e w

eigh

t ga

ins

130



period March 2001 to December 2001.

131

7.3.5 Faecal egg counts and weight gains in yearlings

The arithmetic mean strongyle faecal egg counts for the treated and the un-treated

yearlings during the study period are shown in Figure 7.13 (May 1999 to April 2000)

and Figure 7.14 (April 2000 to March 2001) and that of the cumulative weight gains

in Figures 7.15 (June 1999 to April 2000) and 7.16 (May 2000 to March 2001). The

egg counts for the treated groups were significantly lower (p < 0.05) than those of

the un treated controls. The cumulative weight gains were significantly higher (p <

0.05) for the treated than the un treated controls. Generally, the trends in the

cumulative weight gains decreased from the start o f the experiment in May 1999 and

April 2000 to reach the lowest levels in November and increased again in December.

Mea

n gr

oup

epg

cou

nts

132


Dorper yearlings given strategic albendazole treatments and the un

treated control group during the period May 1999 to April 2000.

Mea

n g

roup

epg

cou

nts

133


Dorper yearlings given strategic albendazole treatments and the un

treated control group during the period April 2000 to March 2001.

Cum

mul

ativ

e w

eigh

t gai

ns

134

*9

Figure 7.15: The cumulative weight gains for Dorper yearlings given strategic


period June 1999 to April 2000.

Cum

mul

ativ

e w

eigh

t ga

ins

135

Figure 7.16: The cumulative weight gains for Dorper yearlings given strategic


period May 2000 to March 2001.

136

7.4 DISCUSSION

Gastrointestinal nematode parasites impose severe economic constraints on sheep

production worldwide. However, the eradication of such infections is not practical,

is undesirable and control measures generally aim at the suppression of parasite

burdens in the host at levels above which economic losses may occur (Brunsdon,

1980). Where permanent pastures are utilized, most farmers rely solely on

anthelmintic treatments in their flocks (Soulsby, 1982). The effects of such

anthelmintic treatments are manifested directly as improved reproductive

performance, enhanced growth rates and increased productivity in the flock or

indirectly by alteration of pasture infectivity (Darvil, Arundel and Brown, 1978). The

strategic treatments of sheep in the present study resulted in decreased faecal egg

output and thus pasture infectivity, improved weight gains, decreased weight losses.

Treatments of breeding ewes 2 weeks before mating is an important part of the

"flushing" programme and is one of the strategic uses of anthelmintics (Fraser et al.,

1986). This treatment improves on ewe fertility, weight gains during gestation and

on the birth weights of lambs. Birth weights on the other hand influence the survival

rates of lambs in their early lives, are positively correlated with the post-natal weight

gains and with the subsequent achievement of commercially desirable slaughter

weights or maturity (Carles, 1983; Fraser et a l., 1986; Gatongi 1995). The pre

mating treatment of ewes in the present study resulted in reduction of worm burdens,

higher weight gains when pastures were available, lower weight losses in times of

feed scarcities and higher birth weights for lambs.

137

The pre-lambing treatments are of epidemiological significance in that they reduce the

worm population before parturition and subsequently the post-parturient rise in egg

output. In the present study, the pre-lambing treatment reduced the faecal egg output

in early lactation and increased the rate of post-partum weight gains. However, peri-

parturient ewes are highly susceptible to re-infections as a result of the relaxation in

acquired immunity (Gibbs and Barger, 1986). Therefore suckling ewes may require

another treatment 4-8 weeks post-lambing and the animals moved to clean pastures.

Where clean pastures are not available the treatment may be given monthly until

weaning (Carles, 1983). Better control is achieved by a combination of the

anthelmintic treatments and early weaning preferably at 12 weeks post-lambing.

Where fat Iambs are being produced and weaning at 4-5 months is desirable, then

treatments of ewes and lambs at 10-12 weeks post-lambing combined with movement

to clean pastures may be practiced (Carles, 1983; Blood et al., 1997). Such a

programme does not only give optimal economic control but also aids in preventing

the development of anthelmintic resistance due to frequent drench usage. The

treatment in mid-lactation in the present study produced this desired effect by

reducing the worm burdens acquired in early lactation and possibly improved the

performance of the ewes in the subsequent lactation period without unduly increasing

the risk of anthelmintic resistance.

The increased nematode parasite burdens, particularly Haemonchus contortus in the

peri-parturient ewes may not only cause clinical or subclinical disease, but also causes

a decrease in milk production with negative effects on the growth of lambs (Connan,

1976; Darvil et al., 1978; Thomas and Ali, 1983). In the present study, it was

138

observed that lambs from the treated ewes had higher birth weights and weight gains

at 6 weeks than those from un treated ewes. This observation could be attributed to

improved feed utilization by the treated ewes resulting in increased availability of

nutrients for foetal growth during gestation and increased milk production during

lactation. This in turn led to higher birth weights and improved growth rate in the

Iambs.

Lambs do not suffer from gastrointestinal nematode infections before the age of 10-12

weeks as long as the ewes have adequate milk (Carles, 1983; Blood et al., 1997). In

the present study, the lambs had very low faecal egg counts at the age of 9 weeks

(Chapter 4) and thus received their first treatment at around the age o f 3 months (12

weeks). This treatment gave effective protection against the effects o f gastrointestinal

nematodes at a time when the lambs were most vulnerable. The egg output from the

lambs remained relatively low till weaning and they had improved weight gains.

Weaning seriously compromises growth rates in lambs largely as a result of cessation

of milk intake and lowered feed intake as the lambs spend more time calling and

searching for their dams (Watson and Gill, 1991). In addition the stress imposed by

weaning results in immunosuppression and consequently lead to increased

susceptibility to infections and faecal egg output (Parillo and Fauci, 1979; Watson and

Gill, 1991). Though the higher egg output may be short lived, the negative impact on

the health o f the weaned lambs may persist for long. The effects of the weaning stress

in the present study were more evident in the year 2000 where both the treated and

control lambs lost weight, but the loss was higher in the control group. The higher

139

weight loss observed here might also have been caused by the low levels of nutrition

at around the time of weaning since the long rains were inadequate that year.

Generally, the treated groups of lambs had higher weight gains and or lower weight

losses than the control groups during the study period.

The use of anthelmintics in the control of gastrointestinal helminths in weaned lambs

and the yearlings should be related to the rainfall and pasture infectivity (Carles,

1983). The control measures aim at improving weight gains and reducing the levels

of pasture contaminations. Generally, anthelmintic treatments should be given 3-4

weeks after a significant amount of rainfall and at the beginning of the dry season or

in mid-dry season. The dry season treatments are particularly beneficial to sheep as

they reduce the worm burdens at a time of pasture scarcities and also decreases

pasture infectivity. In the present study, treatment of lambs and yearlings 3 weeks

into the rains and during the dry seasons resulted in significant reduction in faecal egg

output, increased weight gains when pastures were good and lower weight losses in

times of scarcities.

It is a well established principle that poorly fed animals are more susceptible to the

effects of internal parasites and are more inclined to carry worm burdens because of

their failure to throw off infestations quickly (Blood el al., 1997). The nutritional

levels of most tropical pastures are adequate for animal production only for a few

months of the year when the pastures are young (Reynolds and Adediran, 1987).

Consequently, there is usually severe seasonal shortages leading to wide spread

malnutrition and sometimes heavy parasitism, particularly in the semi-arid and

140

savanna zones (Schillhorn van Veen, 1974; Charles, 1989). In the present study the

pasture quality and availability (Chapter 5, Figure 5.8) was greatly influenced by the

rainfall distribution pattern. The availability and quality of pastures improved shortly

after the onset of the rains and generally resulted in improved weight gains in all

groups of sheep. As the dry season advanced the availability and quality of the

pastures declined and the animals lost weight. The treated groups had higher rates of

weight gains and lower rates of weight losses. The results of this study therefore

indicated that strategic treatments of sheep can greatly improve on production in the

study area, but there is need to improve on the feeding programmes for better results.

141

CHAPTER 8

8.0 GENERAL DISCUSSION, CONCLUSIONS AND SIGNIFICANCE OF

THE STUDY

8.1 General discussion and conclusions


production worldwide. For rational and sustainable control of these parasites,

comprehensive knowledge on the epidemiology of the parasite as it interacts with the

host in a specific climatic, management and production environment is crucial

(Barger, 1999). The helminth infections have primarily been controlled by use of

anthelmintics due to their ease of application and high efficiency. However, in

developing countries, there are poor or ineffective set plans of prophylactic control

o f gastrointestinal helminths and the use of anthelmintics is mainly irregular and

haphazard (Mbaria el al., 1995). No previous information was available on the

epidemiology and control strategies of gastrointestinal helminths for Kajiado District.

The main objective of this work was therefore to establish the epidemiology and

control strategies of gastrointestinal helminths in sheep in this area.

The epidemiological studies were carried out by conducting surveys on the prevalence

and intensities of helminth infections in sheep, the dynamics of the free-living stages

of nematodes in pastures and the post-mortem total and differential worm counts. A

one year prevalence survey carried out on Dorper and Red Maasai lambs, yearlings

and adult breeding ewes indicated that the prevalence of helminth infections was

highest for the lambs and lowest for the yearlings in both breeds. The higher

142

susceptibility of the lambs was attributed to their immunological hypo-responsiveness

(Watson and Gill, 1991; Colditz el al., 1996). In older animals, lower levels of

infection were observed, possibly as a result of acquired immunity. The higher

prevalence of infection in breeding ewes compared to the yearlings was associated

with the loss of acquired immunity in the peri-parturient ewes (Gibbs and Barger,

1986). Significantly higher levels of infection occurred in the Dorpers than in the Red

Maasai sheep in all age groups. This observation confirmed earlier reports on the

resistance of the Red Maasai to infections with gastrointestinal nematodes compared

to exotic breeds of sheep in Kenya (Preston and Allonby, 1979a; Bain et al., 1993;

Baker, 1995). The proportions of infected animals were higher during the wet seasons

than in the dry seasons. Similar observations have been made in other parts of the

country (Gatongi, 1995; Maingi, 1996). Control strategies in the study area should

be planned to offer maximum protection for the lambs. They should also aim at

reducing the levels of infection during the wet and the dry seasons in all age groups

and breeds. Farmers from the study area should be encouraged to keep the more

resistant Red Maasai or their crosses.

An investigation carried out to establish the occurrence of peri-parturient rise in faecal

egg output in breeding ewes confirmed the occurrence of the phenomenon in the study

area. Significant rise in faecal egg output occurred at the time of lambing and

throughout the lactation period. The cause of the PPR has been attributed to poor

nutrition, stress, lack of antigenic stimulation and hormonal suppression of immunity,

of which the latter is overwhelmingly favoured (Barger, 1993). In the present study

most of the gestation period and the early parts of the lactation coincided with the dry

143

season, a time when the level of nutrition was low. The animals were further stressed

by the longer distances they had to walk in search of pastures and water. The faecal

egg output in ewes remained high throughout the lactation period and the ewes were

also unable to effectively self-cure. This observation may be attributed to lack of

antigenic stimulation and hormonal suppression of immunity (Connan, 1968b;

O ’Sullivan and Donald 1970; Barger, 1999).

Connan (1968b) and O ’Sullivan and Donald (1970) suggested that the rise in faecal

egg output and worm burdens in the peri-parturient ewes are derived from maturation

of previously arrested larvae, increased establishment of newly acquired larvae and

increased fecundity of acquired and established female worms. In the present study,

the magnitude of the PPR was highest when lambing coincided with the resumption

of development of hypobiotic larvae and the faecal egg output was higher in the peri-

parturient ewes than in the un-bred yearlings during both the wet and the dry seasons.

The PPR increased the level of pasture contamination when the number of susceptible

lambs are increasing. Control strategies in this area should therefore aim at reducing

the effects o f the peri-parturient rise by treating ewes just before lambing and during

lactation. Where possible, the level of nutrition for breeding ewes should also be

improved during gestation and lactation.

The results of the two year study on the prevalence and intensity of infection with

gastrointestinal nematode parasites in Dorper lambs showed that infection in lambs

occurred at around the age 9 to 12 weeks when they started to rely heavily on

pastures. The time at which this happens largely depends on the availability of the

144

milk from the dam and the farm management practice (Carles 1983; Blood el

al., 1997). In the present study, peak faecal egg output in lambs occurred at around

the time of weaning. Weaning is known to impose severe stress on lambs and increase

their susceptibility to helminth infections (Watson and Gill, 1991). The weaning stress

also contributes to delayed development of acquired immunity which generally occurs

at the age of 6 to 7 months (Watson and Gill, 1991; Colditz et al., 1996). The decline

in faecal egg output at the age of 7 months and the ability to self-cure in the 10 to 12

month old Iambs was attributed to the development of acquired immunity (Watson and

Gill, 1991; Colditz et al., 1996). Results of this study therefore indicate that the use

of anthelmintics in the control of gastrointestinal helminths in lambs within the study

area should start at the age of 9 to 12 weeks. A second treatment should be

administered at the time of weaning (4 to 5 months), and lambs moved to "clean"

pastures where possible.

In the study on the dynamics of free-living stages of gastrointestinal nematodes of

sheep, rainfall distribution was found to be the major factor governing the

development, survival and availability of infective stages on pastures. This

observation rendered further support to earlier findings by workers in the tropical

environment where temperatures are always conducive for the transmission of the

parasites (Dinnik and Dinnik, 1961; Altaif and Yakoob, 1987; Banks et al., 1990;

Tembely, 1998; Waruiru, 1998). In the present study, infective larvae were always

recovered from the pastures during the wet season, but not during the hot dry season.

This was attributed to the fact that during the wet season, the environment was

conducive for the development and translocation of infective larvae on pastures, but

145

the extremes of temperature and intense drought causes rapid desiccation and deaths

of eggs and larvae (Barger, 1999). The lack of infective larvae on pastures during the

dry season and their relatively short survival time during the wet season provides an

opportunity for the use of pasture spelling as a means of helminth control in the study

area.

The results of the study on the seasonal spectrum of gastrointestinal nematode

infections in sheep indicated that mixed infections occurred in the study area and that

Trichostrongylus and Haemonchus were the most prevalent. The higher abundance of

Trichostrongylus species observed in this study indicates that the species may play a

more important role in the aetiology of parasitic gastroenteritis in sheep in this area

than was previously thought. The mean total worm counts in the study area were

considered as moderate during both the wet and the dry seasons (McKenna, 1981;

Hansen and Perry, 1994). Such infections are normally sub-clinical and are a potential

problem in the production of sheep in this area. The problem is further aggravated

by the frequent droughts in the semi-arid areas and may be a major constraint to

sheep production in this region. The study also showed that the adult and the

immature worm populations co-existed in proportions that varied with seasons. The

proportions of adult to immature parasites during the wet and the dry season

confirmed the occurrence of hypobiosis of //. contortus in the study area and

indicated that Trichostrongylus species mainly survive the dry season as an adult

population. These findings were in agreement with those of other workers in the

tropics (Ogunsusi, 1979b; Gatongi, 1995). Control measures should therefore aim at

reducing the levels of infection during both the wet and the dry seasons. The results

146

also indicate that the use of narrow spectrum anthelmintics such as closantel that only

eliminate Haemonchus while Trichosirongylus species predominate and the application

of treatments based on a system such as Fafa Malan Chart (FAMACIIA) that assumes

that Haemonclms is the predominant species may be inappropriate to apply in this

area.

The evaluation of strategic use of anthelmintics in the control o f gastrointestinal

nematode infections in sheep indicated that such strategies are both effective and

desirable. The treatment of breeding ewes at pre-mating, pre-lambing and in mid

lactation resulted in improved birth weight, better weight gains for lambs and

improved weights for the ewes. Higher birth weights and weight gains in Iambs are

important in that they influence positively on their survival and reduce the time

required to attain maturity and market weights (Carles, 1983; Fraser el al., 1986;

Gatongi, 1995). Also improved weight recovery in peri-parturient ewes improves on

their reproductive performance in the subsequent breeding season (Connan, 1976).

The decrease in the faecal egg output resulting from these treatments was of

epidemiological significance in that it resulted in lower pasture contamination at a

time when the population of susceptible lambs was increasing. Based on the

observations made during the epidemiological study and the treatment trials, it is

recommended that breeding ewes in the study area be treated pre-mating, pre-lambing

and in mid-lactation.

Due to the greater susceptibility of young animals to infections, the most important

strategic treatments are those planned to provide maximum protection until weaning

147

and at weaning when the young animals suffer their greatest nutritional stress (Blood

et al., 1997). In the present study, the strategic treatment of lambs at the age of 3

months and around the time of weaning (4-5 months) resulted in significantly higher

weight gains and lower faecal egg output. In weaned lambs and yearlings, strategic

treatments are usually given in relation to the rainfall and pasture infectivity (Carles

1993). The aim is to improve on the weight gain and to reduce pasture contamination.

In the present study, treatment of this category of animals three weeks into the rains,

at the onset of the dry season and in mid-dry season resulted in improved body

weights and lower faecal egg outputs compared to the un treated controls. Based on

the results obtained in this study, it is recommended that within the study area, lambs

be treated at around the age of 3 months and at the time of weaning. Weaned lambs

and yearlings should be treated 3 weeks into the long and the short rains and in mid

dry season.

8.2 Significance of the study

1. The different aspects of gastrointestinal helminthosis in sheep investigated in

this study gave an insight into the epidemiology of the parasites in a semi-arid area

of Kajiado District. The intensity of infection was greatly influenced by host factors

of age, breed and physiological status and by climatic factors. The rainfall distribution

pattern was the major climatic factor influencing the prevalence and intensity of

infection as it determined the development and survival of the pre-parasitic stages in

pastures. The results obtained in this study can be used in the design of strategic

control programmes of the parasites in sheep within the study area. Tart of this

information was used in the evaluation of the strategic use of anthelmintics in the

control of gastrointestinal nematodes of sheep within the study area.

148

2. Results from faecal cultures and post-mortem examination revealed that

Trichostrongylus spp. are the predominant nematode species in sheep within the study

area. This indicates that the species may play a more important role in the occurrence

of nematodosis in sheep in this area than was previously thought. This observation

differed with that of Gatongi (1995) who reported a higher occurrence of Haemonchus

in sheep and goats in a similar environment in Naivasha. The variation in these

observations shows the danger of designing control programmes based on the

extrapolation of studies carried elsewhere and underscores the need to carry out

epidemiological studies for specific localities.

3. This study established the occurrence of hypobiosis involving Haemonchus

contortus in sheep within the study area. This is an important phenomenon in the

epidemiology of helminthosis in that the resumption of development of hypobiotic

larvae is often associated with clinical haemonchosis and should be taken into

consideration when designing control programmes. Whereas the observations in the

present study supported those of Gatongi (1995) under a similar environment in

Naivasha, the two studies differed on the time of resumption of larval development.

In Kajiado the resumption of larval development was targeted to the favourable

environment created by the short rains and not the long rains as was the case in

Naivasha. This observation further underscores the need for localised epidemiological

studies.

149

4. The study also established the occurrence and significance of the peri-

parturient rise in trichostrongylid nematode egg output in ewes. This is an important

epidemiological phenomenon in that it leads to increased pasture contamination thus

acting as a source of infection for lambs. This then necessitates the design of special

strategic control programmes for breeding ewes in the study area.

5. In this study, positive correlation between faecal strongyle egg counts and the

worm burdens in sheep was observed during the wet and the dry seasons. This

differed with the report of Gatongi (1995) who observed positive correlation between

the egg counts and the worm burdens in sheep and goats under a similar environment

in Naivasha during the wet season only. Differences in the predominant nematode

species in the two areas may have contributed to the variations in these observations.

Results from this study and those from other parts of the country indicate that the

usefulness o f faecal egg counts in the diagnosis and assessment of levels of infections

with gastrointestinal nematodes need to be evaluated for different regions.

6 . The results of this study clearly demonstrate that application of a well planned

strategic control programme for gastrointestinal nematodes of sheep in the study area

can lead to higher birth weights, improved growth rates and weight gains. This is

especially important in this area where the use of anthelmintics is mostly haphazard

or non-existent.

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