This article was downloaded by: [LIBRARY OF THE UNIVERSITY OF VETERINARY MEDICINE VIENNA] On: 07 May 2013, At: 23:05 Publisher: Taylor & Francis Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK British Poultry Science Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/cbps20 Dietary plant bioactives for poultry health and productivity Professor R.J. Wallace a , W. Oleszek b , C. Franz c , I. Hahn c , K.H.C. Baser d , A. Mathe e & K. Teichmann f a Rowett Institute of Nutrition and Health, University of Aberdeen, Aberdeen, AB21 9SB, UK b Institute of Soil Science and Plant Cultivation, State Research Institute, Pulawy, Poland c University of Veterinary Medicine, Vienna, Austria d Department of Pharmacognosy, Faculty of Pharmacy, Anadolu University, Eskisehir, Turkey e Western Hungarian University, Department of Botany, Hungary f BIOMIN Research Center, Tulln, Austria Published online: 30 Sep 2010. To cite this article: Professor R.J. Wallace , W. Oleszek , C. Franz , I. Hahn , K.H.C. Baser , A. Mathe & K. Teichmann (2010): Dietary plant bioactives for poultry health and productivity, British Poultry Science, 51:4, 461-487 To link to this article: http://dx.doi.org/10.1080/00071668.2010.506908 PLEASE SCROLL DOWN FOR ARTICLE Full terms and conditions of use: http://www.tandfonline.com/page/terms-and-conditions This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. The publisher does not give any warranty express or implied or make any representation that the contents will be complete or accurate or up to date. The accuracy of any instructions, formulae, and drug doses should be independently verified with primary sources. The publisher shall not be liable for any loss, actions, claims, proceedings, demand, or costs or damages whatsoever or howsoever caused arising directly or indirectly in connection with or arising out of the use of this material.
Transcript
This article was downloaded by: [LIBRARY OF THE UNIVERSITY OF VETERINARY MEDICINE VIENNA]On: 07 May 2013, At: 23:05Publisher: Taylor & FrancisInforma Ltd Registered in England and Wales Registered Number: 1072954 Registered office: MortimerHouse, 37-41 Mortimer Street, London W1T 3JH, UK
British Poultry SciencePublication details, including instructions for authors and subscription information:http://www.tandfonline.com/loi/cbps20
Dietary plant bioactives for poultry health andproductivityProfessor R.J. Wallace a , W. Oleszek b , C. Franz c , I. Hahn c , K.H.C. Baser d , A. Mathee & K. Teichmann fa Rowett Institute of Nutrition and Health, University of Aberdeen, Aberdeen, AB21 9SB,UKb Institute of Soil Science and Plant Cultivation, State Research Institute, Pulawy, Polandc University of Veterinary Medicine, Vienna, Austriad Department of Pharmacognosy, Faculty of Pharmacy, Anadolu University, Eskisehir,Turkeye Western Hungarian University, Department of Botany, Hungaryf BIOMIN Research Center, Tulln, AustriaPublished online: 30 Sep 2010.
To cite this article: Professor R.J. Wallace , W. Oleszek , C. Franz , I. Hahn , K.H.C. Baser , A. Mathe & K. Teichmann(2010): Dietary plant bioactives for poultry health and productivity, British Poultry Science, 51:4, 461-487
To link to this article: http://dx.doi.org/10.1080/00071668.2010.506908
PLEASE SCROLL DOWN FOR ARTICLE
Full terms and conditions of use: http://www.tandfonline.com/page/terms-and-conditions
This article may be used for research, teaching, and private study purposes. Any substantial or systematicreproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form toanyone is expressly forbidden.
The publisher does not give any warranty express or implied or make any representation that the contentswill be complete or accurate or up to date. The accuracy of any instructions, formulae, and drug dosesshould be independently verified with primary sources. The publisher shall not be liable for any loss, actions,claims, proceedings, demand, or costs or damages whatsoever or howsoever caused arising directly orindirectly in connection with or arising out of the use of this material.
British Poultry Science Volume 51, Number 4 (August 2010), pp. 461—487
INVITED REVIEW PAPER
Dietary plant bioactives for poultry health and productivity
R.J. WALLACE, W. OLESZEK1, C. FRANZ2, I. HAHN2, K.H.C. BASER3,A. MATHE4
AND K. TEICHMANN5
Rowett Institute of Nutrition and Health, University of Aberdeen, Aberdeen, AB21 9SB, UK, 1Institute ofSoil Science and Plant Cultivation, State Research Institute, Pulawy, Poland, 2University of VeterinaryMedicine, Vienna, Austria, 3Department of Pharmacognosy, Faculty of Pharmacy, Anadolu University,Eskisehir, Turkey, 4Western Hungarian University, Department of Botany, Hungary, and 5BIOMINResearch Center, Tulln, Austria
Abstract 1. Plants and their biologically active chemical constituents, sometimes called secondarymetabolites or bioactives, present numerous opportunities for the improvement of livestock productionby inclusion in the diet.2. Many such plant derived materials have well established therapeutic values in man; however, theirpotential as feed additives in animal production, particularly of poultry, remains largely unexploited.3. There is increasing evidence indicating that they can be efficient in controlling diseases, and plantbioactives may also influence production parameters such as feed efficiency and product quality.4. It has been reported that they may even replicate some of the effects of antibiotic growthpromoters, which were banned from use in Europe from 2006.5. This review assesses the status of plant bioactives in poultry production and their mode of actionon avian physiology, particularly in the digestive tract.
INTRODUCTION
Interest in plants, plant extracts and derivedphytochemicals (botanicals) as components oflivestock feedstuffs has increased during the lastdecade. Much of the impetus for revisiting theplant kingdom to look for new, useful additivesthat can enhance health and productivity resultsfrom concerns about the safety and sustainabilityof antibiotic growth promoters. If transmissibleantibiotic resistance factors result from the useof growth-promoting antimicrobials (GPA) inanimal production, the efficacy of similar anti-biotics in therapy for human diseases may becompromised. Hence, the EU introduced a banon GPA in 2006. Other nations may follow. Beforethe ban, poultry production had a high depen-dence on GPA to control intestinal pathogenssuch as Escherichia coli, Clostridium perfringens
and coccidial infection. Since then, improvedmanagement has compensated for some of theproduction-benefit losses, but not all. Consumerpressure also plays a part in the move to more‘‘naturally’’ produced foods (Rickard, 2004). Theincreasing demand for organically producedfoods also drives the search for alternative feedadditives (Griggs and Jacob, 2005).
Botanicals should not be considered only asreplacements for GPA, however. They have usefulproperties not shared by GPA. Herbs, spices andtheir extracts can stimulate feed intake andendogenous secretions (Wenk, 2003). Many bota-nicals have antioxidant activities that can improvethe oxidative stability of poultry meat and eggs,increasing their shelf life. They may stimulateimmunity directly, improving birds’ resistance todisease. They also have the potential to modifycholesterol metabolism, leading to a product with
Correspondence to: Professor R.J. Wallace, University of Aberdeen, Rowett Institute of Nutrition and Health, Bucksburn, Aberdeen, AB21 9SB, UK.
healthier implications for human production.Even reproduction may be improved by increas-ing semen quality (Durape, 2007).
A final consideration, indeed the mostimportant of all, is that many plants and phyto-chemicals have adverse effects on animals wheningested. Acamovic and Brooker (2005) remindus: ‘‘The effects depend to a great extent on thechemistry of the compounds, their concentrationin the diet and the amount consumed, and arefurther dependent on the health status of theanimals. Traditionally, most studies of the effectsof these compounds on animals have focused ontheir adverse effects and how to alleviate them.However, recent public concern about the use ofsynthetic compounds in animal diets to enhanceperformance and health and welfare issues,coupled with changes in regulations on the useof synthetic medicaments, has stimulated interestand research in the use and effects of phytochem-icals in the diets of farmed animals.Phytochemicals vary in their chemistry but canbe divided into hydrophilic and hydrophobiccompounds, of which a wide variety of polyphe-nolic and terpenoid compounds, as well asalkaloids, carbohydrates and non-protein aminoacids, invoke special interest’’.
The use of botanicals in human and animalhealth undoubtedly has potential value — manywidely used therapeutic drugs originate from theplant kingdom — but the use of botanicals inanimal production is less well established. It isimportant to provide a good description of eachplant, its active phytochemicals and their mole-cular mode of action against microorganisms ortheir interaction with the host. Given the vastnessand diversity of the plant kingdom, variationsbetween cultivars, variation in applications, andmany other factors, such a complete descriptionwill never be attainable. Nevertheless, it mightreasonably be expected that botanicals incommon use or intended for widespread applica-tion should have a body of efficacy, safety andmechanistic information to enable users to assessand understand the biological activity of thebotanical in question. The aim of this review wasto report on the status of the botanicals field inpoultry in relation to these benchmark criteria.
The review itself was prompted by two maindrivers. One was the EC Framework 7 SpecificSupport Action, contract 43077, FEED-SEG,a consortium whose broad objective is ‘‘todisseminate state-of-the-art research results infeed quality topics. . . (and to). . . develop strate-gies and recommendations for European policies(e.g. research, health, agriculture)’’. The secondwas the publication of an excellent review forbotanicals and ruminants (Rochfort et al., 2008).The challenge that we as authors of this articleaccepted was to attempt to replicate the review of
Rochfort et al. (2008), with poultry rather thanruminants as the subject group of animals.Poultry production encompasses broilers, layersand breeders from different species — chicken,turkey, and duck principally. Much less is knownabout the ostrich (Vispo and Karasov 1996), inspite of its growing commercial importance. Thisreview focusses on plant bioactives, poultryproduction and its underlying science, and doesnot repeat the comprehensive sections in theRochfort et al. (2008) review on social andregulatory issues, to which the reader is referred.
THE STATUS OF PLANT BIOACTIVESAS FEED ADDITIVES
Generally speaking, feed additives are consideredas being applied in the feed by the farmer tohealthy animals not only for nutritional purposesbut also additional functionality on a long-termbasis (possibly along the entire production periodof the respective species), in contrast to veterinarydrugs used only to treat health problems undercontrol of a veterinarian, applied for a limitedperiod only. As per definition from Regulation(EC) No. 1831/2003, ‘‘feed additives are sub-stances or preparations — other than feed materialor premixtures — which are intentionally added tofeed or water in order to
— favourably affect the characteristics of feed, ase.g. flavouring or antioxidant,
— affect the characteristics of animal productsregarding microbial load, shelf life or taste,
— affect the environmental consequences of espe-cially large-scale livestock production e.g. byreduction of ammonia excretion or methaneproduction,
— favourably influence animal production, perfor-mance or welfare by affecting the gastrointestinalmicrobiota and the digestibility of feeding stuffs, or
— have a coccidiostatic or histomonostatic effect’’.
Thus, this review, for the most part (asbenefits to productivity are inevitably linkedwith the control of disease) concentrates onplant bioactives as feed additives rather thantherapeutics. Valuable effects on, for example,fowl typhoid (Waihenya et al., 2002a) would notnormally be covered.
Presently, herbal products are used by thefeed industry predominantly as sensory additives,flavouring and appetising substances. Althoughan understanding of their mode of action wouldbe a prerequisite for their optimal applicationin terms of efficacy, a full understanding ofthese aspects in animals is not yet achieved.For example, aromatic compounds and essentialoils (EO) act along the animal digestive tract
462 R.J. WALLACE ET AL.
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to improve appetite, bacterial modulation,and are able to induce a number of benefits onwell being (Kamel, 2001). The antimicrobialproperties of EOs and extracts can be dose-dependently bacteriostatic and/or bactericidal.In addition, several investigations have shown anantioxidative effect or changes in digestivephysiology and digestion at weaning (Zabielskiet al., 1999), the microbiology of the gut (Jensen,1998) and the implementation of test models inpoultry (Hess, 2002). Another complication isthat plant bioactive compounds occur in natureas complex mixtures rather than as singlecompounds, and synergy between individualcomponents may be an important feature oftheir action.
Plant bioactives are often proposed aspossible replacements for AGP. Their efficacyin achieving the same effects remains open toquestion, but an undoubted advantage of plantbioactives over GPA is that resistance is less likely
to become a problem than with conventionalsynthetic compounds.
It must also be remembered that plantscontain many poisonous compounds, includingsome of the most toxic known to man. Someplant extracts may therefore be detrimental forpoultry and by numerous mechanisms maydecrease body weight, feed intake (FI) and feedconversion ratio (FCR) and digestibility. Theycan also influence mortality, muscular conditionsand in some instances can be neurotoxic.
BIOACTIVE COMPOUNDS AND THEIREFFECTS ON PRODUCTION
Production efficiency and incidenceof disease
Numerous feeding trials have been performedwith plant extracts, aromatic herbs and EOsadditives, to investigate production parameters
Figure. Structures, estimated range and numbers of plant secondary metabolites (re-drawn from Acamovic and Brooker (2005), withpermission).
PLANT BIOACTIVES: A REVIEW 463
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Tab
le1
.P
erfo
rman
ceef
fect
sof
plan
tm
ater
ial
and
plan
tex
trac
tsu
sed
asfe
edad
diti
ves
inpo
ult
ryn
utr
itio
n
Per
form
ance
effe
ct
Pla
nt
spec
ies/
extr
act
Do
seB
enef
icia
lN
oef
fect
Det
rim
enta
lL
iter
atu
re
Aes
culu
shi
ppoc
asta
nu
m0
—10
mg
/g
bo
dy
Dep
ress
ion
Wil
liam
san
dO
lsen
(19
84
)M
usc
ula
rin
coo
rdin
atio
np
aral
ysis
Alf
alfa
extr
act
0.0
6%
Th
ymu
san
dsp
leen
wei
gh
tF
IA
bd
om
inal
fat
wei
gh
tD
on
get
al.
(20
07
)B
urs
alw
eig
ht
FC
RIm
mu
nit
yA
loe
secu
ndi
flor
aex
trac
t—
Red
uce
dm
ort
alit
yin
New
cast
led
isea
sein
fect
ion
,In
crea
seo
fin
terl
euk
in6
An
tib
od
yle
vels
—W
aih
enya
etal
.(2
00
2a,
b)
Art
ich
ok
ew
ater
extr
act
5%
DM
Hu
mo
ral
imm
un
ere
spo
nse
——
Sto
evet
al.
(20
00
)O
rgan
wei
gh
tP
rote
ctio
nag
ain
sto
chra
toxi
nA
Bal
anit
esae
gypt
iaca
sap
on
ins
5—2
50
mg
/k
g/
day
To
tal
cho
lest
ero
lB
od
yw
eig
ht
Nak
hla
etal
.(1
99
2)
Cal
endu
laof
fici
nal
isex
trac
tD
rin
kin
gw
ater
Mea
nw
eig
ht
FC
RIm
mu
ne
resp
on
seB
arb
ou
ret
al.
(20
04
)M
ort
alit
yB
urs
alw
eig
ht
ind
exC
assi
aob
tusi
foli
a2
%b
od
yw
eig
ht
—W
eig
ht
gai
nF
IH
eber
tan
dF
lory
(19
83
)C
assi
aoc
cide
nta
lis
——
Wei
gh
tG
razi
ano
etal
.(1
98
3)
Mu
scu
lar
wea
kn
ess
Cit
rus
extr
act
10
—10
00
g/
tL
ive
wei
gh
tM
etab
oli
sab
leen
erg
y—
Juin
etal
.(2
00
3)
FI
Col
chin
chin
am
omor
dica
5—8
0mg
/d
ose
An
tib
od
yle
vel
——
Raj
pu
tet
al.
(20
07
)ex
trac
tD
aily
wei
gh
tg
ain
EO
(th
ymo
l,ci
nn
amal
de-
hyd
e,co
mm
erci
alp
rep
arat
ion
)
10
0p
pm
—F
I—
Lee
etal
.(2
00
3)
Wei
gh
tg
ain
FC
RL
iver
wei
gh
tIl
eal
dig
esti
bil
ity
Fer
men
ted
wh
eat
ger
mex
trac
t—
Su
pp
ress
ion
of
Myc
opla
sma
gall
isep
ticu
min
fect
ion
Bo
dy
wei
gh
tg
ain
s—
Sti
pk
ovi
tset
al.
(20
04
)
FC
RF
ield
bea
nta
nn
inh
ull
s—
—D
iges
tib
ilit
yF
lore
set
al.
(19
94
)T
ME
nG
arli
cex
trac
t3
.8%
gar
lic
Ch
ole
ster
ol
leve
l—
—Q
ure
shi
etal
.(1
98
3)
pas
teE
nzy
me
sup
pre
ssio
nG
rap
ese
edex
trac
t2
.59
—5.1
8%
Pos
tm
orte
mm
eat
par
amet
ers
Wei
gh
tg
ain
Lau
and
Kin
g(2
00
3)
Hem
pse
edm
eal
—C
on
cen
trat
ion
of
pal
mit
icac
idan
dh
igh
erli
no
leic
acid
sin
egg
s
Eg
gp
rod
uct
ion
Sil
vers
ides
and
Lef
ran
cois
(20
05
)
FI
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Fee
def
fici
ency
Var
iou
sh
erb
s(t
hym
e,o
reg
ano
,m
arjo
ram
,ro
sem
ary,
yarr
ow
)an
dth
eir
EO
10
g/
kg
Per
form
ance
Inte
stin
alm
icro
flo
raE
nd
og
eno
us
sial
icac
idse
cret
ion
Cro
sset
al.
(20
07
)
Ap
par
ent
met
abo
lisa
ble
ener
gy
Dig
esti
bil
ity
Lab
iata
eex
trac
t(s
age,
thym
e,ro
sem
ary)
50
00
pp
mA
pp
aren
tfa
ecal
dig
esti
bil
ity
CP
dig
esti
bil
ity
—H
ern
and
ezet
al.
(20
04
)
Eth
erex
trac
td
iges
tib
ilit
yW
eig
ht
of
org
ans
Len
tin
us
edod
es0
.5—4
g/
kg
Bo
dy
wei
gh
tg
ain
Rel
ativ
ew
eig
hts
of
org
ans
and
GIT
—G
uo
etal
.(2
00
4b)
Tre
mel
lafu
cifo
rmis
FC
RF
IL
inse
edm
eal
20
%S
elen
ium
toxi
city
Gro
wth
rate
—Je
nse
nan
dC
han
g(1
97
6)
Man
gife
rain
dica
seed
ker
nel
mea
l5
0—2
50
mg
/k
gm
eal
Bo
dy
wei
gh
tF
I—
Od
un
si(2
00
5)
Bo
dy
wei
gh
tg
ain
Fee
def
fici
ency
Org
anw
eig
hts
Myr
isti
cafr
agra
nce
——
—D
eep
slee
pin
you
ng
chic
ken
Sh
erry
etal
.(1
98
2)
Nep
eta
cata
ria
25
—10
00
mg
/k
g—
—In
crea
sed
nu
mb
erif
slee
pin
gch
ick
sS
her
ryan
dH
un
ter
(19
79
)
Ore
gan
o,
cin
nam
on
and
pep
per
esse
nti
alo
ils
20
0p
pm
—F
I—
Her
nan
dez
etal
.(2
00
4)
FC
RO
reg
ano
esse
nti
alo
il5
0—1
00
mg
/k
g—
Gro
wth
Mal
on
dia
ldeh
yde
inti
ssu
eB
ots
og
lou
etal
.(2
00
2)
Pla
nt
extr
acts
con
tain
ing
5%
carv
acro
l,3
%ci
nn
a-m
ald
ehyd
e,2
%ca
psi
-cu
mo
leo
resi
n
10
0m
g/
kg
Vil
li-r
elat
edp
rote
ctiv
eac
tivi
ty—
—Ja
mro
zet
al.
(20
06
)
Ad
hes
ion
of
E.
coli
and
C.
perf
rin
gen
sP
lan
tex
trac
tsco
nta
inin
gca
psa
icin
,ci
nn
amal
de-
hyd
ean
dca
rvac
rol
10
0m
g/
kg
Bre
ast
mu
scle
pro
po
rtio
nIl
eal
dig
esti
bil
ity
of
nu
trie
nts
—Ja
mro
zet
al.
(20
05
)
Em
pty
bo
dy
wei
gh
tE
.co
lian
dC
.pe
rfri
nge
ns
nu
mb
ers
Lac
toba
cill
us
spp
.n
um
ber
Lip
ase
acti
vity
Ro
sem
ary
extr
act
50
0—1
00
0m
g/
kg
—L
ipid
oxi
dat
ion
par
amet
ers
—G
alo
bar
tet
al.
(20
01
)R
yeex
trac
t—
—W
eig
ht
gai
nD
ayan
dT
ho
mas
(19
80
)Sa
ccha
rum
offi
cin
aru
m5
00
mg
/k
g/
day
Ph
ago
cyti
cac
tivi
tyo
fp
erip
her
alb
loo
dle
uco
cyte
——
Hik
osa
ka
etal
.(2
00
7)
An
tib
od
yre
spo
nse
Imm
un
ost
imu
lati
ng
acti
vity
(Con
tin
ued
).
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Tab
le1
.C
onti
nu
ed.
Per
form
ance
effe
ct
Pla
nt
spec
ies/
extr
act
Do
seB
enef
icia
lN
oef
fect
Det
rim
enta
lL
iter
atu
re
Sen
na
occi
den
tali
sse
eds
Ext
ensi
veax
on
ald
amag
eN
euro
tox
icC
alo
reet
al.
(19
98
)Si
lybu
mm
aria
nu
mfr
uit
extr
act
40
—80
pp
msy
lim
arin
Dec
reas
eo
fsl
aug
hte
rin
gyi
eld
sG
row
thra
te—
Sch
iavo
ne
etal
.(2
00
7)
Red
uct
ion
of
lip
idco
nte
nt
inm
eat
Hep
ato
pro
tect
ion
Syn
clis
iasc
abri
daex
trac
ts—
Ap
om
orp
hin
e-in
du
ced
ster
eoty
pe
beh
avio
ur
——
So
ko
mb
aet
al.
(19
86
)
Pse
udo
man
asan
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466 R.J. WALLACE ET AL.
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such as feed intake, weight gain and feedconversion rate (Table 1; see also Windischet al., 2008). Comparison of these data hasoften been very difficult, however, as differentexperiments were performed with different andwidely ranged doses. Some authors reported thedose in mg per body weight, some in percentagein the feedstuff, while the others calculated basedon the concentration of active principles. Inmany cases FI and FCR have been influenced byplant extracts. However, in a number of cases FIand FCR were not changed but the extracts stillhad positive effects on body weight, body weightgain, organ weight and/or energy utilisation.This results from the strong link betweenproductivity and health. Plant extracts maystimulate the immune system (extracts fromalfalfa, artichoke, Saccharum officinarum, Table 1and elsewhere in this review), suppressionof harmful microorganisms (Pseudomonas,Staphyloccoccus, E. coli, Eimeria spp., C. perfringens,Mycoplasma gallisepticum), stimulation of benefi-cial microbes such as Lactobacillus spp. (extractscontaining capsaicin, cinnamaldehyde and carva-crol), the regulation of the activity of someenzymes (e.g. lipase), protection of gut villi andbacterial adhesion parameters. Plant extracts mayalso influence the post-mortem quality of meat,especially cholesterol concentration, lipids con-tent, oxidative stability, as well as the quality ofeggs, although sometimes better quality wasaccompanied by reduced weight gain (grapeseed extract). An important parameter that caninfluence growth performance is the protectiongiven by plant extracts against some toxins thatcan be found in feedstuffs, e.g. ochratoxin A andselenium.
An extract of sugar cane, which was theresidue after removing glucose, fructose andsucrose from sugar cane juice was fed at thedose of 0.5 g/kg/d (El-Abasy et al., 2002;Yamauchi et al., 2006) to broilers. A higherbody weight gain, gain in body weight/day andlower feed conversion ratio were observed underthis treatment, but, like many similar studies, thephytochemical(s) responsible were not identified.Besides some alterations in intestinal histology(higher values of villus height, villus area,epithelial cell area and cell mitosis) promotinggrowth and showing immunostimulating effectswere observed. Chinese herbs were shown to beeffective feed additives replacing antibiotics inPekin meat duck diets (Wang and Zhou, 2007),and a similar conclusion was drawn by Jamrozand Kamel (2002) who observed improvementsin daily gain and feed conversion ratio in poultryfed on a diet supplemented with plant extracts.Plant extracts from milk thistle (90 and 180 mg/kg feed), yarrow (900 and 1800 mg/kg), garlic(8230 and 16460 mg/kg), oregano, juniper
(450 and 6000 mg/kg) and horseradish (450and 6000 mg/kg) showed beneficial effects onmale broiler chickens (Lewis et al., 2003). Basedon feed conversion efficiency (FCE), two extractse.g. yarrow and garlic were indicated as promis-ing. Garlic (1 g/kg feed) and thyme (1 g/kg feed)were also most promising herb feed additive inthe research performed using 5 commercial feedssupplemented with NorSpice� powders (Demiret al., 2003). Two additional commercial phyto-genic feed additives XTRACTTM containingcarvacrol (5%), cinnamaldehyde (3%) andCapsicum oleoresin (2%) as well as Sangrovit�
containing ground roots of Sanguinaria canaden-sis rich in the alkaloids sanguinarin and cheler-ythrin had no effect on chicken growthperformance, nutrient utilisation or threonineefficiency, but slightly improved daily gain(þ3.7%) and feed conversion ratio (þ1.7%).
Dietary supplementation of an EO mixtureHerbromix� (oregano herb (Origanum onites),laurel leaf (Laurus nobilis), sage leaf (Salviafruticosa), fennel fruit (Foeniculum vulgare),myrtle leaf (Myrtus communis) and citrus peel(rich in limonene) to broilers significantlyimproved feed conversion rate above that ofthe control group (Alcicek et al., 2004; Cabuktet al., 2006a). In laying hens, cracked-broken eggrate was decreased with the dietary supplementof EO (Cabukt et al., 2006b). Supplying OreganoEO reduced daily feed intake of broilers com-pared to control animals. Enrichment with EOsignificantly improved feed efficiency in broilers(Halle et al., 2008). Most studies have shownno significant difference in feed intake caused byherbal or EO additives, but growth was oftenenhanced and FCR rate improved. Since poultryare known to adjust feed intake strongly accord-ing to the demand of energy, FCR is therefore avery sensitive parameter in responses to growthpromoters. Published results are, however, con-tradictory. Lee et al. (2003a) fed broilers with200 mg/kg feedingstuff carvacrol or thymol.Carvacrol reduced feed intake, weight gain andfeed conversion rate, whereas thymol showed noeffect. Addition of oregano herb in quantities of2—20 g/kg feed or oregano oil (100—1000 mg/kgfeed) resulted, in contrast, in all cases in betterperformance of broiler chicks (Halle et al., 2004),whilst another trial of the same group(Westendarp et al., 2006) using carvacrol,p-cymene and g-terpinene as pure substancesin approximate 50 (carvacrol) or 25 (terpinene,p-cymene) mg/kg had almost no effect. Recently,Haselmeyer (2007) studied the effect of thymol in4 concentrations from 0.1 to 1.0% as a feedadditive in broilers. No significant difference inperformance was obtained over the whole grow-ing period (35 d). Turkeys fed with 1.25—3.75 g/kg dried oregano leaves showed, in contrast,
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a clearly improved feed conversion rate(Bampidis et al., 2005). Adding 60 mg/kg carva-crol-rich thyme oil to the diet resulted insignificantly higher body weight gain and betterfeed efficiency as well as decreased abdominal fatweight in quails (Denli et al., 2004). A dietarysupplementation of oregano EO (300 mg/kg)showed a positive effect on performance ofbroiler chickens experimentally infected withEimeria tenella (Giannenas et al., 2003).
In conclusion, the number of trials on theeffects of plant extracts on performance inpoultry is large. Recently, Windisch et al. (2008)also evaluated some of the available studies inbroilers, turkeys and quails and concluded that amajority of the studies showed a reduction in FIdue to the use of dietary plant extracts, a largelyunchanged body weight gain and as a result animprovement in FCR. However, for eachresponse parameter (feed intake, body weightgain and feed conversion ratio) differences in thequantitative response were found in differentstudies. Whether such a general statement is validis doubtful, as each plant extract or phytogenicplant compound will most likely have a differentmode of action and result in different types ofeffects on animal performance. A number ofstudies have also shown no response or a positiveeffect on feed intake and/or body weight gain. Inaddition, the experimental conditions in whichthe compounds are tested may greatly influencethe outcome of the evaluation, e.g. the nature ofthe negative control treatment, experimentalconditions with regard to health status of thebirds and/or challenges imposed to the birdsduring evaluation of the feed additives, or theconcentration of the compounds tested.Moreover, it can be assumed that there will bea publication bias in this area, meaning thatproducts or studies showing no or negativeeffects have less chance of being published in arefereed journal.
Product quality
Many plants or plant extracts contain bioactivecompounds that improve the quality of poultryproducts, including both meat and eggs. Themain quality indices of interest are organolepticproperties, storage stability and the ‘‘healthiness’’of the product for consumption by man.Although including herbs in the diet might beexpected to influence taste in particular, thereseem to be surprisingly few structured reports onthe influence of phytochemicals on the organo-leptic qualities of poultry products (Rizza et al.,2008; Windisch et al., 2008). Thus, the qualityaspects reviewed here will cover predominantlythe effects on stability and healthiness.
Antioxidants
Many plants and phytochemicals, including EOplants and EO, are known for their antioxidativeproperties based mainly on phenolic compoundsin the oil or in other phytochemical fractions.Some non-phenolic substances may show aremarkable antioxidative potential. Such sub-stances contribute to antioxidative benefits inthree respects. Firstly, they may protect feedcomponents from oxidative damage, substitutingpartly the use of �-tocopheryl acetate and relatedcompounds as feed additives or preservativesrespectively. They may also affect oxidativemetabolism in the animal: examples will begiven below. Finally, oxidative stability to alarge extent determines the shelf life of fat,meat and eggs (Botsoglou et al., 1997; Govariset al., 2005), and many plant bioactive feedadditives have been shown to benefit storagequality.
The dietary supply of thyme oil or thymolto ageing rats showed a beneficial effect on theantioxidative enzymes superoxide dismutase andglutathione peroxidase as well as on polyunsatu-rated fatty acid composition in various tissues(Youdim and Deans, 1999). Animals receivingthese supplements had higher enzyme levels andhigher concentrations of polyunsaturated fattyacids in phospholipids of the brain than theuntreated control (Youdim and Deans, 2000).Oregano EO added in doses of 50—100 mg/kgto the diet of chickens exerted an antioxidanteffect in the animal tissues (Botsoglou et al.,2002). Such antioxidant effects would beexpected to improve the health of poultrylivestock as they do in other animals, includingman.
Storage quality is generally linked to theoxidation of fats. Dietary thyme improved theoxidative stability of eggs (Botsoglou et al., 1997;Liu et al., 2009); although thymol is the EOcompound most associated with biological effectsin thyme, other components also appeared to beinvolved (Botsoglou et al., 1997). Saffron (Crocussativus L.; Botsoglou et al., 2005), oregano(Radwan et al., 2009), rosemary (Lopez-Boteet al., 1998; Florou-Paneri et al., 2006; Radwanet al., 2009), sage (Lopez-Bote et al., 1998),turmeric (Curcuma longa; Radwan et al., 2009),tea catechins (Yilmaz, 2006), mulberry leaf,Japanese honeysuckle and goldthread (Liu et al.,2009) had similar benefits to the oxidativestability of eggs. The effects of rosemary werenot seen in another study (Galobart et al., 2001).Also with rosemary and sage extracts, theconcentration of total cholesterol oxidationproducts (COPS) was reduced, and a similartrend was observed in microsomal fractionisolates in which the rate of metmyoglobin/
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hydrogen peroxide-catalysed lipid peroxidationwas lower in birds receiving these plant extractsin comparison with the control fed on basal dietonly (Lopez-Bote et al., 1998). Thus, many plantscan improve the oxidative stability aspect ofproduct quality, although the phytochemicalsresponsible have not been identified.
Lipid metabolism
Fatty acid and cholesterol metabolism in the birdis influenced by many plants and phytochemicals,leading to improvements in the fatty acidcomposition and particularly cholesterol contentof meat and eggs. Garlic is probably the bestcharacterised plant to lower the cholesterolcontent of poultry meat (Konjufka et al., 1997;Lim et al., 2006) and eggs (Chowdhury et al.,2002; Mottaghitalab and Taraz, 2004; Yalcin et al.,2006, 2007). Other plants and herbs have alsobeen reported to be beneficial in this respect,including green tea (Uuganbayar et al., 2005) ofwhich Chinese green tea was best (Uuganbayaret al., 2006), and mixed herbs (Poltowicz andWezyk, 2001). The mechanism whereby garlicdecreases cholesterol involves lower serum con-centrations of cholesterol (Horton et al., 1991;Chowdhury et al., 2002; Mottaghitalab and Taraz,2004; Lim et al., 2006; Yalcin et al., 2006), whichthen presumably limits the cholesterol availableto be taken up into muscle and eggs. The resultsof Santoso et al. (2005) suggest that Sauropusandrogynus (Katuk) extract acts in a similarmanner to garlic. Broiler chicks fed onCodonopsis lanceolata root (a plant used inKorean cuisine) showed decreased serum levelsof triglyceride, total cholesterol and low densitylipoprotein cholesterol compared to the controlgroup, and decreased triglycerides and totalcholesterol levels in liver and breast muscle.The effect appeared to be linked to biliarycholesterol excretion being increased by 15%.Whether this is a common mechanism ofproduct-cholesterol-lowering plants is not yetclear. The pattern of fatty acids in the abdominalfat of chicken was also altered by oregano oil(Wald, 2002), and dietary carvacrol loweredplasma triglycerides (Lee et al., 2003a).
Yolk colour is also a quality trait that isinfluenced by plant additives. Green teadecreased the yellowness of the yolk(Uuganbayar et al., 2005), as did mixed herbs(Poltowicz and Wezyk, 2001), while other dietaryingredients/additives, including alfalfa concen-trate, tomato powder and marigold extractincreased the colour intensity of yolk (Karadaset al., 2006). These natural additives would bepreferred over some synthetic pigments thathave been fed to poultry for many years but
which are now less acceptable to consumers(Karadas et al., 2006).
BIOACTIVE COMPOUNDS AND THEGASTROINTESTINAL ENVIRONMENT
Normal flora
Most of the gut microbiological analysis ofpoultry used in food production has been donein the broiler chicken. The two main sites ofmicrobial activity are the crop and the caecum(Smith, 1965), although microbe-host interac-tions elsewhere in the digestive tract may haveimportant consequences for health (Lan et al.,2005). Before the advent of molecular commu-nity profiling techniques, cultivation-based analy-sis indicated that the anterior part of the tract(crop, gizzard, small intestine) was dominated byfacultative bacteria, principally Lactobacillus spp.,while the caecum contained mainly strict anae-robes (Fuller, 1984). Numbers were high, up to1011 per g of digesta. More recently, terminalrestriction fragment length polymorphism (T-RFLP) analysis, also based on 16S gene sequenceanalysis, indicated that the bacterial communitiesat different parts of the gut were different, exceptwhen comparing jejunum and duodenum (Toroket al., 2008). Lu et al. (2003) confirmed thisdifference when comparing 16S rRNA genelibraries from the ileum and caecum. Theformer contained nearly 70% Lactobacillus spp.,while the latter had only 8% Lactobacillus and wasdominated by Clostridiaceae-related species. Fuller(1984) estimated that there may be more than200 species in the avian gut. Gong et al. (2002a)and Zhu et al. (2002) found that many of the 16SrRNA sequences from caecal clone libraries weredissimilar to known bacteria. The librarysequences obtained by Zhu et al. contained 40%related to Sporomusa or enteric bacteria related tog-proteobacteria, such as E. coli, a result that wasnot replicated in the other molecular studies.Smaller numbers of bacteria colonise the smallintestine, yet they represent a surprisingly diversecommunity (Knarreborg et al., 2002; van derWielen et al., 2002). A specific communitycolonises the caecal mucosa, different from thatinhabiting the lumen (Gong et al., 2002b). Allsequence analysis studies report that there arelarge numbers of unknown bacteria present(Apajalahti et al., 2001; Gong et al., 2002a,b; Luet al., 2003; Apajalahti et al., 2004). While somemight assume that these bacteria might beunculturable (e.g. Apajalahti et al., 2004), thereis no reason to suppose that they will befunctionally different to known gut species andthat they may eventually be cultured.
Both diet and age have a major influence onthe composition of the gut bacterial community.
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The first report of the effect of diet on thecommunity by molecular techniques was that ofApajalahti et al., (2001), who used a G þ Cprofiling method to demonstrate that diet hada major effect on gut composition. Even arelatively minor change in diet — the supplemen-tation of a barley diet with glycosidases — resultedin 73% dissimilarity between bacterial commu-nities in the ileum and 66% in the caecum (Toroket al., 2008). The changes seemed to occur acrossmany species, with no individual bacterial speciescontributing more than 1 to 5% of the total. Luet al. (2008) made the point that the broilershould be thought of as a young animal whosemature flora has not yet been achieved. Thecaecal and ileal communities were similar up to14 d, diverging thereafter.
Gut microbiota and productivity
How useful or harmful are the resident gutbacteria to health and productivity? Some wouldconsider that the most telling observations aboutthe role of gut microorganisms in the health andproductivity of poultry are (i) that gnotobioticand caecectomised chicken and quail chicks growbetter than their conventional counterparts(Fuller and Coates, 1983; Furuse and Yokota,1984, 1985) and (ii) that antibiotics enhancegrowth efficiency in broiler production (Grahamet al., 2007). Fuller (1984) concluded that,although bacterial glycosidases digested polysac-charides in the feed, there was no evidence of anet benefit to productivity from this activity.Indeed, he went so far as to say ‘‘In fact the neteffect of the flora is harmful’’. Vispo and Karasov(1996), on the other hand, argue that theretention in evolutionary terms of a caecummust indicate that an advantage must be con-ferred by the retention of the structure. Toroket al. (2008) state ‘‘Gut microbiota positivelyinfluence the host’s gastrointestinal develop-ment, biochemistry, immunology, physiology,and nonspecific resistance to infection’’, basingthis assertion on the review by Gordon and Pesti(1971). The review covered mainly mammalianspecies, however, with much less reference topoultry. Nevertheless, Torok et al. (2008) mana-ged, by sophisticated analysis of T-RFLP profiles,to link differences in the gut community compo-sition with improved performance (apparentmetabolisable energy), which has been a goal ofresearchers for many decades.
There are several challenges that pathogens,both acute and sub-acute, present to poultryproduction. C. perfringens, an anaerobic Gram-positive bacterium known to be a commonpathogen in humans, domestic animals and inwildlife, is the primary cause of clostridial entericdisease in poultry production. C. perfringens
associated necrotic enteritis and subclinical dis-eases are serious threats to poultry health,causing a spectrum of effects including subclini-cal infection, mild disease with focal intestinalnecrosis, diarrhoeal illness and liver disease, aswell as the classic form of acute fulminantnecrotising enteritis (Wilson et al., 2005).Necrotic enteritis is estimated to affect up to40% of the commercial broiler flocks in theUnited States and it is believed to cost the USpoultry industry about 5 USD cents per broiler(McDevitt et al., 2006). Fuller et al. (1979) foundthat the poorer growth of conventional vs. germ-free birds was due, in part, to Streptococcusfaecium. The mechanism appeared to involveadhesion to the duodenum (Fuller et al., 1981)and the deconjugation of bile salts, leading tomalabsorption of lipids (Cole et al., 1981). Theother major intestinal disease suffered by poultryis coccidiosis, caused mainly by Eimeria spp.(Kennedy, 2001). The disease is passed from birdto bird via droppings, which means that theproblem is greatest in intensive units unlessmeasures are taken to control oocyte numbers.
Immunity
The nutrient content of the diet has a majoreffect on immunity in poultry (Kidd, 2004),without reference to plant bioactives, but thereis nonetheless growing published evidence forbenefits to be obtained by incorporating plantsrich in certain phytochemicals being beneficialfor immune function in poultry (Swiatkiewiczand Koreleski, 2007). Chinese herbs in particularseem to be cited as positive for immune effects,though other plants and extracts have beenreported to be positive. We have not been ableto find a systematic account of the precisephytochemicals that might be beneficial, sowhat follows is inevitably rather disjointed:there does not appear to be a hypothesis linkingthe different plants. Immune function would beenhanced as a consequence of a more stableintestinal health favoured by feed additives, or byanimals being less exposed to microbial toxins orother undesired metabolites, for example ammo-nia and biogenic amines. Consequently, additiveslike aromatic herbs or volatile oils may relieve theanimals from immune defence stress duringcritical situations, raising the intestinal availabil-ity of essential nutrients for absorption and thus,assist the animal to grow better within its geneticpotential.
Sometimes extracts of plants, not wellcharacterised, have beneficial effect. Ethanolextracts of Allium sativum (garlic), Glycyrrhizaglabra (licorice), Plantago major (plantain) andHippophae rhamnoides (sea buckthorn) all hadsome beneficial immunological effects on cellular
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immunity in laying hens (Dorhoi et al., 2006).Polysavone, an extract of alfalfa, enhancedimmunity in broilers (Dong et al., 2007). Thephagocytic activity of peripheral blood leucocytesin chickens orally administered sugar caneextracts or a polyphenol-rich fraction of thesugar cane extract (500 mg/kg/day) for 3 con-secutive days increased significantly, when com-pared with that of saline-administered controlchickens (Hikosaka et al., 2007). Achyranthan,a low-molecular-weight Chinese herbal polysac-charide, showed immunostimulating effects inboth growth assays and in vitro studies (Chenet al., 2003).
Ligustrum lucidum and Schisandra chinensisimproved antioxidative metabolism and immu-nity of laying strain male chicks (Ma et al., 2007).Aniseed (Pimpinella anisum) used at up to 4%inclusion in laying quail diets provided beneficialeffects on immune responses, although 5%caused negative effects on feed intake and feedconversion ratio (Bayram et al., 2007). Similareffects were found in broiler chicks (Durraniet al., 2007).
Coccidiosis
Coccidiosis is the most important disease inpoultry production (Cox, 1998) causing annualcosts of more than $3 billion to the worldwideindustry as estimated by Dalloul and Lillehoj(2006). Mortality, malabsorption of nutrients,impaired growth rates and rapid and effectivetransmission between animals are characteristicof the disease, which is caused by several speciesof Eimeria. Secondary bacterial infections arefrequently observed and may further increase theseverity of the disease. In-feed medication byanticoccidial drugs has provided good protectionof flocks for decades. Emerging problems withparasite resistances and concerns about drugresidues however have stimulated the search foralternatives. Concomitantly with the ban ofantibiotic growth promoters in animal produc-tion, the European Union (EU) has put toquestion the use of coccidiostats from the year2012 onwards. The decision will have high impacton poultry production within the EU and isexpected to influence also other regions.
Coccidiosis vaccines are mostly used forbreeder and layer chickens, but hardly at all forbroilers (EC, 2008), which is the most numeroustype of chicken. Six Eimeria species are consid-ered economically relevant (Holdsworth et al.,2004), but immunity is highly species-specific andnot all species and relevant strains are includedin most commercial vaccines. To overcome theselimitations, a lot of effort is put into newstrategies for vaccine development (Dalloul andLillehoj, 2006; Shirley et al., 2007).
A summary of reported anticoccidial effectsof plants and plant extracts in poultry is givenin Table 2.
Prooxidants
Allen and Fetterer (2002) provided a compre-hensive review on various feed ingredients andtheir influence on coccidiosis. Flaxseed, flaxseedoil and corn oil, which contain high amounts ofpolyunsaturated fatty acids (PUFA), reducedlesions caused by the chicken parasite Eimeriatenella, but not lesions caused by Eimeria maxima(Allen and Fetterer, 2002; Yang et al., 2006).Artemisinin, a naturally occurring antimalarialcompound, significantly lowered lesions (Allenand Fetterer 2002) and reduced oocyst output(Arab et al., 2006) from E. tenella when given atlow levels as a feed additive. The mechanisms ofaction of PUFA as well as artemisinin areassumed to involve induction of oxidative stressto the parasites. However, there might bepractical difficulties in including sufficientamounts of PUFA for protection in the diets,also due to antioxidative ingredients which areusually included in feed, as studies by Allen et al.(2000) have shown. Furthermore, this mode ofaction seems to be effective against E. tenella,which is adapted to the specifically anaerobicconditions of the caeca, but not so much againstother Eimeria species.
Antioxidants
Diets supplemented with g-tocopherol, with thespice turmeric or curcumin, which all possessantioxidative properties, reduced small intestinallesion scores and improved weight gains duringE. acervulina and E. maxima infections (Allen andFetterer, 2002). Antioxidative activity is alsosuggested as the mode of action of variousSouth African plant species investigated byNaidoo et al. (2008). Tulbaghia violacea showedimproved FCR and lowered oocyst output duringa mixed Eimeria challenge. Green tea reducedoocyst shedding after an E. maxima infection, butno beneficial effects on weight gain weredetected (Jang et al., 2007). Wang et al. (2008)reported beneficial effects of grape seedproanthocyanidins by counteracting weight loss,mortality and lesion scores and lowering oxida-tive stress in intestinal tissues. All these com-pounds may exert their anticoccidial activityby protecting infected tissues from oxidativedamage and therefore reducing the severity ofcoccidiosis. Similar to compounds causing oxida-tive stress, the effect of antioxidants seems tobe restricted to certain Eimeria species only,especially E. acervulina and E. maxima (Allen andFetterer, 2002).
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Essential oils
Amelioration of coccidiosis was observed whensupplementing commercial feed additives con-taining oregano EO (Giannenas et al., 2003;Batungbacal et al., 2007) or ground aerial partsof oregano (Giannenas et al., 2004). Both
applications protected significantly from weightloss or improved feed efficiency and reducedoocyst output and lesion scores in a coccidiosischallenge. Improvement of the negativeimpact of coccidiosis was also reported forsupplementation with Olympus tea (Sideritis
Table 2. Plants and plant extracts with anticoccidial activity
Plant species/extract Scientific name Activity/Mode of action Literature
Flaxseed meal, flaxseed oil,n-3 fatty acids
Linum usitatissimum E. tenella (not E. maxima) lesions,parasitation, development.Induction of oxidative stress
Allen et al. (1998, 2000), Allen andFetterer (2002)
Corn oil Zea mays E. tenella body weight, higher IgA,lower plasma carotenoids,
Yang et al. (2006)
Artemisia annua dried herb,Artemisinin, 1,8-Cineol,Camphor, A. sieberi pet-roleum ether extract ofaerial parts, A. afraacetone/water extractfrom aerial parts
Artemisia annua,A. sieberi. A. afra
E. tenella lesions, oocyst output,E. acervulina oocyst output.(not E. maxima) Induction ofoxidative stress. Eimeria mix(Eten, Emax, Eace): FCR. 1,8-cineol and camphor: weightgain, lesions
Allen et al. (1997,1998), Allen andFetterer (2002), Arab et al.(2006), Naidoo et al. (2008)
Sophora flavescens rootdecoction
Sophora flavescens E. tenella weight gain, mortality,bloody diarrhoea,
Allen and Fetterer (2002), Younand Noh (2001)
Turmeric spice rhizome,Curcumin
Curcuma longa E. maxima lesions, weight gain.E. acervulina (not E. tenella)Antioxidative
Allen et al. (1998), Allen andFetterer (2002)
g-Tocopherol e.g. from Linum usi-tatissimum, var-ious seed oils
E. maxima lesions, weight gain.E. acervulina (not E. tenella).Antioxidative
Allen et al. (2000), Allen andFetterer (2002)
Betaine e.g. from sugar beet(Beta vulgaris ssp.vulgaris var.altissima)
E. acervulina (and E. tenella, butless effective) invasion anddevelopment when used incombination with salinomycin.E. maxima weight gain (notE. tenella, E. acervulina)
Allen et al. (2000), Allen andFetterer (2002), Fetterer et al.(2003), Klasing et al. (2002),Waldenstedt et al. (1999)
Oregano aerial parts andessential oil (containingcarvacrol and thymol)
Green tea leaves Camellia sinensis E. maxima oocyst output Jang et al. (2007)Oriental plum, Japanese
plumPrunus salicina E. acervulina body weight gain,
OPG, IFN-g and IL-15(mRNAs) of IEL, spleen cellproliferation. Phenolics,antioxidants,
Lee et al. (2008)
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scardica; Florou-Paneri et al., 2004). The EOconstituents 1,8-cineole and camphor, fromArtemisia annua protected weight gain andreduced E. tenella as well as E. acervulina lesions(Allen and Fetterer, 2002).
Various other plants/products
Youn and Noh (2001) tested 15 therapeuticplants against an E. tenella challenge and founda root decoction of Sophora flavescens to be mostactive in protecting weight gain and reducingmortality and bloody diarrhoea. Moreover, asugar cane extract had protective effects wheninoculated in the crop of chicken simultaneouslywith a challenge. Body weight gain, haemor-rhages, oocyst output, lesion scores and antibodyresponse were improved (El-Abasy et al., 2003).Betaine, an osmoprotectant ubiquitous amongplants, enhanced the activity of anticoccidialdrugs in some cases (Allen and Fetterer 2002;Fetterer et al., 2003), but failed to do so in others(Waldenstedt et al., 1999). Apparently, its effectis restricted to certain Eimeria species only.
Immunomodulation
Immunomodulatory effects are assumed to beresponsible for protection by plum powder(Prunus salicina) against an E. acervulina chal-lenge (Lee et al., 2008). Body weight gain, oocystshedding, IFN-g and IL-15 levels were signifi-cantly improved. Furthermore, Guo et al.(2004a,b) found enhanced cellular and humoralimmune responses of E. tenella-infected chickenswhen supplementing a polysaccharide extractfrom Astragalus membranaceus, which maybecome particularly interesting when used inconjunction with vaccination.
Future perspectives
In summary, plants and products derived thereofhave clearly shown the potential to alleviatecoccidiosis and reduce its severity in severalstudies. Moreover they might play a role incounteracting subclinical infections and second-ary bacterial infections associated with thedisease. Most of the active plant materials couldimprove some, but not all of the relevantparameters in coccidiosis and variable effective-ness against the different Eimeria species wasobserved in some cases. To date, no alternative toanticoccidial drugs is yet known with comparableefficacy and economy of use in broiler produc-tion, and a recently published EC report stronglyrecommends to maintain the actual status ofso-called ‘‘coccidiostatic drugs’’ as feed additiveswithin the EU (EC, 2008). Nevertheless, plantproducts may have increasing significance in
organic farming, whenever antibiotic-free rearingof animals is desired, as supporting agent forvaccination (adjuvants), or in combination withconventional anticoccidial drugs, especially in thelight of possible bans or reduction of approveddrugs in large economies like the EU. This shouldbe a great incentive for stimulating research inthe field of alternatives to conventional antic-occidial drugs in general and especially on therole of plants and plant products.
Difficulties in comparing research data arisefrom the use of different experimental modelsand different strains of Eimeria. Parasite strainsare known to possess variable virulence and maycause variable severity of challenge in differentexperiments. An important effort to harmonisetechniques in coccidiosis research and models forevaluation of drug efficacy against coccidiosiswas taken in the course of the COST 89/820programme and by Holdsworth et al. (2004).Guidelines for efficacy testing are also publishedby regulative authorities, e.g. the recently pub-lished EFSA ‘‘guidance for the preparation ofdossiers for coccidiostats and histomonostats’’(EFSA, 2008). Such guidelines should also betaken into consideration when alternatives toanticoccidial drugs are investigated in orderto provide sound and comparable scientificresults.
Necrotic enteritis
Necrotic enteritis (NE) is a disease in poultrycausing high economic costs and seriouslyimpairs animal welfare. Due to the ban on sub-therapeutic antibiotic usage, NE has becomeincreasingly prevalent in the EU. Demands forsafer food have put pressure on the developmentof alternative management or dietary strategiesto control this disease. C. perfringens, a Gram-positive, anaerobic, spore-forming toxigenic bac-terium is found in soil, dust, faeces, feed andpoultry litter and has been identified as the maincausative agent causing NE in poultry (Brantonet al., 1997; Annett et al., 2002; Dahiya et al., 2006;McDevitt et al., 2006). C. perfringens is principallya normal inhabitant of the chicken intestine butunder certain circumstances it can begin toproliferate rapidly, accompanied by increasedtoxin production causing the intestinal mucosalnecrosis characteristic of NE (Branton et al.,1997; Collier et al., 2003; Dahiya et al., 2005,2006). However, even high doses of C. perfringensin the intestinal tract of broiler chickens do notalways lead to the development of NE, as the gutflora of healthy birds can apparently preventits pathogenicity (Fukata et al., 1991). Variouspredisposing factors, among them dietary com-position and incidence of coccidiosis (Williams,2005), may lead to over-proliferation of
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C. perfringens, and the subsequent progression todisease is still poorly understood. Host specificvirulence factors like production of �-toxin areassumed to play a role, and recent findings pointtowards the importance of the netB gene,necessary for the production of the respectivetoxin (NetB) (Keyburn et al., 2006; Chalmerset al., 2008; Timbermont et al., 2008). However,control of C. perfringens seems to be essential anddietary ingredients have a great influence on theincidence of NE in broiler chickens.
Reports of the effects of plants and theirextracts on mainly avian C. perfringens aresummarised in Table 3. Dahiya et al. (2006)reviewed the potential of plant-derived feedingredients to control C. perfringens and NE.Numerous plants and plant products have beenfound to possess inherent antimicrobial activityagainst clostridia, although mostly their effectswere only determined in vitro. Oregano, blackpepper, cloves and the EO components carvacroland eugenol possess antibacterial activity againstclostridia as well as E. coli, Staphylococcus aureusand Salmonella pullorum. Furthermore, lemonmyrtle (Wilkinson et al., 2003), Artemisia princepsvar. orientalis (Cho et al., 2003), Hypericumscabrum (Sokmen et al., 1999) and Aristolochiapaucinervis (Gadhi et al., 1999) displayedin vitro activity against C. perfringens and otherbacteria.
Reports on in vivo investigations are scarce:according to Dahiya et al. (2006), supplementa-tion of flaxseed may have benefits by modifica-tion of intestinal microbial colonisation.Linolenic acid, the main constituent of flaxseedfatty acids, may prevent the adhesion of bacteriato intestinal epithelial cells and mucus, whereasaddition of pectin and guar gum to diets hasreportedly eliminated NE from sick birds.Specific blends of EO components like thymol,carvacrol and eugenol (Mitsch et al., 2004) aswell as astaxanthin from the microalgae,Haematococcus pluvalis, were found to be effectivein controlling C. perfringens colonisation andproliferation in the gut of broilers (Waldenstedtet al., 2003). Finally, lupulone from hops, whenadministered in drinking water, inhibitedproliferation of artificially inoculated C. perfrin-gens in the chicken gastrointestinal tract (Siragusaet al., 2008).
Escherichia coli
Escherichia coli is the most common bacterialpathogen of poultry and responsible for signifi-cant losses in the world’s industry. Although ourunderstanding of pathogenicity has increased inthe past years, the virulence factors (genes) whichlead to disease remain to be fully unravelled (LaRagione and Woodward 2002). For practical
reasons, E. coli isolated from diseased chickenare termed avian pathogenic E. coli (APEC).Colisepticaemia or colibacillosis manifests itselfmost commonly as an infection of the respiratorytract, in rare cases also as enteritis. E. coli arecommon inhabitants of poultry intestinal micro-biota, thus the gastrointestinal tract is seenas a possible reservoir for infection (Ewerset al., 2009) and incidence of the disease mightbe reduced by keeping intestinal E. colinumbers low.
Reports of the effects of plants and theirextracts on APEC are summarised in Table 3.There are numerous studies on in vitro effective-ness of plant-derived extracts and compounds, aswell as EO against (avian) E. coli (Smith-Palmeret al., 1998; Penalver et al., 2005b,c,d; Fisher andPhillips 2006; Horosova et al., 2006; Prakash,2006; Geidam et al., 2007). EO containing a highpercentage of phenolic components (e.g.carvacrol and thymol) show higher inhibitorycapacity compared to the oils containing, forexample, the monoterpenic alcohol linalool(Penalver et al., 2005a). However, literaturesupporting actual in vivo activity is scarce. Analternative strategy to suppress intestinal E. colimight involve preventing their adhesion to theintestinal mucosa. This may be achieved byfeeding compounds which increase mucus pro-duction, thus reducing the possibility of bacterialadhesion to the intestinal epithelium. A mixtureof cavracrol, cinnamaldehyde and capsaicincaused the release of large amounts of mucuson glandular stomach and wall of jejunum inchickens when incorporated into their diets(Jamroz et al., 2006). Becker and Galletti (2008)exploited the ability of E. coli to adhere tomannose receptors and mannose-containinganalogues to find food and feed componentswith gut health-promoting effects. Out of 18dietary components tested, artichoke and sesameseed extracts performed well in bindingvarious E. coli strains. Sesame seed extract wasalso most effective in binding chicken Salmonellaisolates.
Antiviral effects
Although a vast range of plants possess antiviralactivity (Jassim and Naji, 2003), they are probablyunderexplored and underutilised for this pur-pose in poultry farming. Actually, the mostimportant viral diseases are sought to be con-trolled by vaccination. A polyphenolic extractfrom Geranium sanguineum aerial roots and anextract of the red marine alga Ceramium rubrumshowed excellent in vitro inhibition of humanand chicken influenza A viruses (Serkedjievaand Hay, 1998). The very scarce animal trialscomprise sulfated Astragalus polysaccharides
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(Huang et al., 2008), Ocimum sanctum and leaf gallsof Ficus racemosa (Kolte et al., 1999), which showedeffects against infectious bursal disease (IBD) andAloe secundiflora, which reduced mortality andseverity of clinical signs during a NewcastleDisease infection (Waihenya et al., 2002b).
Zoonotic infection
Of major concern to consumers are the hazardspresented by zoonotic infection from contami-nated poultry meat. Campylobacter spp. is thegreatest hazard in terms of numbers of infectionsand days lost through illness (Friedman et al.,
Table 3. Plants with activity against Escherichia coli and Clostridium perfringens
Plant species/extract Scientific name Activity/Mode of action Literature
Flaxseed, linolenic acid Linum usitatissimum Prevents adhesion of pathogenic bacteria Dahiya et al. (2006)Guar gum, pectin Cyamopsis
tetragonolobusUnknown Dahiya et al. (2006)
Thymol, carvacrol andeugenol
Inhibit C. perfringens colonisation andproliferation
Dahiya et al. (2006), Mitschet al. (2004)
Turmeric, EO fromrhizome
Curcuma longa Inhibits C. perfringens Dahiya et al. (2006)
Eugenol, EO from clove Syzygium aromaticum Inhibits C. perfringens Dahiya et al. (2006)Astaxanthin, from red
algaeHaematococcus
pluvalisInhibits C. perfringens caecal
colonisationWaldenstedt et al. (2003)
Lupulone, from hops Humulus lupulus Inhibits intestinal C. perfringens Siragusa et al. (2008)Lemon myrtle, leaf paste Backhousia citriodora Inhibits C. perfringens (in vitro) Wilkinson et al. (2003)Japanese mugwort, seco-
tanapartholidesArtemisia princeps
var. orientalisInhibits C. perfringens (in vitro) Cho et al. (2003)
Hypericum, acetoneextract from aerial parts
Hypericum scabrum Inhibits C. perfringens (in vitro) Sokmen et al. (1999)
Aristolochia paucinervis,defatted chloroformextract of rhizome
Aristolochiapaucinervis
Inhibits C. perfringens (in vitro) Gadhi et al. (1999)
Oregano, EO Origanum vulgare Bactericidial effect Horosova et al. (2006)Agave, extract Agave picta Inhibits C. perfringens (in vitro) Verastegui et al. (1996)Paper daisy, petroleum
ether and ethanolextracts of flowers
Helichrysum sp. Growth inhibition of various Helicobacterspecies
Prevents adhesion of of E. coli Jamroz et al. (2006)
Lemon, EO Citrus limon Growth inhibition by the disc diffusionmethod
Fisher and Phillips (2006)
Sweet orange, EO Citrus sinensis Growth inhibition by the disc diffusionmethod
Fisher and Phillips (2006)
Bergamont, EO Citrus bergamia Growth inhibition by the disc diffusionmethod
Fisher and Phillips (2006)
Shiitake, extract Lentinus edodes Increases the number of desirable bac-teria in order to inhibit colonisationof invading pathogens
Guo et al. (2004c)
White jelly, herb polysac-charide extract
Tremella fuciformes Increases the number of desirable bac-teria in order to inhibit colonisationof invading pathogens
Guo et al. (2004c)
Huang Qi, herb polysac-charide extract
Astragalusmembranacea
Increases the number of desirable bac-teria in order to inhibit colonisationof invading pathogens
Guo et al. (2004c)
Spanish origanum, EO Coridothymuscapitatus
Antimicrobial activity Penalver et al. (2005)
Thyme, EO Thymus mastichinia Antimicrobial activity Penalver et al. (2005)Geranium, EO from steam
distillationPelargonium sp. Partly greater efficacy against E.coli than
commercial thyme oilPenalver et al. (2005)
Guava, aqueous extract Psidium guajava Prevents adhesion of of E. coli Geidam et al. (2005)Artichoke Cynara cardunculus
var scolymusAdhesion of E.coli (in vitro) Becker and Galletti (2008)
Sesame seed extract Sesamum indicum Adhesion of E.coli (in vitro) Becker and Galletti (2008)Palm kernel, extract Aracaceae elais Adhesion of E.coli (in vitro) Becker and Galletti (2008)Tomato Solanum lycopersicum Adhesion of E.coli (in vitro) Becker and Galletti (2008)Betel pepper, aqueous
extractPiper betel Inhibition zone in agar gel plates Prakash (2006)
Senna, aqueous extract Cassia auriculata Inhibition zone in agar gel plates Prakash (2006)
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2000). However, the infection is usually short-term and self-limiting. Campylobacter jejuni readilycolonise the gastrointestinal tract (GIT) ofpoultry, without causing any disease in the hostbirds. The principal site of colonisation is thelower GIT, especially the caeca, large intestineand cloacae (Beery et al., 1988; Stern et al., 1988).Campylobacters do not adhere to the intestinalsurface but are highly motile and rapidly trackalong intestinal mucus, preferentially withincaecal and cloacal crypts (Beery et al., 1988).Commercial broiler flocks rarely start sheddingCampylobacter before 2 weeks of age however,when shedding occurs, Campylobacter is spreadrapidly throughout the flock (Corry and Atabay,2001; Mead, 2002; Newell and Fearnly, 2003).Until now, the main approaches evaluated forhandling the Campylobacter problem in practiceinclude hygienic barriers, diagnostics at the flocklevel, competitive exclusion, decontaminationand intervention efforts targeting the lower GIT(Hariharan et al., 2004). Despite major efforts,however, there are currently no really successfulstrategies for reduction or elimination of C. jejunifrom the food chain. Salmonella infections in manthat result from the consumption of poultryproducts are less numerous, but much moresevere. Human infection by two common sero-vars, S. enteritidis and S. typhimurium usually occursvia food-borne transmission. Consumption of rawor undercooked contaminated eggs usually causesS. enteritidis infection, while S. typhimurium istransmitted by contaminated chicken meat (Babuand Raybourne, 2008). Dietary interventions,including fatty acid modifications, probiotic orprebiotic treatment have been investigated (Babuand Raybourne, 2008), but our understanding ofconditions that lead to the proliferation of thesezoonotic bacteria is patchy (Mead, 2004).
Antibiotic growth promoters, now bannedin Europe but still permitted elsewhere, are soeffective that their withdrawal has caused majordifficulties in poultry production (Casewell et al.,2003). But how do they achieve that growthpromotion? Is it due to the suppression of majorpathogens like C. perfringens? Or sub-pathogenicspecies like S. faecium? Or is it due simply to adecreased bacterial load (Windisch et al., 2008),or perhaps due to the anti-inflammatory effectsof AGP via the inhibition of production andexcretion of catabolic mediators by intestinalinflammatory cells (Niewold, 2007)? Finding theanswer to these questions is vital, because with-out that knowledge it will be difficult to selectphytochemical replacements for AGP. Molecularecological analysis described changes in themicrobiota in response to bacitracin-virginiamy-cin (Lu et al., 2008), but other than a decreasedcommunity diversity in birds receiving the GPA,it was difficult to explain why production benefits
should occur. Indeed, the decreased numbers ofLactobacillus contradicted the usual perception ofthese being beneficial bacteria, the basis of theiruse as probiotics (Fuller, 1989).
SPECIFIC PLANT BIOACTIVES
Acamovic and Brooker (2005) estimated thatplants produced around 5100 different second-ary compounds (Figure). One of the mostcommon problems of research performed usingplant extracts in poultry nutrition has been thepoor characterisation of the plant material orextracts and their standardisation. In many cases,the identity or concentration of active principlehas been generally unknown. Due to the possiblevariation in plant material under differentenvironmental conditions, harvest time, dryingand storage conditions, repetition of the experi-ments is generally impossible to identify them.This is probably why different results areobtained in independent experiments evenwhen using the same plant species. Thus, thedevelopment of analytical methods and theproper standardisation of the material used forfeeding is crucial if the benefit of the knowledgeis to be maximised. Moreover, feeding experi-ments have often been performed using negativecontrols only. To be able to compare data fromdifferent experiments, the commonly acceptedGPA might be recommended as a positivecontrol. The effects of some of the mostcommon categories of plant bioactives and theirphysiological mode of action are described infollowing sections.
Essential oils
EO are steam-volatile or pressed-volatile (e.g.citrus extracts) extracts of plants, used tradition-ally by man for many centuries for the pleasantodour of their essence, their flavour, or theirantiseptic and/or preservative properties.Although commonly thought of as being derivedfrom herbs and spices, they are present to somedegree in many plants for their protective roleagainst bacterial, fungal or insect attack. Theycomprise mainly cyclic hydrocarbons (monoter-penes) and their alcohol, aldehyde or esterderivatives (Figure). EO appear as feed additivesin the form of the EOs themselves, or as EO-richplants, or as pure compounds, sometimes syn-thetic or ‘‘nature-identical’’.
The number of papers published on the useof EO and especially those containing thephenolic compounds carvacrol and thymol hasincreased dramatically over the last few years.The majority report, however, on productionparameters (feed uptake, feed conversion, weight
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gain) only. Comparatively little information isgiven on their mode of action, metabolism orgenerally on science based functionality due tothe fact that many reports deal with results ofcommercial products, avoiding statements onpharmacological effects or health claims.
EO used as feed additives for broilerswere shown to enhance activities of trypsin, ofamylase in tissue homogenates of pancreas, aswell as the jejunal chyme content (Lee et al.,2003b; Jang et al., 2004). A mixture of carvacrol,cinnamaldehyde and capsaicin also stimulatedthe intestinal secretion of mucus. Jamroz et al.(2006) stated that the increased release of largeamounts of mucus and the creation of a thicklayer of mucus on glandular stomach andjejunum wall in chicks fed with the above mixturecould be responsible for the reduced adherenceof pathogens (E. coli, C. perfringens and others) tothe gut epithelium. This confirms — as alreadyknown from human nutrition physiology(Teuscher, 2003) and phytopharmacology(Hansel and Sticher, 2004) — the mode of actionof spices and EO on gut function, namely that itinvolves at least partly an irritation of theexposed tissues and leading to higher secretionof mucus and enzymes.
In general, antimicrobial activity of EO andEO compounds, whether bacteriostatic or bacter-icidal, or against other microorganisms likefungi, protozoa or food-borne pathogens, iswell documented (Smith-Palmer et al., 1998,Dorman and Deans, 2000; Chao et al., 2000;Burt, 2004; Si et al., 2006). Most active in thisrespect are the phenolic compounds carvacrol,thymol and eugenol but also other substances,including phenylpropane, limonene, geraniol orcitronellal, may be involved (Deans and Ritchie,1987; Pauli, 1994).
The action of EO compounds as antimicro-bials occurs via at least two separate mechanisms.The first is by rapidly depleting the intracellularATP pool, through inhibiting ATP synthesis asa result of their effects on the transmembraneelectrical potential. The leakage of ions such aspotassium and phosphate out of the cell indicatesclearly the membrane damage resulting indisturbances of the osmotic pressure of the cells(Ultee et al., 1999; Lambert et al., 2001;Veldhuizen et al. 2006). Furthermore, changesin the fatty acid composition of bacterial cellmembranes have been observed at sublethaldoses of several EO compounds (Di Pasquaet al., 2006). A second growth-inhibitory mechan-ism is that substances like carvacrol prevent thesynthesis of flagellin, causing bacterial/cells to beaflagellate and therefore nonmotile. Such cellsare significantly less able to adhere to epithelialcells, which renders bacteria non-infective (Burtet al., 2007), a mechanism similar to that known
from acid galacturonides in the diet(Guggenbichler et al., 2004). The anti-flagellateactivity of EOs obtained from fresh leaves ofCinnamomum aromaticum, Citrus limon pericarpsand Allium sativum bulbs was investigated in vitroon Tetratrichomonas gallinarum and Histomonasmeleagridis with positive results (Zenner et al.,2003).
As EOs comprise a large number of compo-nents, it is likely that their mode of actioninvolves several targets in the bacterial cell.The hydrophobicity of EOs enables them topartition in the lipids of the cell membrane andmitochondria, rendering them permeable andleading to leakage of cell contents. Physicalconditions that improve the action of EOsinclude low pH, low temperature and lowoxygen levels. Synergism has been observedbetween carvacrol and its precursor p-cymeneand between cinnamaldehyde and eugenol (Burt,2004). Thus, extrapolating from the effects ofsingle EO compounds to the effects of mixturesmust be done with caution.
In vitro antimicrobial activities have beenmeasured with a number of EOs and singlecompounds mainly against enteropathogenicstrains of E. coli, Salmonella sp., Cl. perfringensand others. Using either the broth microdilutionmethod or the agar diffusion test, EOs with ahigher percentage of phenolic compoundsshowed the best inhibitory capacity in terms ofMIC (minimum inhibitory concentration; Jugl-Chizzola et al., 2005; Penalver et al., 2005; BenArfa et al., 2006). The combination of oreganoEO with fluoroquinolones, doxycycline, lincomy-cin, and maquindox florfenicol to treat infectionscaused by ESBL-producing E. coli were reportedto lower, to a great extent, the effective doseof these antibiotics and thus minimise the sideeffects of antibiotics (Si et al., 2008). Differenceshave been observed, however, in the activities ofplant species and plant parts on one side and thesensitivity of species and strains of the micro-organisms on the other. This is due to the varyingchemical composition of the used plant material(chemotype, morpho- and ontogenetic variation),a factor quite often neglected in microbiologicalor animal studies. The in vitro active concentra-tions exceeded furthermore in general the diet-ary doses accepted by the animals, which resultsin few studies being available so far demonstrat-ing the efficacy of EO compounds againstspecific pathogens in vivo.
Some studies with poultry showed a clearreduction of C. perfringens in the jejunum andcaecum of broilers fed with a mixture of EOcomponents (Losa and Koehler, 2001; Mitschet al., 2004). The same blend of components aswell as oregano oil or crude drug was effectiveagainst Eimeria ssp. infections in broilers, thus
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reducing the application of coccidiostats(Giannenas et al., 2003, 2004; Oviedo-Rondonet al., 2005, 2006). The components of Artemisiaannua, camphor and 1,8-cineole, at 119 mg/kg,also protected weight gains, and reduced E.tenella lesion scores. Camphor decreased E.acervulina lesions (Allen et al., 1997, 1998).Carvacrol, cinnamaldehyde, oregano oil andthymol also inhibit C. perfringens spore germina-tion and outgrowth in ground turkey duringchilling. Cinnamaldehyde was significantly moreeffective than the other compounds at a lowerconcentration (0.5%) at the most abusive chillingrate evaluated (Juneja and Friedman, 2007). Astudy to test the efficiency of carvacrol, thymol,trans-cinnamaldehyde and tetrasodium pyropho-sphate on the radiosensitisation of E. coli andSalmonella typhi in chicken breast demonstratedthat these active compounds helped reducesignificantly the numbers of E. coli and S. typhi(Lacroix et al., 2004). A combined administrationof Lactobacillus fermentum and EOs of Origanumvulgare and Thymus vulgaris decreased the per-centage of crop, caecum, liver and spleencolonisation by Salmonella enterica var. dusseldorfin chicks when compared to the control groupwithout any treatment (Koscova et al., 2006). In astudy to test the effects of the antibioticavilamycin and anise oil supplementation onbroilers’ body weight, including carcass charac-teristics and organoleptic analysis of meat, it wasconcluded that anise oil, at a dose of 400 mg/kg,can be used as an alternative to antibiotics forgrowth promotion in broiler diets (Simseket al., 2007).
It is sometimes assumed or implied thateffects of the inclusion of aromatic herbs in thediet will be caused by the terpenes that comprisetheir EO. Cross et al. (2007) demonstratedthat this need not always be true: thymeand yarrow had different effects on broilerperformance to their corresponding EO.With oregano, marjoram and rosemary, theeffects were similar.
Two further antimicrobial benefits can the-oretically be achieved by adding EO to animalfeed: the reduction of feed microbial load andthe improvement of the microbial hygiene of thecarcase (Aksit et al., 2006). The number ofreports in this area is, however, much too limitedto draw conclusions.
Tannins
Tannins comprise a complex mixture of higherplant, water-soluble polyphenolic compounds ofvarying molecular masses that have the ability toreact with proteins, polysaccharides and othermacromolecules. They tend to be consideredantinutritional, because they decrease the
digestibility and metabolisable energy of feedsthrough direct interaction with proteins andcarbohydrates from both exogenous and endo-genous sources. In ruminants, tannins may beuseful in limiting protein degradation in therumen, thereby permitting more dietary aminoacids to flow to the abomasum (McSweeney et al.,2001). In poultry, contrastingly, growth is sup-pressed by vegetable tannins (Ahmed et al.,1991). Amino acid absorption is compromisedby tannins, especially of methionine, histidineand lysine (Mansoori and Acamovic, 2007). Hightannin extracts did not alter the mortality ofchickens, however they reduced the absorptionof minerals such as calcium, magnesium, potas-sium, sodium and phosphorus from the feed(Hassan et al., 2003). In another experimenttannins extracted from Vicia faba seeds increasedmortality, reduced body weight, feed intake andpoorer feed conversion ratio (Ortiz et al., 1994)as well as decreased the digestibility of proteinand the activity of digestive enzymes (Yuste et al.,1992). There do not seem to be reports ofbeneficial effects of tannins in poultry.
Saponins
Some research has been performed on theapplication of plant saponins to poultry produc-tion, the compounds being recognised as naturaldetergents. Extracts from two saponins-richplants, Yucca schidigera and Quillaja saponaria(Cheeke, 2000; Yeo and Kim, 1997; Preston et al.,1999), had no clear effect on broiler chickperformance. Some effects, like increased foodintake, body weight gain and energy utilisationwere reported in one experiment (Preston et al.,1999), while in another the feed intake was notaffected when a 0.2% concentration of theextract was incorporated (Yeo and Kim, 1997).It should, however, be made clear that the claimthat it is the saponins present in Yucca or Quillajaextracts that are responsible for their positiveeffects has not been justified. These extracts aresimply condensed juice pressed from the trunk,in which saponins are one of the dominantgroups of compounds present in this matrix.Polysaccharides are also abundant, and theirinfluence on nutritional parameters cannot beneglected. Structurally undefined saponins(75 mg/kg/day) showed positive effects ongrowth and carcase quality (Miah et al., 2004),while Balanites aegiptica kernel saponinstended to reduce body weight in chicks(Nakhala et al., 1992).
Betaine
Although betaine is a generic description of atype of zwitterionic chemical compound, the
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term used in poultry nutrition refers to a plantextract or a feed additive containing one parti-cular betaine, namely trimethyl glycine. Thisreview covers the effects of betaine only summa-rily, because a comprehensive review of betaineand poultry was published very recently (Metzler-Zebeli et al., 2009). Betaine is an osmoprotectantpresent in all plants and particularly abundant insugar beet and its byproducts. Benefits from itsuse as a feed additive include the prevention ofheat stress and inhibition of Eimeria parasiticinfection, both presumably due to the ionicnature of the molecule. Its methyl groups arethought also partly to substitute other methylgroup donors such as methionine and choline.Both modes of action lead to improved nutrientdigestibility and growth performance.
Other plant bioactives
A large group of phytochemicals that are widelydistributed in plants is phenolics. Among these,the flavonoids (Figure) are the group which hasbeen indicated as possibly most beneficial forpoultry performance. The addition to feed of300 mg/kg of flavonoids (rutin, hesperidine,quercetin and naringenin) together with manna-noligosaccharides (MOS) had a significant stimu-latory effect on feed conversion ratio (Batistaet al., 2007). Additionally there was lower meatoxidation both after refrigeration and freezingwhen birds were fed flavonoids þ MOS, whichmay be attributed to antioxidant effect offlavonoids; quercetine and hesperidine are con-sidered the strongest antioxidants of the flavo-noid family (Burda and Oleszek, 2001). Extractscontaining isoflavones significantly increasedserum testosterone levels in male chickens anddecreased serum uric acids and abdominal fat(Zhengkang et al., 2006). Supplementation withdaidzein (3 mg/kg/day) significantly increasedlaying rate, average egg weight and eggcholesterol level in laying hens and ducks(Wang et al., 1994).
Other phenolics of interest in poultry feedsupplements are catechins and their complexes,proanthocyanidins, flavolignans, tannins andphenolic acids. Green tea (Camellia sinensis)extract containing catechins and their gallatesminimised hyperlipidemia and oxidative stressinduced by corticosterone treatment in broilerchickens (Eid et al., 2003). Tea also acts as anantioxidant in meat storage. Silimarin, the poly-phenolic extract from Silybum marianum andCynara cardunculus containing flavolignans,which are strong antioxidants protecting theliver from toxins and pollutants by preventingfree radical damage, was fed in broiler chickensat rates of 40 and 80 mg/kg. The treatment withsilimarin had no effect on growth performance
and had no specific haematoprotective effect,but slightly decreased slaughter yields. The lipidcontent of breast and thigh was decreased andthe resistance of muscles to oxidative stressincreased under this treatment (Schiavone et al.,2007). Moreover it was shown that silimarinphytosome can provide protection against thenegative effects of aflatoxin B1 in broiler chicks(Tedesco et al., 2004). Similarly, it protectsagainst pollutants such as carbon monoxide,pesticides and herbicides, by breaking themdown from potentially lethal substances intothose that are less destructive to the humanbody. Polyphenol rich grape pomace (peels andseeds) added at the rate of 5—30 g/kg of dietreduced the lipid oxidation in meat duringrefrigerated storage and increased liver �-toco-pherol concentration (Goni et al., 2007). Grapeseed extract in the rate of 2.59—5.28% of the feedreduced post mortem development of thiobarbi-turic acid reactive substances in dark poultrymeat but had also detrimental effect on the bodyweight gain (Lau et al., 2003).
Extracts from sage, thyme and rosemary(5000 mg/kg), rich in rosmarinic acid, anothernatural antioxidant, had no influence on feedintake and feed conversion, but from 14 to 21 dof age broilers grew faster and improvedapparent whole tract and an improved ilealdigestibility of nutrients was observed(Hernandez et al., 2004).
An alcohol extract of Propolis (honey beeglue) containing polyphenols used at the rate of50—250 mg/kg diet significantly increased aver-age weight gain, feed consumption and feedefficiency in broiler chicks. The mortality ratedetermined after 21 d of growth was decreasedas compared to the control diet (Khojasteh andShivazad, 2006).
CURRENT RESEARCH PROJECTS
The global trend to move away from in-feedantibiotics and coccidiostats has strengthenedsince 2006, when the use of GPA was bannedwithin the EU member states. Therefore researchgroups and poultry industries worldwide aresearching to develop alternatives. Some haveperformed clinical trials with herbal feedadditives.
At present different herbal preparations inpoultry feeding are examined for their antibac-terial, antiparasitic, antioxidative and/or otherhealth and performance promoting propertieslike feed intake, feed conversion, body weight,weight gain, growth performance, feedconversion ratio, gizzard function, gut develop-ment, nutrient digestibility, digestibility oforganic matter and crude protein, gut microflora
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or content on metabolisable energy of feedmixture.
For example at this time in Austria somecompanies are working in these fields: RichterPharma AG www.richter-pharma.at, DelaconPhytogenic Feed Additives www.delacon.com,Indian Herbs GmbH www.indianherbs.at andBiomin AG www.biomin.at. They are conductingclinical trials in feeding herbal additives todifferent poultry, e g. laying hens, broilers andturkeys. In Australia, PRATU (Poultry Researchand Teaching Unit, www.poultryhub.org) isinvolved in many aspects of poultry scienceincluding nutrition and physiology, health andwelfare, disease, production and environmentand they have funded research projects in allthese sectors. There are also other researchgroups all over the world (both from universities,institutes and companies) as in Germany, UnitedKingdom, Poland, Finland, Spain, TheNetherlands, Turkey, China, Taiwan, India,Pakistan, Ukraine, Lithuania, United States,Canada, Australia, and Brazil which are doingresearch in these fields of activity. Unfortunatelydetails of these projects are for the most part notpublicly available currently.
CONCLUSIONS
The banning of GPA was intended mainly toprotect the human population from transmissibleantibiotic resistance reaching human pathogens,rendering them refractory to treatment. Thebenefits of the ban extend to less stress onthe environment in general, for example in termsof loss of microbial diversity in soils fertilisedwith manure from animals receiving GPA(Opalinski et al., 1998). The main downside ofthe ban was the problems it presented tolivestock producers, significantly poultry produ-cers. The examples presented here demonstratethat there is a strong basis for looking to theplant kingdom for solutions to the problems, andindeed for new opportunities to benefit poultryproduction.
Although this is a lengthy review, it is byno means comprehensive. Plants or theirbioactives have production or health benefitsacross a wide range of effects other than thosedescribed here, including fertility (Cerolini et al.,2005), minimising lead concentrations in meat(Hanafy et al., 1994), and relief of heatstress (Rajmane and Sonawane, 1997). We hopethat the present review sets a framework foridentifying some plant bioactives that holdparticular promise for future research andapplication.
ACKNOWLEDGMENTS
This review forms part of the objectives of theEuropean Commission-funded project, FEED-SEG(FOOD-CT-2007-043077). The Rowett Institute ofNutrition and Health receives funding from theScottish Government Rural and EnvironmentResearch and Analysis Directorate (RERAD). Partof the work (WO) was supported by the IUNG,project 2.6.We thank Vicki Saint and Mary Mowatfor their work in editing the manuscript andgathering and collating references, and AlfonsJansmann for commenting on the manuscript.
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