Performance of kala-azar surveillance in Gaffargaon subdistrict of

Mymensingh, Bangladesh

AUTHORS AND AFFILIATIONS

Kazi Mizanur Rahman1,2, Indira Samarawickrema2, David Harley2, Anna Olsen3, Colin D

Butler2,4, Dinesh Mondal1, Shariful Amin Sumon1, Subrata Kumar Biswas1, Stephen P

Luby1,5, Adrian C Sleigh2

1International Centre for Diarrhoeal Disease Research, Bangladesh, Dhaka, Bangladesh2Australian National University, Canberra, ACT, Australia3University of New South Wales, Sydney, NSW, Australia4University of Canberra, Canberra, ACT, Australia5Stanford University, Stanford, CA, USA

ABSTRACT

Background: Elimination of kala-azar is planned for South Asia and this will require good

surveillance along with other strategies. We assessed surveillance in Gaffargaon upazila (a

subdistrict of 13 unions) of Mymensingh district, an area of Bangladesh highly endemic for

kala-azar.

Methods: In 4703 randomly sampled households within nine randomly sampled villages

drawn from three randomly sampled unions, we actively searched for kala-azar cases with

onset between January 2010 and December 2011. We then searched for medical records of

these cases in the patient registers of Gaffargaon upazila health complex (UHC). These

records form the data source for monthly reporting. We also investigated factors associated

with the medical recording by interviewing the cases and their families. We also did a general

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observation of UHC recording systems and interviewed health staff responsible for the

monthly reports of kala-azar cases.

Results: Our active case finding detected 58 cases but 29 were not recorded in the

Gaffargaon UHC patient and laboratory registers. Thus, only 50% of cases were reportable

via the government surveillance system. Interviews with health staff reveal the heavy

reporting burden for multiple diseases, variation in staff experience and high demands on the

staff time. Recording was more likely for those age 18 years or more, males, with an

educated father, palpable spleens and abdominal pain. The odds of being recorded in the

UHC registers were 18 times higher for patients treated with miltefosine than sodium

antimony gluconate (95% CI = 3.4 – 100.3). Conclusions: Fifty percent of kala-azar cases

occurring in one highly endemic area of Bangladesh were recorded in registers that were the

source for monthly reports to the national surveillance system. Recording was influenced by

patient, treatment, and staff factors. Our findings have policy implications for the national

surveillance system.

Keywords: Visceral leishmaniasis, kala-azar, elimination, surveillance, Bangladesh

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INTRODUCTION

Visceral leishmaniasis (VL) is caused by Leishmania protozoan parasites transmitted by

Phlebotomine sandflies[1]. VL is a systemic illness with significant morbidity and mortality

and is characterized by fever and splenomegaly. The disease is endemic in impoverished

tropical areas globally [2, 3]. In South Asia the disease is known as kala-azar meaning ‘black-

fever’ and only affects humans, but elsewhere VL is also enzootic.

A memorandum of understanding signed by the governments of India, Bangladesh and Nepal

in 2005 states that kala-azar will be eliminated by 2015. Elimination is defined as annual

incidence of less than 1 per 10,000 population at the district or sub-district level [4]. The

elimination programme has four phases – preparatory, attack, consolidation, and

maintenance. By late 2013 the elimination programme had reached the end of the preparatory

phase (establishment of strategies including pilot insecticide spraying, facilities for diagnosis,

treatment, and surveillance, passive and active case detection and vector monitoring). The

attack phase is beginning in 2014 and will include implementation and monitoring of all

elimination strategies[5], and additional vector control activities. Accordingly the focus is on

vector control (indoor spraying, treated bed nets, environmental management and community

participation) as well as access to early diagnosis and complete case management, and

continued transmission surveillance.

Surveillance is crucial in monitoring disease and is identified as one of the main elimination

strategies for kala-azar [5]. India’s surveillance system reports 12 – 20 percent of incident

cases with improving ascertainment noted by 2010 [6-8]. In Bangladesh, the surveillance

provides estimates and trends of the nationwide occurrence of kala-azar [9]. Kala-azar is

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reported every month starting from the upazila or subdistrict level. There are also research

data for selected endemic sub-districts extending back up to eight years and they usually

provide kala-azar rates higher than the government surveillance system [3, 10-12]. But a

variety of methods were used and results are not comparable with surveillance data.

Furthermore, they cannot be repeated regularly nationwide. Thus, the government led passive

surveillance system provides the only ongoing nationwide data and hence the only

nationwide indicator of progress towards the elimination goal.

Here we report a community-based study of kala-azar surveillance in a highly endemic sub-

district of Bangladesh. We estimate the proportion of incident kala-azar cases actually

recorded in the medical registers of the sub-district health facility, the source of data for the

report of monthly case counts. We analyse factors influencing case recording and make

recommendations to improve surveillance.

METHODS

Study setting

The study was conducted in Gaffargaon sub-district of Mymensingh district in Bangladesh.

Gaffargaon is located 80km north-east of Dhaka, the capital of Bangladesh. The sub-district

occupies 398 sq. km. with a population of 430,000 [13]. Gaffargaon is divided into 15 unions

and 214 villages. Around half of the population of Gaffargaon are male and half are literate.

The majority of the working population are farmers. Among the sub-districts , Gaffargaon

reported the third highest number of cases of kala-azar in 2011 [14].

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Study sample and case detection

The sampling strategy here reported was developed for a larger study identifying barriers to

early diagnosis and case management of kala-azar in Fulbaria and Gaffargaon sub-districts of

Mymensingh district. In the barriers study we compared the two sub-districts measuring

diagnostic delay of incident cases arising over a two year period (Jan 1, 2010 – Dec 31, 2011)

as an indicator of the success of the two different elimination programmes - international

non-governmental organization (Fulbaria) and Bangladesh government (Gaffargaon). We

calculated the sample size of incident kala-azar cases using an estimate of 20 days difference

(i.e. 60 vs 40) in mean delay to diagnosis between the two sub-districts, 80% power, 95%

confidence and a design effect of 1.3 (clustering of unions and villages in a multistage

sampling). These statistical assumptions were based on findings from a survey conducted by

KMR in 2009 in Fulbaria (unpublished data). We thus concluded that 75 kala-azar cases were

required from each of the two sub-districts for the barriers study.

For the surveillance study reported here, we initially calculated sample size needed in each of

the two sub-districts to detect 50% under-reporting with 10% precision and 90% confidence

level. A sample of 68 kala-azar cases – a smaller number than that needed for the overarching

barriers study – was indicated on the basis of the power calculation using Epi Info StatCalc to

calculate the sample size needed to measure a single proportion. Therefore, the sample size of

75 needed for each of the two sub-districts for the barriers study also suffices for the

surveillance study. We focused on Gaffargaon because passive reporting via the government

system operates here. We also cross-checked in Fulbaria by noting medical recording of kala-

azar cases by the treating clinic operated by Médecins Sans Frontières (MSF) [15].

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We expected our house to house case finding in Gaffargaon would yield 75 kala-azar cases

from 5400 households based on cumulative incidence of 1.4 cases per 100 households over

two years in Fulbaria (data not published). We did multistage cluster sampling in Gaffargaon

(Figure 1). First, we excluded two of 15 unions as they were part of the Gaffargaon central

administrative area where the upazila health complex (UHC) is located and we expected that

careseeking would be different from the other 13 unions. Then, from the remaining 13 unions

we randomly sampled three unions and in each of these unions we randomly selected three

villages. We then sampled households in each village, aiming for about 600 households per

village. If the village was large, we sub-divided it into different para or clusters, and

randomly sampled clusters to get 600 households. The resulting sample included a total of

4703 households and we sought current or past kala-azar cases in each of these sampled

households.

Going from house to house in the period December 2011 to May 2012, we sought cases that

had occurred between January 2010 and December 2011. In each household the informant

was a case or a senior family member. Our case definition required diagnosis by a qualified

health care provider based on clinical presentation and a positive confirmatory diagnostic

test.

Data collection: interviews, observations and UHC records

If there was more than one kala-azar case in a household, we studied the earliest case. Kala-

azar cases and their families were interviewed using a structured questionnaire. For cases less

than 18 years of age, a parent or carer was interviewed. Surviving family members of

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deceased cases were interviewed. We collected demographic and economic data, date of

symptom onset, signs and symptoms, care seeking experiences and diagnosis.

We also studied recording and reporting of kala-azar cases making general observations at

the Gaffargaon UHC. As well, we interviewed three key health service staff from the

Gaffargaon UHC who were involved in the kala-azar reporting system. We asked them to

detail their role in kala-azar reporting. We asked about obstacles to reporting and how the

reporting system could be improved. These semi-structured interviews were audio-recorded.

We examined Gaffargaon UHC records to determine if cases we detected had been entered in

the registers. Inpatient, outpatient and laboratory registers were reviewed. We sought record

entries in the 2010-2011 period for all kala-azar cases we detected in the community. We

used the name and address to confirm identification of the patients in the register books.

Data management and analysis

Quantitative data were digitized using Epi Info (version 3.5.3). Information from the patients

and families was recorded in MS Excel in a file which also noted whether the patient was

recorded in the UHC registers. Qualitative data included extensive notes on general

observations and interview recordings. The recordings were transcribed in the Bengali

language for the three UHC staff.

Quantitative data were analysed using STATA (version 8). We calculated the proportion of

our study cases found in the Gaffargaon UHC records and compared frequencies of patient

and health system factors for those found and not found in the hospital records. The factors

were age, sex, education, symptoms, companion to clinic, place of diagnosis, involvement of

private providers, treatment location, drug and year.

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Interview transcripts were compared and contrasted for recurring themes and informative

quotations related to the research questions. Quotations used in this publication were

translated into English by author KMR. All analyses were supported by the general

observations.

Ethics

Informed written consent was obtained from participants. For illiterate interviewees, the

consent form was read out loud and the participants’ fingerprints were obtained on the

consent forms. Before conducting the study of the kala-azar reporting system and

interviewing staff of Gaffargaon UHC, written permission was obtained from the relevant

authority based centrally in Dhaka and at Gaffargaon. Individual consent was also obtained

from interviewed staff who were advised that they would not be identified. Ethical approvals

were provided by the Human Research Ethics Committee of the Australian National

University and the Ethical Review Committee of the International Centre for Diarrhoeal

Disease Research, Bangladesh (icddr,b).

RESULTS

Study participants

We screened 4703 households and identified 89 people fulfilling our case definition of kala-

azar. After exclusions (refused to participate, migrated out, extra cases in a family and

special care), 58 cases remained for analysis in the study (Figure 2).

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Kala-azar patient flow and monthly reporting

Our general observations revealed the flow of kala-azar patients and related information at

Gaffargaon UHC (Figure 3). We identified three registers (laboratory, kala-azar and

admission) where staff recorded the patient name and other details. Each month, using the

kala-azar register as the final source of the information, the responsible nurse reports to the

UHC statistician the consolidated data on the number of kala-azar cases (by age, sex,

treatment status). Then the statistician compiles a monthly kala-azar tally along with the

routine ‘disease profile’ report and sends this information to the Civil Surgeon’s office which

is responsible for that district (Figure 4).

Surveillance of kala-azar in Gaffargaon: active vs passive case detection

After reviewing the UHC registers we concluded that there were no records for 29 of our 58

actively detected cases. Thus, overall, only 50% were detectable by the government passive

surveillance system - 44% in 2010 and 59% in 2011.

Factors influencing kala-azar reporting

Using the survey data we explored patient (Table 1) and health system factors (Table 2) as

determinants of reporting. Age 18 years or more, male sex, educated father, palpable spleen

and abdominal pain increased the likelihood of being recorded by the UHC; these effects

were quite substantial but (constrained by the small sample size) were not statistically

significant (Table 1). We did not find any association between wealth and reporting (data not

shown).

Almost all (55 of 58) the study patients visited the Gaffargaon UHC in seeking care,

indicating that non-attendance was not associated with non-recording. Twenty four patients

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(41%) were diagnosed at the UHC and 31 (54%) were diagnosed by a private health care

provider. The odds of recording were lower for those diagnosed at public, relative to private,

facilities (OR = 0.7; 95% CI = 0.2-1.9) (Table 2).Thirty received oral miltefosine tablet and

28 received injectable sodium antimony gluoconate (SAG). The odds of being recorded in the

UHC registers were 18 times higher for patients treated with miltefosine than SAG (95% CI

= 3.4-100.3). The proportion supplied with any kala-azar treatment drug from the UHC was

100% and 78% among those recorded and not recorded, respectively. Receiving kala-azar

treatment at the UHC, relative to elsewhere, was associated with 80% lower odds of being

recorded.

Interviews with staff indicated a number of factors influencing reporting including a lack of

confidence in their knowledge of kala-azar. There were other issues such as the burden of

recording numerous notifiable diseases on the monthly ‘disease profile’ report.

“It is not just one report that we need to prepare from the hospital every month … All

diarrhoea, ARI, kala-azar (cases) …(plus)… reports from the field (administrative

level lower than the subdistrict), we send all these consolidated figures.”

As well, the reporting system itself has changed, leading to new routines along with a new

kala-azar reporting form.

“We used to send the report on kala-azar with other diseases in the monthly ‘disease

profile’. In that form there was a row for kala-azar. Later a separate form for kala-azar

was introduced. We now send reports on kala-azar both through the ‘disease profile’

as well as in the separate form.”

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The informant indicated that reporting channels were sometimes complex and duplicated.

This reflected the need to get the information through quickly but this can be difficult in hard

copy due to the need for a signature by the Upazila Health and Family Planning Officer

(otherwise known as the Thana Health Administrator or THA).

“We send the reports to the office of Civil Surgeon. We often send them through

email. Sometimes we send the numbers over telephone if there is any hurry. Even

through mobile phone. …We send the hard copies after getting it signed by the THA.”

In addition, different nursing staff recorded the patient data at different times. This may cause

the quality or completeness of recording to vary. However, the system used was unlikely to

duplicate reporting.

“We put a serial number ... this serial number is the registration number. …

We show the patient only once.”

DISCUSSION

Only half of the kala-azar cases arising in Gaffargaon sub-district, a highly endemic area

within Mymensingh district, were recorded in the upazila health records. Consequently the

monthly tallies of kala-azar cases reported to the government of Bangladesh represent only

about half of the actual cases that occur. Investigation of socio-demographic and health

system factors associated with non-recording was generally uninformative – most factors

were not significantly associated and effect estimates had wide confidence limits. Limits

were exceptionally wide for the odds ratio linking miltefosine to recording (3.4 – 100.3), but

the point estimate indicated a strong association for this health system factor (18.4).

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Previous population based studies in Bangladesh have not reported surveillance performance

in any way comparable to our study [3, 10-12]. In India, Singh et al (2006) assessed kala-azar

surveillance in Bihar in 2003. They searched households for people with fever for over 15

days duration and confirmed kala-azar with microscopic parasite identification in spleen or

bone marrow aspirates. Sixty-five cases were detected through their active case search and

only 8 (12.3%) were reported [7]. The same group in a later study found that only 17% of the

cases were reported [8]. Those over 30 years of age were significantly less likely to be

reported, but no other patient, family or health system factor was shown to be important.

Our study was done on a two-year sample of kala-azar patients in a geo-demographically

defined segment of the Bangladesh population in a highly endemic area. We achieved our

principal aim of estimating with reasonable accuracy the proportion of incident kala-azar

cases being recorded by the health system (i.e. 50%). But our sample size did not have

statistical power to enable conclusive sub-analyses of factors related to surveillance.

However, the qualitative data we collected were able to provide some perspective on the

issue of preparing tallies and reporting to the government. The system in use involves

recording in a kala-azar register and an admission register which are sources for reporting

kala-azar to the statistician to enable the monthly tally. The staff we interviewed made

comments about the data flow and forms, and the figure we produced showed a rather

complex system that could be simplified.

We were not able to determine the actual proportion reported because we could not separate

the contribution expected from our sample from the contribution expected from the rest of the

population served by the same UHC. If we could have searched for cases in the entire

population of Gaffargaon (around 430,000) for a particular month then we would be able to

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compare the number of cases detected in the community and number of cases reported from

the UHC. But this would require substantial resources.

We infer from our study that around 50% of kala-azar cases in a highly endemic area of

Bangladesh are not detectable by the national surveillance system. Obstacles to reporting

were related to the reporting system and the reporting burden for multiple diseases.

CONCLUSIONS

The kala-azar passive surveillance system in Bangladesh needs to improve in order to record

the 50% of cases currently missed. The reporting system could be simplified. For example, if

treatment was restricted to those with a positive result, the only record used for reporting

could be the rK-39 diagnostic test result. An improved surveillance system would help

programme managers deploy resources more effectively and monitor progress towards

elimination.

ACKNOWLEDGEMENT

The study was funded by the Core Research Fund of the International Centre for Diarrhoeal

Disease Research, Bangladesh (icddr,b) which supported all the data collection related

expenditure. Icddr,b is thankful to the Governments of Australia, Bangladesh, Canada,

Sweden and the UK for providing core/unrestricted support. The PhD research fund of the

Australian National University provided additional support. KMR also received support

through the Endeavour Postgraduate Award of the Australian Government.

We are grateful to Communicable Disease Control, Directorate General of Health Services,

Ministry of Health and Family Welfare, Bangladesh and Upazila Health Complex of

Gaffargaon for providing all sorts of supports needed for the study.

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Staff involved in data collection for the study worked to their utmost sincerity, hard-work and

honesty. This research work would not be possible without the spontaneous participation of

the community members of Gaffargaon.

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REFERENCES

1. Control of the leishmaniasis: report of a meeting of the WHO Expert Committee on the Control ofLeishmaniases, Geneva, 22-26 March 2010., in WHO technical report series; no.949. 2010, WHO: Geneva.

2. Boelaert, M., et al., The poorest of the poor: a poverty appraisal of households affected by visceral leishmaniasis in Bihar, India. Trop Med Int Health, 2009. 14(6): p. 639-44.

3. Bern, C., et al., Risk factors for kala-azar in Bangladesh. Emerg Infect Dis, 2005. 11(5): p. 655-62.

4. SEARO. Kala-azar Disease Burden in SEA Region. [cited 18/07/2013]; Available from: http://www.searo.who.int/entity/vector_borne_tropical_diseases/data/Kala-azar/en/index.html.

5. SEARO, Regional strategic framework for elimination of kala-azar from the South-East Asia Region (2011-2015). 2012.

6. Mubayi, A., et al., Transmission dynamics and underreporting of Kala-azar in the Indian state of Bihar. J Theor Biol, 2009. 262(1): p. 177-85.

7. Singh, S.P., et al., Serious underreporting of visceral leishmaniasis through passive case reporting in Bihar, India. Trop Med Int Health, 2006. 11(6): p. 899-905.

8. Singh, V.P., et al., Estimation of under-reporting of visceral leishmaniasis cases in Bihar, India. Am J Trop Med Hyg, 2010. 82(1): p. 9-11.

9. Training Module on Kala-azar Elimination Program, D.G.H.S. Disease Control Unit, Ministry of Health and Family Welfare, Government of Bangladesh, Editor. 2010.

10. Bern, C. and R. Chowdhury, The epidemiology of visceral leishmaniasis in Bangladesh: prospects for improved control. Indian J Med Res, 2006. 123(3): p. 275-88.

11. Ferdousi, F., et al., Visceral Leishmaniasis Eradication is a Reality: Data from a Community-based Active Surveillance in Bangladesh.Trop Med Health. 40(4): p. 133-9.

12. Rahman, K.M., et al., Increasing incidence of post-kala-azar dermal leishmaniasis in a population-based study in Bangladesh. Clin Infect Dis, 2010. 50(1): p. 73-6.

13. BBS, Community Report: Mymensigh Zilla. Population and Housing Census 2011. , in Population and Housing Census 2011. 2012, Bangladesh Bureau of Statistics, Ministry of Planning.

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14. DGHS, Health Bulletin 2012. 2012, Management Information System, DGHS. Ministry of Health and Family Welfare, GOB.

15. [cited 2012 September 13 ]; Available from: http://www.msf.org.au/media-room/press-releases/press-release/article/hope-for-kala-azar-sufferers-in-bangladesh.html.

16. Rahman, M., et al. Healthcare-seeking from Village Doctor for Kala-azar in Bangladesh. in 13th Annual Scietific Conference of ICDDR,B. 2011. Dhaka, Bangladesh: ICDDR,B.

17. Mondal, D., et al., Visceral leishmaniasis elimination programme in India, Bangladesh, and Nepal: reshaping the case finding/case management strategy. PLoS neglected tropical diseases, 2009. 3(1): p. e355.

18. Zafar Ullah, A.N., et al., Effectiveness of involving the private medical sector in the National TB Control Programme in Bangladesh: evidence from mixed methods. BMJ Open. 2(6).

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Figure 1: Study sampling

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Figure 2: Study participants and exclusions

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Households screened = 4703

Kala-azar cases identified = 89

Cases finally analysed = 58

Cases refused to participate = 2 Extra cases in a household = 15

Cases migrated out = 5

Cases receiving special clinical care

or care from outside Gaffargaon = 9

Figure 3: KA patient flow and reporting system observed in Gaffargaon UHC, 2012

Note: KA = kala-azar; UHC = upazila health complex; MO = medical officer

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Figure 4: UHC kala-azar recording and reporting

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Table 1: Patient factors influencing UHC recording of kala-azar patients

Factor Kala-azar cases Odds ratio(OR)

95% CI

Recorded by UHC n (%)

Not recorded by UHC n (%)

Age in years

18 years or more 13 (45) 8 (28) 1.0

< 18 years 16 (55) 21 (72) 0.5 0.2-1.4

Sex

Female 8 (28) 12 (41) 1.0

Male 21 (72) 17 (59) 1.9 0.6-5.7

Education: >= 5 years completed (reference: < 5 years)

Patient 11 (50) 5 (36) 1.8 0.4-7.4

Father 6 (38) 3 (15) 3.4 0.6-18.1

Mother 4 (25) 5 (25) 1.0 0.2-4.7

HH head 16 (72) 14 (58) 1.9 0.4-8.0

Patient accompanied by spouse 7 (24) 11 (38) 0.5 0.2-1.7

Patient accompanied by parents 14 (48) 13 (45) 1.2 0.4-3.3

Kala-azar symptoms/signs

Abdominal distension 17 (59) 17 (59) 1.0 0.4-2.9

Abdominal pain 19 (66) 15 (52) 1.8 0.6-5.2

Palpable spleen reported by a health care provider

11 (38) 8 (28) 1.6 0.5-4.9

Skin darkening 21 (72) 20 (69) 1.2 0.4-3.7

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Table 2: Health system factors influencing UHC recording of kala-azar patients

Factor Kala-azar cases Odds ratio(OR)

95% CI

Recorded by UHC n (%)

Not recorded by UHC n (%)

Facility/ provider confirmed kala-azar for the first time

Private 18 (62) 13 (44) 1.0

Public 11 (38) 13 (45) 0.7 0.2-1.9

KA drug administered

Not at UHCAt UHC 5 (17) 16 (55)

1.00.2 0.04-0.6

KA drug received for treatment

SAG 5 (17) 23 (79) 1.0

Miltefosine 24 (83) 6 (21) 18.4 3.4-100.3

KA treatment year

2010 16 (55.2)) 20 (69.0) 1.0

2011 13 (44.8) 9 (31.0) 1.8 0.60-5.40

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