Prevalence and intensity of soil-transmitted helminth infections among pre-school age children in 12 kindergartens in Jimma Town, southwest Ethiopia

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Trans R Soc Trop Med Hyg doi:10.1093/trstmh/tru178

Daniel Danaa, Zeleke Mekonnena, Daniel Emanaa, Mio Ayanaa, Mestawet Getachewb, Netsanet Worknehc, Jozef Vercruyssed and Bruno Levecked,*

*Corresponding author: Tel: +329 264 7404; Fax: +329 264 7496; E-mail: [email protected]

Received 29 April 2014; revised 23 September 2014; accepted 7 October 2014 Background: Pre-school age children (preSAC) remain difficult to reach in mass drug administration (MDA) programmes to control soil-transmitted helminth (STH) infections. Kindergartens provide a unique platform to increase the coverage of MDA in preSAC in Ethiopia, but surveys assessing STHs among preSAC in kindergartens are scarce. Methods: We report the prevalence and intensity of STH infections among 622 preSAC in 12 kindergartens in Jimma, Ethiopia. Results: STHs were found in all kindergartens, with prevalence exceeding 50% in 8 kindergartens. The majority of the infections were of low intensity. Conclusions: This study highlights the importance of kindergartens as an additional opportunity for MDA in Ethiopia. Keywords: Infection intensity, Mass drug administration, Pre-school age children, Soil-transmitted helminths

Introduction Soil-transmitted helminths (STHs), including Ascaris lumbricoides, Trichuris trichiura and hookworm cause the highest burden among all neglected tropical diseases (NTDs). In 2010, more than 1.4 billion people were infected with at least one of the three STHs, resulting in a global burden of approximately 5.2 million disability-adjusted life-years (DALYs) (20% of total number of DALYs attributable to NTDs).1 Mass drug administration (MDA) in which anthelminthic drugs are periodically administered to both pre-school age (preSAC) and school-age children (SAC) is the main strategy to control the morbidity caused by these helminths.2 However, a large proportion of the children in need of MDA are still not receiving any anthelminthic drugs (global coverage ¼ 36%).3 MDA is particularly challenging for preSAC. In contrast to SAC who can be largely reached through schoolbased MDA, preSAC usually stay at home, and hence are difficult to reach. This difference in accessibility may have contributed to the increasing MDA coverage in SAC over the last 3 years (from 28% in 2010 to 36% in 2012), but decreasing coverage in

preSAC over the same period (from 37% in 2010 to 25% in 2012).3 In Ethiopia, parents are increasingly encouraged to send their preSAC to kindergartens to prepare them for formal schooling. Although these kindergartens provide a unique platform to increase the coverage of MDA in preSAC in Ethiopia, little is known about the prevalence and infection intensity of STH among preSAC in kindergartens.

Materials and methods Between November and December 2013, a cross-sectional survey was performed to assess prevalence and intensity of STH infections among preSAC in kindergartens of Jimma Town, southwest Ethiopia. In Jimma Town there were 27 155 preSAC (aged 1 to 5 years). Approximately 20% (5491/27 155) of the total number of preSAC attended 1 of the 44 kindergartens in the town. According to the town health office report, since 2009, albendazole is administered to preSAC (aged between 2 and 5 years) twice a

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a Department of Medical Laboratory Sciences and Pathology, College of Public Health and Medical Sciences, Jimma University, Jimma, Ethiopia; bDepartment of Pharmacy, College of Public Health and Medical Sciences, Jimma University, Jimma, Ethiopia; cDepartment of Paediatrics, College of Public Health and Medical Sciences, Jimma University, Jimma, Ethiopia; dDepartment of Virology, Parasitology and Immunology, Ghent University, Faculty of Veterinary Medicine, Merelbeke, Belgium

D. Dana et al.

study. The participation of the subject during the last round of MDA was determined via a questionnaire. All children excreting any STH eggs were given a single oral dose of albendazole (200 mg for children of 1 to 2 years of age, and 400 mg for children ≥2 years of age). The overall prevalence (percentage of children excreting eggs) was calculated for any STH and the three STH species separately. In addition, the overall proportion of low, moderate and high intensity infections according to WHO thresholds were calculated for each STH.5 The prevalence of STH infections was determined for the 12 kindergartens, 2 sexes, 5 age groups and the history of anthelminthic drug administration, separately. Finally, the correlation of prevalence results (any STH, A. lumbricoides, T. trichiura and hookworm combined) between kindergartens and primary schools were assessed by means of the Spearman correlation coefficient. The level of significance was set at p,0.05.

Results and Discussion Of the 629 subjects recruited in the survey, 7 were excluded as they could not provide a stool sample after multiple attempts (n¼5), or received an anthelminthic treatment within 3 weeks before stool sample collection (n¼2). Out of the 622 participating children, STH Infections were found in 290 (46.6%; 290/622)

Table 1. Prevalence and intensity of soil-transmitted helminth infections (STH, Ascaris lumbricoides, Trichuris trichiura and hookworm) among pre-school age children in 12 kindergartens in Jimma Town (southwest Ethiopia) Sample size School 1 2 3 4 5 6 7 8 9 10 11 12 Sex Female Male Age (years) 1 2 3 4 5 History of anthelminthic drug administration No Yes Total

62 61 41 84 64 38 32 35 34 58 60 53

STH (%)

A. lumbricoides (%)

T. trichiura (%)

Hookworm (%)

16 53 34 69 50 68 56 489 71 35 53 13

3 26 15 39 6 37 22 23 38 7 30 2

145 44 24 56 48 58 38 37 62 35 40 11

0 2 5 6 0 13 13 9 6 2 18 0

360 262

48.9 43.5

21.4 18.8

40.6 36.6

4.7 6.5

6 12 97 266 241

0.0 33 46 48.6 46.6

0 8 20 20.7 21.2

0 33 39 38 41.1

0 0 7 5.3 5.4

430 192 622

54.4 29.2 46.7

24.4 10.9 20.3

44.9 25.5 38.9

7.1 1.0 5.5

A. lumbricoides: Ascaris lumbricoides; STH: soil-transmitted helminths; T. trichiura: Trichuris trichiura.

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year. The last round of MDA took place in October 2013 (coverage was estimated to be 80%). To compare with STH data previously obtained among SAC in primary schools, only kindergartens within the compounds or in close proximity to primary schools were included. Based on STH prevalence observed in these primary schools, we stratified these primary schools into high, moderate and low level of endemicity (Mekonnen et al., unpublished data). A total of 853 children were present at these kindergartens. All children aged 1 to 5 years (n¼629) were recruited. A stool sample was collected from each of the children. For preSAC aged 1 to 2 years, the parents and instructors of the kindergartens assisted in collecting stool samples immediately after defecation. For preSAC aged 3 to 5 years, children were asked to provide a stool on a clean sheet of plastic. Experienced data collectors immediately transferred a sufficient amount of stool into a pre-labelled container. Samples, in batches of 20 stool samples, were transported to the laboratory (less than 15 min drive away), where all samples were subsequently processed within 4 hours using the McMaster egg counting method.4 Only those children who were willing to participate, and whose parents or guardians signed the written informed consent form were included in the study. Children who received an anthelminthic treatment within 3 weeks prior to stool sample collection were excluded from the

Transactions of the Royal Society of Tropical Medicine and Hygiene

Strongyloides, another STH, or other important parasites such as Giardia, Entamoeba and Schistosoma mansoni. The 12 kindergartens included in the survey were selected based on previous epidemiological data from the primary schools, and hence they do not represent a random sample. Therefore, any extrapolation to all kindergartens or preSAC in Jimma Town should be done with care, particularly when these kindergartens are linked to governmental schools that are mostly attended by children of a lower socio-economic status. As a result, prevalence results might be overestimated.

Authors’ contributions: DD, ZM and BL designed the survey; DD, ZM, DE, MG and NW conducted the survey; DD, ZM, JV, MA, BL analyzed and interpreted the data; DD and BL wrote the manuscript; ZM, NW and JV reviewed the manuscript. All authors read and approved the final manuscript. DD is the guarantor of the paper. Acknowledgements: The authors are grateful to the kindergarten teachers, study subjects and their parents who allowed their children to participate. In addition, they would like to thank the staff of the Medical Laboratory Sciences, Jimma University, including Bizuwarke Sharew, Yesuf Seid, Yerosa Dinsa and Tigist Mulugeta for processing and examining the stool samples. Funding: This study was funded by the VLIR-UOS programme with Jimma University. BL is a postdoctoral fellow of FWO [05–05 1.2.853.13]. ZM is supported by the Infectious Diseases and Epidemiology Project within a VLIR-UOS programme. Competing interests: None declared. Ethical approval: The protocol for this study was approved by Institutional Review Board Committee of the College of Public Health and Medical Science, Jimma University, Ethiopia. All subjects included in the study signed an informed consent form by their parents and guardians.

References 1 Pullan RL, Smith JL, Jasrasaria R, Brooker SJ. Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasit Vectors 2014;7:37. 2 WHO. Helminth control in school-age children: a guide for managers of control programmes. Geneva: World Health Organization; 2011. 3 WHO. Soil-transmitted helminthiases: number of children treated in 2012. Week Epidemiol Rec 2014;89:133–9. 4 Levecke B, Behnke JM, Ajjampur SS et al. A comparison of the sensitivity and fecal egg counts of the McMaster egg counting and Kato-Katz thick smear methods for soil-transmitted helminths. PLoS Negl Trop Dis 2011;5:e1201. 5 WHO. Guidelines for the evaluation of soil-transmitted helminthiasis and schistosomiasis at community level. A guide for control programme managers. Geneva: World Health Organization; 1998. 6 Mekonnen Z, Meka S, Ayana M et al. Comparison of individual and pooled stool samples for the assessment of soil-transmitted helminth infection intensity and drug efficacy. PLoS Negl Trop Dis 2013;7:e2189. 7 WHO. Preventive chemotherapy in human helminthiasis. Geneva: World Health Organization; 2006.

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children. T. trichiura was the most prevalent (38.9%; 242/622), followed by A. lumbricoides (20.3%; 126/622). Hookworm infections were found in 5.5% of the children (34/622). These prevalence estimates are comparable to those obtained from SAC in the same study area and during the same season in 14 primary schools where STH prevalence was 52.4% (440/840) (A. lumbricoides 23.8% [200/840]; T. trichiura 39.2% [329/840] and hookworms 11.4% [96/840]).6 The majority of the infections were classified as low, and only a minority were classified as high. For T. trichiura infections, 77.3% (187/242) were classified as low, 22.3% (54/242) as moderate and 0.4% (1/242) as high infection intensity. For A. lumbricoides infections, these proportions were 44.4% (56/126), 54.0% (68/126) and 1.7% (2/126) for low, moderate and high infection intensity, respectively. For hookworm infections, the level of infection intensity was low for all cases (96/96). Table 1 reports the prevalence of STH infections across the 12 kindergartens, 2 sexes, 5 age groups and history of anthelminthic drug administration. Both T. trichiura and A. lumbricoides infections, and hence any STH infection, were observed in all 12 kindergartens involved in the survey. However, there was a large variation in the proportion of infected children across the kindergartens. This proportion ranged from 13% (7/53) to 71% (24/34) for any STH infection (in half of the schools more than 50% of the children excreted STH eggs), from 11% (6/53) to 62% (21/34) for T. trichiura infections, and from 2% (1/53) to 39% (33/84) for A. lumbricoides infections. The proportion of children excreting hookworm eggs in the 9 schools where STH eggs were observed ranged from 2% (1/61) to 18% (11/60). The difference in STH infections across sex was less pronounced. Females were more infected with any STH, A. lumbricoides and T. trichiura, but less infected with hookworms. The prevalence of any STH and the three STH species separately, increased from the age of 1 to 3 years, after which the prevalence became relatively unchanged. Children that received an anthelminthic drug were less infected with STHs compared to those who were reported not to have had antheminthic drugs previously. Prevalence results between kindergartens and school were significantly correlated (correlation coefficient¼0.85; p,0.001). Our results indicate that STH infections are highly prevalent among preSAC, emphasizing the need for continuing to control the morbidity caused by these parasites through MDA. These unexpected high prevalence results might be explained by the poor coverage of MDA. We did not observe the high coverage of preSAC reported by the health office. In addition, it is clear that targeting only preSAC to control STH will not be sufficient in Jimma Town, as SAC remain an important source of on-going transmission. The correlation between prevalence results between kindergartens and primary schools confirm that data on SAC obtained through schools may indirectly provide epidemiological information on preSAC, and hence there is no need for programme managers to invest in additional surveys.7 Finally, they highlight the importance of kindergartens as an additional platform for MDA in Jimma Town, particularly when these kindergartens are often located within the same compound as the primary schools, allowing both to be reached with minimum additional effort. Two limitations of the study are the choice of diagnostic method and sampling strategy. We used the McMaster method, which has previously been shown to be userfriendly, robust and accurate for enumeration of Ascaris lumbricoides, T. trichiura and hookworms, but less sensitive when intensity of infection is low. Moreover, it does not allow the detection of

Prevalence and intensity of soil-transmitted helminth infections among pre-school age children in 12 kindergartens in Jimma Town, southwest Ethiopia.

Pre-school age children (preSAC) remain difficult to reach in mass drug administration (MDA) programmes to control soil-transmitted helminth (STH) inf...
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