Factors associated with soil-transmitted helminths infection in Benin: Findings from the DeWorm3 study

Euripide F G A Avokpaho, Parfait Houngbégnon, Manfred Accrombessi, Eloïc Atindégla, Elodie Yard, Arianna Rubin Means, David S Kennedy, D Timothy J Littlewood, André Garcia, Achille Massougbodji, Sean R Galagan, Judd L Walson, Gilles Cottrell, Moudachirou Ibikounlé, Kristjana Hrönn Ásbjörnsdóttir, Adrian J F Luty, Euripide F G A Avokpaho, Parfait Houngbégnon, Manfred Accrombessi, Eloïc Atindégla, Elodie Yard, Arianna Rubin Means, David S Kennedy, D Timothy J Littlewood, André Garcia, Achille Massougbodji, Sean R Galagan, Judd L Walson, Gilles Cottrell, Moudachirou Ibikounlé, Kristjana Hrönn Ásbjörnsdóttir, Adrian J F Luty

Abstract

Background: Despite several years of school-based MDA implementation, STH infections remain an important public health problem in Benin, with a country-wide prevalence of 20% in 2015. The DeWorm3 study is designed to assess the feasibility of using community-based MDA with albendazole to interrupt the transmission of STH, through a series of cluster-randomized trials in Benin, India and Malawi. We used the pre-treatment baseline survey data to describe and analyze the factors associated with STH infection in Comé, the study site of the DeWorm3 project in Benin. These data will improve understanding of the challenges that need to be addressed in order to eliminate STH as a public health problem in Benin.

Methods: Between March and April 2018, the prevalence of STH (hookworm spp., Ascaris and Trichuris trichiura) was assessed by Kato-Katz in stool samples collected from 6,153 residents in the community of Comé, Benin using a stratified random sampling procedure. A standardized survey questionnaire was used to collect information from individual households concerning factors potentially associated with the presence and intensity of STH infections in pre-school (PSAC, aged 1-4), school-aged children (SAC, aged 5-14) and adults (aged 15 and above). Multilevel mixed-effects models were used to assess associations between these factors and STH infection.

Results: The overall prevalence of STH infection was 5.3%; 3.2% hookworm spp., 2.1% Ascaris lumbricoides and 0.1% Trichuris. Hookworm spp. were more prevalent in adults than in SAC (4.4% versus 2.0%, respectively; p = 0.0001) and PSAC (4.4% versus 1.0%, respectively; p<0.0001), whilst Ascaris lumbricoides was more prevalent in SAC than in adults (3.0% versus 1.7%, respectively; p = 0.004). Being PSAC (adjusted Odds Ratio (aOR) = 0.2, p< 0.001; adjusted Infection Intensity Ratio (aIIR) = 0.1, p<0.001) or SAC (aOR = 0.5, p = 0.008; aIIR = 0.3, p = 0.01), being a female (aOR = 0.6, p = 0.004; aIIR = 0.3, p = 0.001), and having received deworming treatment the previous year (aOR = 0.4, p< 0.002; aIIR = 0.2, p<0.001) were associated with a lower prevalence and intensity of hookworm infection. Lower income (lowest quintile: aOR = 5.0, p<0.001, 2nd quintile aOR = 3.6, p = 0.001 and 3rd quintile aOR = 2.5, p = 0.02), being a farmer (aOR = 1.8, p = 0.02), medium population density (aOR = 2.6, p = 0.01), and open defecation (aOR = 0.5, p = 0.04) were associated with a higher prevalence of hookworm infection. Lower education-no education, primary or secondary school- (aIIR = 40.1, p = 0.01; aIIR = 30.9, p = 0.02; aIIR = 19.3, p = 0.04, respectively), farming (aIIR = 3.9, p = 0.002), natural flooring (aIIR = 0.2, p = 0.06), peri-urban settings (aIIR = 6.2, 95%CI 1.82-20.90, p = 0.003), and unimproved water source more than 30 minutes from the household (aIIR = 13.5, p = 0.02) were associated with a higher intensity of hookworm infection. Improved and unshared toilet was associated with lower intensity of hookworm infections (aIIR = 0.2, p = 0.01). SAC had a higher odds of Ascaris lumbricoides infection than adults (aOR = 2.0, p = 0.01) and females had a lower odds of infection (aOR = 0.5, p = 0.02).

Conclusion: Hookworm spp. are the most prevalent STH in Comé, with a persistent reservoir in adults that is not addressed by current control measures based on school MDA. Expanding MDA to target adults and PSAC is necessary to substantially impact population prevalence, particularly for hookworm.

Trial registration: ClinicalTrials.gov NCT03014167.

Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1. Geographical location of Comé district,…
Fig 1. Geographical location of Comé district, in Benin republic, West Africa.
(A) Location of Benin republic in Africa (https://www.mapsland.com/africa/benin/large-location-map-of-benin-in-africa). (B) Administrative boundaries of Comé district. Adapted by AMBERO-ALPHA OMEGA, May 2017. From Benin Tourism Card, National Geographic Institute 1998.[18].
Fig 2. Flow diagram of stool sample…
Fig 2. Flow diagram of stool sample collection for Benin site DeWorm3 baseline prevalence survey in Comé.
Fig 3. Soil Transmitted Helminths unweighted prevalence…
Fig 3. Soil Transmitted Helminths unweighted prevalence across age-groups.
*PSAC: Pre-School Aged Children, **SAC: School Aged Children.
Fig 4. Age-infection profiles for hookworm.
Fig 4. Age-infection profiles for hookworm.
(A) Prevalence (black lines) and intensity (grey lines) of hookworm infection by age for males (solid line and circles) and females (dashed lines and empty circles). Vertical bars represent confidence intervals.
Fig 5. Age-infection profiles for Ascaris lumbricoides…
Fig 5. Age-infection profiles for Ascaris lumbricoides.
(A) Prevalence (black lines) and intensity (grey lines) of Ascaris infection by age for males (solid line and circles) and females (dashed lines and empty circles). Vertical bars represent confidence intervals.
Fig 6. Cluster level correlation between prevalence…
Fig 6. Cluster level correlation between prevalence and intensity of hookworm and Ascaris lumbricoides infection in the study population.
(A) Hookworm infection in study population; (B) Ascaris lumbricoides infection in study population.

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