Effects of single and integrated water, sanitation, handwashing, and nutrition interventions on child soil-transmitted helminth and Giardia infections: A cluster-randomized controlled trial in rural Kenya

Amy J Pickering, Sammy M Njenga, Lauren Steinbaum, Jenna Swarthout, Audrie Lin, Benjamin F Arnold, Christine P Stewart, Holly N Dentz, MaryAnne Mureithi, Benard Chieng, Marlene Wolfe, Ryan Mahoney, Jimmy Kihara, Kendra Byrd, Gouthami Rao, Theodora Meerkerk, Priscah Cheruiyot, Marina Papaiakovou, Nils Pilotte, Steven A Williams, John M Colford Jr, Clair Null, Amy J Pickering, Sammy M Njenga, Lauren Steinbaum, Jenna Swarthout, Audrie Lin, Benjamin F Arnold, Christine P Stewart, Holly N Dentz, MaryAnne Mureithi, Benard Chieng, Marlene Wolfe, Ryan Mahoney, Jimmy Kihara, Kendra Byrd, Gouthami Rao, Theodora Meerkerk, Priscah Cheruiyot, Marina Papaiakovou, Nils Pilotte, Steven A Williams, John M Colford Jr, Clair Null

Abstract

Background: Helminth and protozoan infections affect more than 1 billion children globally. Improving water quality, sanitation, handwashing, and nutrition could be more sustainable control strategies for parasite infections than mass drug administration, while providing other quality of life benefits.

Methods and findings: We enrolled geographic clusters of pregnant women in rural western Kenya into a cluster-randomized controlled trial (ClinicalTrials.gov NCT01704105) that tested 6 interventions: water treatment, improved sanitation, handwashing with soap, combined water treatment, sanitation, and handwashing (WSH), improved nutrition, and combined WSH and nutrition (WSHN). We assessed intervention effects on parasite infections by measuring Ascaris lumbricoides, Trichuris trichiura, hookworm, and Giardia duodenalis among children born to the enrolled pregnant women (index children) and their older siblings. After 2 years of intervention exposure, we collected stool specimens from 9,077 total children aged 2 to 15 years in 622 clusters, including 2,346 children in an active control group (received household visits but no interventions), 1,117 in the water treatment arm, 1,160 in the sanitation arm, 1,141 in the handwashing arm, 1,064 in the WSH arm, 1,072 in the nutrition arm, and 1,177 in the WSHN arm. In the control group, 23% of children were infected with A. lumbricoides, 1% with T. trichiura, 2% with hookworm, and 39% with G. duodenalis. The analysis included 4,928 index children (median age in years: 2) and 4,149 older siblings (median age in years: 5); study households had an average of 5 people, <10% had electricity access, and >90% had dirt floors. Compared to the control group, Ascaris infection prevalence was lower in the water treatment arm (prevalence ratio [PR]: 0.82 [95% CI 0.67, 1.00], p = 0.056), the WSH arm (PR: 0.78 [95% CI 0.63, 0.96], p = 0.021), and the WSHN arm (PR: 0.78 [95% CI 0.64, 0.96], p = 0.017). We did not observe differences in Ascaris infection prevalence between the control group and the arms with the individual interventions sanitation (PR: 0.89 [95% CI 0.73, 1.08], p = 0.228), handwashing (PR: 0.89 [95% CI 0.73, 1.09], p = 0.277), or nutrition (PR: 86 [95% CI 0.71, 1.05], p = 0.148). Integrating nutrition with WSH did not provide additional benefit. Trichuris and hookworm were rarely detected, resulting in imprecise effect estimates. No intervention reduced Giardia. Reanalysis of stool samples by quantitative polymerase chain reaction confirmed the reductions in Ascaris infections measured by microscopy in the WSH and WSHN groups. Trial limitations included imperfect uptake of targeted intervention behaviors, limited power to detect effects on rare parasite infections, and that it was not feasible to blind participants and sample collectors to treatment status. However, lab technicians and data analysts were blinded to treatment status. The trial was funded by the Bill & Melinda Gates Foundation and the United States Agency for International Development.

Conclusions: Integration of improved water quality, sanitation, and handwashing could contribute to sustainable control strategies for Ascaris infections, particularly in similar settings with recent or ongoing deworming programs. Combining nutrition with WSH did not provide further benefits, and water treatment alone was similarly effective to integrated WSH. Our findings provide new evidence that drinking water should be given increased attention as a transmission pathway for Ascaris.

Trial registration: ClinicalTrials.gov NCT01704105.

Conflict of interest statement

I have read the journal’s policy and the authors of this manuscript have the following competing interests: CN, CPS, JMC, AJP, SN, AL, BFA, RM, JK, KB, GR, TM, PC, MP, LS received funding for part of their salary and travel expenses from the research grant provided for this project by the Bill and Melinda Gates Foundation. AJP and CN received funds for part of their salary and travel expenses from the United States Agency for International Development.

Figures

Fig 1. Trial profile and participant flow.
Fig 1. Trial profile and participant flow.
STH, soil-transmitted helminth.
Fig 2. Effect of the interventions on…
Fig 2. Effect of the interventions on infection with Ascaris and Giardia: Data includes all index children and older siblings combined.
Prevalence ratios estimated by targeted maximum likelihood estimation. Error bars show 95% confidence intervals for the prevalence ratios. WSH, water treatment, sanitation, and handwashing.
Fig 3. Effect of the combined interventions…
Fig 3. Effect of the combined interventions on infection with Ascaris estimated with Kato–Katz microscopy (left) and by qPCR (right).
Prevalence ratios estimated by targeted maximum likelihood estimation. Error bars show 95% confidence intervals for the prevalence ratios. qPCR, quantitative PCR; WSH, water treatment, sanitation, and handwashing.

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