Date Published: June 26, 2019
Publisher: Public Library of Science
Author(s): 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, Clair Null, Peter Byass
Abstract: BackgroundHelminth 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 findingsWe 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.ConclusionsIntegration 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 registrationClinicalTrials.gov NCT01704105.
Partial Text: Intestinal soil-transmitted helminth (STH) infections, including Ascaris lumbricoides, Trichuris trichiura, and hookworm, and the protozoan Giardia duodenalis are common parasitic infections among children in low-resource settings and are neglected tropical diseases. Globally, STHs are estimated to affect 1.45 billion people , while Giardia has been cited as the most common enteropathogen in low-income countries . STH and Giardia infections can result in poor absorption of nutrients and weight loss [3,4]. There is some evidence that STH and Giardia infections, even when asymptomatic, may contribute to growth faltering and impaired cognitive development [5–8]. Longitudinal cohort studies in Bangladesh and Brazil have identified early infection with Giardia as a risk factor for stunting among children [7,9]. In Peru, children with multiple Giardia infections per year during the first 2 years of life had lower cognitive function scores at age 9 years than children with 1 or fewer Giardia infections . Evidence on the effect of child STH infections on child growth, cognitive development, and school performance has been mixed and strongly debated by experts, with some suggesting additional evidence is needed [5,6,11–14].
Our findings demonstrate that an integrated water, sanitation, and handwashing intervention targeting the household environment in rural Kenya reduced Ascaris infection prevalence by 22%, while a water treatment intervention reduced Ascaris infection by 18%. Almost identical effect estimates generated by analyzing stool samples with microscopy and qPCR in a subset of arms lent additional credibility to the overall results (Fig 3). In addition, we found that improved nutrition did not enhance the effectiveness of the WSH intervention. Trichuris and hookworm prevalence were too low to precisely assess intervention impact in this setting, and Giardia was unaffected by the interventions. Although the integrated WSH intervention did not succeed in improving child growth or reducing symptomatic diarrhea in this trial , our findings confirm that WSH can effectively reduce helminth infection prevalence.