Effect of Sanitation on Soil-Transmitted Helminth Infection: Systematic Review and Meta-Analysis

Abstract

A systematic review and meta-analysis by Kathrin Ziegelbauer and colleagues finds that sanitation is associated with a reduced risk of transmission of helminthiases to humans.

Abstract

Background

In countries of high endemicity of the soil-transmitted helminth parasites Ascaris lumbricoides, Trichuris trichiura, and hookworm, preventive chemotherapy (i.e., repeated administration of anthelmintic drugs to at-risk populations) is the main strategy to control morbidity. However, rapid reinfection of humans occurs after successful deworming, and therefore effective preventive measures are required to achieve public health goals with optimal efficiency and sustainability.

Methods and Findings

We conducted a systematic review and meta-analysis to assess the effect of sanitation (i.e., access and use of facilities for the safe disposal of human urine and feces) on infection with soil-transmitted helminths. PubMed, Embase, ISI Web of Science, and the World Health Organization Library Database were searched without language restrictions and year of publication (search performed until December 31, 2010). Bibliographies of identified articles were hand-searched. All types of studies reporting data on sanitation availability (i.e., having access at own household or living in close proximity to sanitation facility), or usage, and soil-transmitted helminth infections at the individual level were considered. Reported odds ratios (ORs) of the protective effect of sanitation on soil-transmitted helminth infections were extracted from the papers or calculated from reported numbers. The quality of published studies was assessed with a panel of criteria developed by the authors. Random effects meta-analyses were used to account for observed heterogeneity. Thirty-six publications, consisting of 39 datasets, met our inclusion criteria. Availability of sanitation facilities was associated with significant protection against infection with soil-transmitted helminths (OR  =  0.46 to 0.58). Regarding the use of sanitation, ORs of 0.54 (95% confidence interval [CI] 0.28–1.02), 0.63 (95% CI 0.37–1.05), and 0.78 (95% CI 0.60–1.00) were determined for T. trichiura, hookworm, and A. lumbricoides, respectively. The overall ORs, combining sanitation availability and use, were 0.51 (95% CI 0.44–0.61) for the three soil-transmitted helminths combined, 0.54 (95% CI 0.43–0.69) for A. lumbricoides, 0.58 (95% CI 0.45–0.75) for T. trichiura, and 0.60 (95% CI 0.48–0.75) for hookworm.

Conclusions

Despite a number of limitations (e.g., most studies used a cross-sectional design and were of low quality, with potential biases and considerable heterogeneity), our results reveal that sanitation is associated with a reduced risk of transmission of helminthiases to humans. Access to improved sanitation should be prioritized alongside preventive chemotherapy and health education to achieve a durable reduction of the burden of helminthiases.

Please see later in the article for the Editors' Summary

Editors' Summary

Background

Worldwide, more than a billion people are infected with soil-transmitted helminths, parasitic worms that live in the human intestine (gut). Roundworm, whipworm, and hookworm infections mainly occur in tropical and subtropical regions and are most common in developing countries, where personal hygiene is poor, there is insufficient access to clean water, and sanitation (disposal of human feces and urine) is inadequate or absent. Because infected individuals excrete helminth eggs in their feces, in regions where people regularly defecate in the open, the soil becomes contaminated with eggs. People pick up roundworm or whipworm infections when they ingest these eggs after they have matured in the environment by eating raw, unwashed vegetables or by not washing their hands after handling contaminated soil (a common transmission route for children). In the case of hookworm, the immature, infective stages of the worms, which hatch in the soil, can penetrate human skin, and people usually become infected by walking barefoot on contaminated soil. Mild infections with soil-transmitted helminths rarely have symptoms, but severe infections can cause abdominal pain and diarrhea, weakness, and malnutrition that can impair physical and mental development. Many soil-transmitted helminth infections can be safely and effectively treated with anthelmintic drugs, but there is rapid reinfection after successful treatment.

Why Was This Study Done?

In 2001, the World Health Organization endorsed preventative chemotherapy as the global strategy to control soil-transmitted helminthiasis. The key component of this strategy is regular administration of anthelmintic drugs to at-risk groups—children, women of childbearing age, and adults in high-risk occupations such as nightsoil reuse and farming. Although this strategy reduces illness caused by soil-transmitted helminths, it does not prevent rapid reinfection. To interrupt transmission and to achieve local elimination of helminthiasis, integrated control approaches that include access to sanitation and other complementary interventions of a primary prevention nature are needed. In this systematic review and meta-analysis, the researchers investigate whether the availability and/or use of sanitation facilities (latrines or toilets) lowers the risk of soil-transmitted helminth infections. A systematic review uses predefined criteria to identify all the research on a given topic; a meta-analysis is a statistical method that combines the results of several studies.

What Did the Researchers Do and Find?

The researchers identified 36 publications that included data on sanitation availability and/or use and the number of people in the study population infected with one or more of three types of soil-transmitted helminths. Meta-analysis of the data from these publications indicates that, compared to people with no access to sanitation facilities, people with access to sanitation facilities were half as likely to be infected with soil-transmitted helminths. Specifically, the odds ratios (ORs; chances) of infection with soil-transmitted helminths among people with access to latrines compared to people without access to latrines were 0.46, 0.56, and 0.58 for roundworm, whipworm, and hookworm, respectively; for all three helminths combined, the OR was 0.49. Use of (as opposed to access to) sanitation facilities also protected against soil-transmitted helminth infection (ORs of 0.78, 0.54, and 0.63 for roundworm, whipworm, and hookworm infections, respectively). Finally, combining the data for both access and use, people who either had or used a latrine were half as likely to be infected with a soil-transmitted helminth as people who neither had or used a latrine (OR 0.51).

What Do These Findings Mean?

The studies included in this systematic review and meta-analysis have several shortcomings. For example, most were cross-sectional surveys—studies that examined the effect of the availability/use of sanitation on helminth infections in a population at a single time point. Given this study design, people who had latrines may have shared other characteristics that were actually responsible for the observed reductions in the risk of soil-transmitted helminth infections. Moreover, the data on latrine availability and use was derived from questionnaires and may, therefore, be inaccurate because people are often ashamed to admit that they defecate outside. Finally, the overall quality of the included studies was low. Nevertheless, these findings confirm that providing access to, and promoting use of, sanitation facilities is an effective control measure for soil-transmitted helminthiasis. Thus, there should be more emphasis on expanding access to adequate sanitation in control strategies for soil-transmitted helminths. This change in emphasis would reinforce the effects of preventative chemotherapy and ongoing health education on helminthiasis, in an economic, sustainability, and public health sense. Importantly, it would also improve the control of other neglected tropical diseases such as schistosomiasis and trachoma and would reduce the incidence of diarrhea, and thus child mortality, in developing countries.

Additional Information

Please access these websites via the online version of this summary at http://dx.doi.org/10.1371/journal.pmed.1001162.

• The US National Institute of Allergy and Infectious Disease provides information on infections caused by soil-transmitted helminths

• The US Centers for Disease Control and Prevention also provides detailed information on roundworm, whipworm, and hookworm infections

• The World Health Organization provides information on soil-transmitted helminths, including a description of the current control strategy; the Partners for Parasite Control newsletter Action Against Worms focuses on specific areas of worm control; a teacher's resource book entitled A Lively and Healthy Me that deals with educating children about worm infections is also available

• The Global Network for Neglected Tropical Diseases, an advocacy initiative dedicated to raising the awareness, political will, and funding necessary to control and eliminate the most common neglected tropical diseases, provides information on infections with roundworm (ascariasis), whipworm (trichuriasis), and hookworm

• Two international programs promoting water sanitation are the World Health Organization Water Sanitation and Health program and the World Health Organization/United Nations Childrens Fund Joint Monitoring Programme for Water Supply and Sanitation

• The Water Supply and Sanitation Collaborative Council and Practical Action have information about approaches and technologies for sanitation