Combined effectiveness of anthelmintic chemotherapy and WASH among HIV-infected adults

Arianna R Means, Lisette van Lieshout, Eric Brienen, Krista Yuhas, James P Hughes, Paul Ndungu, Benson Singa, Judd L Walson, Arianna R Means, Lisette van Lieshout, Eric Brienen, Krista Yuhas, James P Hughes, Paul Ndungu, Benson Singa, Judd L Walson

Abstract

Introduction: Current global helminth control guidelines focus on regular deworming of targeted populations for morbidity control. However, water, sanitation, and hygiene (WASH) interventions may also be important for reducing helminth transmission. We evaluated the impact of different potential helminth protective packages on infection prevalence, including repeated treatment with albendazole and praziquantel with and without WASH access.

Methodology/principal findings: We conducted a cohort study nested within a randomized trial of empiric deworming of HIV-infected adults in Kenya. Helminth infections and infection intensity were diagnosed using semi-quantitative real-time PCR. We conducted a manual forward stepwise model building approach to identify if there are packages of interventions that may be protective against an STH infection of any species (combined outcome) and each helminth species individually. We conducted secondary analyses using the same approach only amongst individuals with no anthelmintis exposure. We used interaction terms to test for potential intervention synergy. Approximately 22% of the 701 stool samples provided were helminth-infected, most of which were of low to moderate intensity. The odds of infection with any STH species were lower for individuals who were treated with albendazole (aOR:0.11, 95%CI: 0.05, 0.20, p<0.001), adjusting for age and sex. Although most WASH conditions demonstrated minimal additional benefit in reducing the probability of infection with any STH species, access to safe flooring did appear to offer some additional protection (aOR:0.34, 95%CI: 0.20, 0.56, p<0.001). For schistosomiasis, only treatment with praziquantel was protective (aOR:0.30 95%CI: 0.14, 0.60, p = 0.001). Amongst individuals who were not treated with albendazole or praziquantel, the most protective intervention package to reduce probability of STH infections included safe flooring (aOR:0.34, 95%CI: 0.20, 0.59, p<0.001) and latrine access (aOR:0.59, 95%CI: 0.35, 0.99, p = 0.05). Across all species, there was no evidence of synergy or antagonism between anthelmintic chemotherapy with albendazole or praziquantel and WASH resources.

Conclusions/significance: Deworming is effective in reducing the probability of helminth infections amongst HIV-infected adults. With the exception of safe flooring, WASH offers minimal additional benefit. However, WASH does appear to significantly reduce infection prevalence in adults who are not treated with chemotherapy.

Trial registration: ClinicalTrials.gov, NCT00507221.

Conflict of interest statement

The authors have declared that no competing interests exist.

References

    1. WHO (2015) Soil-transmitted helminth infections. World Health Organization. pp. Media Centre.
    1. WHO (2002) Prevention and control of schistosomiasis and soil-transmitted helminthiasis: report of a WHO expert committee. Geneva. 1–57 p.
    1. WHO (2013) Rolling out and scaling up integrated preventive chemotherapy for selected neglected tropical diseases. Geneva: World Health Organization; 161–172 p.
    1. Keiser J, Utzinger J (2008) Efficacy of current drugs against soil-transmitted helminth infections: systematic review and meta-analysis. Jama 299: 1937–1948. doi:
    1. Utzinger J, Raso G, Brooker S, De Savigny D, Tanner M, et al. (2009) Schistosomiasis and neglected tropical diseases: Towards integrated and sustainable control and a word of caution. Parasitology 136: 1859–1874. doi:
    1. Utzinger J, Bergquist R, Shu-Hua X, Singer BH, Tanner M (2003) Sustainable schistosomiasis control—the way forward. Lancet 362: 1932–1934. doi:
    1. Hotez P (2006) Helminth Infections: Soil-transmitted Helminth Infections and Schistosomiasis Disease Control Priorities in Developing Countries. 2nd ed: World Bank.
    1. Brooker S, Clements AC, Bundy DA (2006) Global epidemiology, ecology and control of soil-transmitted helminth infections. Adv Parasitol 62: 221–261. doi:
    1. Coffeng LE, Bakker R, Montresor A, de Vlas SJ (2015) Feasibility of controlling hookworm infection through preventive chemotherapy: a simulation study using the individual-based WORMSIM modelling framework. Parasit Vectors 8: 541 doi:
    1. Anderson R, Truscott J, Hollingsworth TD (2014) The coverage and frequency of mass drug administration required to eliminate persistent transmission of soil-transmitted helminths. Philos Trans R Soc Lond B Biol Sci 369: 20130435 doi:
    1. Strunz EC, Addiss DG, Stocks ME, Ogden S, Utzinger J, et al. (2014) Water, sanitation, hygiene, and soil-transmitted helminth infection: a systematic review and meta-analysis. PLoS Med 11: e1001620 doi:
    1. Ziegelbauer K, Speich B, Mäusezahl D, Bos R, Keiser J, et al. (2012) Effect of Sanitation on Soil-Transmitted Helminth Infection: Systematic Review and Meta-Analysis. PLoS Med.
    1. Clasen T, Boisson S, Routray P, Torondel B, Bell M, et al. (2014) Effectiveness of a rural sanitation programme on diarrhoea, soil-transmitted helminth infection, and child malnutrition in Odisha, India: a cluster-randomised trial. The Lancet Global Health 2.
    1. Patil SR, Arnold BF, Salvatore AL, Briceno B, Ganguly S, et al. (2014) The effect of India's total sanitation campaign on defecation behaviors and child health in rural Madhya Pradesh: a cluster randomized controlled trial. PLoS Med 11: e1001709 doi:
    1. Nikolay B, Mwandawiro CS, Kihara JH, Okoyo C, Cano J, et al. (2015) Understanding Heterogeneity in the Impact of National Neglected Tropical Disease Control Programmes: Evidence from School-Based Deworming in Kenya. PLoS Negl Trop Dis 9: e0004108 doi:
    1. Freeman MC, Ogden S, Jacobson J, Abbott D, Addiss DG, et al. (2013) Integration of water, sanitation, and hygiene for the prevention and control of neglected tropical diseases: a rationale for inter-sectoral collaboration. PLoS Negl Trop Dis 7: e2439 doi:
    1. Campbell SJ, Savage GB, Gray DJ, Atkinson JA, Soares Magalhaes RJ, et al. (2014) Water, Sanitation, and Hygiene (WASH): a critical component for sustainable soil-transmitted helminth and schistosomiasis control. PLoS Negl Trop Dis 8: e2651 doi:
    1. Freeman MC, Clasen T, Brooker SJ, Akoko DO, Rheingans R (2013) The impact of a school-based hygiene, water quality and sanitation intervention on soil-transmitted helminth reinfection: a cluster-randomized trial. Am J Trop Med Hyg 89: 875–883. doi:
    1. Dumba R, Kaddu JB, Wabwire-Mangen F (2013) Design and implementation of participatory hygiene and sanitation transformation (PHAST) as a strategy to control soil-transmitted helminth infections in Luweero, Uganda. Afr Health Sci 13: 512–517. doi:
    1. Walson J, Singa B, Sangare L, Naulikha J, Piper B, et al. (2012) Empiric deworming to delay HIV disease progression in adults with HIV who are ineligible for initiation of antiretroviral treatment (the HEAT study): a multi-site, randomised trial. Lancet Infect Dis 12: 925–932. doi:
    1. Kaisar MM BE, Djuardi Y, Sartono E, Yazdanbakhsh M, Verweij JJ, Supali T, Van Lieshout L (2017) Improved diagnosis of Trichuris trichiura by using a bead-beating procedure on ethanol preserved stool samples prior to DNA isolation and the performance of multiplex real-time PCR for intestinal parasites. Parasitology (IN PRESS).
    1. Kaisar MMM, Brienen EAT, Djuardi Y, Sartono E, Yazdanbakhsh M, et al. (2017) Improved diagnosis of Trichuris trichiura by using a bead-beating procedure on ethanol preserved stool samples prior to DNA isolation and the performance of multiplex real-time PCR for intestinal parasites. Parasitology 144: 965–974. doi:
    1. Pillay P, Taylor M, Zulu SG, Gundersen SG, Verweij JJ, et al. (2014) Real-time polymerase chain reaction for detection of Schistosoma DNA in small-volume urine samples reflects focal distribution of urogenital Schistosomiasis in primary school girls in KwaZulu Natal, South Africa. Am J Trop Med Hyg 90: 546–552. doi:
    1. Rubin D (1987) Multiple imputation for nonresponse in surveys. New York: John Wiley & Sons.
    1. Beknazarova M, Whiley H, Ross K (2016) Advocating for both Environmental and Clinical Approaches to Control Human Strongyloidiasis. Pathogens 5.
    1. Liu R, Dong HF, Guo Y, Zhao QP, Jiang MS (2011) Efficacy of praziquantel and artemisinin derivatives for the treatment and prevention of human schistosomiasis: a systematic review and meta-analysis. Parasit Vectors 4: 201 doi:
    1. Campbell SJ, Nery SV, Wardell R, D'Este CA, Gray DJ, et al. (2017) Water, Sanitation and Hygiene (WASH) and environmental risk factors for soil-transmitted helminth intensity of infection in Timor-Leste, using real time PCR. PLoS Negl Trop Dis 11: e0005393 doi:
    1. Echazu A, Bonanno D, Juarez M, Cajal SP, Heredia V, et al. (2015) Effect of Poor Access to Water and Sanitation As Risk Factors for Soil-Transmitted Helminth Infection: Selectiveness by the Infective Route. PLoS Negl Trop Dis 9: e0004111 doi:
    1. Xu LQ, Xiao DH, Zhou CH, Zhang XQ, Lan SG, et al. (2001) [On cleanliness of hands in diminution of Ascaris lumbricoides infection in children]. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 19: 294–297.
    1. Bieri FA, Gray DJ, Williams GM, Raso G, Li YS, et al. (2013) Health-education package to prevent worm infections in Chinese schoolchildren. N Engl J Med 368: 1603–1612. doi:
    1. Gyorkos TW, Maheu-Giroux M, Blouin B, Casapia M (2013) Impact of health education on soil-transmitted helminth infections in schoolchildren of the Peruvian Amazon: a cluster-randomized controlled trial. PLoS Negl Trop Dis 7: e2397 doi:
    1. Mahmud MA, Spigt M, Bezabih AM, Pavon IL, Dinant GJ, et al. (2015) Efficacy of Handwashing with Soap and Nail Clipping on Intestinal Parasitic Infections in School-Aged Children: A Factorial Cluster Randomized Controlled Trial. PLoS Med 12: e1001837; discussion e1001837. doi:
    1. Gelaw A, Anagaw B, Nigussie B, Silesh B, Yirga A, et al. (2013) Prevalence of intestinal parasitic infections and risk factors among schoolchildren at the University of Gondar Community School, Northwest Ethiopia: a cross-sectional study. BMC Public Health. pp. 304.
    1. Grimes JE, Croll D, Harrison WE, Utzinger J, Freeman MC, et al. (2015) The roles of water, sanitation and hygiene in reducing schistosomiasis: a review. Parasit Vectors.
    1. Soares Magalhaes RJ, Barnett AG, Clements AC (2011) Geographical analysis of the role of water supply and sanitation in the risk of helminth infections of children in West Africa. Proc Natl Acad Sci U S A 108: 20084–20089. doi:
    1. Alemu A, Atnafu A, Addis Z, Shiferaw Y, Teklu T, et al. (2011) Soil transmitted helminths and schistosoma mansoni infections among school children in Zarima town, northwest Ethiopia. BMC Infect Dis 11: 189 doi:
    1. Steinmann P, Yap P, Utzinger J, Du ZW, Jiang JY, et al. (2014) Control of soil-transmitted helminthiasis in Yunnan province, People's Republic of China: experiences and lessons from a 5-year multi-intervention trial. Acta Trop 141: 271–280. doi:
    1. Asaolu SO, Ofoezie IE (2003) The role of health education and sanitation in the control of helminth infections. Acta Trop 86: 283–294.
    1. Nery SV, McCarthy JS, Traub R, Andrews RM, Black J, et al. (2015) A cluster-randomised controlled trial integrating a community-based water, sanitation and hygiene programme, with mass distribution of albendazole to reduce intestinal parasites in Timor-Leste: the WASH for WORMS research protocol. BMJ Open 5.
    1. Arndt MB, John-Stewart G, Richardson BA, Singa B, van Lieshout L, et al. (2013) Impact of helminth diagnostic test performance on estimation of risk factors and outcomes in HIV-positive adults. PLoS One 8: e81915 doi:
    1. Freeman MC, Chard AN, Nikolay B, Garn JV, Okoyo C, et al. (2015) Associations between school- and household-level water, sanitation and hygiene conditions and soil-transmitted helminth infection among Kenyan school children. Parasit Vectors 8: 412 doi:
    1. Means AR, Burns P, Sinclair D, Walson JL (2016) Antihelminthics in helminth-endemic areas: effects on HIV disease progression. Cochrane Database Syst Rev 4: Cd006419 doi:
    1. Campbell SJ, Nery SV, McCarthy JS, Gray DJ, Soares Magalhaes RJ, et al. (2016) A Critical Appraisal of Control Strategies for Soil-Transmitted Helminths. Trends Parasitol 32: 97–107. doi:
    1. Means AR, Jacobson J, Mosher AW, Walson JL (2016) Integrated Healthcare Delivery: A Qualitative Research Approach to Identifying and Harmonizing Perspectives of Integrated Neglected Tropical Disease Programs. PLoS Negl Trop Dis 10: e0005085 doi:

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