Effects, equity, and cost of school-based and community-wide treatment strategies for soil-transmitted helminths in Kenya: a cluster-randomised controlled trial

Abstract

Background: School-based deworming programmes can reduce morbidity attributable to soil-transmitted helminths in children but do not interrupt transmission in the wider community. We assessed the effects of alternative mass treatment strategies on community soil-transmitted helminth infection.

Methods: In this cluster-randomised controlled trial, 120 community units (clusters) serving 150 000 households in Kenya were randomly assigned (1:1:1) to receive albendazole through annual school-based treatment targeting 2-14 year olds or annual or biannual community-wide treatment targeting all ages. The primary outcome was community hookworm prevalence, assessed at 12 and 24 months through repeat cross-sectional surveys. Secondary outcomes were Ascaris lumbricoides and Trichuris trichiura prevalence, infection intensity of each soil-transmitted helminth species, and treatment coverage and costs. Analysis was by intention to treat. This trial is registered with ClinicalTrials.gov, number NCT02397772.

Findings: After 24 months, prevalence of hookworm changed from 18·6% (95% CI 13·9-23·2) to 13·8% (10·5-17·0) in the annual school-based treatment group, 17·9% (13·7-22·1) to 8·0% (6·0-10·1) in the annual community-wide treatment group, and 20·6% (15·8-25·5) to 6·2% (4·9-7·5) in the biannual community-wide treatment group. Relative to annual school-based treatment, the risk ratio for annual community-wide treatment was 0·59 (95% CI 0·42-0·83; p<0·001) and for biannual community-wide treatment was 0·46 (0·33-0·63; p<0·001). More modest reductions in risk were observed after 12 months. Risk ratios were similar across demographic and socioeconomic subgroups after 24 months. No adverse events related to albendazole were reported.

Interpretation: Community-wide treatment was more effective in reducing hookworm prevalence and intensity than school-based treatment, with little additional benefit of treating every 6 months, and was shown to be remarkably equitable in coverage and effects.

Funding: Bill & Melinda Gates Foundation, the Joint Global Health Trials Scheme of the Medical Research Council, the UK Department for International Development, the Wellcome Trust, and the Children's Investment Fund Foundation.

Copyright © 2019 The Author(s). Published by Elsevier Ltd. This is an Open Access article under CC-BY 4.0 license. Published by Elsevier Ltd.. All rights reserved.

Figures

Figure 1

Study profile 120 community units were randomly assigned to either routine school-based deworming or community-wide treatment delivered once or twice a year. No community units were lost to follow up, and none discontinued the intervention. All communities were included in the analysis at 12 and 24 months. Reported cluster sizes are based on the updated sampling frame used for the 24-month evaluation survey. Additional information regarding households and individuals not reached are provided in appendix.

Figure 2

Map of the study area Kwale County consists of four subcounties, all of which were included in the trial. The inset shows the location of Kwale County in Kenya.

References

1. 1. WHO . World Health Organization; Geneva: 2012. Accelerating work to overcome the global impact of neglected tropical diseases. A roadmap for implementation.
   2. WH, ccelerating work to overcome the global impact of neglected tropical diseases. A roadmap for implementatio, n 201, 2 World Health Organizatio, eneva
2. 1. WHO . World Health Organization; Geneva: 2017. Guideline: preventive chemotherapy to control soil-transmitted helminth infections in at-risk population groups.
   2. WH, uideline: preventive chemotherapy to control soil-transmitted helminth infections in at-risk population group, s 201, 7 World Health Organizatio, eneva
3. 1. WHO Schistosomiasis and soil-transmitted helminthiases: number of people treated in 2016. Wkly Epidemiol Rec. 2017;49:749–760.
   2. WH, chistosomiasis and soil-transmitted helminthiases: number of people treated in 2016. Wkly Epidemiol Rec, 49, 2017, 749–760
4. 1. Truscott JE, Hollingsworth TD, Brooker SJ, Anderson RM. Can chemotherapy alone eliminate the transmission of soil transmitted helminths? Parasit Vectors. 2014;7:266.
   2. JE Truscott, TD Hollingsworth, SJ Brooker, RM Anderson. Can chemotherapy alone eliminate the transmission of soil transmitted helminths?. Parasit Vectors, 7, 2014, 266
5. 1. Anderson R, Truscott J, Hollingsworth TD. The coverage and frequency of mass drug administration required to eliminate persistent transmission of soil-transmitted helminths. Philos Trans R Soc B. 2014;369:20130435.
   2. R Anderson, J Truscott, TD Hollingsworth. The coverage and frequency of mass drug administration required to eliminate persistent transmission of soil-transmitted helminths. Philos Trans R Soc B, 369, 2014, 20130435
6. 1. Clarke NE, Clements ACA, Doi SA. Differential effect of mass deworming and targeted deworming for soil-transmitted helminth control in children: a systematic review and meta-analysis. Lancet. 2017;389:287–297.
   2. NE Clarke, ACA Clements, SA Doi. Differential effect of mass deworming and targeted deworming for soil-transmitted helminth control in children: a systematic review and meta-analysis. Lancet, 389, 2017, 287–297
7. 1. Uniting to Combat Neglected Tropical Diseases . Uniting to Combat Neglected Tropical Diseases; 2018. Reaching a billion. Ending neglected tropical diseases: a gateway to universal health coverage. Fifth progress report on the London Declaration on NTDs.
   2. Uniting to Combat Neglected Tropical Disease, eaching a billion. Ending neglected tropical diseases: a gateway to universal health coverage. Fifth progress report on the London Declaration on NTD, s 201, 8 Uniting to Combat Neglected Tropical Diseases
8. 1. Bangert M, Molyneux DH, Lindsay SW, Fitzpatrick C, Engels D. The cross-cutting contribution of the end of neglected tropical diseases to the sustainable development goals. Infect Dis Poverty. 2017;6:73.
   2. M Bangert, DH Molyneux, SW Lindsay, C Fitzpatrick, D Engels. The cross-cutting contribution of the end of neglected tropical diseases to the sustainable development goals. Infect Dis Poverty, 6, 2017, 73
9. 1. Fitzpatrick C, Engels D. Leaving no one behind: a neglected tropical disease indicator and tracers for the Sustainable Development Goals. Int Health. 2016;8(suppl 1):i15–i18.
   2. C Fitzpatrick, D Engels. Leaving no one behind: a neglected tropical disease indicator and tracers for the Sustainable Development Goals. Int Health, , 8 suppl 1 2016, i15–i18
10. 1. Okoyo C, Nikolay B, Kihara J. Monitoring the impact of a national school based deworming programme on soil-transmitted helminths in Kenya: the first three years, 2012–2014. Parasit Vectors. 2016;9:408.
    2. C Okoyo, B Nikolay, J Kihara. Monitoring the impact of a national school based deworming programme on soil-transmitted helminths in Kenya: the first three years, 2012–2014. Parasit Vectors, 9, 2016, 408
11. 1. Njomo DW, Amuyunzu-Nyamongo M, Magambo JK, Njenga SM. The role of personal opinions and experiences in compliance with mass drug administration for lymphatic filariasis elimination in Kenya. PLoS One. 2012;7:e48395.
    2. DW Njomo, M Amuyunzu-Nyamongo, JK Magambo, SM Njenga. The role of personal opinions and experiences in compliance with mass drug administration for lymphatic filariasis elimination in Kenya. PLoS One, 7, 2012, e48395
12. 1. Brooker SJ, Mwandawiro CS, Halliday KE. Interrupting transmission of soil-transmitted helminths: a study protocol for cluster randomised trials evaluating alternative treatment strategies and delivery systems in Kenya. BMJ Open. 2015;5:e008950.
    2. SJ Brooker, CS Mwandawiro, KE Halliday. Interrupting transmission of soil-transmitted helminths: a study protocol for cluster randomised trials evaluating alternative treatment strategies and delivery systems in Kenya. BMJ Open, 5, 2015, e008950
13. 1. Wilkinson T, Sculpher MJ, Claxton K. The international decision support initiative reference case for economic evaluation: an aid to thought. Value Health. 2016;19:921–928.
    2. T Wilkinson, MJ Sculpher, K Claxton. The international decision support initiative reference case for economic evaluation: an aid to thought. Value Health, 19, 2016, 921–928
14. 1. The World Bank . The World Bank; 2018. Official exchange rate (LCU per US$, period average)
    2. The World Ban, fficial exchange rate (LCU per US$, period average) 201, 8 The World Ban, ttps://
15. 1. Asbjornsdottir KH, Ajjampur SSR, Anderson RM. Assessing the feasibility of interrupting the transmission of soil-transmitted helminths through mass drug administration: the DeWorm3 cluster randomised trial protocol. PLoS Negl Trop Dis. 2018;12:e0006166.
    2. KH Asbjornsdottir, SSR Ajjampur, RM Anderson. Assessing the feasibility of interrupting the transmission of soil-transmitted helminths through mass drug administration: the DeWorm3 cluster randomised trial protocol. PLoS Negl Trop Dis, 12, 2018, e0006166
16. 1. Victora CG, Wagstaff A, Schellenberg JA, Gwatkin D, Claeson M, Habicht J-P. Applying an equity lens to child health and mortality: more of the same is not enough. Lancet. 2003;362:233–241.
    2. CG Victora, A Wagstaff, JA Schellenberg, D Gwatkin, M Claeson, J-P Habicht. Applying an equity lens to child health and mortality: more of the same is not enough. Lancet, 362, 2003, 233–241
17. 1. McCollum R, Gomez W, Theobald S, Taegtmeyer M. How equitable are community health worker programmes and which programme features influence equity of community health worker services? A systematic review. BMC Public Health. 2016;16:419.
    2. R McCollum, W Gomez, S Theobald, M Taegtmeyer. How equitable are community health worker programmes and which programme features influence equity of community health worker services? A systematic review. BMC Public Health, 16, 2016, 419
18. 1. Silumbwe A, Zulu JM, Halwindi H. A systematic review of factors that shape implementation of mass drug administration for lymphatic filariasis in sub-Saharan Africa. BMC Public Health. 2017;17:484.
    2. A Silumbwe, JM Zulu, H Halwindi. A systematic review of factors that shape implementation of mass drug administration for lymphatic filariasis in sub-Saharan Africa. BMC Public Health, 17, 2017, 484
19. 1. Turner HC, Truscott JE, Hollingsworth TD, Bettis AA, Brooker SJ, Anderson RM. Cost and cost-effectiveness of soil-transmitted helminth treatment programmes: systematic review and research needs. Parasit Vectors. 2015;8:355.
    2. HC Turner, JE Truscott, TD Hollingsworth, AA Bettis, SJ Brooker, RM Anderson. Cost and cost-effectiveness of soil-transmitted helminth treatment programmes: systematic review and research needs. Parasit Vectors, 8, 2015, 355
20. 1. Walker A, Willams K. What is the cost of deworming? A 2016 update. Evidence Action. 2016.
    2. A Walker, K Willams. What is the cost of deworming? A 2016 update. Evidence Action, , e 2016
21. 1. WHO . World Health Organization; Geneva: 2018. Report of the WHO Advisory Group on deworming in girls and women of reproductive age. Rockefeller Foundation Bellagio Center, Bellagio, Italy. 28–30 June 2017.
    2. WH, eport of the WHO Advisory Group on deworming in girls and women of reproductive age. Rockefeller Foundation Bellagio Center, Bellagio, Italy. 28–30 June 2017 201, 8 World Health Organizatio, eneva
22. 1. Anderson RM, May RM. Helminth infections of humans: mathematical models, population dynamics, and control. Adv Parasitol. 1985;24:1–101.
    2. RM Anderson, RM May. Helminth infections of humans: mathematical models, population dynamics, and control. Adv Parasitol, 24, 1985, 1–101
23. 1. Farrell SH, Truscott JE, Anderson RM. The importance of patient compliance in repeated rounds of mass drug administration (MDA) for the elimination of intestinal helminth transmission. Parasit Vectors. 2017;10:291.
    2. SH Farrell, JE Truscott, RM Anderson. The importance of patient compliance in repeated rounds of mass drug administration (MDA) for the elimination of intestinal helminth transmission. Parasit Vectors, 10, 2017, 291
24. 1. Palmeirim MS, Hurlimann E, Knopp S. Efficacy and safety of co-administered ivermectin plus albendazole for treating soil-transmitted helminths: a systematic review, meta-analysis and individual patient data analysis. PLoS Negl Trop Dis. 2018;12:e0006458.
    2. MS Palmeirim, E Hurlimann, S Knopp. Efficacy and safety of co-administered ivermectin plus albendazole for treating soil-transmitted helminths: a systematic review, meta-analysis and individual patient data analysis. PLoS Negl Trop Dis, 12, 2018, e0006458
25. 1. WHO . World Health Organization; Geneva: 2017. The selection and use of essential medicines: report of the WHO Expert Committee, 2017 (including the 20th WHO Model List of Essential Medicines and the 6th WHO Model List of Essential Medicines for Children)
    2. WH, he selection and use of essential medicines: report of the WHO Expert Committee, 2017 (including the 20th WHO Model List of Essential Medicines and the 6th WHO Model List of Essential Medicines for Children) 201, 7 World Health Organizatio, eneva
26. 1. Pion SDS, Chesnais CB, Weil GJ, Fischer PU, Missamou F, Boussinesq M. Effect of 3 years of biannual mass drug administration with albendazole on lymphatic filariasis and soil-transmitted helminth infections: a community-based study in Republic of the Congo. Lancet Infect Dis. 2017;17:763–769.
    2. SDS Pion, CB Chesnais, GJ Weil, PU Fischer, F Missamou, M Boussinesq. Effect of 3 years of biannual mass drug administration with albendazole on lymphatic filariasis and soil-transmitted helminth infections: a community-based study in Republic of the Congo. Lancet Infect Dis, 17, 2017, 763–769
27. 1. Strunz EC, Addiss DG, Stocks ME, Ogden S, Utzinger J, Freeman MC. Water, sanitation, hygiene, and soil-transmitted helminth infection: a systematic review and meta-analysis. PLoS Med. 2014;11:e1001620.
    2. EC Strunz, DG Addiss, ME Stocks, S Ogden, J Utzinger, MC Freeman. Water, sanitation, hygiene, and soil-transmitted helminth infection: a systematic review and meta-analysis. PLoS Med, 11, 2014, e1001620
28. 1. Clasen T, Boisson S, Routray P. Effectiveness of a rural sanitation programme on diarrhoea, soil-transmitted helminth infection, and child malnutrition in Odisha, India: a cluster-randomised trial. Lancet Glob Health. 2014;2:e645–e653.
    2. T Clasen, S Boisson, P Routray. Effectiveness of a rural sanitation programme on diarrhoea, soil-transmitted helminth infection, and child malnutrition in Odisha, India: a cluster-randomised trial. Lancet Glob Health, 2, 2014, e645–e653
29. 1. Freeman MC, Clasen T, Brooker SJ, Akoko DO, Rheingans R. 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. 2013;89:875–883.
    2. MC Freeman, T Clasen, SJ Brooker, DO Akoko, R Rheingans. 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, 2013, 875–883
30. 1. Vercruysse J, Albonico M, Behnke JM. Is anthelmintic resistance a concern for the control of human soil-transmitted helminths? Int J Parasitol Drugs Drug Res. 2011;1:14–27.
    2. J Vercruysse, M Albonico, JM Behnke. Is anthelmintic resistance a concern for the control of human soil-transmitted helminths?. Int J Parasitol Drugs Drug Res, 1, 2011, 14–27
31. 1. Nikolay B, Brooker SJ, Pullan RL. Sensitivity of diagnostic tests for human soil-transmitted helminth infections: a meta-analysis in the absence of a true gold standard. Int J Parasitol. 2014;44:765–774.
    2. B Nikolay, SJ Brooker, RL Pullan. Sensitivity of diagnostic tests for human soil-transmitted helminth infections: a meta-analysis in the absence of a true gold standard. Int J Parasitol, 44, 2014, 765–774
32. 1. Meurs L, Polderman AM, Vinkeles Melchers NVS. Diagnosing polyparasitism in a high-prevalence setting in Beira, Mozambique: detection of intestinal parasites in fecal samples by microscopy and real-Time PCR. PLoS Negl Trop Dis. 2017;11:e0005310.
    2. L Meurs, AM Polderman, NVS Vinkeles Melchers. Diagnosing polyparasitism in a high-prevalence setting in Beira, Mozambique: detection of intestinal parasites in fecal samples by microscopy and real-Time PCR. PLoS Negl Trop Dis, 11, 2017, e0005310
33. 1. Werkman M, Wright JE, Truscott JE. Testing for soil-transmitted helminth transmission elimination: analysing the impact of the sensitivity of different diagnostic tools. PLoS Negl Trop Dis. 2018;12:e0006114.
    2. M Werkman, JE Wright, JE Truscott. Testing for soil-transmitted helminth transmission elimination: analysing the impact of the sensitivity of different diagnostic tools. PLoS Negl Trop Dis, 12, 2018, e0006114