Coverage of community-wide mass drug administration platforms for soil-transmitted helminths in Benin, India, and Malawi: findings from the DeWorm3 project.


Journal

Infectious diseases of poverty
ISSN: 2049-9957
Titre abrégé: Infect Dis Poverty
Pays: England
ID NLM: 101606645

Informations de publication

Date de publication:
08 Oct 2024
Historique:
received: 05 06 2024
accepted: 12 09 2024
medline: 9 10 2024
pubmed: 9 10 2024
entrez: 8 10 2024
Statut: epublish

Résumé

Soil-transmitted helminths (STH) affect approximately 1.5 billion people globally. The current STH control strategy is annual or twice-annual preventive chemotherapy, typically school-based deworming targeting children and women of reproductive age. Mathematical modeling suggests that it may be possible to interrupt STH transmission through high-coverage community-wide mass drug administration (cMDA). DeWorm3 is a cluster randomized trial testing cMDA for prevalence reduction and transmission interruption. The purpose of this study is to describe coverage of cMDA in study clusters over time and correlates of coverage at individual and cluster levels. From 2018-2020, DeWorm3 delivered six rounds of cMDA with 400 mg albendazole at sites in Benin, India, and Malawi. We report coverage, treatment uptake, and directly observed therapy across all rounds. Factors associated with coverage at the cluster level were identified using binomial generalized estimating equations, while factors associated with non-treatment at the individual level were identified using binomial mixed-effects models. Coverage was high across all clusters and rounds, exceeding the WHO target of 75% in all sites and across all rounds (78% to 95%); cluster-level coverage tended to increase over time. Younger, unmarried, and migratory adults were more likely to be untreated at all sites; adult males were more likely to be untreated in Benin and Malawi. Among children, girls were more likely to be untreated, as were non-school-attending and migratory children. Higher adult education was associated with greater odds of non-treatment among adults, but lower odds among children in the household. Belonging to a less wealthy or minority language-speaking household was associated with non-treatment among both adults and children. It is possible to deliver community-wide MDA with high coverage. Unique individual and community-level factors influence treatment across settings, and these may be addressed through targeted programming. Field Studies on the Feasibility of Interrupting the Transmission of Soil-transmitted Helminths (STH), NCT03014167.

Sections du résumé

BACKGROUND BACKGROUND
Soil-transmitted helminths (STH) affect approximately 1.5 billion people globally. The current STH control strategy is annual or twice-annual preventive chemotherapy, typically school-based deworming targeting children and women of reproductive age. Mathematical modeling suggests that it may be possible to interrupt STH transmission through high-coverage community-wide mass drug administration (cMDA). DeWorm3 is a cluster randomized trial testing cMDA for prevalence reduction and transmission interruption. The purpose of this study is to describe coverage of cMDA in study clusters over time and correlates of coverage at individual and cluster levels.
METHODS METHODS
From 2018-2020, DeWorm3 delivered six rounds of cMDA with 400 mg albendazole at sites in Benin, India, and Malawi. We report coverage, treatment uptake, and directly observed therapy across all rounds. Factors associated with coverage at the cluster level were identified using binomial generalized estimating equations, while factors associated with non-treatment at the individual level were identified using binomial mixed-effects models.
RESULTS RESULTS
Coverage was high across all clusters and rounds, exceeding the WHO target of 75% in all sites and across all rounds (78% to 95%); cluster-level coverage tended to increase over time. Younger, unmarried, and migratory adults were more likely to be untreated at all sites; adult males were more likely to be untreated in Benin and Malawi. Among children, girls were more likely to be untreated, as were non-school-attending and migratory children. Higher adult education was associated with greater odds of non-treatment among adults, but lower odds among children in the household. Belonging to a less wealthy or minority language-speaking household was associated with non-treatment among both adults and children.
CONCLUSIONS CONCLUSIONS
It is possible to deliver community-wide MDA with high coverage. Unique individual and community-level factors influence treatment across settings, and these may be addressed through targeted programming.
TRIAL REGISTRATION BACKGROUND
Field Studies on the Feasibility of Interrupting the Transmission of Soil-transmitted Helminths (STH), NCT03014167.

Identifiants

pubmed: 39380086
doi: 10.1186/s40249-024-01241-0
pii: 10.1186/s40249-024-01241-0
doi:

Substances chimiques

Soil 0
Albendazole F4216019LN
Anthelmintics 0

Banques de données

ClinicalTrials.gov
['NCT03014167']

Types de publication

Journal Article Randomized Controlled Trial

Langues

eng

Sous-ensembles de citation

IM

Pagination

72

Subventions

Organisme : Bill and Melinda Gates Foundation
ID : OPP1129535

Informations de copyright

© 2024. The Author(s).

Références

World Health Organization. Soil-transmitted helminth infections. https://www.who.int/news-room/fact-sheets/detail/soil-transmitted-helminth-infections . Accessed 13 Feb 2024.
Jourdan PM, Lamberton PH, Fenwick A, Addiss DG. Soil-transmitted helminth infections. The Lancet. 2018;391(10117):252–65.
doi: 10.1016/S0140-6736(17)31930-X
Campbell SJ, Nery SV, Doi SA, Gray DJ, Soares Magalhães RJ, McCarthy JS, et al. Complexities and perplexities: a critical appraisal of the evidence for soil-transmitted helminth infection-related morbidity. PLoS Negl Trop Dis. 2016;10(5): e0004566.
doi: 10.1371/journal.pntd.0004566 pubmed: 27196100 pmcid: 4873196
WHO. Preventive chemotherapy to control soil-transmitted helminth infections in at-risk population groups. Geneva: World Health Organization; 2017.
Macfarlane CL, Dean L, Thomson R, Garner P. Community drug distributors for mass drug administration in neglected tropical disease programmes: systematic review and analysis of policy documents. J Glob Health. 2019. https://doi.org/10.7189/jogh.09.020414 .
doi: 10.7189/jogh.09.020414 pubmed: 31662849 pmcid: 6790237
Clarke NE, Clements AC, Doi SA, Wang D, Campbell SJ, Gray D, et al. Differential effect of mass deworming and targeted deworming for soil-transmitted helminth control in children: a systematic review and meta-analysis. Lancet. 2017;389(10066):287–97.
doi: 10.1016/S0140-6736(16)32123-7 pubmed: 27979381
Pullan RL, Halliday KE, Oswald WE, Mcharo C, Beaumont E, Kepha S, et al. Effects, equity, and cost of school-based and community-wide treatment strategies for soil-transmitted helminths in Kenya: a cluster-randomised controlled trial. Lancet. 2019;393(10185):2039–50.
doi: 10.1016/S0140-6736(18)32591-1 pubmed: 31006575 pmcid: 6525786
Brooker SJ, Mwandawiro CS, Halliday KE, Njenga SM, Mcharo C, Gichuki PM, et al. 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(10): e008950.
doi: 10.1136/bmjopen-2015-008950 pubmed: 26482774 pmcid: 4611208
Njenga SM, Mwandawiro CS, Muniu E, Mwanje MT, Haji FM, Bockarie MJ. Adult population as potential reservoir of NTD infections in rural villages of Kwale district, Coastal Kenya: implications for preventive chemotherapy interventions policy. Parasit Vectors. 2011;4(1):1–6.
doi: 10.1186/1756-3305-4-175
Hasegawa M, Pilotte N, Kikuchi M, Means AR, Papaiakovou M, Gonzalez AM, et al. What does soil-transmitted helminth elimination look like? Results from a targeted molecular detection survey in Japan. Parasit Vectors. 2020;13:1–11.
doi: 10.1186/s13071-019-3875-z
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 Lond B Biol Sci. 2014;369(1645):20130435.
doi: 10.1098/rstb.2013.0435 pubmed: 24821921 pmcid: 4024228
Anderson RM, Turner HC, Truscott JE, Hollingsworth TD, Brooker SJ. Should the goal for the treatment of soil transmitted helminth (STH) infections be changed from morbidity control in children to community-wide transmission elimination? PLoS Negl Trop Dis. 2015;9(8): e0003897.
doi: 10.1371/journal.pntd.0003897 pubmed: 26291538 pmcid: 4546270
Anderson RM, Truscott JE, Pullan RL, Brooker SJ, Hollingsworth TD. How effective is school-based deworming for the community-wide control of soil-transmitted helminths? PLoS Negl Trop Dis. 2013;7(2): e2027.
doi: 10.1371/journal.pntd.0002027 pubmed: 23469293 pmcid: 3585037
Truscott JE, Werkman M, Wright JE, Farrell SH, Sarkar R, Ásbjörnsdóttir K, et al. Identifying optimal threshold statistics for elimination of hookworm using a stochastic simulation model. Parasit Vectors. 2017;10(1):1–12.
doi: 10.1186/s13071-017-2256-8
Truscott J, Hollingsworth TD, Anderson R. Modeling the interruption of the transmission of soil-transmitted helminths by repeated mass chemotherapy of school-age children. PLoS Negl Trop Dis. 2014;8(12): e3323.
doi: 10.1371/journal.pntd.0003323 pubmed: 25474477 pmcid: 4256169
Krentel A, Fischer PU, Weil GJ. A review of factors that influence individual compliance with mass drug administration for elimination of lymphatic filariasis. PLoS Negl Trop Dis. 2013;7(11): e2447.
doi: 10.1371/journal.pntd.0002447 pubmed: 24278486 pmcid: 3836848
Krentel A, Damayanti R, Titaley CR, Suharno N, Bradley M, Lynam T, et al. Improving coverage and compliance in mass drug administration for the elimination of LF in two ‘endgame’districts in Indonesia using micronarrative surveys. PLoS Negl Trop Dis. 2016;10(11): e0005027.
doi: 10.1371/journal.pntd.0005027 pubmed: 27812107 pmcid: 5094770
Oswald WE, Kepha S, Halliday KE, Mcharo C, Witek-McManus S, Hardwick RJ, et al. Patterns of individual non-treatment during multiple rounds of mass drug administration for control of soil-transmitted helminths in the TUMIKIA trial, Kenya: a secondary longitudinal analysis. Lancet Glob Health. 2020;8(11):e1418–26.
doi: 10.1016/S2214-109X(20)30344-2 pubmed: 33069302 pmcid: 7564382
Gwayi-Chore M-C, Aruldas K, Avokpaho E, Chirambo CM, Kaliappan SP, Houngbégnon P, et al. Defining optimal implementation packages for delivering community-wide mass drug administration for soil-transmitted helminths with high coverage. BMC Health Serv Res. 2022;22(1):1–10.
doi: 10.1186/s12913-022-08080-5
Astale T, Sata E, Zerihun M, Nute AW, Stewart AE, Gessese D, et al. Population-based coverage survey results following the mass drug administration of azithromycin for the treatment of trachoma in Amhara, Ethiopia. PLoS Negl Trop Dis. 2018;12(2): e0006270.
doi: 10.1371/journal.pntd.0006270 pubmed: 29451881 pmcid: 5833287
Jose R, Bougma R, Drabo F, Tukahebwa EM, Mkwanda S, Gass K, et al. Proxy responses for mass drug administration coverage surveys: the trends and biases when others are allowed to respond. Am J Trop Med Hyg. 2022;106(1):268.
doi: 10.4269/ajtmh.21-0817
Ásbjörnsdóttir KH, Ajjampur SSR, Anderson RM, Bailey R, Gardiner I, Halliday KE, et al. Assessing the feasibility of interrupting the transmission of soil-transmitted helminths through mass drug administration: the DeWorm3 cluster randomized trial protocol. PLoS Negl Trop Dis. 2018;12(1): e0006166.
doi: 10.1371/journal.pntd.0006166 pubmed: 29346377 pmcid: 5773085
Means AR, Ajjampur SS, Bailey R, Galactionova K, Gwayi-Chore M-C, Halliday K, et al. Evaluating the sustainability, scalability, and replicability of an STH transmission interruption intervention: the DeWorm3 implementation science protocol. PLoS Negl Trop Dis. 2018;12(1): e0005988.
doi: 10.1371/journal.pntd.0005988 pubmed: 29346376 pmcid: 5773078
Morozoff C, Avokpaho E, Kaliappan SP, Simwanza J, Gideon SP, Lungu W, et al. Costs of community-wide mass drug administration and school-based deworming for soil-transmitted helminths: evidence from a randomised controlled trial in Benin, India and Malawi. BMJ Open. 2022;12(7): e059565.
doi: 10.1136/bmjopen-2021-059565 pubmed: 35803632 pmcid: 9272108
Oswald WE, Kennedy DS, Farzana J, Kaliappan SP, Atindegla E, Houngbégnon P, et al. Development and application of an electronic treatment register: a system for enumerating populations and monitoring treatment during mass drug administration. Glob Health Action. 2020;13(1):1785146.
doi: 10.1080/16549716.2020.1785146 pubmed: 32666905 pmcid: 7480461
Cui J. QIC: Stata module to compute model selection criterion in GEE analyses. 2008.
WHO. Ending the neglect to attain the Sustainable Development Goals: a road map for neglected tropical diseases 2021–2030. Geneva: World Health Organization; 2020.
Saxena M, Roll A, Walson JL, Pearman E, Legge H, Nindi P, et al. “Our desire is to make this village intestinal worm free”: Identifying determinants of high coverage of community-wide mass drug administration for soil transmitted helminths in Benin, India, and Malawi. PLoS Negl Trop Dis. 2024;18(2): e0011819.
doi: 10.1371/journal.pntd.0011819 pubmed: 38319937 pmcid: 10846705
Cohn DA, Kelly MP, Bhandari K, Zoerhoff KL, Batcho WE, Drabo F, et al. Gender equity in mass drug administration for neglected tropical diseases: data from 16 countries. Int Health. 2019;11(5):370–8.
doi: 10.1093/inthealth/ihz012 pubmed: 30845318 pmcid: 6748770
Theobald S, MacPherson EE, Dean L, Jacobson J, Ducker C, Gyapong M, et al. 20 years of gender mainstreaming in health: lessons and reflections for the neglected tropical diseases community. BMJ Glob Health. 2017;2(4): e000512.
doi: 10.1136/bmjgh-2017-000512 pubmed: 29177100 pmcid: 5687534
Avokpaho EF, Houngbégnon P, Accrombessi M, Atindégla E, Yard E, Means Rubin A, et al. Factors associated with soil-transmitted helminths infection in Benin: findings from the DeWorm3 study. PLoS Negl Trop Dis. 2021;15(8): e0009646.
doi: 10.1371/journal.pntd.0009646 pubmed: 34403424 pmcid: 8396766
Witek-McManus S, Simwanza J, Chisambi AB, Kepha S, Kamwendo Z, Mbwinja A, et al. Epidemiology of soil-transmitted helminths following sustained implementation of routine preventive chemotherapy: demographics and baseline results of a cluster randomised trial in southern Malawi. PLoS Negl Trop Dis. 2021;15(5): e0009292.
doi: 10.1371/journal.pntd.0009292 pubmed: 33979325 pmcid: 8224978
Ajjampur SS, Kaliappan SP, Halliday KE, Palanisamy G, Farzana J, Manuel M, et al. Epidemiology of soil transmitted helminths and risk analysis of hookworm infections in the community: Results from the DeWorm3 trial in southern India. PLoS Negl Trop Dis. 2021;15(4): e0009338.
doi: 10.1371/journal.pntd.0009338 pubmed: 33930024 pmcid: 8184002
Avokpaho E, Lawrence S, Roll A, Titus A, Jacob Y, Kaliappan SP, et al. It depends on how you tell: a qualitative diagnostic analysis of the implementation climate for community-wide mass drug administration for soil-transmitted helminth. BMJ Open. 2022;12(6): e061682.
doi: 10.1136/bmjopen-2022-061682 pubmed: 35701056 pmcid: 9198697
Silumbwe A, Zulu JM, Halwindi H, Jacobs C, Zgambo J, Dambe R, et al. A systematic review of factors that shape implementation of mass drug administration for lymphatic filariasis in sub-Saharan Africa. BMC Public Health. 2017;17:1–15.
doi: 10.1186/s12889-017-4414-5

Auteurs

Arianna Rubin Means (AR)

Department of Global Health, University of Washington, Seattle, Washington, USA. aerubin@uw.edu.
The DeWorm3 Project, University of Washington, Seattle, Washington, USA. aerubin@uw.edu.

Kristjana Hrönn Ásbjörnsdóttir (KH)

Centre of Public Health Sciences, University of Iceland, Reykjavík, Iceland.
The DeWorm3 Project, University of Washington, Seattle, Washington, USA.

Katherine C Sharrock (KC)

Department of Global Health, University of Washington, Seattle, Washington, USA.
The DeWorm3 Project, University of Washington, Seattle, Washington, USA.

Sean R Galagan (SR)

Department of Global Health, University of Washington, Seattle, Washington, USA.
The DeWorm3 Project, University of Washington, Seattle, Washington, USA.

Kumudha Aruldas (K)

The Wellcome Trust Research Laboratory, Division of Gastrointestinal Sciences, Christian Medical College, Vellore, India.

Euripide Avokpaho (E)

Institut de Recherche Clinique du Bénin, Abomey-Calavi, Bénin.

Félicien Chabi (F)

Institut de Recherche Clinique du Bénin, Abomey-Calavi, Bénin.

Katherine E Halliday (KE)

Department of Disease Control, Faculty of Infectious and Tropical Diseases, London School of Hygiene & Tropical Medicine, London, UK.

Parfait Houngbegnon (P)

Institut de Recherche Clinique du Bénin, Abomey-Calavi, Bénin.

Gideon John Israel (GJ)

The Wellcome Trust Research Laboratory, Division of Gastrointestinal Sciences, Christian Medical College, Vellore, India.

Saravanakumar Puthupalayam Kaliappan (SP)

The Wellcome Trust Research Laboratory, Division of Gastrointestinal Sciences, Christian Medical College, Vellore, India.

David Kennedy (D)

Department of Disease Control, Faculty of Infectious and Tropical Diseases, London School of Hygiene & Tropical Medicine, London, UK.

Hugo Legge (H)

Department of Disease Control, Faculty of Infectious and Tropical Diseases, London School of Hygiene & Tropical Medicine, London, UK.

William E Oswald (WE)

Department of Disease Control, Faculty of Infectious and Tropical Diseases, London School of Hygiene & Tropical Medicine, London, UK.
Global Health Division, International Development Group, Research Triangle Institute (RTI) International, Research Triangle Park, NC, USA.

Gokila Palanisamy (G)

The Wellcome Trust Research Laboratory, Division of Gastrointestinal Sciences, Christian Medical College, Vellore, India.

Elliott Rogers (E)

Department of Disease Control, Faculty of Infectious and Tropical Diseases, London School of Hygiene & Tropical Medicine, London, UK.
Division of Medicine, University College London, London, UK.

Joseph Timothy (J)

Department of Disease Control, Faculty of Infectious and Tropical Diseases, London School of Hygiene & Tropical Medicine, London, UK.

Emily Pearman (E)

The DeWorm3 Project, University of Washington, Seattle, Washington, USA.

Rohan Michael Ramesh (RM)

The Wellcome Trust Research Laboratory, Division of Gastrointestinal Sciences, Christian Medical College, Vellore, India.

James Simwanza (J)

Blantyre Institute for Community Outreach, Lions Sight First Eye Hospital, Blantyre, Malawi.

Jasmine Farzana Sheik-Abdullah (JF)

The Wellcome Trust Research Laboratory, Division of Gastrointestinal Sciences, Christian Medical College, Vellore, India.

Mariyam Sheikh (M)

Department of Global Health, University of Washington, Seattle, Washington, USA.
The DeWorm3 Project, University of Washington, Seattle, Washington, USA.

Comlanvi Innocent Togbevi (CI)

Institut de Recherche Clinique du Bénin, Abomey-Calavi, Bénin.

Stefan Witek-McManus (S)

Department of Disease Control, Faculty of Infectious and Tropical Diseases, London School of Hygiene & Tropical Medicine, London, UK.
Department of Population Health, Faculty of Epidemiology and Population Health, London School of Hygiene & Tropical Medicine, London, UK.

Rachel L Pullan (RL)

Department of Disease Control, Faculty of Infectious and Tropical Diseases, London School of Hygiene & Tropical Medicine, London, UK.

Robin Bailey (R)

Clinical Research Department, Faculty of Infectious and Tropical Diseases, London School of Hygiene & Tropical Medicine, London, UK.
Blantyre Institute for Community Outreach, Lions Sight First Eye Hospital, Blantyre, Malawi.

Khumbo Kalua (K)

Blantyre Institute for Community Outreach, Lions Sight First Eye Hospital, Blantyre, Malawi.
School of Population and Public Health, University of British Columbia, Vancouver, British Columbia, Canada.

Moudachirou Ibikounlé (M)

Institut de Recherche Clinique du Bénin, Abomey-Calavi, Bénin.
Tropical Infectious Diseases Research Center (TIDRC)Université d'Abomey-Calavi, Abomey-Calavi, Bénin.

Adrian J F Luty (AJF)

Université Paris Cité, Institut de Recherche pour le Développement, MERIT, Paris, F-75006, France.

Sitara S R Ajjampur (SSR)

The Wellcome Trust Research Laboratory, Division of Gastrointestinal Sciences, Christian Medical College, Vellore, India.

Judd L Walson (JL)

The DeWorm3 Project, University of Washington, Seattle, Washington, USA.
Department of International Health, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD, USA.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH