Coverage of community-wide mass drug administration platforms for soil-transmitted helminths in Benin, India, and Malawi: findings from the DeWorm3 project.
Humans
Malawi
/ epidemiology
Mass Drug Administration
/ statistics & numerical data
Female
Helminthiasis
/ drug therapy
Male
Soil
/ parasitology
Benin
/ epidemiology
India
/ epidemiology
Child
Adolescent
Adult
Albendazole
/ therapeutic use
Anthelmintics
/ therapeutic use
Young Adult
Child, Preschool
Helminths
/ drug effects
Middle Aged
Prevalence
Albendazole
Community
Coverage
Mass drug administration
Soil-transmitted helminths
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
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
72Subventions
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