{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,27]],"date-time":"2026-02-27T19:23:38Z","timestamp":1772220218691,"version":"3.50.1"},"reference-count":34,"publisher":"Public Library of Science (PLoS)","issue":"6","license":[{"start":{"date-parts":[[2025,6,3]],"date-time":"2025-06-03T00:00:00Z","timestamp":1748908800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100010269","name":"Wellcome Trust","doi-asserted-by":"publisher","award":["220211"],"award-info":[{"award-number":["220211"]}],"id":[{"id":"10.13039\/100010269","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001322","name":"South African Medical Research Council","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100001322","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000865","name":"Bill and Melinda Gates Foundation","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000865","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100012640","name":"ExxonMobil Foundation","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100012640","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS One"],"abstract":"<jats:p>\n                    To address the current threat of antimalarial resistance, countries need innovative solutions for timely and informed decision-making. Integrating molecular surveillance for drug-resistant malaria into routine malaria surveillance in pre-elimination contexts offers a potential early warning mechanism for further investigation and response. However, there is limited evidence on what influences the performance of such a system in resource-limited settings. From March 2018 to February 2020, a sequential mixed-methods study was conducted in primary healthcare facilities in a South African pre-elimination setting to explore factors influencing the flow, quality and linkage of malaria case notification and molecular resistance marker data. Using a process-oriented framework, we undertook monthly and quarterly data linkage and consistency analyses at different levels of the health system, as well as a survey, focus group discussions and interviews to identify potential barriers to, and enhancers of, the roll-out and uptake of this integrated information system. Over two years, 4,787 confirmed malaria cases were notified from 42 primary healthcare facilities in the Nkomazi sub-district, Mpumalanga, South Africa. Of the notified cases, 78.5% (n\u2009=\u20093,758) were investigated, and 55.1% (n\u2009=\u20092,636) were successfully linked to their\n                    <jats:italic>Plasmodium falciparum<\/jats:italic>\n                    molecular resistance marker profiles. Five tangible processes\u2014malaria case detection and notification, sample collection, case investigation, analysis and reporting\u2014were identified within the process-oriented logic model. Workload, training, ease of use, supervision, leadership, and resources were recognized as cross-cutting influencers affecting the program\u2019s performance. Approaching malaria elimination, linking molecular markers of antimalarial resistance to routine malaria surveillance is feasible. However, cross-cutting barriers inherent in the healthcare system can influence its success in a resource-limited setting.\n                  <\/jats:p>","DOI":"10.1371\/journal.pone.0305885","type":"journal-article","created":{"date-parts":[[2025,6,3]],"date-time":"2025-06-03T13:37:14Z","timestamp":1748957834000},"page":"e0305885","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":0,"title":["Factors affecting integration of an early warning system for antimalarial drug resistance within a routine surveillance system in a pre-elimination setting in Sub-Saharan Africa"],"prefix":"10.1371","volume":"20","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-4608-7167","authenticated-orcid":true,"given":"Frank 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Smart surveillance towards malaria elimination in Mpumalanga, South Africa (SS4ME): novel approaches for mapping antimalarial resistance (Protocol). 2017 (Unpublished)."},{"key":"pone.0305885.ref016","volume-title":"Malaria Elimination Strategic Plan for South Africa 2019 - 2023","author":"National Department of Health South Africa.","year":"2019"},{"key":"pone.0305885.ref017","volume-title":"National guidelines for the treatment of malaria, South Africa 2018 (Updated January 2019)","author":"National Institute for Communicable Diseases.","year":"2019"},{"issue":"7676","key":"pone.0305885.ref018","first-page":"979","article-title":"Developing and evaluating complex interventions: the new Medical Research Council guidance.","volume":"337","author":"P Craig","year":"2008","journal-title":"Br Med J"},{"issue":"1","key":"pone.0305885.ref019","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1002\/jrsm.1254","article-title":"Towards a taxonomy of logic models in systematic reviews 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