{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,25]],"date-time":"2026-07-25T17:59:39Z","timestamp":1785002379787,"version":"3.55.0"},"reference-count":52,"publisher":"Public Library of Science (PLoS)","issue":"5","license":[{"start":{"date-parts":[[2023,5,9]],"date-time":"2023-05-09T00:00:00Z","timestamp":1683590400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000054","name":"National Cancer Institute","doi-asserted-by":"publisher","award":["U01CA275033"],"award-info":[{"award-number":["U01CA275033"]}],"id":[{"id":"10.13039\/100000054","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000054","name":"National Cancer Institute","doi-asserted-by":"publisher","award":["U01CA275033"],"award-info":[{"award-number":["U01CA275033"]}],"id":[{"id":"10.13039\/100000054","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000054","name":"National Cancer Institute","doi-asserted-by":"publisher","award":["U01CA275033"],"award-info":[{"award-number":["U01CA275033"]}],"id":[{"id":"10.13039\/100000054","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100007338","name":"Foundation for Barnes-Jewish Hospital","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100007338","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100007338","name":"Foundation for Barnes-Jewish Hospital","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100007338","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"<jats:sec id=\"sec001\"><jats:title>Background<\/jats:title><jats:p>Cervical cancer is the leading cause of cancer death in Zambia, where HIV prevalence is also high (11.3%). HIV heightens the risk of developing and dying from cervical cancer. The human papillomavirus (HPV) vaccine can prevent 90% of cervical cancers, and in Zambia is recommended for adolescent girls ages 14\u201315 years, including those with HIV. Currently they mainly deliver HPV vaccination via school-based campaigns, which may exclude the most vulnerable adolescents\u2014those out-of-school or who irregularly attend. Adolescents living with HIV (ALHIV) are more likely to have these vulnerabilities. Further, school-based campaigns are not tailored to the WHO-recommended HPV vaccination schedule for ALHIV (3 versus 2 doses). Integrating HPV vaccination into routine care in adolescent HIV clinics may ensure that ALHIV have access to vaccine at the WHO-recommended schedule. Such integration requires a multilevel approach, stakeholder engagement, and diversified implementation strategies, given known challenges of providing the HPV vaccine in LMICs, including Zambia.<\/jats:p><\/jats:sec><jats:sec id=\"sec002\"><jats:title>Methods<\/jats:title><jats:p>Our study aims to integrate HPV vaccination into routine care in adolescent HIV clinics. To achieve success, we will co-design a package of implementation strategies using a previously successful implementation research approach developed for cervical cancer prevention in LMICs: the Integrative Systems Praxis for Implementation Research (INSPIRE). INSPIRE is a novel, comprehensive approach to develop, implement, and evaluate implementation science efforts. Following key elements of INSPIRE, our specific aims are to: 1) Identify the unique multilevel contextual factors (barriers and facilitators) across HIV settings (rural, urban, peri-urban) that influence HPV vaccine uptake; 2) Use Implementation Mapping to translate stakeholder feedback and findings from Aim 1 into a package of implementation strategies to integrate HPV vaccine into HIV clinics; 3) Conduct a Hybrid Type 3 effectiveness-implementation trial to evaluate the package of multilevel implementation strategies for integrating HPV vaccine into HIV clinics.<\/jats:p><\/jats:sec><jats:sec id=\"sec003\"><jats:title>Discussion<\/jats:title><jats:p>Our research team has strong support, technical expertise, and resources (e.g., vaccines) from the Zambian Ministry of Health; and political will for scale-up. This stakeholder-based implementation model has the potential to be transported to HIV clinics across Zambia and serve as a model to address cancer prevention priorities for those with HIV in other LMICs.<\/jats:p><\/jats:sec><jats:sec id=\"sec004\"><jats:title>Trial registration<\/jats:title><jats:p>To be registered prior to Aim 3, when implementation strategies finalized.<\/jats:p><\/jats:sec>","DOI":"10.1371\/journal.pone.0285031","type":"journal-article","created":{"date-parts":[[2023,5,9]],"date-time":"2023-05-09T20:29:44Z","timestamp":1683664184000},"page":"e0285031","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":11,"title":["Leveraging health infrastructure to optimize HPV vaccination for adolescents in Zambia: Protocol for an implementation study"],"prefix":"10.1371","volume":"18","author":[{"given":"Sam","family":"Miti","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Thembekile","family":"Shato","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Comfort","family":"Asante","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ana","family":"Baumann","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3303-308X","authenticated-orcid":true,"given":"Gershom","family":"Chongwe","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0058-845X","authenticated-orcid":true,"given":"Patricia M.","family":"Bobo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michelle I.","family":"Silver","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4516-4407","authenticated-orcid":true,"given":"Jean M.","family":"Hunleth","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2023,5,9]]},"reference":[{"issue":"6","key":"pone.0285031.ref001","first-page":"394","article-title":"Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries","volume":"68","author":"F Bray","year":"2018","journal-title":"CA: a cancer journal for clinicians"},{"issue":"3","key":"pone.0285031.ref002","doi-asserted-by":"crossref","first-page":"209","DOI":"10.3322\/caac.21660","article-title":"Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries","volume":"71","author":"H Sung","year":"2021","journal-title":"CA Cancer J Clin"},{"key":"pone.0285031.ref003","unstructured":"WHO. Zambia: Cancer Country Profile 2020. 2020."},{"issue":"10224","key":"pone.0285031.ref004","doi-asserted-by":"crossref","first-page":"575","DOI":"10.1016\/S0140-6736(20)30068-4","article-title":"Impact of HPV vaccination and cervical screening on cervical cancer elimination: a comparative modelling analysis in 78 low-income and lower-middle-income countries","volume":"395","author":"M Brisson","year":"2020","journal-title":"The Lancet"},{"issue":"32","key":"pone.0285031.ref005","doi-asserted-by":"crossref","first-page":"4830","DOI":"10.1016\/j.vaccine.2018.02.023","article-title":"Model-estimated effectiveness of single dose 9-valent HPV vaccination for HIV-positive and HIV-negative females in South Africa","volume":"36","author":"N Tan","year":"2018","journal-title":"Vaccine"},{"key":"pone.0285031.ref006","doi-asserted-by":"crossref","first-page":"106399","DOI":"10.1016\/j.ypmed.2020.106399","article-title":"HPV vaccination introduction worldwide and WHO and UNICEF estimates of national HPV immunization coverage 2010\u20132019","volume":"144","author":"L Bruni","year":"2021","journal-title":"Preventive Medicine"},{"key":"pone.0285031.ref007","unstructured":"World Health Organization. Global strategy to accelerate the elimination of cervical cancer as a public health problem. 2020. 9240014101."},{"key":"pone.0285031.ref008","unstructured":"UNAIDS. Zambia: HIV and AIDS Estimates Country Factsheet 2020."},{"issue":"2","key":"pone.0285031.ref009","doi-asserted-by":"crossref","first-page":"e161","DOI":"10.1016\/S2214-109X(20)30459-9","article-title":"Estimates of the global burden of cervical cancer associated with HIV","volume":"9","author":"D Stelzle","year":"2021","journal-title":"The Lancet Global Health"},{"issue":"19","key":"pone.0285031.ref010","first-page":"241","article-title":"Human papillomavirus vaccines: WHO position paper, May 2017","volume":"92","author":"Organization WH","year":"2017","journal-title":"Weekly Epidemiological Record=Relev\u00e9 \u00e9pid\u00e9miologique hebdomadaire"},{"issue":"43","key":"pone.0285031.ref011","doi-asserted-by":"crossref","first-page":"5753","DOI":"10.1016\/j.vaccine.2017.05.069","article-title":"Electronic address swi. Human papillomavirus vaccines: WHO position paper, May 2017-Recommendations","volume":"35","author":"World Health Organization","year":"2017","journal-title":"Vaccine"},{"issue":"6","key":"pone.0285031.ref012","doi-asserted-by":"crossref","first-page":"e0177773","DOI":"10.1371\/journal.pone.0177773","article-title":"Lessons learnt from human papillomavirus (HPV) vaccination in 45 low- and middle-income countries","volume":"12","author":"KE Gallagher","year":"2017","journal-title":"PLoS One"},{"key":"pone.0285031.ref013","unstructured":"Human papillomavirus vaccines: WHO position paper, December 2022. 2022. Accessed 11 January 2023."},{"issue":"1","key":"pone.0285031.ref014","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s13643-019-0980-1","article-title":"Challenges and support for quality of life of youths living with HIV\/AIDS in schools and larger community in East Africa: a systematic review","volume":"8","author":"E Kimera","year":"2019","journal-title":"Systematic reviews"},{"key":"pone.0285031.ref015","first-page":"1","article-title":"Effects of HIV on gender gaps in school attendance of children in Zimbabwe: a non-linear multivariate decomposition analysis","author":"T Zinyemba","year":"2021","journal-title":"Education Economics"},{"issue":"1","key":"pone.0285031.ref016","first-page":"s4","article-title":"HIV and adolescents\u2019 educational attainment in South Africa: Disentangling the effect of infection in children and household members","volume":"2018","author":"J Akinyemi","year":"2018","journal-title":"South African Journal of Child Health"},{"key":"pone.0285031.ref017","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1016\/j.childyouth.2014.03.033","article-title":"Responding to adolescents living with HIV in Zambia: a social\u2013ecological approach","volume":"45","author":"G Mburu","year":"2014","journal-title":"Children and Youth Services Review"},{"key":"pone.0285031.ref018","unstructured":"WHO. Costing the National Strategic Plan on Prevention and Control of Cervical Cancer: Zambia, 2019\u20132023. 2020."},{"key":"pone.0285031.ref019","doi-asserted-by":"crossref","first-page":"370","DOI":"10.1186\/1471-2458-12-370","article-title":"Assessment of eight HPV vaccination programs implemented in lowest income countries","volume":"12","author":"J Ladner","year":"2012","journal-title":"BMC Public Health"},{"issue":"11","key":"pone.0285031.ref020","doi-asserted-by":"crossref","first-page":"821","DOI":"10.2471\/BLT.11.089862","article-title":"Human papillomavirus vaccine delivery strategies that achieved high coverage in low- and middle-income countries","volume":"89","author":"DS LaMontagne","year":"2011","journal-title":"Bull World Health Organ"},{"issue":"35","key":"pone.0285031.ref021","doi-asserted-by":"crossref","first-page":"4399","DOI":"10.1016\/j.vaccine.2014.06.064","article-title":"Achieving high uptake of human papillomavirus vaccine in Cameroon: lessons learned in overcoming challenges","volume":"32","author":"JG Ogembo","year":"2014","journal-title":"Vaccine"},{"issue":"3","key":"pone.0285031.ref022","doi-asserted-by":"crossref","first-page":"61","DOI":"10.3390\/vaccines6030061","article-title":"Prevention of cervical cancer in Sub-Saharan Africa: the advantages and challenges of HPV vaccination","volume":"6","author":"E Black","year":"2018","journal-title":"Vaccines"},{"issue":"37","key":"pone.0285031.ref023","doi-asserted-by":"crossref","first-page":"3811","DOI":"10.1016\/j.vaccine.2013.06.016","article-title":"Human papillomavirus (HPV) vaccine implementation in low and middle-income countries (LMICs): health system experiences and prospects","volume":"31","author":"J Wigle","year":"2013","journal-title":"Vaccine"},{"issue":"6","key":"pone.0285031.ref024","doi-asserted-by":"crossref","first-page":"701","DOI":"10.1093\/heapol\/czaa017","article-title":"Health systems constraints and facilitators of human papillomavirus immunization programmes in sub-Saharan Africa: a systematic review","volume":"35","author":"E Amponsah-Dacosta","year":"2020","journal-title":"Health Policy Plan"},{"issue":"32 Pt A","key":"pone.0285031.ref025","doi-asserted-by":"crossref","first-page":"4761","DOI":"10.1016\/j.vaccine.2018.02.003","article-title":"Status of HPV vaccine introduction and barriers to country uptake","volume":"36","author":"KE Gallagher","year":"2018","journal-title":"Vaccine"},{"issue":"1","key":"pone.0285031.ref026","first-page":"1","article-title":"Communication around HPV vaccination for adolescents in low-and middle-income countries: a systematic scoping overview of systematic reviews","volume":"8","author":"HS Foss","year":"2019","journal-title":"Systematic reviews"},{"issue":"5","key":"pone.0285031.ref027","article-title":"Stakeholders\u2019 Understandings of Human Papillomavirus (HPV) Vaccination in Sub-Saharan Africa: A Rapid Qualitative Systematic Review","volume":"9","author":"C Deignan","year":"2021","journal-title":"Vaccines (Basel)"},{"key":"pone.0285031.ref028","doi-asserted-by":"crossref","first-page":"274","DOI":"10.1016\/j.ypmed.2014.08.035","article-title":"HPV vaccine acceptability in Africa: a systematic review","volume":"69","author":"MS Cunningham","year":"2014","journal-title":"Preventive medicine"},{"issue":"9","key":"pone.0285031.ref029","doi-asserted-by":"crossref","first-page":"1710","DOI":"10.1158\/1055-9965.EPI-20-0501","article-title":"Integrative Systems Praxis for Implementation Research (INSPIRE): An Implementation Methodology to Facilitate the Global Elimination of Cervical Cancer","volume":"29","author":"PE Gravitt","year":"2020","journal-title":"Cancer Epidemiol Biomarkers Prev"},{"issue":"1","key":"pone.0285031.ref030","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1186\/s13012-020-0977-0","article-title":"Evaluating and optimizing the consolidated framework for implementation research (CFIR) for use in low- and middle-income countries: a systematic review","volume":"15","author":"AR Means","year":"2020","journal-title":"Implement Sci"},{"key":"pone.0285031.ref031","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1186\/1748-5908-4-50","article-title":"Fostering implementation of health services research findings into practice: a consolidated framework for advancing implementation science","volume":"4","author":"LJ Damschroder","year":"2009","journal-title":"Implement Sci"},{"issue":"1","key":"pone.0285031.ref032","doi-asserted-by":"crossref","first-page":"e126","DOI":"10.1017\/cts.2021.789","article-title":"Understanding and applying the RE-AIM framework: Clarifications and resources","volume":"5","author":"JS Holtrop","year":"2021","journal-title":"Journal of Clinical and Translational Science"},{"key":"pone.0285031.ref033","doi-asserted-by":"crossref","DOI":"10.4324\/9780429286650","volume-title":"Rapid Ethnographic Assessments: A Practical Approach and Toolkit for Collaborative Community Research","author":"T Sangaramoorthy","year":"2020"},{"key":"pone.0285031.ref034","doi-asserted-by":"crossref","DOI":"10.4135\/9781529682687","volume-title":"Doing Rapid Qualitative Research","author":"C. Vindrola-Padros","year":"2021"},{"issue":"5","key":"pone.0285031.ref035","doi-asserted-by":"crossref","first-page":"700","DOI":"10.1177\/1049732318809940","article-title":"Value and Limitations of Broad Brush Surveys Used in Community-Randomized Trials in Southern Africa","volume":"29","author":"V Bond","year":"2019","journal-title":"Qualitative Health Research"},{"key":"pone.0285031.ref036","doi-asserted-by":"crossref","DOI":"10.1080\/23323256.2021.1974908","article-title":"Co-producing Knowledge and Care in Team-Based Fieldwork in the Covid-19 Era","volume":"44","author":"C Asante","year":"2021","journal-title":"Anthropology Southern Africa"},{"issue":"10","key":"pone.0285031.ref037","first-page":"1280","article-title":"Children\u2019s Role in Enhanced Case Finding in Zambia","volume":"14","author":"V Bond","year":"2010","journal-title":"International Journal of Tuberculosis and Lung Disease"},{"key":"pone.0285031.ref038","unstructured":"Bond V, Clay S, Chiiya C, et al. Sweeping the Bedroom, Children in Domestic Work in Zambia. United Nations Joint Programme on Trafficking, UN report;2012."},{"issue":"1","key":"pone.0285031.ref039","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1177\/0907568210371234","article-title":"Beyond on or with: Questioning Power Dynamics and Knowledge Production in \u201cChild-Oriented\u201d Research Methodology","volume":"18","author":"J. Hunleth","year":"2011","journal-title":"Childhood"},{"issue":"6","key":"pone.0285031.ref040","doi-asserted-by":"crossref","first-page":"763","DOI":"10.1080\/09540121.2012.748878","article-title":"\u201cARVs\u201d as sickness and medicine: Examining children\u2019s knowledge and experience in the HIV era in urban Zambia","volume":"25","author":"J. Hunleth","year":"2013","journal-title":"AIDS Care"},{"issue":"2","key":"pone.0285031.ref041","doi-asserted-by":"crossref","first-page":"292","DOI":"10.1111\/maq.12028","article-title":"Children\u2019s roles in tuberculosis treatment regimes: Constructing childhood and kinship in urban Zambia","volume":"27","author":"J. Hunleth","year":"2013","journal-title":"Medical Anthropology Quarterly"},{"key":"pone.0285031.ref042","doi-asserted-by":"crossref","DOI":"10.26530\/OAPEN_627650","volume-title":"Children as Caregivers: The Global Fight Against Tuberculosis and HIV in Zambia","author":"J. Hunleth","year":"2017"},{"issue":"2","key":"pone.0285031.ref043","doi-asserted-by":"crossref","first-page":"155","DOI":"10.14506\/ca34.2.01","article-title":"Zambian children\u2019s imaginal caring: On fantasy, play, and imagination in an epidemic","volume":"34","author":"J. Hunleth","year":"2019","journal-title":"Cultural Anthropology"},{"issue":"3","key":"pone.0285031.ref044","article-title":"Care at the Gate","volume":"62","author":"J Hunleth","year":"2021","journal-title":"Anthropology News"},{"issue":"5","key":"pone.0285031.ref045","doi-asserted-by":"crossref","first-page":"501","DOI":"10.1080\/14733285.2014.893280","article-title":"School holidays: Examining childhood, gender norms, and kinship in children\u2019s shorter-term residential mobility in urban Zambia","volume":"13","author":"J Hunleth","year":"2014","journal-title":"Children\u2019s Geographies"},{"key":"pone.0285031.ref046","unstructured":"Eldredge LKB, Markham CM, Ruiter RAC, Fern\u00e1ndez ME, Kok G, Parcel GS. Planning Health Promotion Programs: An Intervention Mapping Approach. Wiley; 2016."},{"issue":"158","key":"pone.0285031.ref047","article-title":"Implementation Mapping: Using Intervention Mapping to Develop Implementation Strategies","volume":"7","author":"ME Fernandez","year":"2019","journal-title":"Frontiers in Public Health"},{"issue":"1","key":"pone.0285031.ref048","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1177\/0163278712446066","article-title":"What does it mean to \"employ\" the RE-AIM model?","volume":"36","author":"RS Kessler","year":"2013","journal-title":"Eval Health Prof"},{"issue":"1","key":"pone.0285031.ref049","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1186\/s13012-015-0209-1","article-title":"A refined compilation of implementation strategies: results from the Expert Recommendations for Implementing Change (ERIC) project","volume":"10","author":"BJ Powell","year":"2015","journal-title":"Implementation Science"},{"key":"pone.0285031.ref050","doi-asserted-by":"crossref","first-page":"112513","DOI":"10.1016\/j.psychres.2019.112513","article-title":"An introduction to effectiveness-implementation hybrid designs","volume":"280","author":"SJ Landes","year":"2019","journal-title":"Psychiatry Res"},{"issue":"1","key":"pone.0285031.ref051","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1186\/s12913-018-2938-8","article-title":"Qualitative approaches to use of the RE-AIM framework: rationale and methods","volume":"18","author":"JS Holtrop","year":"2018","journal-title":"BMC Health Services Research"},{"key":"pone.0285031.ref052","volume-title":"Designing and Conducting Mixed Methods Research","author":"JW Cresswell","year":"2018"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0285031","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,10,20]],"date-time":"2024-10-20T02:17:04Z","timestamp":1729390624000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0285031"}},"subtitle":[],"editor":[{"given":"Johannes","family":"Stortz","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2023,5,9]]},"references-count":52,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2023,5,9]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0285031","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,5,9]]}}}