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Implementation science for integration of HIV and non-communicable disease services in sub-Saharan Africa: a systematic review

Kemp, Christopher G.a,*; Weiner, Bryan J.a,*; Sherr, Kenneth H.a; Kupfer, Linda E.b; Cherutich, Peter K.a,c; Wilson, Davidd; Geng, Elvin H.e; Wasserheit, Judith N.a

doi: 10.1097/QAD.0000000000001897
SUPPLEMENT ARTICLE
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Objective: As the burden of chronic non-communicable diseases (NCDs) rises across sub-Saharan Africa (SSA), global donors and governments are exploring strategies to integrate HIV and NCD care. Implementation science is an emerging research paradigm that can help such programs achieve health impact at scale. We define implementation science as a systematic, scientific approach to ask and answer questions about how to deliver what works in populations who need it with greater speed, appropriate fidelity, efficiency, and relevant coverage. We identified achievements and gaps in the application of implementation science to HIV/NCD integration, developed an HIV/NCD implementation science research agenda, and detailed opportunities for capacity building and training.

Design: We conducted a systematic review of the application of implementation science methods to integrated HIV/NCD programs in SSA.

Methods: We searched PubMed, CINAHL, PsycINFO, and EMBASE for evaluations of integrated programs in SSA reporting at least one implementation outcome.

Results: We identified 31 eligible studies. We found that most studies used only qualitative, economic, or impact evaluation methods. Only one study used a theoretical framework for implementation science. Acceptability, feasibility, and penetration were the most frequently reported implementation outcomes. Adoption, appropriateness, cost, and fidelity were rare; sustainability was not evaluated.

Conclusions: Implementation science has a promising role in supporting HIV/NCD integration, although its impact will be limited unless theoretical frameworks, rigorous study designs, and reliable measures are employed. To help support use of implementation science, we need to build sustainable implementation science capacity. Doing so in SSA and supporting implementation science investigators can help expedite HIV/NCD integration.

aDepartment of Global Health, University of Washington, Seattle, Washington, USA

bFogarty International Center, National Institutes of Health, Bethesda, Maryland, USA

cMinistry of Health, Nairobi, Kenya

dThe World Bank Group, Washington, District of Columbia, USA

eUCSF, San Francisco, California, USA.

Correspondence to Christopher G. Kemp, MPH, PhDc, Department of Global Health, University of Washington, Ninth and Jefferson Building, 13th Floor, Box 359932, 908 Jefferson Street, Seattle, WA 98104, USA. Tel: +1 206 765 0989; e-mail: kempc@uw.edu

Received 1 November, 2017

Revised 23 April, 2018

Accepted 14 May, 2018

Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal's Website (http://www.AIDSonline.com).

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Introduction

Non-communicable diseases (NCDs) are outstripping infectious disease and maternal and child health problems as leading burdens of disease across sub-Saharan Africa (SSA), and are already responsible for 60% of death and disability worldwide [1,2]. NCDs, including cardiovascular disease, diabetes, cancer, and mental health problems, are common among people living with HIV (PLHIV) and threaten the progress of HIV treatment programs. Recognizing this, global donors are exploring strategies to leverage HIV platforms to address the growing burden of NCDs. These platforms offer an array of tools, models, and methods that could be adapted to meet the needs of integrated NCD services for PLHIV, and are among the first chronic disease services to perform at scale in SSA [3].

HIV/NCD integration, defined as the coordination, co-location, or simultaneous delivery of HIV and NCD services to people who need them, when they need them, requires a focus on evidence and assessment of available resources. This is particularly true in the context of overburdened health systems. In the United States, it takes an average of 17 years to transform 14% of original research into practices, programs, or policies that improve patient care and population health [4]. In low and middle-income countries (LMICs), given scarce resources, it may take even longer to close this ‘know-do gap.’ Efficacious interventions are often not effective when introduced at scale, particularly in overburdened health systems or new social, political, or demographic contexts, without appropriate adaptation [5].

Implementation science is an emerging research paradigm that uses rigorous interdisciplinary methods to close this gap and inform implementation of efficacious interventions, technologies, and approaches to achieve health impact at scale. A critical feature of implementation science is that stakeholders work with scientists early and throughout the research process to promote successful service delivery. This ensures that programs and policies are informed by research evidence and that researchers are aware of realities on the ground. Implementation science can play a key role in learning how to efficiently and effectively leverage HIV program investments to address NCDs. We conducted a systematic review of the application of implementation science to HIV/NCD integration in LMICs to understand how implementation science has been used to inform the integration of NCD and HIV services. Based on our review, we identify research questions to guide future work related to integration of NCD and HIV services, highlight critical or underused research methods, and detail ongoing opportunities for capacity building and training in implementation science.

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Definitions of implementation science

Implementation science addresses the ‘know-do gap’ in the context of health interventions – the chasm between what we know works based on empirical evidence, and what we do to apply that knowledge at the population level. Like many emerging fields, implementation science currently lacks a consensus definition [6,7]. We define implementation science as a systematic, scientific approach to ask and answer questions about how to deliver what works in populations who need it with greater speed, appropriate fidelity, efficiency, and relevant coverage. Essential to this definition is a conclusive evidence base establishing intervention efficacy (’what works’) from rigorous efficacy/effectiveness trials, or strong observational data when efficacy trials are not feasible or practical. Our definition promotes the systematic application of methods from diverse disciplines as essential to understand dynamics and processes as we move from intervention development, to implementation, and ultimately scale-up to achieve population-level health benefits. Though not exhaustive, we have identified ten disciplines, methods, or tools that feature prominently in implementation science (Fig. 1).

Fig. 1

Fig. 1

A distinguishing feature of implementation science is its focus on deliberate actions to introduce or change the delivery of new technologies, practices, and services. Implementation science examines outcomes of such actions that range from proximal implementation outcomes, including acceptability, appropriateness, adoption, costs, feasibility, fidelity, penetration, and sustainability [18]; to intermediate service delivery outcomes such as efficiency, equity, timeliness, and patient-centeredness; to distal health outcomes such as blood pressure or depressive symptoms. These three categories of outcomes form a synergistic continuum, but are conceptually and empirically distinct. While improvements in intermediate service delivery and distal health outcomes provide the ultimate criteria for evaluating the relative effectiveness of implementation strategies, proximal implementation outcomes may serve as critical, early indicators of implementation success, and as preconditions for attaining desired changes in service delivery and health. Our broad definition of implementation science embraces the examination of all three types of outcomes.

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Methods

We followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines for conducting a systematic review to survey the application of implementation science to integrated NCD and HIV programs in LMICs [19]. We searched four electronic bibliographic databases (PubMed, CINAHL, PsycINFO, and EMBASE) from database inception through 6 January 2017. Electronic search terms are presented in Supplemental Digital Content 1 (text) (http://links.lww.com/QAD/B293). We did not restrict the searches based on language, year of publication, or publication status. We also hand-searched reference lists of included studies.

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Study selection

After removing duplicate studies, two reviewers (C.K. and B.W.) independently screened all titles and abstracts of records, and assessed the full text of potentially eligible studies for review. Disagreements were resolved through discussion with co-authors until consensus was reached. Study inclusion criteria included: written in English; based in LMICs; evaluating interventions, programs, or services providing preventive and/or therapeutic NCD care through HIV platforms; and reporting at least one proximal implementation outcome as defined by Proctor et al.[20]. We defined NCDs as any form of cardiovascular disease, diabetes, cancer, or mental illness. We defined the HIV platform as the investment made by funders to strengthen the existing local public health systems and services to address HIV prevention and treatment. We considered interventions, programs, and services to be organized activities delivered to achieve a specific and intended result [21]. We defined an evaluation as the ‘examination of the worth, merit, or significance of an object’ [22]. We excluded studies that did not evaluate implementation strategies or explain variation in implementation outcomes, and thus did not meet our definition of implementation science. We excluded unpublished and nonpeer reviewed research.

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Data abstraction

Two reviewers (C.K. and E.N.) independently used a structured data abstraction form to extract key information from each included article. Disagreements were resolved through discussion with coauthors until consensus was reached. Abstracted information included: study and publication details; NCDs targeted; study population; service/program integration model, delivery site, and description; implementation strategy employed; implementation science method, tool, and framework employed; program duration; proximal implementation outcomes examined; intermediate service delivery and distal patient health outcomes reported; research question; and study findings, limitations, and conclusions or lessons learned. Our abstraction was informed by the above-mentioned taxonomy of implementation science, Proctor et al.'s [23] criteria for describing implementation strategies, and Proctor et al.'s [20] definitions of implementation outcomes. We then created tables to display and analyze the extracted information. Because several studies focused on the same program, we present summary statistics at both the study and program levels.

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Results

We screened 1661 studies. From these, 191 full-text articles were assessed for eligibility, and 31 studies met inclusion criteria (Fig. 2). Included studies are described in Table 1; a list of studies excluded after full-text review is reported in Supplemental Digital Content 2 (text) (http://links.lww.com/QAD/B293).

Fig. 2

Fig. 2

Table 1

Table 1

Table 1

Table 1

Table 1

Table 1

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Study characteristics

The 31 studies were published from 2009 to 2017, with half published since 2015 (Table 2) [24–54]. All were conducted in SSA. The full range of implementation science disciplines, methods, and tools was not employed. Qualitative methods were most commonly used: 26 (83.9%) interviewed staff or patients to determine acceptability and feasibility. Evaluation of program impact and cost were rare, occurring in only 2 (6.5%) and 4 (12.9%) studies, respectively. Only one study used a theoretical framework for implementation science research: Wagner et al.[53] used the Reach Effectiveness Adoption Implementation Maintenance (RE-AIM) framework [55]. Most studies focused on patients (24, 77.4%). Providers, community members, program managers, and policymakers were less frequently studied.

Table 2

Table 2

Patient or provider acceptability (17 studies, 54.8%) and feasibility (12 studies, 38.7%) were the most commonly reported implementation outcomes. Penetration, calculated as the number of persons receiving a NCD service divided by the number eligible for the service, was also commonly reported (8 studies, 25.8%). Adoption, appropriateness, cost, and fidelity were less frequently assessed; sustainability was not evaluated. While intermediate service delivery outcomes like community or facility-based screening and diagnosis outcomes were frequently reported (14 studies, 45.2%), as was receipt of treatment (21 studies, 67.7%), distal patient health outcomes such as blood pressure, hemoglobin A1c, blood/urine glucose, or depressive symptoms, were infrequently reported (4 studies, 12.9%).

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Program characteristics

These 31 studies evaluated 26 different HIV/NCD integration programs (Table 2). Half (50.0%) of the programs focused on cancer, and all of these focused on cervical cancer. Eleven (42.3%) served patients with depression; eight of these also served patients with other mental disorders like anxiety or posttraumatic stress. Hypertension and diabetes services were always implemented together (15.4%). Eleven (42.3%) targeted multiple NCDs. Although a few services/programs (15.4%) occurred in community sites, many combined clinic- and hospital-based services. Eighteen (69.2%) offered prevention or screening services, 17 (65.4%) offered referral services, and 17 (65.4%) offered treatment. Over half (69.2%) offered NCD services only to patients with HIV, and in most programs (88.5%), patients entered via HIV-related care. A minority (26.9%) of programs were pilot or short-term, as opposed to ongoing or sustained over multiple years.

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Discussion

Accomplishments

Implementation science has a nascent but growing role in supporting the integration of NCD services into HIV care settings. Pre-implementation, formative, qualitative studies of patients and providers have often been used to assess the acceptability and feasibility of integrated services. These indicate that although many patients have limited awareness of NCDs or NCD screening or treatment options [24,40,45], most would find it acceptable to receive NCD services in an HIV care setting [32,40], even if they are not living with HIV [45]. Likewise, HIV care providers see benefits to offering NCD services and are willing to provide them, but express concerns about the feasibility of doing so [34]. Concerns include lack of space, high staff workload, lack of training, inadequate supplies, and potential adverse effects on other services [30,34,40,41,49,51].

Several examples highlight the findings of implementation science studies of HIV/NCD integration. Integrated screening and treatment for depression and other mental disorders in HIV care settings is still in the formative or pilot phase [38,41,42,49]; however, a randomized controlled trial demonstrated that high rates of screening, diagnostic evaluation, and treatment for depression can be achieved in HIV clinics [53]. Integrated hypertension and diabetes screening services are less common than other services, though studies have demonstrated high penetration [29] and low cost [48] when implemented in community settings through screening events, and high acceptability when delivered through medicine adherence clubs [52]. Studies indicate that multi-disease campaigns can achieve high uptake of diagnostic, preventive, treatment, and referral services for HIV and NCDs, if preceded by community mobilization [29]. HIV/NCD medication adherence clubs can be effective in providing guideline-concordant testing and treatment outside the clinical setting with minimal loss to follow-up [52].

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Gaps and opportunities

The contribution of implementation science is enhanced when theoretical frameworks, rigorous study designs, and valid measures are used. The recent, rapid increase in implementation science publications reflected in our review highlights the growing role that implementation science is playing in guiding HIV/NCD integration. However, implementation science conceptual frameworks were rarely applied, and there are major gaps in methodological coverage. Surprisingly, only one study in our review employed a formal theoretical framework for implementation science [53]. Such frameworks improve the external validity and replicability of implementation research [56]. They can be used to develop strategies and processes to achieve successful service delivery, identify and understand determinants of implementation success, and evaluate implementation [57]. However, given that currently available implementation science theoretical frameworks were developed in high-income countries (HICs), they may need to be adapted or expanded to be more appropriate for SSA and other LMICs.

Few studies evaluated the impact of integrated care models [26,53] or conducted economic analyses [29,43,48,54]. These will be critical for evidence-based decision-making. While randomized controlled trials play an important role in implementation science, other quasi-experimental and observational study designs can generate robust, useful evidence when rigorously developed and conducted. Only one study used stakeholder or policy analysis to bring program implementers and policymakers together through the research process [38]. This method strengthens implementation approaches and paves the way for scale-up and sustainability. Although we found several studies that used retrospective analyses of routine program data to document the delivery and expansion of integrated services, and several reporting penetration into eligible populations [58–69], these did not seek to explain or predict variation in implementation or service delivery outcomes, nor did they experiment with implementation strategies and report estimates of clinical or implementation effectiveness. Therefore, they did not meet our definition of implementation science, and were excluded from our sample. Moving forward, similar studies could pair routine program data with qualitative data collection, or use statistical models to estimate associations between implementation strategies and implementation outcomes. Finally, widespread use of standardized measures of implementation outcomes will accelerate the synthesis of knowledge across studies, facilitating the translation of research findings from implementation science into practice and policy. Work is underway to survey and develop reliable and valid measures for implementation outcomes in HIC settings [70]; it will be critical for LMIC-based researchers to develop, test, or adapt measures suitable to their context.

The NCDs and range of outcomes addressed were also limited. Few programs tackled hypertension, despite its prevalence, morbidity, and relative ease of management. None served patients with stroke, myocardial infarction, substance abuse, or cancers other than cervical cancer. The dearth of distal clinical health outcomes may reflect the early phase of HIV/NCD integration in most of SSA. Yet, even proximal implementation outcomes were poorly covered. Few studies assessed the fidelity of service delivery, the cost of integrated services, or the sustainability of integrated programs. Fidelity – whether an intervention is implemented as prescribed in the original protocol or as intended by the program developers – is crucial to ensuring that investments in service delivery are not wasted, that core procedures are implemented as designed and tested, and that success is replicated across implementation contexts [71]. Cost and cost-effectiveness are key considerations for any program, given finite and time-bound resources. Two single-facility studies indicate that visual inspection of the cervix with acetic acid has the lowest estimated per-screening cost [54] and is more cost-effective than other cervical cancer screening approaches [43]. However, more studies are needed. Cost and cost-effectiveness may vary substantially depending, for example, on how the screening service operates in different facilities. Finally, the sustainability of program delivery and program outcomes is critical, yet unexplored.

Implementation science can pave the way forward by addressing key research questions to inform decisions to scale up integrated services and refine them over the long-term (Table 3). For example, through surveillance, impact evaluation, and economic analysis, implementation science can determine the effects of integrated service on NCD incidence, morbidity, mortality, and cost. Operations research and quality improvement methods can help optimize delivery and increase quality of integrated services. Finally, dissemination research and social marketing can increase the reach and appeal of integrated services among both PLHIV and the broader population. However, for implementation science to achieve its promise and produce evidence to guide HIV/NCD integration, we will need to build a SSA-based workforce trained in implementation science [72].

Table 3

Table 3

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Implementation science capacity building in sub-Saharan Africa

We can build implementation science capacity in SSA in several ways. We can deliver implementation science training rapidly through short courses and workshops, especially to trainees with relevant expertise or experience. We can also deliver training through graduate programs in clinical science or public health at the masters and doctoral levels. Both the National Institutes of Health (NIH) and WHO's Tropical Disease Research (TDR) Program support implementation science training for scientists and other stakeholders in SSA (see Table, Supplemental Digital Content 3, http://links.lww.com/QAD/B293). Some of these research training grants pair universities in HICs and in SSA (‘North-South’) such that classroom training is split between the two, and field research is conducted in SSA ('sandwich programs’). Others pair one university in SSA with another ('South-South’) that has an established implementation science program. As of August 2017, NIH supports 21 research training grants that offer short or long-term training in implementation science in the region, about half of which focus on NCDs. WHO/TDR supports seven regional training centers that focus on implementation science related to infectious diseases, including three in SSA offering graduate programs in public health with an emphasis on implementation science. To expand their reach and capacity, the seven WHO/TDR centers are developing a massive open online course (MOOC) in implementation science, and also an improved on-line ‘tool-box’ that can be used to teach implementation science to a variety of stakeholders, including researchers, healthcare service providers, and program staff. Sustainability is a persistent challenge for these programs, as they depend on continued foreign grant support.

In the United States, there are only two established degree-granting programs that emphasize implementation science: one at the masters level (University of California San Francisco) and one at the doctoral level (University of Washington). Both accept students from LMICs and HICs. However, few funding mechanisms exist to support students from LMICs to receive research training from these programs. The University of Washington made its doctoral curriculum in implementation science accessible in SSA by offering a modified version through a 2-year fellowship program developed in partnership with the University of Nairobi and the University of Maryland, with support from NIH, the Fogarty International Center, and the Medical Education Partnership Initiative (MEPI) [73]. While support for this program has ended, other similar programs have taken its place (see Table, Supplemental Digital Content 3, http://links.lww.com/QAD/B293). The University of Washington also offers an online quarter-long introductory course to IS.

Implementation science curricula and competencies are available to guide institutions in the development of programs to meet their needs [74–76]. However, these would benefit from consensus on educational competencies to guide and galvanize the development of sustainable training curricula and programs in LMICs. Support for new investigators, especially in terms of mentoring and networking, is also essential for building capacity in SSA. Because implementation science is an emerging field, there are few mentors or colleagues available [77]. This is especially true in SSA. The NIH has created implementation science alliances to help address this challenge [78]. These serve as platforms that convene implementation scientists, program implementers, and policymakers working in the same area to exchange lessons, explore common implementation challenges, and collaborate to develop implementation science and conduct implementation research. Three such alliances have been created: the NIH-PEPFAR Prevention of Mother-to-Child HIV Transmission Implementation Science Alliance [78], the Clean Cooking Implementation Science Network, and the Adolescent HIV Prevention and Treatment Implementation Science Alliance. In addition, a new NIH K43 grant award mechanism offers research support and protected time for early-stage LMIC investigators trained in implementation science if they hold a faculty position at a LMIC-based academic or research institution.

Finally, building implementation science capacity in SSA will require innovative partnerships and further research. As implementation science gains acceptance, ministries of health, nongovernmental organizations, and civil society will need to play prominent roles in capacity building. Ministries and other implementing agencies could serve as pivotal partners and mentoring platforms, and provide a critical mass of personnel for rapid training in implementation science. Once trained, they could cascade support for implementation science to other health system staff. Universities and colleges could also expand nonmatriculated training in implementation science to create cadres of specialists, mentors, and champions. With funding and support from government agencies, research institutes in SSA could enhance their research and training programs. This would promote the sustainability of implementation science training in SSA and help countries advocate for funding for degree-granting graduate programs. Lastly, as noted in Table 3 above, it will be critical for researchers to study this issue and determine the most effective ways to build in-country research capacity.

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Conclusions

In the 1990s, global stakeholders tried to deliver integrated HIV and sexually transmitted disease (STD) services in recognition of the biological synergies and behavioral co-factors linking these infections. Unfortunately, rigorous evaluations of the impact and cost-effectiveness of alternative integration models were rarely performed; stakeholder and policy analyses were rarely conducted; and iterative quality improvement approaches were rarely applied. A quarter of a century later – though HIV testing and counselling is offered in many STD clinics – across the majority of SSA and other LMICs, integrated HIV-STD prevention and care models are scarce [79].

We need not repeat the mistakes of HIV-STD integration efforts. The theoretical frameworks and methods of implementation science offer systematic, rigorous approaches to inform and facilitate evidence-based HIV/NCD integration efforts in SSA. Implementation studies will require close partnerships among investigators, ministries, and delivery organizations that are established early and nurtured throughout the research process. It will also be essential to build sustainable, local implementation science capacity within countries that are committed to addressing NCDs, and to provide robust funding to support investigators working in this critical new research paradigm. Implementation science can help guide the way forward in HIV/NCD integration.

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Acknowledgements

B.W., K.S., L.K., P.C., D.W., E.G., and J.W. conceived the study. C.K. developed the review protocol and implemented data collection. C.K. and B.W. reviewed studies for inclusion. C.K., B.W., and E.N. abstracted, analyzed, and interpreted the data. All authors drafted the manuscript, and all authors contributed to revisions. All authors read and approved the final manuscript.

We would like to acknowledge and thank Andrew Forsyth, PhD, for his valuable feedback on our manuscript, and Elspeth Nolen, MSc, for her assistance with data abstraction.

Research reported in this publication was supported by NIAID, NCI, NIMH, NIDA, NICHD, NHLBI, NIA, NIGMS, and NIDDK of the National Institutes of Health under award number AI027757.

Source of support: this article as part of the Research to Guide Practice: Enhancing HIV/AIDS Platform to Address Non-Communicable Diseases in sub-Saharan Africa was supported by the U.S. National Institutes of Health Fogarty International Center.

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Conflicts of interest

There are no conflicts of interest.

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References

1. Global, regional, and national disability-adjusted life-years (DALYs) for 315 diseases and injuries and healthy life expectancy (HALE), 1990–2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet 2016; 388:1603–1658.
2. Benziger CP, Roth GA, Moran AE. The global burden of disease study and the preventable burden of NCD. Global Heart 2016; 11:393–397.
3. Rabkin M, El-Sadr WM. Why reinvent the wheel? Leveraging the lessons of HIV scale-up to confront noncommunicable diseases. Global public health 2011; 6:247–256.
4. Balas EA, Boren SA. Managing clinical knowledge for healthcare improvement. Yearb Med Inform 2000. 65–70.
5. Chen L, Evans T, Anand S, Boufford JI, Brown H, Chowdhury M, et al. Human resources for health: overcoming the crisis. Lancet 2004; 364:1984–1990.
6. Odeny TA, Padian N, Doherty MC, Baral S, Beyrer C, Ford N, et al. Definitions of implementation science in HIV/AIDS. Lancet HIV 2015; 2:e178–e180.
7. Means AR, Phillips DE, Lurton G, Njoroge A, Furere SM, Liu R, et al. The role of implementation science training in global health: from the perspective of graduates of the field's first dedicated doctoral program. Global health action 2016; 9:31899.
8. World Bank, Khandker SR, Koolwal GB, Samad HA. Handbook on Impact Evaluation: Quantitative Methods and Practices. 2010; https://openknowledge.worldbank.org/handle/10986/2693
    9. Drummond MF, Sculpher MJ, Claxton K, Stoddard GL, Torrance GW. Methods for the Economic Evaluation of Health Care Programmes: Fourth Edition. Oxford, UK: Oxford University Press; 2015.
      10. Sandelowski M. Using qualitative research. Qual Health Res 2004; 14:1366–1386.
      11. National Academies Press, Fanjiang G, Grossman JH, Compton WD, Reid PP. Building a Better Delivery System: a New Engineering/Healthcare Partnership. 2005.
        12. John Wiley & Sons, Langley GJ, Moen RD, Nolan KM, Nolan TW, Norman CL, Provost LP. The Improvement Guide: a Practical Approach to Enhancing Organizational Performance. 2009.
          13. Weiner BJ. A theory of organizational readiness for change. Implement Sci 2009; 4:67.
            14. Walt G, Shiffman J, Schneider H, Murray SF, Brugha R, Gilson L. ‘Doing’health policy analysis: methodological and conceptual reflections and challenges. Health Policy Plan 2008; 23:308–317.
            15. Schillinger D. An introduction to effectiveness, dissemination and implementation research. From the Series: UCSF Clinical and Translational Science Institute (CTSI) Resource Manuals and Guides to Community-Engaged Research, P Fleisher, ed Clinical Translational Science Institute Community Engagement Program, University of California San Francisco; 2010.
              16. Grier S, Bryant CA. Social marketing in public health. Annu Rev Public Health 2005; 26:319–339.
              17. WHO. Framework and standards for country health information systems. 2nd ed.Geneva: World Health Organization; 2008.
                18. Proctor E, Silmere H, Raghavan R, Hovmand P, Aarons G, Bunger A, et al. Outcomes for implementation research: conceptual distinctions, measurement challenges, and research agenda. Adm Policy Ment Health 2011; 38:65–76.
                19. Moher D, Liberati A, Tetzlaff J, Altman DG. Group P. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 2009; 6:e1000097.
                20. Proctor E, Silmere H, Raghavan R, Hovmand P, Aarons G, Bunger A, et al. Outcomes for implementation research: conceptual distinctions, measurement challenges, and research agenda. Adm Policy Mental Health 2011; 38:65–76.
                21. Centers for Disease Control and Prevention: Program Performance and Evaluation Office. Introduction to program evaluation for public health programs: a self-study guide. Atlanta, GA: U.S. Department of Health and Human Services; 2011.
                22. Scriven M. Minimalist theory: the least theory that practice requires. Am J Eval 1998; 19:57–70.
                23. Proctor EK, Powell BJ, McMillen JC. Implementation strategies: recommendations for specifying and reporting. Implement Sci 2013; 8:139.
                24. Dim CC, Dim NR, Ezegwui HU, Ikeme AC. An unmet cancer screening need of HIV-positive women in southeastern Nigeria. Medscape J Med 2009; 11:19.
                25. Haffejee S, Groeneveld I, Fine D, Patel R, Bowman B. An assessment of counselling and support services for people living withHIV in Gauteng, South Africa: findings of a baseline study. Afr J AIDS Res 2010; 9:367–372.
                26. Parham GP, Mwanahamuntu MH, Sahasrabuddhe VV, Westfall AO, King KE, Chibwesha C, et al. Implementation of cervical cancer prevention services for HIV-infected women in Zambia: measuring program effectiveness. HIV Ther 2010; 4:703–722.
                27. Huchko MJ, Bukusi EA, Cohen CR. Building capacity for cervical cancer screening in outpatient HIV clinics in the Nyanza province of western Kenya. Int J Gynecol Obstet 2011; 114:106–110.
                28. Rabiu K, Akinbami A, Adewunmi A, Akinola O, Wright K. The need to incorporate routine cervical cancer counselling and screening in the management of HIV positive women in Nigeria. Asian Pac J Cancer Prev 2011; 12:1211–1214.
                29. Chamie G, Kwarisiima D, Clark TD, Kabami J, Jain V, Geng E, et al. Leveraging rapid community-based HIV testing campaigns for noncommunicable diseases in rural Uganda. PloS One 2012; 7:e43400.
                30. Mall S, Sorsdahl K, Swartz L, Joska J. I understand just a little...’ Perspectives of HIV/AIDS service providers in South Africa of providing mental healthcare for people living with HIV/AIDS. AIDS Care 2012; 24:319–323.
                31. White HL, Mulambia C, Sinkala M, Mwanahamuntu MH, Parham GP, Moneyham L, et al. ‘Worse than HIV’or ‘not as serious as other diseases’? Conceptualization of cervical cancer among newly screened women in Zambia. Soc Sci Med 2012; 74:1486–1493.
                32. Ezechi OC, Gab-Okafor CV, Ostergren PO, Odberg Pettersson K. Willingness and acceptability of cervical cancer screening among HIV positive Nigerian women. BMC Public Health 2013; 13:46.
                33. Walstrom P, Operario D, Zlotnick C, Mutimura E, Benekigeri C, Cohen MH. ’I think my future will be better than my past’: examining support group influence on the mental health of HIV-infected Rwandan women. Global Public Health 2013; 8:90–105.
                34. Kumakech E, Andersson S, Wabinga H, Berggren V. Integration of HIV and cervical cancer screening perceptions of healthcare providers and policy makers in Uganda. BMC Public Health 2014; 14:810.
                35. Pence BW, Gaynes BN, Atashili J, O’Donnell JK, Kats D, Whetten K, et al. Feasibility, safety, acceptability, and preliminary efficacy of measurement-based care depression treatment for HIV patients in Bamenda, Cameroon. AIDS Behav 2014; 18:1142–1151.
                36. Petersen I, Hancock JH, Bhana A, Govender K. A group-based counselling intervention for depression comorbid with HIV/AIDS using a task shifting approach in South Africa: a randomized controlled pilot study. J Affect Disord 2014; 158:78–84.
                37. Rosser JI, Zakaras JM, Hamisi S, Huchko MJ. Men's knowledge and attitudes about cervical cancer screening in Kenya. BMC Womens Health 2014; 14:138.
                38. Wissow LS, Tegegn T, Asheber K, McNabb M, Weldegebreal T, Jerene D, et al. Collaboratively reframing mental health for integration of HIV care in Ethiopia. Health Policy Plan 2015; 30:791–803.
                39. Belete N, Tsige Y, Mellie H. Willingness and acceptability of cervical cancer screening among women living with HIV/AIDS in Addis Ababa, Ethiopia: a cross sectional study. Gynecol Oncol Res Pract 2015; 2:6.
                40. Bukirwa A, Mutyoba JN, Mukasa BN, Karamagi Y, Odiit M, Kawuma E, et al. Motivations and barriers to cervical cancer screening among HIV infected women in HIV care: a qualitative study. BMC Womens Health 2015; 15:82.
                41. Duffy M, Sharer M, Cornman H, Pearson J, Pitorak H, Fullem A. Integrating mental health and HIV services in Zimbabwean communities: a nurse and community-led approach to reach the most vulnerable. J Assoc Nurses AIDS Care 2017; 28:186–198.
                42. Iheanacho T, Obiefune M, Ezeanolue CO, Ogedegbe G, Nwanyanwu OC, Ehiri JE, et al. Integrating mental health screening into routine community maternal and child health activity: experience from Prevention of Mother-to-child HIV transmission (PMTCT) trial in Nigeria. Soc Psychiatry Psychiatr Epidemiol 2015; 50:489–495.
                43. Lince-Deroche N, Phiri J, Michelow P, Smith JS, Firnhaber C. Costs and cost effectiveness of three approaches for cervical cancer screening among HIV-positive women in Johannesburg, South Africa. PloS One 2015; 10:e0141969.
                44. Odokonyero R, Wagner G, Ngo V, Nakasujja N, Musisi S, Akena D. Giving ‘sadness’ a name: the need for integrating depression treatment into HIV care in Uganda. J Int Assoc Provid AIDS Care 2015; 14:108–111.
                45. Ports KA, Haffejee F, Mosavel M, Rameshbabu A. Integrating cervical cancer prevention initiatives with HIV care in resource-constrained settings: A formative study in Durban, South Africa. Global Public Health 2015; 10:1238–1251.
                46. Rosser JI, Njoroge B, Huchko MJ. Cervical cancer screening knowledge and behavior among women attending an urban HIV clinic in western Kenya. J Cancer Educ 2015; 30:567–572.
                47. Ameh S, Klipstein-Grobusch K, D’Ambruoso L, Kahn K, Tollman SM, Gomez-Olive FX. Quality of integrated chronic disease care in rural South Africa: user and provider perspectives. Health Policy Plan 2017; 32:257–266.
                48. Chang W, Chamie G, Mwai D, Clark TD, Thirumurthy H, Charlebois ED, et al. Implementation and operational research: cost and efficiency of a hybrid mobile multidisease testing approach with high HIV testing coverage in East Africa. J Acquir Immune Defic Syndr 2016; 73:e39–e45.
                49. Dos Santos M, Wolvaardt G. Integrated intervention for mental health co-morbidity in HIV-positive individuals: a public health assessment. Afr J AIDS Res 2016; 15:325–331.
                50. Leung C, Aris E, Mhalu A, Siril H, Christian B, Koda H, et al. Preparedness of HIV care and treatment clinics for the management of concomitant noncommunicable diseases: a cross-sectional survey. BMC Public Health 2016; 16:1002.
                51. Shiferaw N, Salvador-Davila G, Kassahun K, Brooks MI, Weldegebreal T, Tilahun Y, et al. The single-visit approach as a cervical cancer prevention strategy among women with HIV in Ethiopia: successes and lessons learned. Global Health Sci Pract 2016; 4:87–98.
                52. Venables E, Edwards JK, Baert S, Etienne W, Khabala K, Bygrave H. They just come, pick and go.’ The acceptability of integrated medication adherence clubs for HIV and non communicable disease (NCD) patients in Kibera, Kenya. PloS One 2016; 11:e0164634.
                53. Wagner GJ, Ngo V, Goutam P, Glick P, Musisi S, Akena D. A structured protocol model of depression care versus clinical acumen: a cluster randomized trial of the effects on depression screening, diagnostic evaluation, and treatment uptake in Ugandan HIV clinics. PloS One 2016; 11:e0153132.
                54. Vodicka EL, Babigumira JB, Mann MR, Kosgei RJ, Lee F, Mugo NR, et al. Costs of integrating cervical cancer screening at an HIV clinic in Kenya. Int J Gynecol Obstet 2017; 136:220–228.
                55. Glasgow RE, Vogt TM, Boles SM. Evaluating the public health impact of health promotion interventions: the RE-AIM framework. Am J Public Health 1999; 89:1322–1327.
                56. Gardner B, Whittington C, McAteer J, Eccles MP, Michie S. Using theory to synthesise evidence from behaviour change interventions: the example of audit and feedback. Social Sci Med 2010; 70:1618–1625.
                57. Nilsen P. Making sense of implementation theories, models and frameworks. Implement Sci 2015; 10:53.
                58. Batra P, Kuhn L, Denny L. Utilisation and outcomes of cervical cancer prevention services among HIV-infected women in Cape Town. S Afr Med J 2010; 100:39–44.
                59. Horo A, Jaquet A, Ekouevi DK, Toure B, Coffie PA, Effi B, et al. Cervical cancer screening by visual inspection in Cote d’Ivoire, operational and clinical aspects according to HIV status. BMC Public Health 2012; 12:237.
                60. Khabala KB, Edwards JK, Baruani B, Sirengo M, Musembi P, Kosgei RJ, et al. Medication Adherence Clubs: a potential solution to managing large numbers of stable patients with multiple chronic diseases in informal settlements. Trop Med Int Health 2015; 20:1265–1270.
                61. Khozaim K, Orang’o E, Christoffersen-Deb A, Itsura P, Oguda J, Muliro H, et al. Successes and challenges of establishing a cervical cancer screening and treatment program in western Kenya. Int J Gynaecol Obstet 2014; 124:12–18.
                62. Moon TD, Silva-Matos C, Cordoso A, Baptista AJ, Sidat M, Vermund SH. Implementation of cervical cancer screening using visual inspection with acetic acid in rural Mozambique: successes and challenges using HIV care and treatment programme investments in Zambézia Province. J Int AIDS Soc 2012; 15:2.
                63. Msyamboza KP, Phiri T, Sichali W, Kwenda W, Kachale F. Cervical cancer screening uptake and challenges in Malawi from 2011 to 2015: retrospective cohort study. BMC Public Health 2016; 16:806.
                64. Mwanahamuntu MH, Sahasrabuddhe VV, Kapambwe S, Pfaendler KS, Chibwesha C, Mkumba G, et al. Advancing cervical cancer prevention initiatives in resource-constrained settings: insights from the Cervical Cancer Prevention Program in Zambia. PLoS Med 2011; 8:1–5.
                65. Mwanahamuntu MH, Sahasrabuddhe VV, Blevins M, Kapambwe S, Shepherd BE, Chibwesha C, et al. Monitoring the performance of ‘screen-and-treat’ cervical cancer prevention programs. Int J Gynaecol Obstet 2014; 126:88–89.
                66. Odafe S, Torpey K, Khamofu H, Oladele E, Adedokun O, Chabikuli O, et al. Integrating cervical cancer screening with HIV care in a district hospital in Abuja, Nigeria. Niger Med J 2013; 54:176–184.
                67. Parham GP, Mwanahamuntu MH, Kapambwe S, Muwonge R, Bateman AC, Blevins M, et al. Population-level scale-up of cervical cancer prevention services in a low-resource setting: development, implementation, and evaluation of the cervical cancer prevention program in Zambia. PloS One 2015; 10:e0122169.
                68. Pfaendler KS, Mwanahamuntu MH, Sahasrabuddhe VV, Mudenda V, Stringer JS, Parham GP. Management of cryotherapy-ineligible women in a ‘screen-and-treat’ cervical cancer prevention program targeting HIV-infected women in Zambia: lessons from the field. Gynecol Oncol 2008; 110:402–407.
                69. Ramogola-Masire D, de Klerk R, Monare B, Ratshaa B, Friedman HM, Zetola NM. Cervical cancer prevention in HIV-infected women using the ‘see and treat’ approach in Botswana. J Acquir Immune Defic Syndr 2012; 59:3.
                70. Lewis CC, Weiner BJ, Stanick C, Fischer SM. Advancing implementation science through measure development and evaluation: a study protocol. Implement Sci 2015; 10:102.
                71. Carroll C, Patterson M, Wood S, Booth A, Rick J, Balain S. A conceptual framework for implementation fidelity. Implement Sci 2007; 2:40.
                72. Madon T, Hofman KJ, Kupfer L, Glass RI. Implementation science. Science 2007; 318:1728–1729.
                73. Osanjo GO, Oyugi JO, Kibwage IO, Mwanda WO, Ngugi EN, Otieno FC, et al. Building capacity in implementation science research training at the University of Nairobi. Implement Sci 2016; 11:30.
                74. Padek M, Colditz G, Dobbins M, Koscielniak N, Proctor EK, Sales AE, et al. Developing educational competencies for dissemination and implementation research training programs: an exploratory analysis using card sorts. Implement Sci 2015; 10:114.
                75. Gonzales R, Handley MA, Ackerman S, O'Sullivan PS. A framework for training health professionals in implementation and dissemination science. Acad Med 2012; 87:271–278.
                76. Metz A, Louison L, Ward C, Burke K. Global Implementation Specialist Practice Profile: Skills and Competencies for Implementation Practitioners. Chapel Hill, NC: National Implementation Research Network; 2017.
                77. Stamatakis KA, Norton WE, Stirman SW, Melvin C, Brownson RC. Developing the next generation of dissemination and implementation researchers: insights from initial trainees. Implement Sci 2013; 8:29.
                78. Sturke R, Harmston C, Simonds RJ, Mofenson LM, Siberry GK, Watts DH, et al. A multidisciplinary approach to implementation science: the NIH-PEPFAR PMTCT implementation science alliance. J Acquir Immune Defic Syndr 2014; 67 (Suppl 2):S163–S167.
                79. Hope R, Kendall T, Langer A, Bärnighausen T. Health systems integration of sexual and reproductive health and HIV services in sub-Saharan Africa: a scoping study. J Acquir Immune Defic Syndr 2014; 67:S259–S270.

                * Christopher G. Kemp and Bryan J. Weiner are co-first authors.

                Keywords:

                capacity building; health systems strengthening; HIV; implementation science; integration; non-communicable diseases; sub-Saharan Africa

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