The story of the response to HIV/AIDS is an inspiring example of how research, capacity strengthening, and international partnerships successfully transformed a fatal and poorly understood infectious disease into a chronic, treatable disease. International clinical trials provided data that identified combination antiretroviral therapy (ART) regimens that were not only effective in controlling and limiting mortality from HIV but also—by using combinations of drugs—limited the emergence of drug resistance. Given this evidence base, large-scale HIV treatment and prevention programs around the world, supported by donors such as the US President's Emergency Plan for AIDS Relief and the Global Fund to Fight AIDS, Tuberculosis and Malaria, decreased HIV incidence and lowered mortality rates from HIV/AIDS on every continent studied.1,2 The strong fight against HIV/AIDS, with its focus on stopping transmission, implementing treatment protocols, improving drug delivery systems, and strengthening medical facilities, can in many ways serve as a model for the treatment of noncommunicable disease (NCD) in low- and middle-income countries (LMICs).3–11
Today, with over 35 million people living (and aging) with HIV (PLHIV) and over 2 million becoming infected every year,12 we are faced with a new challenge: addressing morbidity and mortality from NCDs—heart disease, stroke, diabetes and metabolic complications, renal disease, cancers, liver disease, and mental illness—that increase with age and may be related to HIV and its treatment.13–16 We are now in an era when PLHIV may experience a reduction in quality of life or die, not from HIV itself, but from a preventable NCD that may be a consequence of HIV-related immunosuppression, antiretroviral drug toxicities, or HIV-related inflammation and hypercoagulation.
The link between treatable HIV disease and increased morbidity and mortality from NCDs poses a familiar challenge: when a primary disorder is treated, but not cured, underlying pathogenic processes may continue and increase vulnerability to other comorbidities. We cite as an example the first case of successful human diabetes treatment with insulin to a patient who then died from pneumonia.17
Leonard Thompson was a 14-year-old Canadian with type 1 diabetes mellitus when he was treated with “pancreatic extract” in 1922. The teenager weighed less than 30 kg and had mental obtundation. Once Leonard received a purified extract, his symptoms improved and his blood sugar normalized. With daily insulin treatment, Leonard resumed his growth and had a good quality of life until he died of pneumonia at age 27.
In this historic case, the patient's first and primary NCD (diabetes) was managed, but he succumbed to an infection. In sub-Saharan Africa today, HIV care is more widely available than in previous decades, but it is not accompanied by parallel care services for NCDs, resulting in preventable, premature morbidity and death. Although an excess risk of NCDs in persons living with HIV/AIDS in LMICs still needs to be better quantified, increasing rates of NCDs among aging persons who have HIV, many of whom are receiving HIV treatment, raise the concern that, if unaddressed, morbidity and mortality from NCDs may set back or even reverse the impressive health gains achieved over the last decade in HIV-infected populations. As we work toward building sustainable models of disease prevention, treatment, and care in LMICs in the context of an increasing, global NCD epidemic, a better understanding of the interactions between long-term HIV, HIV treatment, and NCD comorbidities will enable us to maintain gains in HIV-infected populations while improving NCD control and treatment. More and better data regarding NCDs in aging PLHIV receiving different ART treatments will inform the development of cost-effective interventions and enhancements to existing HIV and health systems in LMICs so that they incorporate both HIV and NCD diagnosis and treatment. Designing and conducting studies will require a paradigm shift in places like sub-Saharan Africa, where, to date, the primary focus has been on HIV prevention and treatment. Just as the advent of widespread ART demanded a seismic shift in global human capacity and health systems for the emergency response to HIV, emerging NCD comorbidities among those with HIV in LMICs will demand no less.
From April 29 to May 1, 2013, the Fogarty International Center and the Office of AIDS Research at the US National Institutes of Health (NIH) assembled a multidisciplinary international group of experts at Fogarty's Center for Global Health Studies for a consultation on HIV and NCD comorbidities in LMICs. This group included representatives of 9 NIH Institutes and Centers (Fogarty International Center, National Cancer Institute, National Heart Lung and Blood Institute, National Institute of Allergy and Infectious Diseases, National Institute of Diabetes and Digestive and Kidney Diseases, National Institute on Drug Abuse, National Institute of Mental Health, National Institute of Neurological Disorders and Stroke, and the Office of AIDS Research at the NIH Office of the Director) and other key agencies (the World Health Organization, the United States Agency for International Development, the US Centers for Disease Control and Prevention, The World Bank Group, and the Office of the Global AIDS Coordinator at the US Department of State), as well as researchers and policymakers with expertise in this field. The consultation provided a scientific forum to:
- Identify key research and research training priorities related to HIV and NCD comorbidities in LMICs and stimulate new research collaborations;
- Inform future investments of the NIH and other funding agencies; and
- Identify ways in which to harness existing research and care platforms to further the research and capacity building that best addresses HIV and NCD comorbidities.
After the consultation, US and LMIC scientists collaborated on articles that articulate the current scientific landscape as well as the urgent research and capacity-building priorities associated with specific HIV and NCD comorbidities featured in this supplement: (1) cancers,18 (2) renal and genitourinary comorbidities,19 (3) metabolic, body, and bone disorders,20 (4) cardiovascular and pulmonary diseases,21 (5) mental, neurological, and substance use disorders,22 and (6) gastrointestinal, hepatic and nutritional aspects,23 as well as key related (7) methodological,24 and (8) cost-effectiveness issues25 on the subject. In addition, given that the focus of these articles is on sub-Saharan Africa, two commentaries were solicited to provide broad perspectives from both Latin American26 and Asian27 contexts. This introductory chapter presents some of the over-arching challenges and opportunities for addressing HIV and NCD comorbidities in LMICs, with the subsequent articles describing these issues and the epidemiology of these comorbidities in greater depth.
HIV AND NCDS IN LMICS: A RESEARCH AGENDA
Data from high-income countries and some LMICs have demonstrated that a variety of NCDs occur more commonly in HIV-infected populations. Although evidence from high-income countries is definitive as to the emerging importance of NCDs for PLHIV, there are far fewer data and research advances regarding such conditions in LMICs, where the great majority of PLHIV reside.28 Research conducted in LMICs is critical to understanding how local environmental and genetic factors may play a role in the prevalence and level of expression of NCD comorbidities, the potential side effects of ART, and the interactions between ART and NCD therapies. Table 1 illustrates some complexities in HIV disease treatment faced in LMICs, where a greater prevalence of other coinfections may weaken immune systems and complicate treatment, and delayed screening, diagnosis, and treatment can be expected to alter NCD progression. As we build an HIV and NCD comorbidities research agenda and set priorities in the LMIC context, gaps and needs in local research capacity will need to be considered, including suboptimal surveillance and variable diagnostic capabilities. Strengthening in-country research capacity in targeted areas with respect to HIV-NCD burdens must be a high priority.
This series sets forth priorities for research and research training related to specific disease and conditions; below, we highlight overarching priorities that cut across multiple disease areas. In addressing these priorities, special attention should be paid to key populations and their comorbid conditions.29–37
Public Health Surveillance and Clinical Epidemiology38–43
- NCD incidence among PLHIV, including key population subgroups.
- Prevalence of different NCD risk factors and measures of their impact among PLHIV.
- Differences in NCD mortality rates and morbidity outcomes among persons with HIV, as compared with those without HIV.
Basic and Clinical Research44-52
- Role of inflammation, coagulation, and immune mechanisms in NCD expression for those infected with HIV.
- Development of NCD biomarkers suitable for use in low-income settings among those living with HIV.
- Differential response to NCD treatment in different subgroups and regions.
- Impact of ART regimens used in LMICs on NCD expression.
- Impact of NCD treatments on prognosis and outcomes.
- Interactions between HIV and NCD pathogenic processes.
- Identification of effective and cost-effective HIV-NCD drug regimens.
Implementation Science and Health Systems53–64
- Efficiency, cost–benefit, and feasibility of existing point-of-care screening tests, affordable diagnostics, and drug delivery tools for NCDs among PLHIV.
- Development of innovative and effective models of integrated NCD and HIV care, including task-sharing strategies.
- Application of existing telemedicine and mobile technologies to cope with shortages of expert staff.
- Effective strategies for transforming vertical HIV programs into horizontal chronic disease care systems.
Infrastructure, Training, Capacity, and Workforce Development65–91
- Training scientists to work in multidisciplinary environments.
- New health workforce development to deliver joint HIV/NCD care.
Research advances related to HIV and NCD comorbidities can build on and help sustain the enormous progress that has been made in combating the global HIV/AIDS epidemic, and further improve the lives and health of those living with HIV. As increasing numbers of those infected with HIV receive long-term treatment and are confronted by NCDs, evidence-based intervention strategies are critical to ensure that health gains in these populations made over the past decade are not threatened by the rising burden of NCDs. The research agenda for HIV and NCD comorbidities in LMICs is substantial and will require sustained investment and attention from a wide range of stakeholders. The expanded availability of ART and concurrent growth of in-country health infrastructure and human capacity provide unique opportunities to obtain real-time, high-quality data sets about the prevalence and characteristics of coexisting NCDs by building on current HIV data collection efforts. Similarly, drug delivery systems now devoted to ART and tuberculosis medicines could add essential and affordable drugs for NCD management and improve the long-term survival and quality of life of those living with HIV, while potentially enhancing adherence to ART. In a time of scarce resources, imaginative enhancement of HIV research and care platforms and expanded training for researchers and providers can strengthen health systems and improve the overall care of persons living with HIV/AIDS. This goal will require creative partnerships among a wide range of stakeholders, including funding agencies, research institutions, LMIC governments, and in-country researchers and program implementers.
In many parts of rural Africa, Latin America, and Asia, clinics are now attempting to provide services beyond acute care to treat long-term HIV, and health systems designed to manage HIV/AIDS are under the strain of managing patients with additional NCD comorbidities. Research will play a critical role in providing the evidence, strategies, and tools that can be deployed to address this new reality, while research training and capacity building programs will enable local scientists to conduct the research needed in their environments. Increased research capacity, the breakdown of disciplinary silos, and scientific vision and leadership will be critical as we address this new challenge to continue to improve the lives of people living with HIV across the globe.
1. Walensky RP, Paltiel AD, Losina E, et al.. The survival benefits of AIDS treatment in the United States. J Infect Dis. 2006;194:11–19.
2. April MD, Wood R, Berkowitz BK, et al.. The survival benefits of antiretroviral therapy in South Africa. J Infect Dis. 2014;209:491–499.
3. Uyei J, Coetzee D, Macinko J, et al.. Integrated delivery of HIV and tuberculosis services in sub-Saharan Africa: a systematic review. Lancet Infect Dis. 2011;11:855–867.
4. Sarnquist CC, Rahangdale L, Maldonado Y. Reproductive health and family planning needs among HIV-infected women in Sub-Saharan Africa. Curr HIV Res. 2013;11:160–168.
5. Boyd MA, Cooper DA. Optimisation of HIV care and service delivery: doing more with less. Lancet. 2012;380:1860–1866.
6. Madzimbamuto FD, Ray S, Mogobe KD. Integration of HIV care into maternal health services: a crucial change required in improving quality of obstetric care in countries with high HIV prevalence. BMC Int Health Hum Rights. 2013;13:27.
7. Kim JY, Farmer P, Porter ME. Redefining global health-care delivery. Lancet. 2013;382:1060–1069.
8. Munderi P, Grosskurth H, Droti B, et al.. What are the essential components of HIV treatment and care services in low and middle-income countries: an overview by settings and levels of the health system? AIDS. 2012;26(suppl 2):S97–S103.
9. Ross DA, South A, Weller I, et al.. HIV treatment and care systems: the way forward. AIDS. 2012;26(suppl 2):S147–S152.
10. Kenny J, Mulenga V, Hoskins S, et al.. The needs for HIV treatment and care of children, adolescents, pregnant women and older people in low-income and middle-income countries. AIDS. 2012;26(suppl 2):S105–S116.
11. Samb B, Desai N, Nishtar S, et al.. Prevention and management of chronic disease: a litmus test for health-systems strengthening in low-income and middle-income countries. Lancet. 2010;376:1785–1797.
13. Magee MJ, Narayan KM. Global confluence of infectious and non-communicable diseases—the case of type 2 diabetes. Prev Med. 2013;57:149–151.
14. Chu C, Selwyn PA. An epidemic in evolution: the need for new models of HIV care in the chronic disease era. J Urban Health. 2011;88:556–566.
15. Bygbjerg IC. Double burden of noncommunicable and infectious diseases in developing countries. Science. 2012;337:1499–1501.
16. Geneau R, Hallen G. Toward a systemic research agenda for addressing the joint epidemics of HIV/AIDS and noncommunicable diseases. AIDS. 2012;26(suppl 1):S7–S10.
17. Bliss M. The Discovery of Insulin. Chicago, IL: University of Chicago Press; 2007:112–121.
18. Adebamowo CA, Casper C, Bhatia K, et al.. Challenges in the detection, prevention, and treatment of HIV-associated malignancies in low- and middle-income countries in Africa. J Acquir Immune Defic Syndr. 2014;67(suppl 1):S17–S26.
19. Kalyesubula R, Wearne N, Semitala FC, et al.. HIV-associated renal and genitourinary comorbidities in Africa. J Acquir Immune Defic Syndr. 2014;67(suppl 1):S68–S78.
20. Ali MK, Magee MJ, Dave JA, et al.. HIV and metabolic, body, and bone disorders: what we know from low- and middle-income countries. J Acquir Immune Defic Syndr. 2014;67(suppl 1):S27–S39.
21. Bloomfield GS, Khazanie P, Morris A, et al.. HIV and noncommunicable cardiovascular and pulmonary diseases in low- and middle-income countries in the ART era: what we know and best directions for future research. J Acquir Immune Defic Syndr. 2014;67(suppl 1):S40–S53.
22. Chibanda D, Benjamin L, Weiss HA, Abas M. Mental, neurological, and substance use disorders in people living with HIV/AIDS in low-and middle-income countries. J Acquir Immune Defic Syndr. 2014;67(suppl 1):S54–S67.
23. Kelly P, Saloojee H, Chen JY, Chung RT. Noncommunicable diseases in HIV infection in low- and middle-income countries: gastrointestinal, hepatic, and nutritional aspects. J Acquir Immune Defic Syndr. 2014;67(suppl 1):S79–S86.
24. Petersen M, Yiannoutsos CT, Justice A, Egger M. Observational research on NCDs in HIV-positive populations: conceptual and methodological considerations. J Acquir Immune Defic Syndr. 2014;67(suppl 1):S8–S16.
25. Hyle EP, Naidoo K, Su AE, et al.. HIV, tuberculosis, and non-communicable diseases: what is known about the costs, effects, and cost-effectiveness of integrated care? J Acquir Immune Defic Syndr. 2014;67(suppl 1):S87–S95.
26. Crabtree-Ramirez B, Del Rio C, Grinsztejn B, Sierra-Madero J. HIV and noncommunicable diseases (NCDs) in Latin America: a call for an integrated and comprehensive response. J Acquir Immune Defic Syndr. 2014;67(suppl 1):S96–S98.
27. Ananworavich J, Avihingsanon A. HIV and noncommunicable Diseases: the Asian perspective. J Acquir Immune Defic Syndr. 2014;67(suppl 1):S99–S103.
28. Vermund SH, Narayan KMV, Glass RI. Non-communicable diseases in HIV Survivors. Sci Transl Med. 2014;6(241):24.
29. Beyrer C, Sullivan PS, Sanchez J, et al.. A call to action for comprehensive HIV services for men who have sex with men. Lancet. 2012;380:424–438.
30. Bachireddy C, Soule MC, Izenberg JM, et al.. Integration of health services improves multiple healthcare outcomes among HIV-infected people who inject drugs in Ukraine. Drug Alcohol Depend. 2014;134:106–114.
31. Greenfield SF, Shields A, Connery HS, et al.. Integrated management of physician-delivered alcohol care for tuberculosis patients: design and implementation. Alcohol Clin Exp Res. 2010;34:317–330.
32. Jenkins R, Othieno C, Okeyo S, et al.. Health system challenges to integration of mental health delivery in primary care in Kenya–perspectives of primary care health workers. BMC Health Serv Res. 2013;13:368.
33. Mall S, Sorsdahl K, Swartz L, et al.. “I understand just a little…” Perspectives of HIV/AIDS service providers in South Africa of providing mental health care for people living with HIV/AIDS. AIDS Care. 2012;24:319–323.
34. Rachlis B, Sodhi S, Burciul B, et al.. A taxonomy for community-based care programs focused on HIV/AIDS prevention, treatment, and care in resource-poor settings. Glob Health Action. 2013;6:1–21.
35. Lindegren ML, Kennedy CE, Bain-Brickley D, et al.. Integration of HIV/AIDS services with maternal, neonatal and child health, nutrition, and family planning services. Cochrane Database Syst Rev. 2012;9:CD010119.
36. Parry CD, Petersen P, Carney T, et al.. Opportunities for enhancing and integrating HIV and drug services for drug using vulnerable populations in South Africa. Int J Drug Policy. 2010;21:289–295.
37. Sylla L, Bruce RD, Kamarulzaman A, et al.. Integration and co-location of HIV/AIDS, tuberculosis and drug treatment services. Int J Drug Policy. 2007;18:306–312.
38. Remais JV, Zeng G, Li G, et al.. Convergence of non-communicable and infectious diseases in low- and middle-income countries. Int J Epidemiol. 2013;42:221–227.
39. Chu C, Selwyn PA. Complications of HIV infection: a systems-based approach. Am Fam Physician. 2011;83:395–406.
40. Narh-Bana SA, Chirwa TF, Mwanyangala MA, et al.. Adult deaths and the future: a cause-specific analysis of adult deaths from a longitudinal study in rural Tanzania 2003–2007. Trop Med Int Health. 2012;17:1396–1404.
41. Chihana M, Floyd S, Molesworth A, et al.. Adult mortality and probable cause of death in rural northern Malawi in the era of HIV treatment. Trop Med Int Health. 2012;17:e74–e83.
42. Chamie G, Kwarisiima D, Clark TD, et al.; SEARCH Collaboration. Leveraging rapid community-based HIV testing campaigns for non-communicable diseases in rural Uganda. PLoS One. 2012;7:e43400.
43. Nishtar S, Bile KM, Ahmed A, et al.. Integrated population-based surveillance of noncommunicable diseases: the Pakistan model. Am J Prev Med. 2005;29(5 suppl 1):102–106.
44. Modjarrad K, Vermund SH. Effect of treating co-infections on HIV-1 viral load: a systematic review. Lancet Infect Dis. 2010;10:455–463.
45. Liao L, Xing H, Su B, et al.. Impact of HIV drug resistance on virologic and immunologic failure and mortality in a cohort of patients on antiretroviral therapy in China. AIDS. 2013;27:1815–1824.
46. Vermund SH, Powderly WG; Infectious Diseases Society of America; HIV Medicine Association of IDSA. Developing a human immunodeficiency virus/acquired immunodeficiency syndrome therapeutic research agenda for resource-limited countries: a consensus statement. Clin Infect Dis. 2003;37(suppl 1):S4–S12.
47. Zulu I, Schuman P, Musonda R, et al.. Priorities for antiretroviral therapy research in sub-Saharan Africa: a 2002 consensus conference in Zambia. J Acquir Immune Defic Syndr. 2004;36:831–834.
48. Hirschhorn LR, Kaaya SF, Garrity PS, et al.. Cancer and the “other” noncommunicable chronic diseases in older people living with HIV/AIDS in resource-limited settings: a challenge to success. AIDS. 2012;26(suppl 1):S65–S75.
49. Mwanahamuntu MH, Sahasrabuddhe VV, Kapambwe S, et al.. Advancing cervical cancer prevention initiatives in resource-constrained settings: insights from the Cervical Cancer Prevention Program in Zambia. PLoS Med. 2011;8:e1001032.
50. Gatanaga H, Hayashida T, Tanuma J, et al.. Prophylactic effect of antiretroviral therapy on hepatitis B virus infection. Clin Infect Dis. 2013;56:1812–1819.
51. Bates M, O'Grady J, Mwaba P, et al.. Evaluation of the burden of unsuspected pulmonary tuberculosis and co-morbidity with non-communicable diseases in sputum producing adult inpatients. PLoS One. 2012;7:e40774.
52. Creswell J, Raviglione M, Ottmani S, et al.. Tuberculosis and noncommunicable diseases: neglected links and missed opportunities. Eur Respir J. 2011;37:1269–1282.
53. Madon T, Hofman KJ, Kupfer L, et al.. Public health. Implementation science. Science. 2007;318:1728–1729.
54. Anand NP, Hofman KJ, Glass RI. The globalization of health research: harnessing the scientific diaspora. Acad Med. 2009;84:525–534.
55. Ciampa PJ, Vaz LM, Blevins M, et al.. The association among literacy, numeracy, HIV knowledge and health-seeking behavior: a population-based survey of women in rural Mozambique. PLoS One 2012;7:e39391.
56. Rabkin M, Melaku Z, Bruce K, et al.. Strengthening health systems for chronic care: leveraging HIV programs to support diabetes services in Ethiopia and Swaziland. J Trop Med. 2012;2012:137460.
57. Mounier-Jack S, Rudge JW, Phetsouvanh R, et al.. Critical interactions between Global Fund-supported programmes and health systems: a case study in Lao People's Democratic Republic. Health Policy Plan. 2010;25(suppl 1):i37–i42.
58. Hanvoravongchai P, Warakamin B, Coker R. Critical interactions between Global Fund-supported programmes and health systems: a case study in Thailand. Health Policy Plan. 2010;25(suppl 1):i53–i57.
59. Lawn SD, Harries AD, Wood R. Strategies to reduce early morbidity and mortality in adults receiving antiretroviral therapy in resource-limited settings. Curr Opin HIV AIDS. 2010;5:18–26.
60. Ekouevi DK, Stringer E, Coetzee D, et al.. Health facility characteristics and their relationship to coverage of PMTCT of HIV services across four African countries: the PEARL study. PLoS One. 2012;7:e29823.
61. Coleman R, Gill G, Wilkinson D. Noncommunicable disease management in resource-poor settings: a primary care model from rural South Africa. Bull World Health Organ. 1998;76:633–640.
62. Rudge JW, Phuanakoonon S, Nema KH, et al.. Critical interactions between Global Fund-supported programmes and health systems: a case study in Papua New Guinea. Health Policy Plan. 2010;25(suppl 1):i48–i52.
63. Atun R, Pothapregada SK, Kwansah J, et al.. Critical interactions between the Global Fund-supported HIV programs and the health system in Ghana. J Acquir Immune Defic Syndr. 2011;57(suppl 2):S72–S76.
64. Johnson K, Kennedy SB, Harris AO, et al.. Strengthening the HIV/AIDS service delivery system in Liberia: an international research capacity-building strategy. J Eval Clin Pract. 2005;11:257–273.
65. Palen J, El-Sadr W, Phoya A, et al.. PEPFAR, health system strengthening, and promoting sustainability and country ownership. J Acquir Immune Defic Syndr. 2012;60(suppl 3):S113–S119.
66. Eholié SP, Aoussi FE, Ouattara IS, et al.. HIV treatment and care in resource-constrained environments: challenges for the next decade. J Int AIDS Soc. 2012;15:17334.
67. Ali MK, Rabadán-Diehl C, Flanigan J, et al.. Systems and capacity to address noncommunicable diseases in low- and middle-income countries. Sci Transl Med. 2013;5:181cm4.
68. Oti SO. HIV and noncommunicable diseases: a case for health system building. Curr Opin HIV AIDS. 2013;8:65–69.
69. Gounder CR, Chaisson RE. A diagonal approach to building primary healthcare systems in resource-limited settings: women-centred integration of HIV/AIDS, tuberculosis, malaria, MCH and NCD initiatives. Trop Med Int Health. 2012;17:1426–1431.
70. Zewdie D, Cahn P, McClure C, et al.. The role of HIV research in building health system capacity in developing countries. Curr Opin HIV AIDS. 2008;3:481–488.
71. Vermund SH, Sidat M, Weil LF, et al.. Transitioning HIV care and treatment programs in southern Africa to full local management. AIDS. 2012;26:1303–1310.
72. Rabkin M, Kruk ME, El-Sadr WM. HIV, aging and continuity care: strengthening health systems to support services for noncommunicable diseases in low-income countries. AIDS. 2012;26(suppl 1):S77–S83.
73. Hogerzeil HV, Liberman J, Wirtz VJ, et al.. Promotion of access to essential medicines for non-communicable diseases: practical implications of the UN political declaration. Lancet. 2013;381:680–689.
74. Amuyunzu-Nyamongo M. Need for a multi-factorial, multi-sectorial and multi-disciplinary approach to NCD prevention and control in Africa. Glob Health Promot. 2010;17(2 suppl l):31–32.
75. Stuckler D, Basu S, McKee M. Drivers of inequality in Millennium Development Goal progress: a statistical analysis. PLoS Med. 2010;7:e1000241.
76. Maher D, Harries AD, Zachariah R, et al.. A global framework for action to improve the primary care response to chronic non-communicable diseases: a solution to a neglected problem. BMC Public Health. 2009;9:355.
77. Odutayo A, Hirji N. Noncommunicable diseases in developing countries: focus on research capacity building. JAMA Intern Med. 2013;173:1031.
78. Rabkin M, Nishtar S. Scaling up chronic care systems: leveraging HIV programs to support noncommunicable disease services. J Acquir Immune Defic Syndr. 2011;57(suppl 2):S87–S90.
79. Boutayeb A. The double burden of communicable and non-communicable diseases in developing countries. Trans R Soc Trop Med Hyg. 2006;100:191–199.
80. Atun R, Bataringaya J. Building a durable response to HIV/AIDS: implications for health systems. J Acquir Immune Defic Syndr. 2011;57(suppl 2):S91–S95.
81. Buvé A, Kalibala S, McIntyre J. Stronger health systems for more effective HIV/AIDS prevention and care. Int J Health Plann Manage. 2003;18(suppl 1):S41–S51.
82. Shigayeva A, Atun R, McKee M, et al.. Health systems, communicable diseases and integration. Health Policy Plan. 2010;25(suppl 1):i4–i20.
83. Ekouevi DK, Karcher S, Coffie PA. Strengthening health systems through HIV monitoring and evaluation in Sub-Saharan Africa. Curr Opin HIV AIDS. 2011;6:245–250.
84. Beaglehole R, Epping-Jordan J, Patel V, et al.. Improving the prevention and management of chronic disease in low-income and middle-income countries: a priority for primary health care. Lancet. 2008;372:940–949.
85. Bassett IV, Walensky RP. Integrating HIV screening into routine health care in resource-limited settings. Clin Infect Dis. 2010;50(suppl 3):S77–S84.
86. Coker R, Balen J, Mounier-Jack S, et al.. A conceptual and analytical approach to comparative analysis of country case studies: HIV and TB control programmes and health systems integration. Health Policy Plan. 2010;25(suppl 1):i21–i31.
87. Kruk ME. HIV and health systems: research to bridge the divide. J Acquir Immune Defic Syndr. 2011;57(suppl 2):S120–S123.
88. El-Sadr WM, Abrams EJ. Scale-up of HIV care and treatment: can it transform healthcare services in resource-limited settings? AIDS. 2007;21(suppl 5):S65–S70.
89. Grépin KA. Leveraging HIV programs to deliver an integrated package of health services: some words of caution. J Acquir Immune Defic Syndr. 2011;57(suppl 2):S77–S79.
90. Sliwa K, Damasceno A, Mayosi BM. Noncommunicable diseases in developing countries: focus on research capacity building–reply. JAMA Intern Med. 2013;173:1031–1032.
91. Tankwanchi ABS, Özden C, Vermund SH. Physician emigration from sub-Saharan Africa to the United States: analysis of the 2011 AMA physician masterfile. PLoS Med. 2013;10.