Is there scope for cost savings and efficiency gains in HIV services? A systematic review of the evidence from low- and middle-income countries

Est-il possible de faire des économies et d'obtenir des gains en termes d'efficacité dans les services anti-VIH? Un examen systématique des éléments de preuve dans les pays à revenu faible et intermédiaire

¿Hay margen para el ahorro de costes y el aumento de la eficacia en los servicios de VIH? Un examen sistemático de la evidencia de países con ingresos bajos y medios

هل يوجد نطاق لتحقيق وفورات التكاليف ومكاسب الكفاءة في خدمات فيروس العوز المناعي البشري؟ استعراض منهجي للبيّنات المستمدة من البلدان المنخفضة الدخل والبلدان المتوسطة الدخل

艾滋病毒服务中是否有实现节本增效的余地?中低收入国家的系统评价

Существуют ли возможности для экономии средств и повышения эффективности в сфере ВИЧ-услуг? Систематический обзор данных из стран с низким и средним уровнями доходов

Mariana Siapka Michelle Remme Carol Dayo Obure Claudia B Maier Karl L Dehne Anna Vassall About the authors

Objective

To synthesize the data available – on costs, efficiency and economies of scale and scope – for the six basic programmes of the UNAIDS Strategic Investment Framework, to inform those planning the scale-up of human immunodeficiency virus (HIV) services in low- and middle-income countries.

Methods

The relevant peer-reviewed and “grey” literature from low- and middle-income countries was systematically reviewed. Search and analysis followed Preferred Reporting Items for Systematic Reviews and Meta-analyses guidelines.

Findings

Of the 82 empirical costing and efficiency studies identified, nine provided data on economies of scale. Scale explained much of the variation in the costs of several HIV services, particularly those of targeted HIV prevention for key populations and HIV testing and treatment. There is some evidence of economies of scope from integrating HIV counselling and testing services with several other services. Cost efficiency may also be improved by reducing input prices, task shifting and improving client adherence.

Conclusion

HIV programmes need to optimize the scale of service provision to achieve efficiency. Interventions that may enhance the potential for economies of scale include intensifying demand-creation activities, reducing the costs for service users, expanding existing programmes rather than creating new structures, and reducing attrition of existing service users. Models for integrated service delivery – which is, potentially, more efficient than the implementation of stand-alone services – should be investigated further. Further experimental evidence is required to understand how to best achieve efficiency gains in HIV programmes and assess the cost–effectiveness of each service-delivery model.


Résumé

Objectif

Synthétiser les données disponibles - sur les coûts, l'efficacité et les économies d'échelle et d'envergure - pour les six programmes de base du Cadre d'investissement stratégique de l'ONUSIDA, afin d'informer les responsables de la planification de l'élargissement des services de lutte contre le virus de l'immunodéficience humaine (VIH) dans les pays à revenu faible et intermédiaire.

Méthodes

Des pairs des pays à revenu faible et intermédiaire ont systématiquement examiné la documentation pertinente «grise» et révisée. La recherche et l'analyse ont appliqué les directives PRISMA (éléments de rapport préférés pour les examens systématiques et les méta-analyses).

Résultats

Des 82 études de coûts et de rendement empiriques identifiées, neuf fournissaient des données sur les économies d'échelle. L'échelle expliquait en grande partie la variation des coûts de plusieurs services anti-VIH, en particulier ceux de la prévention ciblée du VIH dans les populations clés et ceux du dépistage et du traitement du VIH. Il existe certaines preuves d'économies d'envergure, résultant de l'intégration de services de conseil et de dépistage du VIH avec plusieurs autres services. La rentabilité peut également être améliorée en réduisant les prix des intrants, en déléguant des tâches et en améliorant l'adhésion des clients.

Conclusion

Les programmes anti-VIH doivent optimiser l'échelle de prestation des services pour être efficaces. Les interventions qui peuvent améliorer le potentiel des économies d'échelle comprennent l'intensification des activités de création de la demande, la réduction des coûts pour les utilisateurs des services, l'expansion des programmes existants plutôt que la création de nouvelles structures, et la réduction de l'attrition des utilisateurs des services existants. Les modèles de prestation des services intégrés, qui sont potentiellement plus efficaces que la mise en œuvre de services autonomes, doivent faire l'objet d'études approfondies. D'autres éléments de preuve expérimentaux sont requis pour trouver la meilleure façon d'obtenir des gains en termes d'efficacité dans les programmes anti-VIH, mais aussi pour évaluer le rapport coût-efficacité de chaque modèle de prestation de services.

Resumen

Objetivo

Sintetizar los datos disponibles sobre los costes, la eficacia y las economías de escala y alcance de los seis programas básicos del Marco Estratégico de Inversión de ONUSIDA e informar a los responsables de la planificación de la ampliación de los servicios del virus de la inmunodeficiencia humana (VIH) en países con ingresos bajos y medios.

Métodos

Se examinó sistemáticamente la literatura revisada por homólogos y «gris» relevante de países con ingresos bajos y medios. La búsqueda y el análisis se realizaron según las pautas de Ítems de Informe Preferidos para Evaluaciones Sistemáticas y Meta-Análisis.

Resultados

De los 82 estudios empíricos sobre costes y eficacia identificados, nueve de ellos proporcionaron datos sobre las economías de escala. La escala explicó gran parte de la variación de los costes en numerosos servicios de VIH, en particular en aquellos dirigidos a la prevención del VIH en poblaciones clave y las pruebas y el tratamiento del VIH. Hay alguna evidencia de economías de alcance que integran el asesoramiento sobre el VIH y los servicios de pruebas con muchos otros servicios. También sería posible aumentar la costo-eficacia mediante la reducción de los precios de los insumos, la delegación de funciones y la mejora de la fidelidad de los clientes.

Conclusión

Los programas de VIH deben optimizar la escala de prestación de servicios para conseguir ser eficaces. Las intervenciones pueden mejorar el potencial de las economías de escala, por ejemplo, al intensificar las actividades de promoción de demanda, reducir los costes para los usuarios, expandir los programas existentes en lugar de crear estructuras nuevas y reducir el abandono de los usuarios existentes de los servicios. Se deben investigar más los modelos de prestación de servicios integrados, que son posiblemente más eficaces que la implementación de servicios independientes. Es necesario obtener más evidencia experimental para comprender cómo es posible lograr mayor eficacia en los programas de VIH y evaluar la costo-eficacia de cada modelo de prestación de servicios.

ملخص

الغرض

توليف البيانات المتاحة - بشأن التكاليف والكفاءة ووفورات الحجم والنطاق - المتعلقة بالبرامج الأساسية الستة لإطار الاستثمار الاستراتيجي لبرنامج الأمم المتحدة المشترك لمكافحة الإيدز، بغية توفير المعلومات لمن يقومون بتخطيط زيادة حجم خدمات فيروس العوز المناعي البشري في البلدان المنخفضة الدخل والبلدان المتوسطة الدخل.

الطريقة

تم إجراء استعراض منهجي للمنشورات التي خضعت للاستعراض الجماعي والمؤلفات "غير الرسمية" ذات الصلة من البلدان المنخفضة الدخل والبلدان المتوسطة الدخل. واتبع البحث والتحليل البنود المتعلقة بتقديم التقارير المفضلة للمبادئ التوجيهية للاستعراضات المنهجية والتحليلات الوصفية.

النتائج

قدمت تسع دراسات، من إجمالي 82 دراسة تجريبية للتكلفة والكفاءة تم تحديدها، بيانات عن وفورات الحجم. وفسر النطاق الكثير من التفاوت في تكاليف العديد من خدمات فيروس العوز المناعي البشري، لاسيما تلك المتعلقة بالوقاية المستهدفة من فيروس العوز المناعي البشري في الفئات السكانية الرئيسية واختبارات فيروس العوز المناعي البشري وعلاجه. وهناك بعض البيّنات حول وفورات الحجم المستمدة من دمج استشارات فيروس العوز المناعي البشري وخدمات الاختبارات مع عدة خدمات أخرى. ويمكن كذلك تحسين خفض التكاليف عن طريق تقليل أسعار المدخلات وإعادة توزيع المهام وتحسين التزام العميل.

الاستنتاج

يتعين على برامج فيروس العوز المناعي البشري تحسين نطاق تقديم الخدمات بغية تحقيق الكفاءة. وتشمل التدخلات التي يمكنها تعزيز إمكانيات وفورات الحجم تكثيف أنشطة إيجاد الطلب، وتقليل التكاليف التي يتحملها مستخدمو الخدمات، وتوسيع البرامج القائمة بدلاً من إنشاء هياكل جديدة، وتقليل التناقص في مستخدمي الخدمات القائمة. وينبغي إجراء مزيد من التحري لنماذج الإيتاء المتكامل للخدمات، التي يحتمل أن تكون أكثر كفاءة من تنفيذ خدمات قائمة بذاتها. وثمة حاجة لمزيد من البيّنات التجريبية بغية فهم كيفية تحقيق مكاسب الكفاءة في برامج فيروس العوز المناعي البشري وتقييم مردودية كل نموذج من نماذج إيتاء الخدمة.

摘要

目的

综合联合国艾滋病规划署战略投资框架的六种基本规划可用的成本、效率、经济规模和范围的相关数据,为在中低收入国家开展的扩大艾滋病病毒(HIV)服务计划提供信息。

方法

系统评价了中低收入国家相关同行评议的“灰色”文献。根据系统评价和荟萃分析指南的优先报告条目执行搜索和分析。

结果

在所识别的82项实证成本和效率研究中,有九项研究提供了规模经济相关数据。规模解释了数种HIV服务成本的很多变化,尤其是有针对性的重点人群HIV预防和HIV检测和治疗的成本变化。在HIV咨询和测试服务和其他若干服务整合的服务中有一些范围经济的证据。也可以通过降低输入价格、任务切换和提高客户忠诚度来改进成本效益。

结论

HIV计划需要最优化服务提供的规模以实现效益。可提高规模经济潜力的干预措施包括强化需求创建活动、降低服务用户的成本、扩大现有的项目(而不是创建新的结构)以及减少现有服务用户的脱失。整合服务交付模型可能比实施独立服务更有效,需要对其进行进一步的调查。需要进一步的实验证据来理解如何在HIV计划中最好地实现增效以及评估每个服务交付模型的成本效益。

Резюме

Цель

Сопоставить доступные данные по расходам, эффективности и экономии на масштабах и объемах по шести основным программам Рамочной программы стратегических инвестиций ЮНЭЙДС и предоставить информацию тем, кто планирует расширение масштабов оказания услуг, связанных с вирусом иммунодефицита человека (ВИЧ), в странах с низким и средним уровнями доходов.

Методы

Был проведен систематический обзор соответствующей рецензируемой и внеиздательской («серой») литературы из стран с низким и средним уровнями доходов. В процессе поиска и анализа соблюдались положения Руководства по предпочтительным позициям отчетности для систематических обзоров и мета-анализов.

Результаты

Из 82 выявленных эмпирических исследований расчета затрат и эффективности в девяти содержались данные об экономии на масштабах. Масштабом объяснялась большая часть различий в стоимости нескольких ВИЧ-услуг, в особенности тех услуг, которые охватывали профилактику ВИЧ среди целевых групп населения, тестирование на ВИЧ и лечение ВИЧ. Имеется ряд доказательств экономии на масштабах при объединении услуг консультирования по ВИЧ и тестирования на ВИЧ с некоторыми другими услугами. Экономическую эффективность также можно повысить за счет снижения цен на ресурсы, перераспределения задач и повышения уровня лояльности клиентов.

Вывод

В рамках программ по ВИЧ необходимо оптимизировать масштабы предоставления услуг для повышения их эффективности. К числу мер, которые могут повысить потенциал экономии на масштабах, относится более активное проведение мероприятий по стимулированию спроса, снижение затрат пользователей услуг, расширение существующих программ вместо создания новых структур, а также сокращение потерь пользователей существующих услуг. Требуется дальнейшее изучение моделей комплексного оказания услуг, что потенциально является более эффективным, чем оказание отдельных услуг. Требуются дополнительные экспериментальные доказательства для определения наилучших путей достижения эффективности программ по ВИЧ и оценки экономической эффективности каждой модели предоставления услуг.

Introduction

To reach the Millennium Development Goals for human immunodeficiency virus (HIV) infection1The Millennium Development Goals report 2012. New York (NY): United Nations; 2012. and the targets of the Political Declaration on HIV and Acquired Immunodeficiency Syndrome (AIDS),22011 United Nations General Assembly Political Declaration on HIV/AIDS. Geneva: Joint United Nations Programme on HIV/AIDS; 2011. many low- and middle-income countries still need to scale up essential HIV services. Given the scarce financial resources available and competing donor priorities, methods to improve efficiency in the delivery of HIV services are gaining increased global attention.3Creese A, Floyd K, Alban A, Guinness L. Cost-effectiveness of HIV/AIDS interventions in Africa: a systematic review of the evidence. Lancet. 2002;359:1635-43. doi: http://dx.doi.org/10.1016/S0140-6736(02)08595-1 PMID: 12020523
https://doi.org/10.1016/S0140-6736(02)08...
6Together we will end AIDS. Geneva: Joint United Nations Programme on HIV/AIDS; 2012.

In general, an “efficient” HIV service cannot be improved without the further use of existing resources and cannot be maintained at its current level with fewer resources. The word “efficiency” has several dimensions when applied to HIV services. For example, economic theory distinguishes between efficiency from improving social welfare – the “allocative” efficiency that is often assessed in the health sector in terms of cost–effectiveness – and a more contained definition of efficiency that examines how best to use resources to provide individual services – the “technical” efficiency that is commonly assessed in terms of the unit costs of a service. Two potential areas for improving technical efficiency are service scale and service scope. “Economies of scale” are the reductions in the unit cost of a service that might be achieved when the volume of that service’s provision is increased, whereas “economies of scope” are the reductions in the unit cost of a service that might be observed when that service is provided jointly with other services.3Creese A, Floyd K, Alban A, Guinness L. Cost-effectiveness of HIV/AIDS interventions in Africa: a systematic review of the evidence. Lancet. 2002;359:1635-43. doi: http://dx.doi.org/10.1016/S0140-6736(02)08595-1 PMID: 12020523
https://doi.org/10.1016/S0140-6736(02)08...
,4Galárraga O, Colchero MA, Wamai RG, Bertozzi SM. HIV prevention cost-effectiveness: a systematic review. BMC Public Health. 2009;9 Suppl 1;S5. doi: http://dx.doi.org/10.1186/1471-2458-9-S1-S5 PMID: 19922689
https://doi.org/10.1186/1471-2458-9-S1-S...
,7Galárraga O, Wirtz VJ, Figueroa-Lara A, Santa-Ana-Tellez Y, Coulibaly I, Viisainen K, et al. Unit costs for delivery of antiretroviral treatment and prevention of mother-to-child transmission of HIV: a systematic review for low- and middle-income countries. Pharmacoeconomics. 2011;29:579-99. PMID: 216716871212 Walker D. Cost and cost-effectiveness of HIV/AIDS prevention strategies in developing countries: is there an evidence base? Health Policy Plan. 2003;18:4-17. doi: http://dx.doi.org/10.1093/heapol/18.1.4 PMID: 12582104
https://doi.org/10.1093/heapol/18.1.4...

There have been several recent reviews of the data available on the costs and cost–effectiveness of HIV interventions.3Creese A, Floyd K, Alban A, Guinness L. Cost-effectiveness of HIV/AIDS interventions in Africa: a systematic review of the evidence. Lancet. 2002;359:1635-43. doi: http://dx.doi.org/10.1016/S0140-6736(02)08595-1 PMID: 12020523
https://doi.org/10.1016/S0140-6736(02)08...
,4Galárraga O, Colchero MA, Wamai RG, Bertozzi SM. HIV prevention cost-effectiveness: a systematic review. BMC Public Health. 2009;9 Suppl 1;S5. doi: http://dx.doi.org/10.1186/1471-2458-9-S1-S5 PMID: 19922689
https://doi.org/10.1186/1471-2458-9-S1-S...
,7Galárraga O, Wirtz VJ, Figueroa-Lara A, Santa-Ana-Tellez Y, Coulibaly I, Viisainen K, et al. Unit costs for delivery of antiretroviral treatment and prevention of mother-to-child transmission of HIV: a systematic review for low- and middle-income countries. Pharmacoeconomics. 2011;29:579-99. PMID: 216716871313 Santa-Ana-Tellez Y, DeMaria LM, Galárraga O. Costs of interventions for AIDS orphans and vulnerable children. Trop Med Int Health. 2011;16:1417-26. doi: http://dx.doi.org/10.1111/j.1365-3156.2011.02856.x PMID: 21859439
https://doi.org/10.1111/j.1365-3156.2011...
Most of these reviews were focused on allocative efficiency.3Creese A, Floyd K, Alban A, Guinness L. Cost-effectiveness of HIV/AIDS interventions in Africa: a systematic review of the evidence. Lancet. 2002;359:1635-43. doi: http://dx.doi.org/10.1016/S0140-6736(02)08595-1 PMID: 12020523
https://doi.org/10.1016/S0140-6736(02)08...
,4Galárraga O, Colchero MA, Wamai RG, Bertozzi SM. HIV prevention cost-effectiveness: a systematic review. BMC Public Health. 2009;9 Suppl 1;S5. doi: http://dx.doi.org/10.1186/1471-2458-9-S1-S5 PMID: 19922689
https://doi.org/10.1186/1471-2458-9-S1-S...
,7Galárraga O, Wirtz VJ, Figueroa-Lara A, Santa-Ana-Tellez Y, Coulibaly I, Viisainen K, et al. Unit costs for delivery of antiretroviral treatment and prevention of mother-to-child transmission of HIV: a systematic review for low- and middle-income countries. Pharmacoeconomics. 2011;29:579-99. PMID: 21671687,9Sweeney S, Obure CD, Maier CB, Greener R, Dehne K, Vassall A. Costs and efficiency of integrating HIV/AIDS services with other health services: a systematic review of evidence and experience. Sex Transm Infect. 2012;88:85-99. doi: http://dx.doi.org/10.1136/sextrans-2011-050199 PMID: 22158934
https://doi.org/10.1136/sextrans-2011-05...
,1212 Walker D. Cost and cost-effectiveness of HIV/AIDS prevention strategies in developing countries: is there an evidence base? Health Policy Plan. 2003;18:4-17. doi: http://dx.doi.org/10.1093/heapol/18.1.4 PMID: 12582104
https://doi.org/10.1093/heapol/18.1.4...
The results of the few previous studies on the technical efficiency of HIV services indicate not only that there is considerable variation – between service providers and between settings – in the unit costs of providing similar HIV services, but also that there is, in general, much scope for improving the technical efficiency of HIV services.7Galárraga O, Wirtz VJ, Figueroa-Lara A, Santa-Ana-Tellez Y, Coulibaly I, Viisainen K, et al. Unit costs for delivery of antiretroviral treatment and prevention of mother-to-child transmission of HIV: a systematic review for low- and middle-income countries. Pharmacoeconomics. 2011;29:579-99. PMID: 21671687,9Sweeney S, Obure CD, Maier CB, Greener R, Dehne K, Vassall A. Costs and efficiency of integrating HIV/AIDS services with other health services: a systematic review of evidence and experience. Sex Transm Infect. 2012;88:85-99. doi: http://dx.doi.org/10.1136/sextrans-2011-050199 PMID: 22158934
https://doi.org/10.1136/sextrans-2011-05...
,1414 Zeng W, Shepard DS, Chilingerian J, Avila-Figueroa C. How much can we gain from improved efficiency? An examination of performance of national HIV/AIDS programs and its determinants in low- and middle-income countries. BMC Health Serv Res. 2012;12:74. doi: http://dx.doi.org/10.1186/1472-6963-12-74 PMID: 22443135
https://doi.org/10.1186/1472-6963-12-74...
However, these reviews are outdated or were only partial in their coverage of possible interventions.

Given the current interest of policy-makers in reducing the costs of HIV services, there is now an urgent need to update and synthesize the data on the technical efficiency of HIV services. We therefore present here a systematic literature review of the costs of the six basic programmatic activities of the Strategic Investment Framework of the Joint United Nations Programme on HIV/AIDS (UNAIDS): antiretroviral therapy (ART) and counselling and testing; “key-population” programmes – that is, programmes that target groups of individuals who are at particularly high risk of HIV infection; condom distribution and social marketing; voluntary medical male circumcision; programmes to eliminate HIV infections among children and to keep their mothers alive; and programmes of behaviour-change communications targeted at young adults and the general population.1515 Schwartländer B, Stover J, Hallett T, Atun R, Avila C, Gouws E, et al.; Investment Framework Study Group. Towards an improved investment approach for an effective response to HIV/AIDS. Lancet. 2011;377:2031-41. doi: http://dx.doi.org/10.1016/S0140-6736(11)60702-2 PMID: 21641026
https://doi.org/10.1016/S0140-6736(11)60...

Methods

Search strategy and selection criteria

We conducted a systematic review of the peer-reviewed and “grey” literature on HIV services in low- and middle-income countries by following the search and analysis process recommended in the Preferred Reporting Items for Systematic Reviews and Meta-analyses guidelines.1616 Moher D, Liberati A, Tetzlaff J, Altman DG; PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6:e1000097. doi: http://dx.doi.org/10.1371/journal.pmed.1000097 PMID: 19621072
https://doi.org/10.1371/journal.pmed.100...
The PubMed and Eldis databases and the Cochrane library were searched, using AIDS, HIV, acquired immunodeficiency syndrome, cost, cost analysis, efficiency, economies of scale and economies of scope as the search terms. Searches were limited to English-language articles published between January 1990 and October 2013. Manual searches of the web sites of key organizations were also carried out to identify grey literature and minimize the risk of publication bias (Fig. 1).1717 Shepperd S, Lewin S, Straus S, Clarke M, Eccles MP, Fitzpatrick R, et al. Can we systematically review studies that evaluate complex interventions? PLoS Med. 2009;6:e1000086. doi: http://dx.doi.org/10.1371/journal.pmed.1000086 PMID: 19668360
https://doi.org/10.1371/journal.pmed.100...
The World Bank’s definitions were used to categorize countries as low- or middle-income.1818 How we classify countries [Internet]. Washington (DC): World Bank; 2012. Available from: http://data.worldbank.org/about/country-classifications [cited 2013 Oct 19].
http://data.worldbank.org/about/country-...
Although conference abstracts, editorials, commentaries and “letters to the editor” were used to identify related studies – through a “snowballing” process – any data found only in such publications were excluded from the systematic review. Studies of mathematical models that provided no primary data on costs were also excluded. Bibliographies and previous systematic reviews were examined to identify additional studies of relevance. Authors were contacted directly if the full text of a published paper, unpublished paper or report was not available to us. Two researchers screened the identified citations, reviewed the full texts of potentially eligible articles and selected the final articles for inclusion. Data were extracted by one researcher before being checked by another researcher. Whenever there was uncertainty or disagreement about the inclusion of a study, the authors discussed the study until a consensus was reached.

Fig. 1

Flowchart for the selection of studies on costs of the six basic programmes of UNAIDS Strategic Investment Framework

Data on the unit costs of the HIV services of interest were available for seven upper-middle-income countries, 14 lower-middle-income countries and 12 low-income countries. Most of the included studies were categorized as cost analyses but cost data were also extracted from cost–effectiveness and cost–benefit analyses, resource-needs estimations and broad evaluation studies. Authors of only 30 of the included studies undertook sensitivity analyses to assess the levels of uncertainty in their cost estimates.

Data extraction and quality of studies

The quality of studies was assessed using Drummond’s checklist.1919 Drummond MF, Jefferson TO; The BMJ Economic Evaluation Working Party. Guidelines for authors and peer reviewers of economic submissions to the BMJ. BMJ. 1996;313:275-83. doi: http://dx.doi.org/10.1136/bmj.313.7052.275 PMID: 8704542
https://doi.org/10.1136/bmj.313.7052.275...
Additional criteria for the assessment of study quality were included whether all relevant costs were included, the source of the cost estimates, whether a sensitivity analysis was conducted and, if so, what type of sensitivity analysis was used, and the scale of the study – in terms of the number of sites for which costings were made. As we wished to evaluate the overall quality of studies, we included all studies with some empirical basis, irrespective of their quality. However, we took study quality into account when reporting the strength of the evidence.

We used the unit costs of service provision – at the health-provider level – as our primary comparative statistic. However, we also noted whether the data from each study included other, “above-service” costs, such as the out-of-pocket expenses of clients using a particular HIV service. We took a narrative approach in our data synthesis, as has been recommended for reviews of health systems and organizational interventions.1717 Shepperd S, Lewin S, Straus S, Clarke M, Eccles MP, Fitzpatrick R, et al. Can we systematically review studies that evaluate complex interventions? PLoS Med. 2009;6:e1000086. doi: http://dx.doi.org/10.1371/journal.pmed.1000086 PMID: 19668360
https://doi.org/10.1371/journal.pmed.100...

For the purposes of the systematic review, all reported costs were adjusted to United States dollar (US$) values for the year 2011.

Results

Summary of studies

We identified 7108 unique citations of potential relevance and selected 131 of these for full-text review (Fig. 1). Overall, 82 studies met the inclusion criteria: 65 reported in peer-reviewed journals and 17 reported in the grey literature (Table 1). Most (n = 63) of the included studies were classified as fully empirical and 34 included all relevant costs. Costing methods varied between studies but included a “top-down” approach, a “bottom-up” approach and a combination of both of these approaches. Together, the 82 included studies covered 92 unit-cost analyses that related to ART (n = 34), key population programmes (n = 14), HIV counselling and testing (n = 22), programmes to eliminate HIV infections among children and to keep their mothers alive (n = 10), male circumcision (n = 7), condom distribution (n = 4) or behaviour-change communications (n = 1). Many studies were excluded because they did not relate to core HIV or AIDS services, were not conducted in a low- or middle-income country or did not report empirical costs.

Table 1
Quality of studies included in the systematic review

Table 2, Table 3, Table 4, Table 5, Table 6, Table 7 and Table 8 provide summaries of costs reported in the literature that we reviewed. Further details can be found in Table 9, Table 10, Table 11, Table 12, Table 13, Table 14 and Table 15 (available at: http://www.who.int/bulletin/volumes/92/7/13-127639) and in Appendix A (available at: http://researchonline.lshtm.ac.uk/1620414/). The costs reported in the included studies were generally restricted to the unit costs of one or more HIV services at site level. The reporting of “above-service” costs varied and was always only partial. Most studies included the costs of activities such as training and supervision,3636 Jaffar S, Amuron B, Foster S, Birungi J, Levin J, Namara G, et al.; Jinja Trial Team. Rates of virological failure in patients treated in a home-based versus a facility-based HIV-care model in Jinja, southeast Uganda: a cluster-randomised equivalence trial. Lancet. 2009;374:2080-9. doi: http://dx.doi.org/10.1016/S0140-6736(09)61674-3 PMID: 19939445
https://doi.org/10.1016/S0140-6736(09)61...
,3737 Bratt JH, Torpey K, Kabaso M, Gondwe Y. Costs of HIV/AIDS outpatient services delivered through Zambian public health facilities. Trop Med Int. Health 2011;16:110-8. doi: http://dx.doi.org/10.1111/j.1365-3156.2010.02640.x PMID: 20958891
https://doi.org/10.1111/j.1365-3156.2010...
but the costs of several other activities, such as the maintenance of a drugs supply chain, transportation and technical support, were rarely included.

Table 2
Summary of selected mean unit costs of antiretroviral therapy
Table 3
Summary of selected mean unit costs of behaviour-change communications
Table 4
Summary of selected mean unit costs of condom promotion and distribution
Table 5
Summary of selected mean unit costs of human immunodeficiency virus counselling and testing
Table 6
Summary of selected mean unit costs of key-population programmes
Table 7
Summary of selected mean unit costs of voluntary medical male circumcision
Table 8
Summary of selected mean unit costs of the elimination of mother-to-child transmission of human immunodeficiency virus
Table 9
Studies on antiretroviral therapy included in the systematic review
Table 10
Study on behaviour-change communications included in the systematic review
Table 11
Studies on condom distribution included in the systematic review
Table 12
Studies on human immunodeficiency virus counselling and testing included in the systematic review
Table 13
Studies on key-population programmes included in the systematic review
Table 14
Studies on voluntary medical male circumcision included in the systematic review
Table 15
Studies on the elimination of mother-to-child transmission included in the systematic review

Economies of scale

The key findings from 40 studies found exploring costs and economies of scale are summarized in Appendix A. Only nine of these studies had sufficiently large samples to apply econometric methods to explore any associations between scale and costs.2323 Marseille EA, Kevany S, Ahmed I, Feleke G, Graham B, Heller T, et al. Case management to improve adherence for HIV-infected patients receiving antiretroviral therapy in Ethiopia: a micro-costing study. Cost Eff Resour Alloc. 2011;9:18. doi: http://dx.doi.org/10.1186/1478-7547-9-18 PMID: 22185656
https://doi.org/10.1186/1478-7547-9-18...
,6969 Dandona L, Sisodia P, Ramesh YK, Kumar SG, Kumar AA, Rao MC, et al. Cost and efficiency of HIV voluntary counselling and testing centres in Andhra Pradesh, India. Natl Med J India. 2005;18:26-31. PMID: 15835489,7474 Dandona L, Sisodia P, Kumar SG, Ramesh YK, Kumar AA, Rao MC, et al. HIV prevention programmes for female sex workers in Andhra Pradesh, India: outputs, cost and efficiency. BMC Public Health. 2005;5:98. doi: http://dx.doi.org/10.1186/1471-2458-5-98 PMID: 16181491
https://doi.org/10.1186/1471-2458-5-98...
,7575 Guinness L, Kumaranayake L, Rajaraman B, Sankaranarayanan G, Vannela G, Raghupathi P, et al. Does scale matter? The costs of HIV-prevention interventions for commercial sex workers in India. Bull World Health Organ. 2005;83:747-55. PMID: 16283051,7777 Dandona L, Kumar SP, Ramesh Y, Rao MC, Kumar AA, Marseille E, et al. Changing cost of HIV interventions in the context of scaling-up in India. AIDS. 2008;22 Suppl 1;S43-9. doi: http://dx.doi.org/10.1097/01.aids.0000327622.24232.aa PMID: 18664952
https://doi.org/10.1097/01.aids.00003276...
7979 Chandrashekar S, Guinness L, Kumaranayake L, Reddy B, Govindraj Y, Vickerman P, et al. The effects of scale on the costs of targeted HIV prevention interventions among female and male sex workers, men who have sex with men and transgenders in India. Sex Transm Infect. 2010;86 Suppl 1;i89-94. doi: http://dx.doi.org/10.1136/sti.2009.038547 PMID: 20167740
https://doi.org/10.1136/sti.2009.038547...
,9393 Menzies NA, Berruti AA, Blandford JM. The determinants of HIV treatment costs in resource limited settings. PLoS One. 2012;7:e48726. doi: http://dx.doi.org/10.1371/journal.pone.0048726 PMID: 23144946
https://doi.org/10.1371/journal.pone.004...
,9696 Marseille E, Dandona L, Marshall N, Gaist P, Bautista-Arredondo S, Rollins B, et al. HIV prevention costs and program scale: data from the PANCEA project in five low and middle-income countries. BMC Health Serv Res. 2007;7:108. doi: http://dx.doi.org/10.1186/1472-6963-7-108 PMID: 17626616
https://doi.org/10.1186/1472-6963-7-108...
Most of these studies were focused on HIV prevention among key populations. None covered condom distribution, male circumcision or interventions that were targeted at men who have sex with men. Scale was often found to explain statistically significant proportions of the variability seen in unit costs – including 48%, 42%, 28–83%, 25–88% and 45–96% of such variability in an ART programme,2323 Marseille EA, Kevany S, Ahmed I, Feleke G, Graham B, Heller T, et al. Case management to improve adherence for HIV-infected patients receiving antiretroviral therapy in Ethiopia: a micro-costing study. Cost Eff Resour Alloc. 2011;9:18. doi: http://dx.doi.org/10.1186/1478-7547-9-18 PMID: 22185656
https://doi.org/10.1186/1478-7547-9-18...
a programme for the elimination of mother-to-child transmission of HIV infection,9696 Marseille E, Dandona L, Marshall N, Gaist P, Bautista-Arredondo S, Rollins B, et al. HIV prevention costs and program scale: data from the PANCEA project in five low and middle-income countries. BMC Health Serv Res. 2007;7:108. doi: http://dx.doi.org/10.1186/1472-6963-7-108 PMID: 17626616
https://doi.org/10.1186/1472-6963-7-108...
HIV counselling and testing,6969 Dandona L, Sisodia P, Ramesh YK, Kumar SG, Kumar AA, Rao MC, et al. Cost and efficiency of HIV voluntary counselling and testing centres in Andhra Pradesh, India. Natl Med J India. 2005;18:26-31. PMID: 15835489,9696 Marseille E, Dandona L, Marshall N, Gaist P, Bautista-Arredondo S, Rollins B, et al. HIV prevention costs and program scale: data from the PANCEA project in five low and middle-income countries. BMC Health Serv Res. 2007;7:108. doi: http://dx.doi.org/10.1186/1472-6963-7-108 PMID: 17626616
https://doi.org/10.1186/1472-6963-7-108...
and programmes targeting sex workers6969 Dandona L, Sisodia P, Ramesh YK, Kumar SG, Kumar AA, Rao MC, et al. Cost and efficiency of HIV voluntary counselling and testing centres in Andhra Pradesh, India. Natl Med J India. 2005;18:26-31. PMID: 15835489,7474 Dandona L, Sisodia P, Kumar SG, Ramesh YK, Kumar AA, Rao MC, et al. HIV prevention programmes for female sex workers in Andhra Pradesh, India: outputs, cost and efficiency. BMC Public Health. 2005;5:98. doi: http://dx.doi.org/10.1186/1471-2458-5-98 PMID: 16181491
https://doi.org/10.1186/1471-2458-5-98...
,7575 Guinness L, Kumaranayake L, Rajaraman B, Sankaranarayanan G, Vannela G, Raghupathi P, et al. Does scale matter? The costs of HIV-prevention interventions for commercial sex workers in India. Bull World Health Organ. 2005;83:747-55. PMID: 16283051,7777 Dandona L, Kumar SP, Ramesh Y, Rao MC, Kumar AA, Marseille E, et al. Changing cost of HIV interventions in the context of scaling-up in India. AIDS. 2008;22 Suppl 1;S43-9. doi: http://dx.doi.org/10.1097/01.aids.0000327622.24232.aa PMID: 18664952
https://doi.org/10.1097/01.aids.00003276...
,7979 Chandrashekar S, Guinness L, Kumaranayake L, Reddy B, Govindraj Y, Vickerman P, et al. The effects of scale on the costs of targeted HIV prevention interventions among female and male sex workers, men who have sex with men and transgenders in India. Sex Transm Infect. 2010;86 Suppl 1;i89-94. doi: http://dx.doi.org/10.1136/sti.2009.038547 PMID: 20167740
https://doi.org/10.1136/sti.2009.038547...
,9696 Marseille E, Dandona L, Marshall N, Gaist P, Bautista-Arredondo S, Rollins B, et al. HIV prevention costs and program scale: data from the PANCEA project in five low and middle-income countries. BMC Health Serv Res. 2007;7:108. doi: http://dx.doi.org/10.1186/1472-6963-7-108 PMID: 17626616
https://doi.org/10.1186/1472-6963-7-108...
and people who inject drugs,9696 Marseille E, Dandona L, Marshall N, Gaist P, Bautista-Arredondo S, Rollins B, et al. HIV prevention costs and program scale: data from the PANCEA project in five low and middle-income countries. BMC Health Serv Res. 2007;7:108. doi: http://dx.doi.org/10.1186/1472-6963-7-108 PMID: 17626616
https://doi.org/10.1186/1472-6963-7-108...
respectively.

The only evidence of a diseconomy of scale9696 Marseille E, Dandona L, Marshall N, Gaist P, Bautista-Arredondo S, Rollins B, et al. HIV prevention costs and program scale: data from the PANCEA project in five low and middle-income countries. BMC Health Serv Res. 2007;7:108. doi: http://dx.doi.org/10.1186/1472-6963-7-108 PMID: 17626616
https://doi.org/10.1186/1472-6963-7-108...
that we found in the results of econometric studies was the observation that a quadratic function provided a fairly good fit to the cost data observed in one such investigaton.9191 Dandona L, Kumar SG, Ramesh YK, Rao MC, Marseille E, Kahn JG, et al. Outputs, cost and efficiency of public sector centres for prevention of mother to child transmission of HIV in Andhra Pradesh, India. BMC Health Serv Res. 2008;8:26. doi: http://dx.doi.org/10.1186/1472-6963-8-26 PMID: 18234117
https://doi.org/10.1186/1472-6963-8-26...

In several descriptive studies, unit costs for HIV services appeared to be influenced by the link between scale and the achievement of optimal staff workloads.2323 Marseille EA, Kevany S, Ahmed I, Feleke G, Graham B, Heller T, et al. Case management to improve adherence for HIV-infected patients receiving antiretroviral therapy in Ethiopia: a micro-costing study. Cost Eff Resour Alloc. 2011;9:18. doi: http://dx.doi.org/10.1186/1478-7547-9-18 PMID: 22185656
https://doi.org/10.1186/1478-7547-9-18...
,3737 Bratt JH, Torpey K, Kabaso M, Gondwe Y. Costs of HIV/AIDS outpatient services delivered through Zambian public health facilities. Trop Med Int. Health 2011;16:110-8. doi: http://dx.doi.org/10.1111/j.1365-3156.2010.02640.x PMID: 20958891
https://doi.org/10.1111/j.1365-3156.2010...
,5555 Terris-Prestholt F, Kumaranayake L, Obasi AI, Cleophas-Mazige B, Makokha M, Todd J, et al. From trial intervention to scale-up: costs of an adolescent sexual health program in Mwanza, Tanzania. Sex Transm Dis. 2006;33 Suppl;S133-9. doi: http://dx.doi.org/10.1097/01.olq.0000200606.98181.42 PMID: 16652070
https://doi.org/10.1097/01.olq.000020060...
,6464 Obure CD, Vassall A, Michaels C, Terris-Prestholt F, Mayhew S, Stackpool-Moore L, et al.; Integra Research Team. Optimising the cost and delivery of HIV counselling and testing services in Kenya and Swaziland. Sex Transm Infect. 2012;88:498-503. doi: http://dx.doi.org/10.1136/sextrans-2012-050544 PMID: 22859498
https://doi.org/10.1136/sextrans-2012-05...
As a programme ages, unit costs may either increase7979 Chandrashekar S, Guinness L, Kumaranayake L, Reddy B, Govindraj Y, Vickerman P, et al. The effects of scale on the costs of targeted HIV prevention interventions among female and male sex workers, men who have sex with men and transgenders in India. Sex Transm Infect. 2010;86 Suppl 1;i89-94. doi: http://dx.doi.org/10.1136/sti.2009.038547 PMID: 20167740
https://doi.org/10.1136/sti.2009.038547...
or – if the programme scales up over time – decrease.2020 Menzies NA, Berruti AA, Berzon R, Filler S, Ferris R, Ellerbrock TV, et al. The cost of providing comprehensive HIV treatment in PEPFAR-supported programs. AIDS. 2011;25:1753-60. doi: http://dx.doi.org/10.1097/QAD.0b013e3283463eec PMID: 21412127
https://doi.org/10.1097/QAD.0b013e328346...
,2727 Harling G, Bekker LG, Wood R. Cost of a dedicated ART clinic. S Afr Med J. 2007;97:593-6. PMID: 17952216,7373 Guinness L, Vickerman P, Quayyum Z, Foss A, Watts C, Rodericks A, et al. The cost-effectiveness of consistent and early intervention of harm reduction for injecting drug users in Bangladesh. Addiction. 2010;105:319-28. doi: http://dx.doi.org/10.1111/j.1360-0443.2009.02755.x PMID: 19922513
https://doi.org/10.1111/j.1360-0443.2009...
Any cost reductions that occur during scale-up may result from “learning by doing” and task shifting.2020 Menzies NA, Berruti AA, Berzon R, Filler S, Ferris R, Ellerbrock TV, et al. The cost of providing comprehensive HIV treatment in PEPFAR-supported programs. AIDS. 2011;25:1753-60. doi: http://dx.doi.org/10.1097/QAD.0b013e3283463eec PMID: 21412127
https://doi.org/10.1097/QAD.0b013e328346...
,3232 Martinson N, Mohapi L, Bakos D, Gray GE, McIntyre JA, Holmes CB. Costs of providing care for HIV-infected adults in an urban HIV clinic in Soweto, South Africa. J Acquir Immune Defic Syndr. 2009;50:327-30. doi: http://dx.doi.org/10.1097/QAI.0b013e3181958546 PMID: 19194308
https://doi.org/10.1097/QAI.0b013e318195...
,3939 Renaud A, Basenya O, de Borman N, Greindl I, Meyer-Rath G. The cost effectiveness of integrated care for people living with HIV including antiretroviral treatment in a primary health care centre in Bujumbura, Burundi. AIDS Care. 2009;21:1388-94. doi: http://dx.doi.org/10.1080/09540120902884042 PMID: 20024715
https://doi.org/10.1080/0954012090288404...
,4343 Gupta I, Trivedi M, Kandamuthan S. Recurrent costs of India’s free ART program. In: Haacker M, Claeson M, editors. HIV and AIDS in South Asia: an economic development risk. Washington: World Bank; 2009. pp. 191-237.

Economies of scope

We reviewed 23 studies that reported both unit costs and economies of scope, including 12 studies2020 Menzies NA, Berruti AA, Berzon R, Filler S, Ferris R, Ellerbrock TV, et al. The cost of providing comprehensive HIV treatment in PEPFAR-supported programs. AIDS. 2011;25:1753-60. doi: http://dx.doi.org/10.1097/QAD.0b013e3283463eec PMID: 21412127
https://doi.org/10.1097/QAD.0b013e328346...
,2424 Cleary S, Tshehlo R, Jouquet G, Makakole L. Ensuring access to free HIV/AIDS care and treatment in Lesotho. Cape Town: University of Cape Town; 2007. Available from: http://196.202.240.21/mcaweb/documents/Health/HEALTH%20Decentralization%20of%20ART.pdf [cited 2013 Oct 19].
http://196.202.240.21/mcaweb/documents/H...
,3131 Kevany S, Meintjes G, Rebe K, Maartens G, Cleary S. Clinical and financial burdens of secondary level care in a public sector antiretroviral roll-out setting (G.F. Jooste Hospital). S Afr Med J. 2009;99:320-5. PMID: 19588792,3333 Long L, Fox M, Sanne I, Rosen S. The high cost of second-line antiretroviral therapy for HIV/AIDS in South Africa. AIDS. 2010;24:915-9. doi: http://dx.doi.org/10.1097/QAD.0b013e3283360976 PMID: 20042849
https://doi.org/10.1097/QAD.0b013e328336...
,4646 Koenig SP, Riviere C, Leger P, Severe P, Atwood S, Fitzgerald DW, et al. The cost of antiretroviral therapy in Haiti. Cost Eff Resour Alloc. 2008;6:3. doi: http://dx.doi.org/10.1186/1478-7547-6-3 PMID: 18275615
https://doi.org/10.1186/1478-7547-6-3...
,5252 Hsu J, Zinsou C, Parkhurst J, N’Dour M, Foyet L, Mueller DH. Comparative costs and cost-effectiveness of behavioural interventions as part of HIV prevention strategies. Health Policy Plan. 2013;28:20-9. doi: http://dx.doi.org/10.1093/heapol/czs021 PMID: 22411881
https://doi.org/10.1093/heapol/czs021...
,6363 Grabbe KL, Menzies N, Taegtmeyer M, Emukule G, Angala P, Mwega I, et al. Increasing access to HIV counseling and testing through mobile services in Kenya: strategies, utilization, and cost-effectiveness. J Acquir Immune Defic Syndr. 2010;54:317-23. doi: http://dx.doi.org/10.1097/QAI.0b013e3181ced126 PMID: 20453819
https://doi.org/10.1097/QAI.0b013e3181ce...
,6464 Obure CD, Vassall A, Michaels C, Terris-Prestholt F, Mayhew S, Stackpool-Moore L, et al.; Integra Research Team. Optimising the cost and delivery of HIV counselling and testing services in Kenya and Swaziland. Sex Transm Infect. 2012;88:498-503. doi: http://dx.doi.org/10.1136/sextrans-2012-050544 PMID: 22859498
https://doi.org/10.1136/sextrans-2012-05...
,6969 Dandona L, Sisodia P, Ramesh YK, Kumar SG, Kumar AA, Rao MC, et al. Cost and efficiency of HIV voluntary counselling and testing centres in Andhra Pradesh, India. Natl Med J India. 2005;18:26-31. PMID: 15835489,8888 Costing male circumcision in Zimbabwe and impacts of scaling up the circumcision program. Washington (DC): United States Agency for International Development; 2010.,9191 Dandona L, Kumar SG, Ramesh YK, Rao MC, Marseille E, Kahn JG, et al. Outputs, cost and efficiency of public sector centres for prevention of mother to child transmission of HIV in Andhra Pradesh, India. BMC Health Serv Res. 2008;8:26. doi: http://dx.doi.org/10.1186/1472-6963-8-26 PMID: 18234117
https://doi.org/10.1186/1472-6963-8-26...
,9595 Minh HV, Bach TX, Mai NY, Wright P. The cost of providing HIV/AIDS counseling and testing services in Vietnam. Value in Health Regional Issues. 2012;1:36-40. doi: http://dx.doi.org/10.1016/j.vhri.2012.03.012
https://doi.org/10.1016/j.vhri.2012.03.0...
that were not included in the earlier review by Sweeney et al. (2012).9Sweeney S, Obure CD, Maier CB, Greener R, Dehne K, Vassall A. Costs and efficiency of integrating HIV/AIDS services with other health services: a systematic review of evidence and experience. Sex Transm Infect. 2012;88:85-99. doi: http://dx.doi.org/10.1136/sextrans-2011-050199 PMID: 22158934
https://doi.org/10.1136/sextrans-2011-05...
Most of the 23 studies related to HIV counselling and testing (n = 18) or ART (n = 3) but we also analysed single studies on three other types of programme: behaviour-change communications, male circumcision and the elimination of mother-to-child transmission (Appendix A).

Although the integration of voluntary HIV counselling and testing with other health services was found to improve quality, increase the utilization of services and reduce the cost per visit in some programmes,5757 Twahir A, Maggwa BN, Askew I. Integration of STI and HIV/AIDS services with MCH-FP services: a case study of the Mkomani Clinic Society in Mombasa, Kenya. Washington (DC): Population Council; 1996. Available from: http://www.popcouncil.org/pdfs/frontiers/fphivintegrat/Mombassa96.pdf [cited 2013 Oct 19].
http://www.popcouncil.org/pdfs/frontiers...
,6161 Liambila W, Askew I, Ayisi R, Gathitu M, Mwangi J, Homan R, et al. Feasibility, acceptability, effect and cost of integrating counseling and testing for HIV within family planning services in Kenya. Washington (DC): Population Council; 2008. Available from: http://www.popcouncil.org/pdfs/frontiers/FR_FinalReports/Kenya_CT_FP.pdf [cited 2013 Oct 19].
http://www.popcouncil.org/pdfs/frontiers...
,7070 Das R, Biswas K, Panda P, Khan ME, Homan R. Strengthening financial sustainability through integration of voluntary counseling and testing services with other reproductive health services. Washington (DC): Population Council; 2007. Available from: http://www.popcouncil.org/pdfs/frontiers/FR_FinalReports/India_CINI.pdf [cited 2013 Oct 19].
http://www.popcouncil.org/pdfs/frontiers...
it was found to increase costs in other programmes.2020 Menzies NA, Berruti AA, Berzon R, Filler S, Ferris R, Ellerbrock TV, et al. The cost of providing comprehensive HIV treatment in PEPFAR-supported programs. AIDS. 2011;25:1753-60. doi: http://dx.doi.org/10.1097/QAD.0b013e3283463eec PMID: 21412127
https://doi.org/10.1097/QAD.0b013e328346...
,9595 Minh HV, Bach TX, Mai NY, Wright P. The cost of providing HIV/AIDS counseling and testing services in Vietnam. Value in Health Regional Issues. 2012;1:36-40. doi: http://dx.doi.org/10.1016/j.vhri.2012.03.012
https://doi.org/10.1016/j.vhri.2012.03.0...
Compared with the costs of stand-alone services, the integration of HIV counselling and testing with other health services has been reported to reduce unit costs – of the counselling and testing – by between 17% and 79%.9Sweeney S, Obure CD, Maier CB, Greener R, Dehne K, Vassall A. Costs and efficiency of integrating HIV/AIDS services with other health services: a systematic review of evidence and experience. Sex Transm Infect. 2012;88:85-99. doi: http://dx.doi.org/10.1136/sextrans-2011-050199 PMID: 22158934
https://doi.org/10.1136/sextrans-2011-05...
,5757 Twahir A, Maggwa BN, Askew I. Integration of STI and HIV/AIDS services with MCH-FP services: a case study of the Mkomani Clinic Society in Mombasa, Kenya. Washington (DC): Population Council; 1996. Available from: http://www.popcouncil.org/pdfs/frontiers/fphivintegrat/Mombassa96.pdf [cited 2013 Oct 19].
http://www.popcouncil.org/pdfs/frontiers...
,5959 Forsythe S, Arthur G, Ngatia G, Mutemi R, Odhiambo J, Gilks C. Assessing the cost and willingness to pay for voluntary HIV counselling and testing in Kenya. Health Policy Plan. 2002;17:187-95. doi: http://dx.doi.org/10.1093/heapol/17.2.187 PMID: 12000779
https://doi.org/10.1093/heapol/17.2.187...
,6161 Liambila W, Askew I, Ayisi R, Gathitu M, Mwangi J, Homan R, et al. Feasibility, acceptability, effect and cost of integrating counseling and testing for HIV within family planning services in Kenya. Washington (DC): Population Council; 2008. Available from: http://www.popcouncil.org/pdfs/frontiers/FR_FinalReports/Kenya_CT_FP.pdf [cited 2013 Oct 19].
http://www.popcouncil.org/pdfs/frontiers...
,6363 Grabbe KL, Menzies N, Taegtmeyer M, Emukule G, Angala P, Mwega I, et al. Increasing access to HIV counseling and testing through mobile services in Kenya: strategies, utilization, and cost-effectiveness. J Acquir Immune Defic Syndr. 2010;54:317-23. doi: http://dx.doi.org/10.1097/QAI.0b013e3181ced126 PMID: 20453819
https://doi.org/10.1097/QAI.0b013e3181ce...
,6464 Obure CD, Vassall A, Michaels C, Terris-Prestholt F, Mayhew S, Stackpool-Moore L, et al.; Integra Research Team. Optimising the cost and delivery of HIV counselling and testing services in Kenya and Swaziland. Sex Transm Infect. 2012;88:498-503. doi: http://dx.doi.org/10.1136/sextrans-2012-050544 PMID: 22859498
https://doi.org/10.1136/sextrans-2012-05...
,6767 Menzies N, Abang B, Wanyenze R, Nuwaha F, Mugisha B, Coutinho A, et al. The costs and effectiveness of four HIV counseling and testing strategies in Uganda. AIDS. 2009;23:395-401. doi: http://dx.doi.org/10.1097/QAD.0b013e328321e40b PMID: 19114865
https://doi.org/10.1097/QAD.0b013e328321...
,7070 Das R, Biswas K, Panda P, Khan ME, Homan R. Strengthening financial sustainability through integration of voluntary counseling and testing services with other reproductive health services. Washington (DC): Population Council; 2007. Available from: http://www.popcouncil.org/pdfs/frontiers/FR_FinalReports/India_CINI.pdf [cited 2013 Oct 19].
http://www.popcouncil.org/pdfs/frontiers...
,9595 Minh HV, Bach TX, Mai NY, Wright P. The cost of providing HIV/AIDS counseling and testing services in Vietnam. Value in Health Regional Issues. 2012;1:36-40. doi: http://dx.doi.org/10.1016/j.vhri.2012.03.012
https://doi.org/10.1016/j.vhri.2012.03.0...
In terms of the unit costs per HIV infection identified, provider-initiated voluntary testing and counselling was found to be less than half as expensive as client-initiated counselling and testing.6464 Obure CD, Vassall A, Michaels C, Terris-Prestholt F, Mayhew S, Stackpool-Moore L, et al.; Integra Research Team. Optimising the cost and delivery of HIV counselling and testing services in Kenya and Swaziland. Sex Transm Infect. 2012;88:498-503. doi: http://dx.doi.org/10.1136/sextrans-2012-050544 PMID: 22859498
https://doi.org/10.1136/sextrans-2012-05...
When counselling and testing were integrated with other health services, a strong and functioning referral system was found to be important for creating demand.9Sweeney S, Obure CD, Maier CB, Greener R, Dehne K, Vassall A. Costs and efficiency of integrating HIV/AIDS services with other health services: a systematic review of evidence and experience. Sex Transm Infect. 2012;88:85-99. doi: http://dx.doi.org/10.1136/sextrans-2011-050199 PMID: 22158934
https://doi.org/10.1136/sextrans-2011-05...
,2424 Cleary S, Tshehlo R, Jouquet G, Makakole L. Ensuring access to free HIV/AIDS care and treatment in Lesotho. Cape Town: University of Cape Town; 2007. Available from: http://196.202.240.21/mcaweb/documents/Health/HEALTH%20Decentralization%20of%20ART.pdf [cited 2013 Oct 19].
http://196.202.240.21/mcaweb/documents/H...
,2525 Cleary SM, McIntyre D, Boulle AM. The cost-effectiveness of antiretroviral treatment in Khayelitsha, South Africa – a primary data analysis. Cost Eff Resour Alloc. 2006;4:20. doi: http://dx.doi.org/10.1186/1478-7547-4-20 PMID: 17147833
https://doi.org/10.1186/1478-7547-4-20...
,2929 Rosen S, Long L, Sanne I. The outcomes and outpatient costs of different models of antiretroviral treatment delivery in South Africa. Trop Med Int Health. 2008;13:1005-15. doi: http://dx.doi.org/10.1111/j.1365-3156.2008.02114.x PMID: 18631314
https://doi.org/10.1111/j.1365-3156.2008...
,3131 Kevany S, Meintjes G, Rebe K, Maartens G, Cleary S. Clinical and financial burdens of secondary level care in a public sector antiretroviral roll-out setting (G.F. Jooste Hospital). S Afr Med J. 2009;99:320-5. PMID: 19588792,3333 Long L, Fox M, Sanne I, Rosen S. The high cost of second-line antiretroviral therapy for HIV/AIDS in South Africa. AIDS. 2010;24:915-9. doi: http://dx.doi.org/10.1097/QAD.0b013e3283360976 PMID: 20042849
https://doi.org/10.1097/QAD.0b013e328336...
,3535 Babigumira JB, Sethi AK, Smyth KA, Singer ME. Cost effectiveness of facility-based care, home-based care and mobile clinics for provision of antiretroviral therapy in Uganda. Pharmacoeconomics 2009;27:963-73. doi: http://dx.doi.org/10.2165/11318230-000000000-00000 PMID: 19888795
https://doi.org/10.2165/11318230-0000000...
,4545 Kitajima T, Kobayashi Y, Chaipah W, Sato H, Chadbunchachai W, Thuennadee R. Costs of medical services for patients with HIV/AIDS in Khon Kaen, Thailand. AIDS. 2003;17:2375-81. doi: http://dx.doi.org/10.1097/00002030-200311070-00013 PMID: 14571190
https://doi.org/10.1097/00002030-2003110...
,6363 Grabbe KL, Menzies N, Taegtmeyer M, Emukule G, Angala P, Mwega I, et al. Increasing access to HIV counseling and testing through mobile services in Kenya: strategies, utilization, and cost-effectiveness. J Acquir Immune Defic Syndr. 2010;54:317-23. doi: http://dx.doi.org/10.1097/QAI.0b013e3181ced126 PMID: 20453819
https://doi.org/10.1097/QAI.0b013e3181ce...
,6767 Menzies N, Abang B, Wanyenze R, Nuwaha F, Mugisha B, Coutinho A, et al. The costs and effectiveness of four HIV counseling and testing strategies in Uganda. AIDS. 2009;23:395-401. doi: http://dx.doi.org/10.1097/QAD.0b013e328321e40b PMID: 19114865
https://doi.org/10.1097/QAD.0b013e328321...
,6969 Dandona L, Sisodia P, Ramesh YK, Kumar SG, Kumar AA, Rao MC, et al. Cost and efficiency of HIV voluntary counselling and testing centres in Andhra Pradesh, India. Natl Med J India. 2005;18:26-31. PMID: 15835489,7070 Das R, Biswas K, Panda P, Khan ME, Homan R. Strengthening financial sustainability through integration of voluntary counseling and testing services with other reproductive health services. Washington (DC): Population Council; 2007. Available from: http://www.popcouncil.org/pdfs/frontiers/FR_FinalReports/India_CINI.pdf [cited 2013 Oct 19].
http://www.popcouncil.org/pdfs/frontiers...

Other pathways to improve efficiency

Our systematic review revealed evidence of many other determinants of costs and efficiency besides economies of scale and scope (Appendix A). Although task shifting was observed to reduce costs, there were concerns that it might also reduce service quality.3030 Vella V, Govender T, Dlamini S, Taylor M, Moodley I, David V, et al. Evaluation of antiretroviral therapy against HIV/Aids in KwaZulu-Natal, South Africa. Pietermaritzburg: KwaZulu-Natal Department of Health; 2008. Available from: http://www.kznhealth.gov.za/italian/arv.pdf [cited 2013 Oct 19].
http://www.kznhealth.gov.za/italian/arv....
In India, costs incurred above the level of service delivery have been reported to account for 35 to 46% of the unit costs of HIV prevention.4343 Gupta I, Trivedi M, Kandamuthan S. Recurrent costs of India’s free ART program. In: Haacker M, Claeson M, editors. HIV and AIDS in South Asia: an economic development risk. Washington: World Bank; 2009. pp. 191-237. Loss to follow-up may be a key source of inefficiency in ART programmes – resulting in a 15 to 55% increase in the unit costs per patient treated.2929 Rosen S, Long L, Sanne I. The outcomes and outpatient costs of different models of antiretroviral treatment delivery in South Africa. Trop Med Int Health. 2008;13:1005-15. doi: http://dx.doi.org/10.1111/j.1365-3156.2008.02114.x PMID: 18631314
https://doi.org/10.1111/j.1365-3156.2008...
,3131 Kevany S, Meintjes G, Rebe K, Maartens G, Cleary S. Clinical and financial burdens of secondary level care in a public sector antiretroviral roll-out setting (G.F. Jooste Hospital). S Afr Med J. 2009;99:320-5. PMID: 19588792,3333 Long L, Fox M, Sanne I, Rosen S. The high cost of second-line antiretroviral therapy for HIV/AIDS in South Africa. AIDS. 2010;24:915-9. doi: http://dx.doi.org/10.1097/QAD.0b013e3283360976 PMID: 20042849
https://doi.org/10.1097/QAD.0b013e328336...

We found limited evidence of possible gains from targeting specific groups of patients and clients4Galárraga O, Colchero MA, Wamai RG, Bertozzi SM. HIV prevention cost-effectiveness: a systematic review. BMC Public Health. 2009;9 Suppl 1;S5. doi: http://dx.doi.org/10.1186/1471-2458-9-S1-S5 PMID: 19922689
https://doi.org/10.1186/1471-2458-9-S1-S...
,5858 Sweat M, Gregorich S, Sangiwa G, Furlonge C, Balmer D, Kamenga C, et al. Cost-effectiveness of voluntary HIV-1 counselling and testing in reducing sexual transmission of HIV-1 in Kenya and Tanzania. Lancet. 2000;356:113-21. doi: http://dx.doi.org/10.1016/S0140-6736(00)02447-8 PMID: 10963247
https://doi.org/10.1016/S0140-6736(00)02...
,6060 John FN, Farquhar C, Kiarie JN, Kabura MN, John-Stewart GC. Cost effectiveness of couple counselling to enhance infant HIV-1 prevention. Int J STD AIDS. 2008;19:406-9. doi: http://dx.doi.org/10.1258/ijsa.2008.007234 PMID: 18595879
https://doi.org/10.1258/ijsa.2008.007234...
,6363 Grabbe KL, Menzies N, Taegtmeyer M, Emukule G, Angala P, Mwega I, et al. Increasing access to HIV counseling and testing through mobile services in Kenya: strategies, utilization, and cost-effectiveness. J Acquir Immune Defic Syndr. 2010;54:317-23. doi: http://dx.doi.org/10.1097/QAI.0b013e3181ced126 PMID: 20453819
https://doi.org/10.1097/QAI.0b013e3181ce...
,6464 Obure CD, Vassall A, Michaels C, Terris-Prestholt F, Mayhew S, Stackpool-Moore L, et al.; Integra Research Team. Optimising the cost and delivery of HIV counselling and testing services in Kenya and Swaziland. Sex Transm Infect. 2012;88:498-503. doi: http://dx.doi.org/10.1136/sextrans-2012-050544 PMID: 22859498
https://doi.org/10.1136/sextrans-2012-05...
,6767 Menzies N, Abang B, Wanyenze R, Nuwaha F, Mugisha B, Coutinho A, et al. The costs and effectiveness of four HIV counseling and testing strategies in Uganda. AIDS. 2009;23:395-401. doi: http://dx.doi.org/10.1097/QAD.0b013e328321e40b PMID: 19114865
https://doi.org/10.1097/QAD.0b013e328321...
and little examination of the trade-off between the costs of targeting and efficiency gains. We also found no studies in which the cost efficiency of providing more intense services to a particular group was compared with that of providing a minimal service to a larger population group.

Discussion

There is a growing evidence base on the costs of delivering ART, HIV counselling and testing, interventions for condom distribution and the prevention of mother-to-child transmission of HIV, voluntary medical male circumcision and key-population programmes in low- and middle-income countries. While some of the differences observed in the unit costs are likely to be explained by environmental factors, the wide variation indicates there is general room for improvement in the technical efficiency of HIV services.

In our systematic review, evidence of economies of scale in all of the studies enabled a robust examination of the relationship between scale and costs. HIV services should therefore be focused on sites with sufficient demand for such services. In the “free market”, economies of scale generally lead to mergers that create large-scale providers and large production units. However, where populations are dispersed, a balance needs to be sought between provider costs and the costs incurred by clients as they access care. Several of the studies that we reviewed demonstrated the high health care costs for patients.3636 Jaffar S, Amuron B, Foster S, Birungi J, Levin J, Namara G, et al.; Jinja Trial Team. Rates of virological failure in patients treated in a home-based versus a facility-based HIV-care model in Jinja, southeast Uganda: a cluster-randomised equivalence trial. Lancet. 2009;374:2080-9. doi: http://dx.doi.org/10.1016/S0140-6736(09)61674-3 PMID: 19939445
https://doi.org/10.1016/S0140-6736(09)61...
3838 Hounton SH, Akonde A, Zannou DM, Bashi J, Meda N, Newlands D. Costing universal access of highly active antiretroviral therapy in Benin. AIDS Care. 2008;20:582-7. doi: http://dx.doi.org/10.1080/09540120701868303 PMID: 18484329
https://doi.org/10.1080/0954012070186830...
,4040 Kombe G, Galaty D, Nwagbara C. Scaling-up antiretroviral treatment in the public sector in Nigeria: a comprehensive analysis of resource requirements [Internet]. Bethesda (MD): Abt Associates; 2004. Available from: http://www.healthsystems2020.org/content/resource/detail/1489/ [cited 2013 Oct 19].
http://www.healthsystems2020.org/content...
,5858 Sweat M, Gregorich S, Sangiwa G, Furlonge C, Balmer D, Kamenga C, et al. Cost-effectiveness of voluntary HIV-1 counselling and testing in reducing sexual transmission of HIV-1 in Kenya and Tanzania. Lancet. 2000;356:113-21. doi: http://dx.doi.org/10.1016/S0140-6736(00)02447-8 PMID: 10963247
https://doi.org/10.1016/S0140-6736(00)02...
The burden of these “client-side” costs may need to be shifted to service providers – through the provision of more accessible services or, possibly, by reimbursing each patient’s travel costs. Such changes may limit the extent to which economies of scale are realized. Although the high costs to patients of accessing care might be reduced by providing mobile or home-based services, there is little evidence to show that the implementation of such services reduces provider costs. Some degree of trade-off may have to be made between client and provider costs.3535 Babigumira JB, Sethi AK, Smyth KA, Singer ME. Cost effectiveness of facility-based care, home-based care and mobile clinics for provision of antiretroviral therapy in Uganda. Pharmacoeconomics 2009;27:963-73. doi: http://dx.doi.org/10.2165/11318230-000000000-00000 PMID: 19888795
https://doi.org/10.2165/11318230-0000000...
3737 Bratt JH, Torpey K, Kabaso M, Gondwe Y. Costs of HIV/AIDS outpatient services delivered through Zambian public health facilities. Trop Med Int. Health 2011;16:110-8. doi: http://dx.doi.org/10.1111/j.1365-3156.2010.02640.x PMID: 20958891
https://doi.org/10.1111/j.1365-3156.2010...

Unit costs may often be reduced by increasing staff workloads.2828 Harling G, Wood R. The evolving cost of HIV in South Africa: changes in health care cost with duration on antiretroviral therapy for public sector patients. J Acquir Immune Defic Syndr. 2007;45:348-54. PMID: 17496562,3131 Kevany S, Meintjes G, Rebe K, Maartens G, Cleary S. Clinical and financial burdens of secondary level care in a public sector antiretroviral roll-out setting (G.F. Jooste Hospital). S Afr Med J. 2009;99:320-5. PMID: 19588792,3232 Martinson N, Mohapi L, Bakos D, Gray GE, McIntyre JA, Holmes CB. Costs of providing care for HIV-infected adults in an urban HIV clinic in Soweto, South Africa. J Acquir Immune Defic Syndr. 2009;50:327-30. doi: http://dx.doi.org/10.1097/QAI.0b013e3181958546 PMID: 19194308
https://doi.org/10.1097/QAI.0b013e318195...
,3636 Jaffar S, Amuron B, Foster S, Birungi J, Levin J, Namara G, et al.; Jinja Trial Team. Rates of virological failure in patients treated in a home-based versus a facility-based HIV-care model in Jinja, southeast Uganda: a cluster-randomised equivalence trial. Lancet. 2009;374:2080-9. doi: http://dx.doi.org/10.1016/S0140-6736(09)61674-3 PMID: 19939445
https://doi.org/10.1016/S0140-6736(09)61...
,3939 Renaud A, Basenya O, de Borman N, Greindl I, Meyer-Rath G. The cost effectiveness of integrated care for people living with HIV including antiretroviral treatment in a primary health care centre in Bujumbura, Burundi. AIDS Care. 2009;21:1388-94. doi: http://dx.doi.org/10.1080/09540120902884042 PMID: 20024715
https://doi.org/10.1080/0954012090288404...
,4747 Marques HH, Couttolenc BF, Latorre MdoR, Aquino MZ, Aveiro MI, Pluciennik AM. Costs of care provided in a university hospital for children exposed to or infected with the HIV/AIDS. Cad Saude Publica. 2007;23 Suppl 3;S402-13. doi: http://dx.doi.org/10.1590/S0102-311X2007001500008 PMID: 17992346
https://doi.org/10.1590/S0102-311X200700...
,6464 Obure CD, Vassall A, Michaels C, Terris-Prestholt F, Mayhew S, Stackpool-Moore L, et al.; Integra Research Team. Optimising the cost and delivery of HIV counselling and testing services in Kenya and Swaziland. Sex Transm Infect. 2012;88:498-503. doi: http://dx.doi.org/10.1136/sextrans-2012-050544 PMID: 22859498
https://doi.org/10.1136/sextrans-2012-05...
In optimizing staff workloads, supply of staff has to be matched with the demand for services. On the supply side, the extent to which staffing levels are fixed is often either an artefact of human-resource planning – in which staffing complements are defined using norms, irrespective of the workload or demand per site – or a reflection of minimum clinical requirements. In many settings, the creation of demand – where there is a need – may be the only way to optimize workloads. Demand may be increased by identifying new clients, improving adherence and reducing loss to follow-up.5959 Forsythe S, Arthur G, Ngatia G, Mutemi R, Odhiambo J, Gilks C. Assessing the cost and willingness to pay for voluntary HIV counselling and testing in Kenya. Health Policy Plan. 2002;17:187-95. doi: http://dx.doi.org/10.1093/heapol/17.2.187 PMID: 12000779
https://doi.org/10.1093/heapol/17.2.187...
,9999 Stringer EM, Sinkala M, Stringer JS, Mzyece E, Makuka I, Goldenberg RL, et al. Prevention of mother-to-child transmission of HIV in Africa: successes and challenges in scaling-up a nevirapine-based program in Lusaka, Zambia. AIDS. 2003;17:1377-82. doi: http://dx.doi.org/10.1097/00002030-200306130-00012 PMID: 12799559
https://doi.org/10.1097/00002030-2003061...
Within staffing norms, there may still be flexibility within staffing allocations at site level. Site or programme managers must be provided with the data and means to allocate staff in a responsive manner. Task shifting may reduce both provider costs – by lowering the cost of salaries and increasing flexibility around any minimum staffing requirements101101 Task shifting: rational redistribution of tasks among health workforce teams: global recommendations and guidelines. Geneva: World Health Organization; 2008. – and client costs – by allowing services to be delivered from sites that are relatively close to the clients and run by lower-level staff.102102 Zachariah R, Ford N, Philips M, Lynch S, Massaquoi M, Janssens V, et al. Task shifting in HIV/AIDS: opportunities, challenges and proposed actions for sub-Saharan Africa. Trans R Soc Trop Med Hyg. 2009;103:549-58. doi: http://dx.doi.org/10.1016/j.trstmh.2008.09.019 PMID: 18992905
https://doi.org/10.1016/j.trstmh.2008.09...
In the future, new technologies, such as the non-surgical PrePex method of circumcision, may further reduce the need for high-level clinical staff.3030 Vella V, Govender T, Dlamini S, Taylor M, Moodley I, David V, et al. Evaluation of antiretroviral therapy against HIV/Aids in KwaZulu-Natal, South Africa. Pietermaritzburg: KwaZulu-Natal Department of Health; 2008. Available from: http://www.kznhealth.gov.za/italian/arv.pdf [cited 2013 Oct 19].
http://www.kznhealth.gov.za/italian/arv....
,3232 Martinson N, Mohapi L, Bakos D, Gray GE, McIntyre JA, Holmes CB. Costs of providing care for HIV-infected adults in an urban HIV clinic in Soweto, South Africa. J Acquir Immune Defic Syndr. 2009;50:327-30. doi: http://dx.doi.org/10.1097/QAI.0b013e3181958546 PMID: 19194308
https://doi.org/10.1097/QAI.0b013e318195...
,6666 Hausler HP, Sinanovic E, Kumaranayake L, Naidoo P, Schoeman H, Karpakis B, et al. Costs of measures to control tuberculosis/HIV in public primary care facilities in Cape Town, South Africa. Bull World Health Organ. 2006;84:528-36. doi: http://dx.doi.org/10.2471/BLT.04.018606 PMID: 16878226
https://doi.org/10.2471/BLT.04.018606...
,8787 Assessing potential impact and costs of scaling-up medical male circumcision services in Uganda. Washington (DC): United States Agency for International Development; 2010. However, the current evidence of the impact on task shifting on costs remains inconsistent9393 Menzies NA, Berruti AA, Blandford JM. The determinants of HIV treatment costs in resource limited settings. PLoS One. 2012;7:e48726. doi: http://dx.doi.org/10.1371/journal.pone.0048726 PMID: 23144946
https://doi.org/10.1371/journal.pone.004...
and there remain concerns that task shifting may lead to poor morale among lower-paid staff and lower service quality.8585 Martin G, Bollinger L, Pandit-Rajani T, Tshehlo R, Stover J. Costing male circumcision in Lesotho and implications for the cost-effectiveness of circumcision as an HIV intervention. Washington (DC): United States Agency for International Development; 2007. Available from: http://www.aidstar-one.com/sites/default/files/410_1_Lesotho_MC_Costing_FINAL_10_11_07.pdf [cited 2013 Oct 19].
http://www.aidstar-one.com/sites/default...
,102102 Zachariah R, Ford N, Philips M, Lynch S, Massaquoi M, Janssens V, et al. Task shifting in HIV/AIDS: opportunities, challenges and proposed actions for sub-Saharan Africa. Trans R Soc Trop Med Hyg. 2009;103:549-58. doi: http://dx.doi.org/10.1016/j.trstmh.2008.09.019 PMID: 18992905
https://doi.org/10.1016/j.trstmh.2008.09...

Our current findings on economies of scale generally support the assumptions made in the UNAIDS Strategic Investment Framework on the existence of economies of scale with programmes of HIV counselling and testing and HIV prevention for key populations. However, economies of scale at the programme level tend to differ from those at site level. The evidence presented here refers to the relationship between costs and site scale. Although costs incurred above the service level are likely to be fixed, economies of scale derived from site-level costings may often still underestimate the corresponding programmatic economies of scale.2424 Cleary S, Tshehlo R, Jouquet G, Makakole L. Ensuring access to free HIV/AIDS care and treatment in Lesotho. Cape Town: University of Cape Town; 2007. Available from: http://196.202.240.21/mcaweb/documents/Health/HEALTH%20Decentralization%20of%20ART.pdf [cited 2013 Oct 19].
http://196.202.240.21/mcaweb/documents/H...
,3737 Bratt JH, Torpey K, Kabaso M, Gondwe Y. Costs of HIV/AIDS outpatient services delivered through Zambian public health facilities. Trop Med Int. Health 2011;16:110-8. doi: http://dx.doi.org/10.1111/j.1365-3156.2010.02640.x PMID: 20958891
https://doi.org/10.1111/j.1365-3156.2010...
,4343 Gupta I, Trivedi M, Kandamuthan S. Recurrent costs of India’s free ART program. In: Haacker M, Claeson M, editors. HIV and AIDS in South Asia: an economic development risk. Washington: World Bank; 2009. pp. 191-237.,5656 Dandona L, Kumar SG, Kumar GA, Dandona R. Cost-effectiveness of HIV prevention interventions in Andhra Pradesh state of India. BMC Health Serv Res. 2010;10:117. doi: http://dx.doi.org/10.1186/1472-6963-10-117 PMID: 20459755
https://doi.org/10.1186/1472-6963-10-117...
In some cases, programmes may suffer from diseconomies of scale as they increase the number of service providers to reach groups that are particularly hard to reach. We found almost no evidence of diseconomies of scale5656 Dandona L, Kumar SG, Kumar GA, Dandona R. Cost-effectiveness of HIV prevention interventions in Andhra Pradesh state of India. BMC Health Serv Res. 2010;10:117. doi: http://dx.doi.org/10.1186/1472-6963-10-117 PMID: 20459755
https://doi.org/10.1186/1472-6963-10-117...
,6161 Liambila W, Askew I, Ayisi R, Gathitu M, Mwangi J, Homan R, et al. Feasibility, acceptability, effect and cost of integrating counseling and testing for HIV within family planning services in Kenya. Washington (DC): Population Council; 2008. Available from: http://www.popcouncil.org/pdfs/frontiers/FR_FinalReports/Kenya_CT_FP.pdf [cited 2013 Oct 19].
http://www.popcouncil.org/pdfs/frontiers...
,8181 Kumaranayake L, Vickerman P, Walker D, Samoshkin S, Romantzov V, Emelyanova Z, et al. The cost-effectiveness of HIV preventive measures among injecting drug users in Svetlogorsk, Belarus. Addiction. 2004;99:1565-76. doi: http://dx.doi.org/10.1111/j.1360-0443.2004.00899.x PMID: 15585048
https://doi.org/10.1111/j.1360-0443.2004...
but the relevant evidence base was relatively small. It should not be assumed that diseconomies of scale do not exist.

While there is a broad evidence base on the cost–effectiveness of some integrated HIV services,9Sweeney S, Obure CD, Maier CB, Greener R, Dehne K, Vassall A. Costs and efficiency of integrating HIV/AIDS services with other health services: a systematic review of evidence and experience. Sex Transm Infect. 2012;88:85-99. doi: http://dx.doi.org/10.1136/sextrans-2011-050199 PMID: 22158934
https://doi.org/10.1136/sextrans-2011-05...
there is considerably less information available on the corresponding economies of scope.9Sweeney S, Obure CD, Maier CB, Greener R, Dehne K, Vassall A. Costs and efficiency of integrating HIV/AIDS services with other health services: a systematic review of evidence and experience. Sex Transm Infect. 2012;88:85-99. doi: http://dx.doi.org/10.1136/sextrans-2011-050199 PMID: 22158934
https://doi.org/10.1136/sextrans-2011-05...
,6363 Grabbe KL, Menzies N, Taegtmeyer M, Emukule G, Angala P, Mwega I, et al. Increasing access to HIV counseling and testing through mobile services in Kenya: strategies, utilization, and cost-effectiveness. J Acquir Immune Defic Syndr. 2010;54:317-23. doi: http://dx.doi.org/10.1097/QAI.0b013e3181ced126 PMID: 20453819
https://doi.org/10.1097/QAI.0b013e3181ce...
,6767 Menzies N, Abang B, Wanyenze R, Nuwaha F, Mugisha B, Coutinho A, et al. The costs and effectiveness of four HIV counseling and testing strategies in Uganda. AIDS. 2009;23:395-401. doi: http://dx.doi.org/10.1097/QAD.0b013e328321e40b PMID: 19114865
https://doi.org/10.1097/QAD.0b013e328321...
,7070 Das R, Biswas K, Panda P, Khan ME, Homan R. Strengthening financial sustainability through integration of voluntary counseling and testing services with other reproductive health services. Washington (DC): Population Council; 2007. Available from: http://www.popcouncil.org/pdfs/frontiers/FR_FinalReports/India_CINI.pdf [cited 2013 Oct 19].
http://www.popcouncil.org/pdfs/frontiers...
,9595 Minh HV, Bach TX, Mai NY, Wright P. The cost of providing HIV/AIDS counseling and testing services in Vietnam. Value in Health Regional Issues. 2012;1:36-40. doi: http://dx.doi.org/10.1016/j.vhri.2012.03.012
https://doi.org/10.1016/j.vhri.2012.03.0...
The economies of scope that have been reported may only represent the indirect effects of economies of scale – that is, integration may simply have brought HIV services to new clients rather than improved efficiency through the joint provision of services.7070 Das R, Biswas K, Panda P, Khan ME, Homan R. Strengthening financial sustainability through integration of voluntary counseling and testing services with other reproductive health services. Washington (DC): Population Council; 2007. Available from: http://www.popcouncil.org/pdfs/frontiers/FR_FinalReports/India_CINI.pdf [cited 2013 Oct 19].
http://www.popcouncil.org/pdfs/frontiers...

Most of the other factors that have been found to influence unit costs are also potentially within the control of managers of HIV programmes. Reductions in commodity prices, especially those for first- and second-line antiretroviral drugs, have the potential to yield substantial cost savings. Such reductions may be achieved via revised national tenders, joint procurement, improved forecasting, and process efficiency and transparency.3333 Long L, Fox M, Sanne I, Rosen S. The high cost of second-line antiretroviral therapy for HIV/AIDS in South Africa. AIDS. 2010;24:915-9. doi: http://dx.doi.org/10.1097/QAD.0b013e3283360976 PMID: 20042849
https://doi.org/10.1097/QAD.0b013e328336...
,4545 Kitajima T, Kobayashi Y, Chaipah W, Sato H, Chadbunchachai W, Thuennadee R. Costs of medical services for patients with HIV/AIDS in Khon Kaen, Thailand. AIDS. 2003;17:2375-81. doi: http://dx.doi.org/10.1097/00002030-200311070-00013 PMID: 14571190
https://doi.org/10.1097/00002030-2003110...
,4646 Koenig SP, Riviere C, Leger P, Severe P, Atwood S, Fitzgerald DW, et al. The cost of antiretroviral therapy in Haiti. Cost Eff Resour Alloc. 2008;6:3. doi: http://dx.doi.org/10.1186/1478-7547-6-3 PMID: 18275615
https://doi.org/10.1186/1478-7547-6-3...
,4848 Aracena-Genao B, Navarro JO, Lamadrid-Figueroa H, Forsythe S, Trejo-Valdivia B. Costs and benefits of HAART for patients with HIV in a public hospital in Mexico. AIDS. 2008;22 Suppl 1;S141-8. doi: http://dx.doi.org/10.1097/01.aids.0000327635.74919.fd PMID: 18664946
https://doi.org/10.1097/01.aids.00003276...
Cost savings achieved by reducing the price of second-line therapy will continue to be critical in low- and lower-middle-income countries, where patients are particularly likely to switch to second-line regimens over time.

Few of the studies that we reviewed incorporated any analysis of the quality of service provision. However, where quality and costs were jointly examined, cost reduction often led to reduced quality.2626 Deghaye N, Pawinski RA, Desmond C. Financial and economic costs of scaling up the provision of HAART to HIV-infected health care workers in KwaZulu-Natal. S Afr Med J. 2006;96:140-3. PMID: 16532083,2929 Rosen S, Long L, Sanne I. The outcomes and outpatient costs of different models of antiretroviral treatment delivery in South Africa. Trop Med Int Health. 2008;13:1005-15. doi: http://dx.doi.org/10.1111/j.1365-3156.2008.02114.x PMID: 18631314
https://doi.org/10.1111/j.1365-3156.2008...
,3333 Long L, Fox M, Sanne I, Rosen S. The high cost of second-line antiretroviral therapy for HIV/AIDS in South Africa. AIDS. 2010;24:915-9. doi: http://dx.doi.org/10.1097/QAD.0b013e3283360976 PMID: 20042849
https://doi.org/10.1097/QAD.0b013e328336...
,3535 Babigumira JB, Sethi AK, Smyth KA, Singer ME. Cost effectiveness of facility-based care, home-based care and mobile clinics for provision of antiretroviral therapy in Uganda. Pharmacoeconomics 2009;27:963-73. doi: http://dx.doi.org/10.2165/11318230-000000000-00000 PMID: 19888795
https://doi.org/10.2165/11318230-0000000...
,3737 Bratt JH, Torpey K, Kabaso M, Gondwe Y. Costs of HIV/AIDS outpatient services delivered through Zambian public health facilities. Trop Med Int. Health 2011;16:110-8. doi: http://dx.doi.org/10.1111/j.1365-3156.2010.02640.x PMID: 20958891
https://doi.org/10.1111/j.1365-3156.2010...
,4040 Kombe G, Galaty D, Nwagbara C. Scaling-up antiretroviral treatment in the public sector in Nigeria: a comprehensive analysis of resource requirements [Internet]. Bethesda (MD): Abt Associates; 2004. Available from: http://www.healthsystems2020.org/content/resource/detail/1489/ [cited 2013 Oct 19].
http://www.healthsystems2020.org/content...
,4646 Koenig SP, Riviere C, Leger P, Severe P, Atwood S, Fitzgerald DW, et al. The cost of antiretroviral therapy in Haiti. Cost Eff Resour Alloc. 2008;6:3. doi: http://dx.doi.org/10.1186/1478-7547-6-3 PMID: 18275615
https://doi.org/10.1186/1478-7547-6-3...
,9292 Bautista-Arredondo S, Dmytraczenko T, Kombe G, Bertozzi SM. Costing of scaling up HIV/AIDS treatment in Mexico. Salud Publica Mex. 2008;50 Suppl 4;S437-44. doi: http://dx.doi.org/10.1590/S0036-36342008001000004 PMID: 19082254
https://doi.org/10.1590/S0036-3634200800...
In a large review of 15 ART programmes in Africa, Asia and Latin America, it was found that increases in the scale of a programme led to increases in the rates of loss to follow-up.103103 Brinkhof MW, Dabis F, Myer L, Bangsberg DR, Boulle A, Nash D, et al.; ART-LINC, IeDEA. Early loss of HIV-infected patients on potent antiretroviral therapy programmes in lower-income countries. Bull World Health Organ. 2008;86:559-67. doi: http://dx.doi.org/10.2471/BLT.07.044248 PMID: 18670668
https://doi.org/10.2471/BLT.07.044248...
Compared with small programmes, large-scale programmes were less likely to follow up patients actively.103103 Brinkhof MW, Dabis F, Myer L, Bangsberg DR, Boulle A, Nash D, et al.; ART-LINC, IeDEA. Early loss of HIV-infected patients on potent antiretroviral therapy programmes in lower-income countries. Bull World Health Organ. 2008;86:559-67. doi: http://dx.doi.org/10.2471/BLT.07.044248 PMID: 18670668
https://doi.org/10.2471/BLT.07.044248...
Unfortunately, little is known about the potential “cost–quality trade-off” of the alternative service models that may be adopted to reduce unit costs, such as reducing the number of visits required for ART monitoring. Support for managers at the site and district level – for example, to allow costs to be monitored and “blueprint” approaches to be avoided – may be key to ensuring that efforts to improve efficiency do not damage staff morale or service quality.3030 Vella V, Govender T, Dlamini S, Taylor M, Moodley I, David V, et al. Evaluation of antiretroviral therapy against HIV/Aids in KwaZulu-Natal, South Africa. Pietermaritzburg: KwaZulu-Natal Department of Health; 2008. Available from: http://www.kznhealth.gov.za/italian/arv.pdf [cited 2013 Oct 19].
http://www.kznhealth.gov.za/italian/arv....
,5757 Twahir A, Maggwa BN, Askew I. Integration of STI and HIV/AIDS services with MCH-FP services: a case study of the Mkomani Clinic Society in Mombasa, Kenya. Washington (DC): Population Council; 1996. Available from: http://www.popcouncil.org/pdfs/frontiers/fphivintegrat/Mombassa96.pdf [cited 2013 Oct 19].
http://www.popcouncil.org/pdfs/frontiers...
,5858 Sweat M, Gregorich S, Sangiwa G, Furlonge C, Balmer D, Kamenga C, et al. Cost-effectiveness of voluntary HIV-1 counselling and testing in reducing sexual transmission of HIV-1 in Kenya and Tanzania. Lancet. 2000;356:113-21. doi: http://dx.doi.org/10.1016/S0140-6736(00)02447-8 PMID: 10963247
https://doi.org/10.1016/S0140-6736(00)02...
,6464 Obure CD, Vassall A, Michaels C, Terris-Prestholt F, Mayhew S, Stackpool-Moore L, et al.; Integra Research Team. Optimising the cost and delivery of HIV counselling and testing services in Kenya and Swaziland. Sex Transm Infect. 2012;88:498-503. doi: http://dx.doi.org/10.1136/sextrans-2012-050544 PMID: 22859498
https://doi.org/10.1136/sextrans-2012-05...
When setting national and international cost benchmarks, attention must also be taken not to create perverse incentives by emphasizing measurable costs rather than the more intangible aspects of service quality.

We were unable to find much published information on the unit costs of several of the key interventions included in the UNAIDS Strategic Investment Framework. Most notably, there is a dearth of data on the costs of ART for key populations, condom distribution in general, HIV counselling and testing beyond Africa, key population interventions outside India, and large-scale programmes for the prevention of mother-to-child transmission of HIV and male circumcision. Most of the relevant studies in which economies of scale or scope were investigated had small samples. It remains unclear whether economies of scale or scope vary by provider type or other site or service characteristics. Studies that include the full range of costs and uncertainty analysis of cost estimates and have samples large enough to show all cost variation in detail remain rare. There is also a distinct lack of experimental studies that have been designed to detect the sources of inefficiency. Despite these limitations, there are signs of recent improvements in the costing of HIV services. Most of our main findings were derived from studies conducted over the last five years. There is also some evidence that cost reductions are already being achieved as HIV programmes mature9393 Menzies NA, Berruti AA, Blandford JM. The determinants of HIV treatment costs in resource limited settings. PLoS One. 2012;7:e48726. doi: http://dx.doi.org/10.1371/journal.pone.0048726 PMID: 23144946
https://doi.org/10.1371/journal.pone.004...
and, in the future, there may be further scope for efficiency gains as new technologies and service models are developed.

Large-scale costing studies that cover the full range of HIV services are required. Empirical costing studies of activities above the service level are also needed to provide insights into approaches for optimizing programme costs. In the future, experimental studies – especially on actions to enhance planning and management capacity, the utilization of human resources, financial and information systems, demand generation and service integration – could allow efficiency to be improved. If essential HIV services are to be made cheaper and sustainable, the policy-makers involved with HIV will probably have to engage with those involved in improving the efficiency and capacity of general systems for health care and community support.

In conclusion, the general efficiency of HIV services must be improved if core interventions are to be successfully scaled up in environments where resources are scarce. At site level, economies of scale can often be made. The integration of HIV services with other health services may also reduce costs. Further studies are required to determine the best ways of improving the efficiency of HIV services at site level and the likely impact of such improvements on the national costs of HIV services.

Funding:

  • This work was supported by UNAIDS.

Competing interests:

  • None declared.

References

  • 1
    The Millennium Development Goals report 2012. New York (NY): United Nations; 2012.
  • 2
    011 United Nations General Assembly Political Declaration on HIV/AIDS. Geneva: Joint United Nations Programme on HIV/AIDS; 2011.
  • 3
    Creese A, Floyd K, Alban A, Guinness L. Cost-effectiveness of HIV/AIDS interventions in Africa: a systematic review of the evidence. Lancet. 2002;359:1635-43. doi: http://dx.doi.org/10.1016/S0140-6736(02)08595-1 PMID: 12020523
    » https://doi.org/10.1016/S0140-6736(02)08595-1
  • 4
    Galárraga O, Colchero MA, Wamai RG, Bertozzi SM. HIV prevention cost-effectiveness: a systematic review. BMC Public Health. 2009;9 Suppl 1;S5. doi: http://dx.doi.org/10.1186/1471-2458-9-S1-S5 PMID: 19922689
    » https://doi.org/10.1186/1471-2458-9-S1-S5
  • 5
    Financing global health 2012: the end of the golden age? Seattle (WA): Institute for Health Metrics and Evaluation; 2012.
  • 6
    Together we will end AIDS. Geneva: Joint United Nations Programme on HIV/AIDS; 2012.
  • 7
    Galárraga O, Wirtz VJ, Figueroa-Lara A, Santa-Ana-Tellez Y, Coulibaly I, Viisainen K, et al. Unit costs for delivery of antiretroviral treatment and prevention of mother-to-child transmission of HIV: a systematic review for low- and middle-income countries. Pharmacoeconomics. 2011;29:579-99. PMID: 21671687
  • 8
    Johns B, Torres TT; WHO-CHOICE. Costs of scaling up health interventions: a systematic review. Health Policy Plan. 2005;20:1-13. doi: http://dx.doi.org/10.1093/heapol/czi001 PMID: 15689425
    » https://doi.org/10.1093/heapol/czi001
  • 9
    Sweeney S, Obure CD, Maier CB, Greener R, Dehne K, Vassall A. Costs and efficiency of integrating HIV/AIDS services with other health services: a systematic review of evidence and experience. Sex Transm Infect. 2012;88:85-99. doi: http://dx.doi.org/10.1136/sextrans-2011-050199 PMID: 22158934
    » https://doi.org/10.1136/sextrans-2011-050199
  • 10
    Uyei J, Coetzee D, Macinko J, Guttmacher S. Integrated delivery of HIV and tuberculosis services in sub-Saharan Africa: a systematic review. Lancet. Infect Dis. 2011;11:855-67. doi: http://dx.doi.org/10.1016/S1473-3099(11)70145-1 PMID: 22035614
    » https://doi.org/10.1016/S1473-3099(11)70145-1
  • 11
    Vassall A, Compernolle P. Estimating the resource needs of scaling-up HIV/AIDS and tuberculosis interventions in sub-Saharan Africa: a systematic review for national policy makers and planners. Health Policy. 2006;79:1-15. doi: http://dx.doi.org/10.1016/j.healthpol.2005.11.005 PMID: 16388874
    » https://doi.org/10.1016/j.healthpol.2005.11.005
  • 12
    Walker D. Cost and cost-effectiveness of HIV/AIDS prevention strategies in developing countries: is there an evidence base? Health Policy Plan. 2003;18:4-17. doi: http://dx.doi.org/10.1093/heapol/18.1.4 PMID: 12582104
    » https://doi.org/10.1093/heapol/18.1.4
  • 13
    Santa-Ana-Tellez Y, DeMaria LM, Galárraga O. Costs of interventions for AIDS orphans and vulnerable children. Trop Med Int Health. 2011;16:1417-26. doi: http://dx.doi.org/10.1111/j.1365-3156.2011.02856.x PMID: 21859439
    » https://doi.org/10.1111/j.1365-3156.2011.02856.x
  • 14
    Zeng W, Shepard DS, Chilingerian J, Avila-Figueroa C. How much can we gain from improved efficiency? An examination of performance of national HIV/AIDS programs and its determinants in low- and middle-income countries. BMC Health Serv Res. 2012;12:74. doi: http://dx.doi.org/10.1186/1472-6963-12-74 PMID: 22443135
    » https://doi.org/10.1186/1472-6963-12-74
  • 15
    Schwartländer B, Stover J, Hallett T, Atun R, Avila C, Gouws E, et al.; Investment Framework Study Group. Towards an improved investment approach for an effective response to HIV/AIDS. Lancet. 2011;377:2031-41. doi: http://dx.doi.org/10.1016/S0140-6736(11)60702-2 PMID: 21641026
    » https://doi.org/10.1016/S0140-6736(11)60702-2
  • 16
    Moher D, Liberati A, Tetzlaff J, Altman DG; PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6:e1000097. doi: http://dx.doi.org/10.1371/journal.pmed.1000097 PMID: 19621072
    » https://doi.org/10.1371/journal.pmed.1000097
  • 17
    Shepperd S, Lewin S, Straus S, Clarke M, Eccles MP, Fitzpatrick R, et al. Can we systematically review studies that evaluate complex interventions? PLoS Med. 2009;6:e1000086. doi: http://dx.doi.org/10.1371/journal.pmed.1000086 PMID: 19668360
    » https://doi.org/10.1371/journal.pmed.1000086
  • 18
    How we classify countries [Internet]. Washington (DC): World Bank; 2012. Available from: http://data.worldbank.org/about/country-classifications [cited 2013 Oct 19].
    » http://data.worldbank.org/about/country-classifications
  • 19
    Drummond MF, Jefferson TO; The BMJ Economic Evaluation Working Party. Guidelines for authors and peer reviewers of economic submissions to the BMJ. BMJ. 1996;313:275-83. doi: http://dx.doi.org/10.1136/bmj.313.7052.275 PMID: 8704542
    » https://doi.org/10.1136/bmj.313.7052.275
  • 20
    Menzies NA, Berruti AA, Berzon R, Filler S, Ferris R, Ellerbrock TV, et al. The cost of providing comprehensive HIV treatment in PEPFAR-supported programs. AIDS. 2011;25:1753-60. doi: http://dx.doi.org/10.1097/QAD.0b013e3283463eec PMID: 21412127
    » https://doi.org/10.1097/QAD.0b013e3283463eec
  • 21
    Bikilla AD, Jerene D, Robberstad B, Lindtjorn B. Cost estimates of HIV care and treatment with and without anti-retroviral therapy at Arba Minch Hospital in southern Ethiopia. Cost Eff Resour Alloc . 2009;7:6. doi: http://dx.doi.org/10.1186/1478-7547-7-6 PMID: 19364399
    » https://doi.org/10.1186/1478-7547-7-6
  • 22
    Kombe G, Galaty D, Gadhia R, Decker C. The human and financial resource requirements for scaling up HIV/AIDS services in Ethiopia. Bethesda (MD): Abt Associates; 2005. Available from: http://www.abtassociates.com/reports/AB_PNADC109.pdf [cited 2013 Oct 19].
    » http://www.abtassociates.com/reports/AB_PNADC109.pdf
  • 23
    Marseille EA, Kevany S, Ahmed I, Feleke G, Graham B, Heller T, et al. Case management to improve adherence for HIV-infected patients receiving antiretroviral therapy in Ethiopia: a micro-costing study. Cost Eff Resour Alloc. 2011;9:18. doi: http://dx.doi.org/10.1186/1478-7547-9-18 PMID: 22185656
    » https://doi.org/10.1186/1478-7547-9-18
  • 24
    Cleary S, Tshehlo R, Jouquet G, Makakole L. Ensuring access to free HIV/AIDS care and treatment in Lesotho. Cape Town: University of Cape Town; 2007. Available from: http://196.202.240.21/mcaweb/documents/Health/HEALTH%20Decentralization%20of%20ART.pdf [cited 2013 Oct 19].
    » http://196.202.240.21/mcaweb/documents/Health/HEALTH%20Decentralization%20of%20ART.pdf
  • 25
    Cleary SM, McIntyre D, Boulle AM. The cost-effectiveness of antiretroviral treatment in Khayelitsha, South Africa – a primary data analysis. Cost Eff Resour Alloc. 2006;4:20. doi: http://dx.doi.org/10.1186/1478-7547-4-20 PMID: 17147833
    » https://doi.org/10.1186/1478-7547-4-20
  • 26
    Deghaye N, Pawinski RA, Desmond C. Financial and economic costs of scaling up the provision of HAART to HIV-infected health care workers in KwaZulu-Natal. S Afr Med J. 2006;96:140-3. PMID: 16532083
  • 27
    Harling G, Bekker LG, Wood R. Cost of a dedicated ART clinic. S Afr Med J. 2007;97:593-6. PMID: 17952216
  • 28
    Harling G, Wood R. The evolving cost of HIV in South Africa: changes in health care cost with duration on antiretroviral therapy for public sector patients. J Acquir Immune Defic Syndr. 2007;45:348-54. PMID: 17496562
  • 29
    Rosen S, Long L, Sanne I. The outcomes and outpatient costs of different models of antiretroviral treatment delivery in South Africa. Trop Med Int Health. 2008;13:1005-15. doi: http://dx.doi.org/10.1111/j.1365-3156.2008.02114.x PMID: 18631314
    » https://doi.org/10.1111/j.1365-3156.2008.02114.x
  • 30
    Vella V, Govender T, Dlamini S, Taylor M, Moodley I, David V, et al. Evaluation of antiretroviral therapy against HIV/Aids in KwaZulu-Natal, South Africa. Pietermaritzburg: KwaZulu-Natal Department of Health; 2008. Available from: http://www.kznhealth.gov.za/italian/arv.pdf [cited 2013 Oct 19].
    » http://www.kznhealth.gov.za/italian/arv.pdf
  • 31
    Kevany S, Meintjes G, Rebe K, Maartens G, Cleary S. Clinical and financial burdens of secondary level care in a public sector antiretroviral roll-out setting (G.F. Jooste Hospital). S Afr Med J. 2009;99:320-5. PMID: 19588792
  • 32
    Martinson N, Mohapi L, Bakos D, Gray GE, McIntyre JA, Holmes CB. Costs of providing care for HIV-infected adults in an urban HIV clinic in Soweto, South Africa. J Acquir Immune Defic Syndr. 2009;50:327-30. doi: http://dx.doi.org/10.1097/QAI.0b013e3181958546 PMID: 19194308
    » https://doi.org/10.1097/QAI.0b013e3181958546
  • 33
    Long L, Fox M, Sanne I, Rosen S. The high cost of second-line antiretroviral therapy for HIV/AIDS in South Africa. AIDS. 2010;24:915-9. doi: http://dx.doi.org/10.1097/QAD.0b013e3283360976 PMID: 20042849
    » https://doi.org/10.1097/QAD.0b013e3283360976
  • 34
    Long L, Brennan A, Fox MP, Ndibongo B, Jaffray I, Sanne I, et al. Treatment outcomes and cost-effectiveness of shifting management of stable ART patients to nurses in South Africa: an observational cohort. PLoS Med. 2011;8:e1001055. doi: http://dx.doi.org/10.1371/journal.pmed.1001055 PMID: 21811402
    » https://doi.org/10.1371/journal.pmed.1001055
  • 35
    Babigumira JB, Sethi AK, Smyth KA, Singer ME. Cost effectiveness of facility-based care, home-based care and mobile clinics for provision of antiretroviral therapy in Uganda. Pharmacoeconomics 2009;27:963-73. doi: http://dx.doi.org/10.2165/11318230-000000000-00000 PMID: 19888795
    » https://doi.org/10.2165/11318230-000000000-00000
  • 36
    Jaffar S, Amuron B, Foster S, Birungi J, Levin J, Namara G, et al.; Jinja Trial Team. Rates of virological failure in patients treated in a home-based versus a facility-based HIV-care model in Jinja, southeast Uganda: a cluster-randomised equivalence trial. Lancet. 2009;374:2080-9. doi: http://dx.doi.org/10.1016/S0140-6736(09)61674-3 PMID: 19939445
    » https://doi.org/10.1016/S0140-6736(09)61674-3
  • 37
    Bratt JH, Torpey K, Kabaso M, Gondwe Y. Costs of HIV/AIDS outpatient services delivered through Zambian public health facilities. Trop Med Int. Health 2011;16:110-8. doi: http://dx.doi.org/10.1111/j.1365-3156.2010.02640.x PMID: 20958891
    » https://doi.org/10.1111/j.1365-3156.2010.02640.x
  • 38
    Hounton SH, Akonde A, Zannou DM, Bashi J, Meda N, Newlands D. Costing universal access of highly active antiretroviral therapy in Benin. AIDS Care. 2008;20:582-7. doi: http://dx.doi.org/10.1080/09540120701868303 PMID: 18484329
    » https://doi.org/10.1080/09540120701868303
  • 39
    Renaud A, Basenya O, de Borman N, Greindl I, Meyer-Rath G. The cost effectiveness of integrated care for people living with HIV including antiretroviral treatment in a primary health care centre in Bujumbura, Burundi. AIDS Care. 2009;21:1388-94. doi: http://dx.doi.org/10.1080/09540120902884042 PMID: 20024715
    » https://doi.org/10.1080/09540120902884042
  • 40
    Kombe G, Galaty D, Nwagbara C. Scaling-up antiretroviral treatment in the public sector in Nigeria: a comprehensive analysis of resource requirements [Internet]. Bethesda (MD): Abt Associates; 2004. Available from: http://www.healthsystems2020.org/content/resource/detail/1489/ [cited 2013 Oct 19].
    » http://www.healthsystems2020.org/content/resource/detail/1489/
  • 41
    Partners for Health Reformplus. Nigeria: rapid assessment of HIV/AIDS care in the public and private sectors [Internet]. Bethesda (MD): Abt Associates; 2004. Available from: http://www.healthsystems2020.org/content/resource/detail/1619/ [cited 2013 Oct 19].
    » http://www.healthsystems2020.org/content/resource/detail/1619/
  • 42
    Aliyu HB, Chuku NN, Kola-Jebutu A, Abubakar Z, Torpey K, Chabikuli ON. What is the cost of providing outpatient HIV counseling and testing and antiretroviral therapy services in selected public health facilities in Nigeria? J Acquir Immune Defic Syndr. 2012;61:221-5. doi: http://dx.doi.org/10.1097/QAI.0b013e3182683b04 PMID: 22820805
    » https://doi.org/10.1097/QAI.0b013e3182683b04
  • 43
    Gupta I, Trivedi M, Kandamuthan S. Recurrent costs of India’s free ART program. In: Haacker M, Claeson M, editors. HIV and AIDS in South Asia: an economic development risk. Washington: World Bank; 2009. pp. 191-237.
  • 44
    John KR, Rajagopalan N, Madhuri KV. Brief communication: economic comparison of opportunistic infection management with antiretroviral treatment in people living with HIV/AIDS presenting at an NGO clinic in Bangalore, India. MedGenMed. 2006;8:24. PMID: 17415293
  • 45
    Kitajima T, Kobayashi Y, Chaipah W, Sato H, Chadbunchachai W, Thuennadee R. Costs of medical services for patients with HIV/AIDS in Khon Kaen, Thailand. AIDS. 2003;17:2375-81. doi: http://dx.doi.org/10.1097/00002030-200311070-00013 PMID: 14571190
    » https://doi.org/10.1097/00002030-200311070-00013
  • 46
    Koenig SP, Riviere C, Leger P, Severe P, Atwood S, Fitzgerald DW, et al. The cost of antiretroviral therapy in Haiti. Cost Eff Resour Alloc. 2008;6:3. doi: http://dx.doi.org/10.1186/1478-7547-6-3 PMID: 18275615
    » https://doi.org/10.1186/1478-7547-6-3
  • 47
    Marques HH, Couttolenc BF, Latorre MdoR, Aquino MZ, Aveiro MI, Pluciennik AM. Costs of care provided in a university hospital for children exposed to or infected with the HIV/AIDS. Cad Saude Publica. 2007;23 Suppl 3;S402-13. doi: http://dx.doi.org/10.1590/S0102-311X2007001500008 PMID: 17992346
    » https://doi.org/10.1590/S0102-311X2007001500008
  • 48
    Aracena-Genao B, Navarro JO, Lamadrid-Figueroa H, Forsythe S, Trejo-Valdivia B. Costs and benefits of HAART for patients with HIV in a public hospital in Mexico. AIDS. 2008;22 Suppl 1;S141-8. doi: http://dx.doi.org/10.1097/01.aids.0000327635.74919.fd PMID: 18664946
    » https://doi.org/10.1097/01.aids.0000327635.74919.fd
  • 49
    Bautista SA, Dmytraczenko T, Kombe G, Bertozzi SM. Costing of HIV/AIDS treatment in Mexico. Bethesda (MD): Abt Associates; 2003. Available from: www.healthsystems2020.org/files/1574_file_Tech020_fin.pdf [cited 2013 Oct 19].
    » www.healthsystems2020.org/files/1574_file_Tech020_fin.pdf
  • 50
    Contreras-Hernandez I, Becker D, Chancellor J, Kühne F, Mould-Quevedo J, Vega G, et al. Cost-effectiveness of maraviroc for antiretroviral treatment-experienced HIV-infected individuals in Mexico. Value Health. 2010;13:903-14. doi: http://dx.doi.org/10.1111/j.1524-4733.2010.00798.x PMID: 21091827
    » https://doi.org/10.1111/j.1524-4733.2010.00798.x
  • 51
    Loubiere S, el Filal KM, Sodqi M, Loundou A, Luchini S, Cleary S, et al. When to initiate highly active antiretroviral therapy in low-resource settings: the Moroccan experience. Antivir Ther. 2008;13:241-51. PMID: 18505175
  • 52
    Hsu J, Zinsou C, Parkhurst J, N’Dour M, Foyet L, Mueller DH. Comparative costs and cost-effectiveness of behavioural interventions as part of HIV prevention strategies. Health Policy Plan. 2013;28:20-9. doi: http://dx.doi.org/10.1093/heapol/czs021 PMID: 22411881
    » https://doi.org/10.1093/heapol/czs021
  • 53
    Söderlund N, Lavis J, Broomberg J, Mills A. The costs of HIV prevention strategies in developing countries. Bull World Health Organ. 1993;71:595-604. PMID: 8261563
  • 54
    Terris-Prestholt F, Kumaranayake L, Foster S, Kamali A, Kinsman J, Basajja V, et al. The role of community acceptance over time for costs of HIV and STI prevention interventions: analysis of the Masaka Intervention Trial, Uganda, 1996–1999. Sex Transm Dis. 2006;33 Suppl;S111-6. doi: http://dx.doi.org/10.1097/01.olq.0000175389.10289.ba PMID: 16505738
    » https://doi.org/10.1097/01.olq.0000175389.10289.ba
  • 55
    Terris-Prestholt F, Kumaranayake L, Obasi AI, Cleophas-Mazige B, Makokha M, Todd J, et al. From trial intervention to scale-up: costs of an adolescent sexual health program in Mwanza, Tanzania. Sex Transm Dis. 2006;33 Suppl;S133-9. doi: http://dx.doi.org/10.1097/01.olq.0000200606.98181.42 PMID: 16652070
    » https://doi.org/10.1097/01.olq.0000200606.98181.42
  • 56
    Dandona L, Kumar SG, Kumar GA, Dandona R. Cost-effectiveness of HIV prevention interventions in Andhra Pradesh state of India. BMC Health Serv Res. 2010;10:117. doi: http://dx.doi.org/10.1186/1472-6963-10-117 PMID: 20459755
    » https://doi.org/10.1186/1472-6963-10-117
  • 57
    Twahir A, Maggwa BN, Askew I. Integration of STI and HIV/AIDS services with MCH-FP services: a case study of the Mkomani Clinic Society in Mombasa, Kenya. Washington (DC): Population Council; 1996. Available from: http://www.popcouncil.org/pdfs/frontiers/fphivintegrat/Mombassa96.pdf [cited 2013 Oct 19].
    » http://www.popcouncil.org/pdfs/frontiers/fphivintegrat/Mombassa96.pdf
  • 58
    Sweat M, Gregorich S, Sangiwa G, Furlonge C, Balmer D, Kamenga C, et al. Cost-effectiveness of voluntary HIV-1 counselling and testing in reducing sexual transmission of HIV-1 in Kenya and Tanzania. Lancet. 2000;356:113-21. doi: http://dx.doi.org/10.1016/S0140-6736(00)02447-8 PMID: 10963247
    » https://doi.org/10.1016/S0140-6736(00)02447-8
  • 59
    Forsythe S, Arthur G, Ngatia G, Mutemi R, Odhiambo J, Gilks C. Assessing the cost and willingness to pay for voluntary HIV counselling and testing in Kenya. Health Policy Plan. 2002;17:187-95. doi: http://dx.doi.org/10.1093/heapol/17.2.187 PMID: 12000779
    » https://doi.org/10.1093/heapol/17.2.187
  • 60
    John FN, Farquhar C, Kiarie JN, Kabura MN, John-Stewart GC. Cost effectiveness of couple counselling to enhance infant HIV-1 prevention. Int J STD AIDS. 2008;19:406-9. doi: http://dx.doi.org/10.1258/ijsa.2008.007234 PMID: 18595879
    » https://doi.org/10.1258/ijsa.2008.007234
  • 61
    Liambila W, Askew I, Ayisi R, Gathitu M, Mwangi J, Homan R, et al. Feasibility, acceptability, effect and cost of integrating counseling and testing for HIV within family planning services in Kenya. Washington (DC): Population Council; 2008. Available from: http://www.popcouncil.org/pdfs/frontiers/FR_FinalReports/Kenya_CT_FP.pdf [cited 2013 Oct 19].
    » http://www.popcouncil.org/pdfs/frontiers/FR_FinalReports/Kenya_CT_FP.pdf
  • 62
    Negin J, Wariero J, Mutuo P, Jan S, Pronyk P. Feasibility, acceptability and cost of home-based HIV testing in rural Kenya. Trop Med Int Health. 2009;14:849-55. doi: http://dx.doi.org/10.1111/j.1365-3156.2009.02304.x PMID: 19552646
    » https://doi.org/10.1111/j.1365-3156.2009.02304.x
  • 63
    Grabbe KL, Menzies N, Taegtmeyer M, Emukule G, Angala P, Mwega I, et al. Increasing access to HIV counseling and testing through mobile services in Kenya: strategies, utilization, and cost-effectiveness. J Acquir Immune Defic Syndr. 2010;54:317-23. doi: http://dx.doi.org/10.1097/QAI.0b013e3181ced126 PMID: 20453819
    » https://doi.org/10.1097/QAI.0b013e3181ced126
  • 64
    Obure CD, Vassall A, Michaels C, Terris-Prestholt F, Mayhew S, Stackpool-Moore L, et al.; Integra Research Team. Optimising the cost and delivery of HIV counselling and testing services in Kenya and Swaziland. Sex Transm Infect. 2012;88:498-503. doi: http://dx.doi.org/10.1136/sextrans-2012-050544 PMID: 22859498
    » https://doi.org/10.1136/sextrans-2012-050544
  • 65
    McConnel CE, Stanley N, du Plessis JA, Pitter CS, Abdulla F, Coovadia HM, et al. The cost of a rapid-test VCT clinic in South Africa. S Afr Med J. 2005;95:968-71. PMID: 16465359
  • 66
    Hausler HP, Sinanovic E, Kumaranayake L, Naidoo P, Schoeman H, Karpakis B, et al. Costs of measures to control tuberculosis/HIV in public primary care facilities in Cape Town, South Africa. Bull World Health Organ. 2006;84:528-36. doi: http://dx.doi.org/10.2471/BLT.04.018606 PMID: 16878226
    » https://doi.org/10.2471/BLT.04.018606
  • 67
    Menzies N, Abang B, Wanyenze R, Nuwaha F, Mugisha B, Coutinho A, et al. The costs and effectiveness of four HIV counseling and testing strategies in Uganda. AIDS. 2009;23:395-401. doi: http://dx.doi.org/10.1097/QAD.0b013e328321e40b PMID: 19114865
    » https://doi.org/10.1097/QAD.0b013e328321e40b
  • 68
    Tumwesigye E, Wana G, Kasasa S, Muganzi E, Nuwaha F. High uptake of home-based, district-wide, HIV counseling and testing in Uganda. AIDS Patient Care STDS. 2010;24:735-41. doi: http://dx.doi.org/10.1089/apc.2010.0096 PMID: 21067357
    » https://doi.org/10.1089/apc.2010.0096
  • 69
    Dandona L, Sisodia P, Ramesh YK, Kumar SG, Kumar AA, Rao MC, et al. Cost and efficiency of HIV voluntary counselling and testing centres in Andhra Pradesh, India. Natl Med J India. 2005;18:26-31. PMID: 15835489
  • 70
    Das R, Biswas K, Panda P, Khan ME, Homan R. Strengthening financial sustainability through integration of voluntary counseling and testing services with other reproductive health services. Washington (DC): Population Council; 2007. Available from: http://www.popcouncil.org/pdfs/frontiers/FR_FinalReports/India_CINI.pdf [cited 2013 Oct 19].
    » http://www.popcouncil.org/pdfs/frontiers/FR_FinalReports/India_CINI.pdf
  • 71
    Moses S, Plummer FA, Ngugi EN, Nagelkerke NJ, Anzala AO, Ndinya-Achola JO. Controlling HIV in Africa: effectiveness and cost of an intervention in a high-frequency STD transmitter core group. AIDS. 1991;5:407-11. doi: http://dx.doi.org/10.1097/00002030-199104000-00008 PMID: 1905555
    » https://doi.org/10.1097/00002030-199104000-00008
  • 72
    Chang LW, Kagaayi J, Nakigozi G, Serwada D, Quinn TC, Gray RH, et al. Cost analyses of peer health worker and mHealth support interventions for improving AIDS care in Rakai, Uganda. AIDS Care. 2013;25:652-6. doi: http://dx.doi.org/10.1080/09540121.2012.722600 PMID: 22971113
    » https://doi.org/10.1080/09540121.2012.722600
  • 73
    Guinness L, Vickerman P, Quayyum Z, Foss A, Watts C, Rodericks A, et al. The cost-effectiveness of consistent and early intervention of harm reduction for injecting drug users in Bangladesh. Addiction. 2010;105:319-28. doi: http://dx.doi.org/10.1111/j.1360-0443.2009.02755.x PMID: 19922513
    » https://doi.org/10.1111/j.1360-0443.2009.02755.x
  • 74
    Dandona L, Sisodia P, Kumar SG, Ramesh YK, Kumar AA, Rao MC, et al. HIV prevention programmes for female sex workers in Andhra Pradesh, India: outputs, cost and efficiency. BMC Public Health. 2005;5:98. doi: http://dx.doi.org/10.1186/1471-2458-5-98 PMID: 16181491
    » https://doi.org/10.1186/1471-2458-5-98
  • 75
    Guinness L, Kumaranayake L, Rajaraman B, Sankaranarayanan G, Vannela G, Raghupathi P, et al. Does scale matter? The costs of HIV-prevention interventions for commercial sex workers in India. Bull World Health Organ. 2005;83:747-55. PMID: 16283051
  • 76
    Fung IC, Guinness L, Vickerman P, Watts C, Vannela G, Vadhvana J, et al. Modelling the impact and cost-effectiveness of the HIV intervention programme amongst commercial sex workers in Ahmedabad, Gujarat, India. BMC Public Health. 2007;7:195. doi: http://dx.doi.org/10.1186/1471-2458-7-195 PMID: 17683595
    » https://doi.org/10.1186/1471-2458-7-195
  • 77
    Dandona L, Kumar SP, Ramesh Y, Rao MC, Kumar AA, Marseille E, et al. Changing cost of HIV interventions in the context of scaling-up in India. AIDS. 2008;22 Suppl 1;S43-9. doi: http://dx.doi.org/10.1097/01.aids.0000327622.24232.aa PMID: 18664952
    » https://doi.org/10.1097/01.aids.0000327622.24232.aa
  • 78
    Kumar SG, Dandona R, Schneider JA, Ramesh YK, Dandona L. Outputs and cost of HIV prevention programmes for truck drivers in Andhra Pradesh, India. BMC Health Serv Res. 2009;9:82. doi: http://dx.doi.org/10.1186/1472-6963-9-82 PMID: 19457269
    » https://doi.org/10.1186/1472-6963-9-82
  • 79
    Chandrashekar S, Guinness L, Kumaranayake L, Reddy B, Govindraj Y, Vickerman P, et al. The effects of scale on the costs of targeted HIV prevention interventions among female and male sex workers, men who have sex with men and transgenders in India. Sex Transm Infect. 2010;86 Suppl 1;i89-94. doi: http://dx.doi.org/10.1136/sti.2009.038547 PMID: 20167740
    » https://doi.org/10.1136/sti.2009.038547
  • 80
    Siregar AY, Komarudin D, Wisaksana R, van Crevel R, Baltussen R. Costs and outcomes of VCT delivery models in the context of scaling up services in Indonesia. Trop Med Int Health. 2011;16:193-9. doi: http://dx.doi.org/10.1111/j.1365-3156.2010.02675.x PMID: 21070513
    » https://doi.org/10.1111/j.1365-3156.2010.02675.x
  • 81
    Kumaranayake L, Vickerman P, Walker D, Samoshkin S, Romantzov V, Emelyanova Z, et al. The cost-effectiveness of HIV preventive measures among injecting drug users in Svetlogorsk, Belarus. Addiction. 2004;99:1565-76. doi: http://dx.doi.org/10.1111/j.1360-0443.2004.00899.x PMID: 15585048
    » https://doi.org/10.1111/j.1360-0443.2004.00899.x
  • 82
    Vickerman P, Kumaranayake L, Balakireva O, Guinness L, Artyukh O, Semikop T, et al. The cost-effectiveness of expanding harm reduction activities for injecting drug users in Odessa, Ukraine. Sex Transm Dis. 2006;33 Suppl;S89-102. doi: http://dx.doi.org/10.1097/01.olq.0000221335.80508.fa PMID: 16735956
    » https://doi.org/10.1097/01.olq.0000221335.80508.fa
  • 83
    Unit cost repository [Internet]. Glastonbury: Futures Institute; 2010. Available from: http://policytools.futuresinstitute.org/UC/unit_cost_db.aspx [cited 2013 Oct 19].
    » http://policytools.futuresinstitute.org/UC/unit_cost_db.aspx
  • 84
    Binagwaho A, Pegurri E, Muita J, Bertozzi S. Male circumcision at different ages in Rwanda: a cost-effectiveness study. PLoS Med. 2010;7:e1000211. doi: http://dx.doi.org/10.1371/journal.pmed.1000211 PMID: 20098721
    » https://doi.org/10.1371/journal.pmed.1000211
  • 85
    Martin G, Bollinger L, Pandit-Rajani T, Tshehlo R, Stover J. Costing male circumcision in Lesotho and implications for the cost-effectiveness of circumcision as an HIV intervention. Washington (DC): United States Agency for International Development; 2007. Available from: http://www.aidstar-one.com/sites/default/files/410_1_Lesotho_MC_Costing_FINAL_10_11_07.pdf [cited 2013 Oct 19].
    » http://www.aidstar-one.com/sites/default/files/410_1_Lesotho_MC_Costing_FINAL_10_11_07.pdf
  • 86
    Bollinger L, Stover, J. The potential cost and impact of expanding male circumcision in South Africa. Washington (DC): United States Agency for International Development; 2010. Available from: http://www.malecircumcision.org/programs/documents/South_Africa11209.pdf [cited 2013 Oct 19].
    » http://www.malecircumcision.org/programs/documents/South_Africa11209.pdf
  • 87
    Assessing potential impact and costs of scaling-up medical male circumcision services in Uganda. Washington (DC): United States Agency for International Development; 2010.
  • 88
    Costing male circumcision in Zimbabwe and impacts of scaling up the circumcision program. Washington (DC): United States Agency for International Development; 2010.
  • 89
    Orlando S, Marazzi MC, Mancinelli S, Liotta G, Ceffa S, Giglio P, et al. Cost-effectiveness of using HAART in prevention of mother-to-child transmission in the DREAM-Project Malawi. J Acquir Immune Defic Syndr. 2010;55:631-4. doi: http://dx.doi.org/10.1097/QAI.0b013e3181f9f9f5 PMID: 21934555
    » https://doi.org/10.1097/QAI.0b013e3181f9f9f5
  • 90
    Desmond C, Franklin L, Steinberg M. The prevention of mother-to-child HIV transmission: costing the service in four sites in South Africa. Durban: Health Systems Trust; 2004. Available from: http://www.hst.org.za/sites/default/files/PMTCT_Costing.pdf [cited 2013 Oct 19].
    » http://www.hst.org.za/sites/default/files/PMTCT_Costing.pdf
  • 91
    Dandona L, Kumar SG, Ramesh YK, Rao MC, Marseille E, Kahn JG, et al. Outputs, cost and efficiency of public sector centres for prevention of mother to child transmission of HIV in Andhra Pradesh, India. BMC Health Serv Res. 2008;8:26. doi: http://dx.doi.org/10.1186/1472-6963-8-26 PMID: 18234117
    » https://doi.org/10.1186/1472-6963-8-26
  • 92
    Bautista-Arredondo S, Dmytraczenko T, Kombe G, Bertozzi SM. Costing of scaling up HIV/AIDS treatment in Mexico. Salud Publica Mex. 2008;50 Suppl 4;S437-44. doi: http://dx.doi.org/10.1590/S0036-36342008001000004 PMID: 19082254
    » https://doi.org/10.1590/S0036-36342008001000004
  • 93
    Menzies NA, Berruti AA, Blandford JM. The determinants of HIV treatment costs in resource limited settings. PLoS One. 2012;7:e48726. doi: http://dx.doi.org/10.1371/journal.pone.0048726 PMID: 23144946
    » https://doi.org/10.1371/journal.pone.0048726
  • 94
    McMennamin T, Alexander F, Fritsche G. Rwanda HIV/PBF Project: cost and revenue analysis in six Rwandan health centers: 2005 costs and revenues. Washington: United States Agency for International Development ; 2007. Available from: http://www.umuganga.com/docs/statiscs1.pdf [cited 2013 Oct 19].
    » http://www.umuganga.com/docs/statiscs1.pdf
  • 95
    Minh HV, Bach TX, Mai NY, Wright P. The cost of providing HIV/AIDS counseling and testing services in Vietnam. Value in Health Regional Issues. 2012;1:36-40. doi: http://dx.doi.org/10.1016/j.vhri.2012.03.012
    » https://doi.org/10.1016/j.vhri.2012.03.012
  • 96
    Marseille E, Dandona L, Marshall N, Gaist P, Bautista-Arredondo S, Rollins B, et al. HIV prevention costs and program scale: data from the PANCEA project in five low and middle-income countries. BMC Health Serv Res. 2007;7:108. doi: http://dx.doi.org/10.1186/1472-6963-7-108 PMID: 17626616
    » https://doi.org/10.1186/1472-6963-7-108
  • 97
    Wilkinson D, Floyd K, Gilks CF. Antiretroviral drugs as a public health intervention for pregnant HIV-infected women in rural South Africa: an issue of cost-effectiveness and capacity. AIDS. 1998;12:1675-82. doi: http://dx.doi.org/10.1097/00002030-199813000-00016 PMID: 9764788
    » https://doi.org/10.1097/00002030-199813000-00016
  • 98
    Robberstad B, Evjen-Olsen B. Preventing mother to child transmission of HIV with highly active antiretroviral treatment in Tanzania – a prospective cost-effectiveness study. J Acquir Immune Defic Syndr. 2010;55:397-403. doi: http://dx.doi.org/10.1097/QAI.0b013e3181eef4d3 PMID: 20739897
    » https://doi.org/10.1097/QAI.0b013e3181eef4d3
  • 99
    Stringer EM, Sinkala M, Stringer JS, Mzyece E, Makuka I, Goldenberg RL, et al. Prevention of mother-to-child transmission of HIV in Africa: successes and challenges in scaling-up a nevirapine-based program in Lusaka, Zambia. AIDS. 2003;17:1377-82. doi: http://dx.doi.org/10.1097/00002030-200306130-00012 PMID: 12799559
    » https://doi.org/10.1097/00002030-200306130-00012
  • 100
    Nakakeeto ON, Umaranayake L. The global strategy to eliminate HIV infection in infants and young children: a seven-country assessment of costs and feasibility. AIDS. 2009;23:987-95. doi: http://dx.doi.org/10.1097/QAD.0b013e32832a17e9 PMID: 19425224
    » https://doi.org/10.1097/QAD.0b013e32832a17e9
  • 101
    Task shifting: rational redistribution of tasks among health workforce teams: global recommendations and guidelines. Geneva: World Health Organization; 2008.
  • 102
    Zachariah R, Ford N, Philips M, Lynch S, Massaquoi M, Janssens V, et al. Task shifting in HIV/AIDS: opportunities, challenges and proposed actions for sub-Saharan Africa. Trans R Soc Trop Med Hyg. 2009;103:549-58. doi: http://dx.doi.org/10.1016/j.trstmh.2008.09.019 PMID: 18992905
    » https://doi.org/10.1016/j.trstmh.2008.09.019
  • 103
    Brinkhof MW, Dabis F, Myer L, Bangsberg DR, Boulle A, Nash D, et al.; ART-LINC, IeDEA. Early loss of HIV-infected patients on potent antiretroviral therapy programmes in lower-income countries. Bull World Health Organ. 2008;86:559-67. doi: http://dx.doi.org/10.2471/BLT.07.044248 PMID: 18670668
    » https://doi.org/10.2471/BLT.07.044248

Publication Dates

  • Publication in this collection
    01 Apr 2014

History

  • Received
    20 July 2013
  • Reviewed
    26 Dec 2013
  • Accepted
    31 Dec 2013
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