A systematic review of missed opportunities for improving tuberculosis and HIV/AIDS control in Sub-saharan Africa: what is still missed by health experts?

In sub-Saharan Africa, HIV/AIDS and tuberculosis are major public health problems. In 2010, 64% of the 34 million of people infected with HIV were reported to be living in sub-Saharan Africa. Only 41% of eligible HIV-positive people had access to antiretroviral therapy (ART). Regarding tuberculosis, in 2010, the region had 12% of the world's population but reported 26% of the 8.8 million incident cases and 254000 tuberculosis-related deaths. This paper aims to review missed opportunities for improving HIV/AIDS and tuberculosis prevention and care. We conducted a systematic review in PubMed using the terms ‘missed’(Title) AND ‘opportunities’(Title). We included systematic review and original research articles done in sub-Saharan Africa on missed opportunities in HIV/AIDS and/or tuberculosis care. Missed opportunities for improving HIV/AIDS and/or tuberculosis care can be classified into five categories: i) patient and community; ii) health professional; iii) health facility; iv) local health system; and v) vertical programme (HIV/AIDS and/or tuberculosis control programmes). None of the reviewed studies identified any missed opportunities related to health system strengthening. Opportunities that are missed hamper tuberculosis and/or HIV/AIDS care in sub-Saharan Africa where health systems remain weak. What is still missing in the analysis of health experts is the acknowledgement that opportunities that are missed to strengthen health systems also undermine tuberculosis and HIV/AIDS prevention and care. Studying why these opportunities are missed will help to understand the rationales behind the missed opportunities, and customize adequate strategies to seize them and for effective diseases control.


Introduction
Sub-Saharan Africa is the world's region most affected by HIV/AIDS and tuberculosis (TB). In 2010, 64% of the 34 million of people infected by HIV were reported to be living in sub-Saharan Africa [1].
Despite investments and efforts done so far, only 41% of eligible HIV-positive people had access to antiretroviral therapy (ART); only 35% of pregnant women underwent testing for HIV, and only 48% of these HIV-positive pregnant women had access to effective antiretroviral therapy to prevent mother-to-child transmission.
Additionally, only 23% of HIV-positive children had access to ART.
This low access to prevention and treatment contributed to 2.7 million new HIV infections in 2010. Regarding TB, in 2010, sub-Saharan Africa had 12% of the world population but reported 26% of the 8.8 million incident cases -the world's highest incidence at 256 cases per 100000 inhabitants-and 254000 TB-related deaths.
Sub-Saharan Africa counted for 82% of HIV-positive people with TB, and is the sole WHO world region that is not on track to halve the 1990 TB mortality by 2015 [2].
In recent years, there has been a significant increase in global health investment dedicated to disease control programmes in low- In high income countries, the quality of the health systems contributed to offer universal access to health care to people living with HIV/AIDS and/or suffering from TB, and to significantly reverse the epidemic. On the contrary, in sub-Saharan Africa, the extended and persistent HIV/AIDS pandemic and the recrudescence of TB reveal huge uncovered needs of the population by health systems.
Some studies investigated constraints faced by African health systems in delivering effective interventions for the control of major infectious diseases, and have proposed strategies to tackle those constraints [5,6]. Consequently, the persistent high morbidity and mortality related to HIV/AIDS and TB could be the result of opportunities not seized to timely deliver adequate and effective care against these conditions [7].
The objective of this study was to identify, through a systematic review of the literature, missed opportunities (MOs) to deliver effective care to prevent, diagnose and treat HIV/AIDS and TB in sub-Saharan Africa. Knowing these MOs could help health systems stakeholders to develop strategies for actually reversing the two deadly epidemics.

Methods
We searched PubMed on September 9, 2012, using the terms 'missed' (Title) AND 'opportunities' (Title). We found 490 articles which were then independently reviewed by two investigators. The

Study selection
We included systematic review and original research articles done in sub-Saharan Africa on MOs in HIV/AIDS and/or TB care. Viewpoints, letters, and studies conducted outside sub-Saharan Africa were excluded. Date of publication and language were not considered as criteria for exclusion. Initially, 409 articles with topics not related to HIV/AIDS and TB were excluded through the review of their titles (Figure 1). Then the abstracts of the remaining 81 articles were analyzed: 57 on HIV/AIDS, 21 on TB and 3 on TB and HIV/AIDS.
Of the 57 articles related to HIV/AIDS, 42 studies conducted outside Africa and 3 viewpoints were excluded while 12 were relevant for the review. Of the 21 articles related to TB, 15 studies conducted outside Africa and 2 viewpoints were excluded, 4 articles were relevant and one additional article was identified from the reference list. All three studies on HIV/AIDS and TB were relevant. A total of 20 articles were therefore reviewed.

Data extraction
Data were extracted independently by two investigators using a standardized extraction sheet. Data extracted included the characteristics of the study (setting, type, objective, data collection period, publication date) and the MO. Missed opportunities were further inductively classified into five categories: patient and community; health professional; health facility; local health system; and vertical programme (HIV/AIDS and/or TB control programmes).

Current status of knowledge
The 20 relevant articles included in the review were 18 original articles and 2 systematic reviews. The studies were conducted in 6 English-speaking southern and eastern sub-Saharan African countries with high HIV prevalence: Ethiopia, Kenya, South Africa, Tanzania, Uganda and Zambia. The articles were published between 1993 and 2012. Regarding HIV/AIDS, opportunities were not seized to detect HIV (among children from HIV-positive mothers, pregnant women, and general population), to identify people eligible for antiretroviral therapy (ART), or to offer ART for the prevention of mother-to-child transmission of HIV or to eligible HIV-positive persons. For TB, opportunities were not taken to detect TB in suspect patients, to offer chemoprophylaxis to exposed children, to diagnose TB in symptomatic patients, or to create in health facilities conditions for optimal detection of TB.   Table 2 Patient, local organization and community level: Like for HIV/AIDS, patient-related MOs for improving TB control ( Table 2)

Seizing opportunities
This review identifies MOs to improve prevention, detection, diagnosis and adequate care of HIV/AIDS and TB in sub-Saharan African health systems. The limit of this study is that articles were searched only on PubMed while other literature, such as projects reports and programme evaluations, could also provide useful information on MOs. Additionally, studies reviewed were mainly conducted at health facility and community levels whereas other MOs for improving TB and HIV/AIDS control could be related to higher levels of the health system, to health policies, to international procedures of international organizations funding these programmes, and to the quality of the interface between HIV/AIDS and TB control programmes and general health services. However, this study identified sizeable factors that could explain why TB and HIV/AIDS have not yet been controlled in sub-Saharan Africa in spite of the availability of effective interventions.
MOs that are described in sub-Saharan Africa do exist in other settings, but at a much lower scale, indicating that these opportunities can be seized to improve TB and HIV/AIDS care. In developed countries, the low proportion of MOs leads to a much lower incidence and to a high detection rate of HIV and TB cases. However, what is still missing in the analysis of health experts is the identification of health system strengthening's missed opportunities as a leading factor undermining disease control in sub-Saharan Africa. Studying why these opportunities are missed will help to understand the rationales behind the MOs, and customize effective strategies for seizing them.

Competing interests
The authors declare no competing interests.

Authors' contributions
Basile Keugoung designed the study, wrote the protocol, made the internet search of articles, and extracted data. Florent Fouelifack Ymele independently reviewed the articles and extracted data.
Articles selected and data extracted were compared and to reach a consensus. All authors reviewed the protocol, the articles included in the study, the extracted data, and the subsequent versions of the manuscript. All authors approved the final manuscript.