HIV/AIDS research in Africa and the Middle East: participation and equity in North-South collaborations and relationships

To identify the scientific literature on HIV/AIDs, we used the Medical Subject Headings (MeSH) thesaurus of the National Library of Medicine, selecting all of the descriptors related to HIV, human immunodeficiency related to HIV infection, and the development of vaccines for preventing or clinically treating the immunodeficiency. The final MeSH (plus their variants and synonyms) were: HIV, HIV Infections, Acquired Immunodeficiency Syndrome, and AIDS Vaccines.

Although the MeSH thesaurus is linked to the MEDLINE database, which is freely available through the PubMed platform, we performed a second search of the documents identified in MEDLINE and which were also indexed in the Web of Science Core Collection (WoS-CC) databases. Although this database does not cover all of the documents indexed in MEDLINE/PubMed, it does include all of the institutional affiliations (which MEDLINE started listing only in 2014), making it an ideal source for characterizing scientific production by country and the collaboration from Africa and the Middle East in HIV/AIDS publications during the study period.

The collection of journals in the WoS-CC, moreover, represents the information sources with the highest visibility at an international level. Thus, using that source to calculate our bibliometric study indicators allows a vision of the development of the most relevant and impactful research worldwide.

Our literature search yielded 93,031 documents on HIV, 256,354 on HIV Infections, 76,359 on Acquired Immunodeficiency Syndrome, and 7528 on AIDS Vaccines. After removing duplicate descriptors, there were 298,718 unique documents. We then restricted the results to those published from 2010 to 2017 (n = 83,316) in order to focus the analysis on the most recent research. We ruled out the inclusion of documents from 2018 to avoid delays related to indexation, as at least a year is needed to ensure updated information related to the assignment of MeSH terms. We subsequently identified the documents that were also included in the WoS-CC databases by searching for all of the documents from the initial sample using their PMIDs (the PubMed identifier used as a reference in MEDLINE and included as a bibliographic field in WoS-CC). In total, 89.29% (n = 74,375) of the MEDLINE documents were also in the WoS-CC. This set of papers was further restricted to three document types: articles, reviews, and letters (n = 68,808), chosen because they are the most prominent papers for transmitting the results of original research (articles); situating and evaluating the development of research in a highly relevant way for other researchers (reviews); and contributing critical viewpoints, comments, relevant information, and perspectives on published studies (letters). The searches took place in November 2018. Figure 1 presents a flow chart showing the selection process for the sample of documents analyzed in the study.

We also reviewed the standardization and quality of the data. For example, we looked at the years of publication, as the date of some documents’ public dissemination on the journal website differed from the definitive date of publication in the journal (the latter was taken as the reference). Likewise, we consolidated all the information on geographic origins from England, Scotland, Wales, and North Ireland—presented individually in the WoS-CC—under the UK.

To analyze the participation from Africa and the Middle East in HIV/AIDS publications, we took as a reference the UNAIDS (2018) definitions of geographical regions, assigning each country to its respective region as defined in that source. The regions were: North America, Western and Central Europe, Asia and Pacific, Eastern and Southern Africa, Latin America and the Caribbean, West and Central Africa, the Middle East and North Africa, and Eastern Europe and Central Asia.

The indicators and analyses applied in our study are structured in three blocks.

Scientific production on HIV/AIDS is dominated by North America (which participated in 55.60% of all documents analyzed) and by Western and Central Europe (35.79%). Together, these regions participated in 82.13% of global scientific research production on HIV/AIDS that was indexed in the sources consulted. For their part, the three regions of Africa and the Middle East participated in 21.61% of the documents, albeit contributions from Eastern and Southern Africa (17.80%) were much higher than those from Western and Central Africa (3.34%) and Middle East and North Africa (1.18%) (Table 1). This limited scientific production contrasts with the high percentages of collaboration observed in these regions; in Eastern and Southern Africa, 82.42% of the papers were published in collaboration with authors from countries in other regions, and in Western and Central Africa, 78.39%. In contrast, 43.22% of the documents from North America were produced in inter-regional collaboration, and 47.99% from Western and Central Europe. Looking only at documents produced with inter-regional collaboration, authors from Africa and the Middle East occupied the first position on just 30 to 36% of the papers, compared to 45% for Western and Central Europe and 54% for North America (Table 1).

Research production in Africa and the Middle East is concentrated in South Africa, whose researchers participated in 40.94% of the documents from these regions. At some distance are several other countries from Eastern and Southern Africa: Uganda (12.97%), Kenya (10.71%), Malawi (6.19%) and Tanzania (6.03%). Thirteen other countries show values ranging from 1.32 to 4.73%. Nigeria is the most prominent producer in Western and Central Africa, at 4.59%, while Iran leads production in the Middle East and North Africa (2.02%). Another 45 countries in Africa and the Middle East contributed to less than 1 % of the total research output (Table 2). Among the most productive countries (> 100 documents), Iran, Ethiopia, Nigeria, and South Africa present the lowest degree of international collaboration and the highest participation as first authors. Many of these show values of international collaboration that exceed 90%, with participation as first author under 30%. This situation is similar or even more pronounced in most low-producing countries (Table 2).

Generally speaking, African research output on HIV/AIDS is characterized by its cooperative links, particularly with the USA, UK, and other European countries (75 to 93% of the collaborations). However, South Africa also stands out for its intraregional ties, and it has become the main reference for research collaboration on HIV/AIDS, both in Eastern and Southern Africa and among the top 10 most productive African countries. It has collaborated with 34 different countries, led 41.44% of the collaborations, and participated in 35.76% of the papers led by other African countries. Uganda ranks second in terms of collaborative leadership within Africa, albeit with values that are much more modest, having led 14.06% of its collaborative research and participated in 11.11% of papers led by other African countries. The rest of the countries contribute less than 10% to the total collaborative links established. Except for South Africa, Uganda, and a few other countries like Zimbabwe, the collaborative links between different countries in Africa are few and far between, constituting weak and sporadic ties (Table 3).

Figure 2 shows a graphic representation of the collaboration network. The USA is in the center as the main reference for international collaboration on scientific output on HIV/AIDS, while the UK, Canada, and other European countries like France, Switzerland, the Netherlands, and Belgium also occupy prominent locations. South Africa is the main African reference for HIV/AIDS publications, reflecting not only its collaborations with the USA, Canada and the European countries but also its prominent role in intraregional collaborations.

The correlation analysis on scientific HIV/AIDS output, produced by all countries worldwide, by African countries alone, and through Africa+global collaborations, shows differences in disciplinary orientations and research topics. In terms of disciplines involved, the lowest degree of correlation pertains to global publications versus solely African publications (k = 0.73; Table 4). There is also certain discordance between solely African publications and Africa+global collaborations (k = 0.79). In contrast, there is great affinity between global research output and output from Africa+global collaborations (k = 0.97). Of note, HIV/AIDS publications from Africa alone was dominated by papers in the field of “Public, Environmental & Occupational Health,” while the disciplines of “Infectious Diseases” and “Immunology” occupy the first rankings both globally and in African+global collaborations. The disciplines of “Medicine, General & Internal” and “Health Policy & Services” were also of great relevance in the publications from African countries alone (Table 4).

Our comparison of the MeSH qualifiers revealed similar disparities (Table 5). The lowest degrees of correlation were between global versus solely African research output (k = 0.68) and between global versus Africa+global collaborations (k = 0.69). However, there was a high degree of correlation between solely African publications and Africa+global collaborations (k = 0.97). With regard to the most prominent MeSH qualifiers, epidemiological studies occupy the top spot in both global and solely African publications. However, “Drug therapy” and “Therapeutic use” are more popular orientations in solely African publications than “Inmmunology,” “Genetics,” and “Metabolism” (Table 5).

Finally, with regard to MeSH descriptors, publications from Africa and the Middle East reflects the high prioritization of terms related to prevalence and treatment approaches (Table 6). Furthermore, global scientific production on HIV/AIDS suggests gender parity in terms of the research focus (both the “Male” and “Female” terms were assigned to 55% of the documents). However, for publications produced by researchers from solely African countries, the “Female” term is present in 73.38% of the documents, and for publications produced by Africa+global collaborations, this MeSH appeared in 76.71% of the documents.

Figure 3 presents a visualization of the main MeSH terms used to represent Africa and Middle East HIV/AIDS research topics and the links between them. Overall, studies that analyze anti-HIV agents, prevalence, and risk factors constitute the main subject areas that articulate the research. Incidence and its relation to sexual behaviors and health education (knowledge, prevention, acceptance of treatment for the disease) is also an important topic, as is research on pregnancy, maternal health, and prenatal care. Other relevant areas focus on co-infection (with tuberculosis, hepatitis B, hepatitis C, meningitis), resistance to anti-viral agents, and the use of certain medicines to treat the infection (lamivudine, tenofovir etc.).

Our analysis shows that scientific production on HIV/AIDS is still dominated by researchers from North America and Western and Central Europe, which together participated in 82% of the documents analyzed, although just 6% of people with HIV live in these regions. In contrast, researchers from countries in Africa and the Middle East participated in less than a quarter of the research papers on HIV/AIDS published between 2010 and 2017 (22%), although two-thirds of all people who are infected with the virus live there. Nevertheless, in relation to previous studies analyzing HIV/AIDS publications produced by researchers from African countries, our results indicate two highly relevant trends: (a) the notable growth in scientific production on HIV/AIDS in this region and (b) the elevated participation in scientific publications with greater visibility and international impact. In absolute terms, the number of documents we identified are double those reported by Macías-Chapula & Mijangos-Nolasco [8], based on their analysis of HIV/AIDS literature from sub-Saharan Africa included in the National Library of Medicine from 1980 to 2000, and by Uthman [9] analyzing scientific production on HIV/AIDS from sub-Saharan Africa and indexed in PubMed from 1981 to 2009.

At a country level, the advances made in research are even more significant. In their study on HIV/AIDS literature included in the National Library of Medicine, Onyancha & Ocholla [10] reported negligible contributions from Uganda and Kenya in the form of journal articles published from 1989 to 1998 (n = 11 and n = 16, respectively). Our results show that these two countries have now become the second and third most productive on the continent, with a high number of contributions to journals indexed in the WoS-CC (n = 1921 documents from Uganda and n = 1586 in Kenya). Uthman [11] studied HIV/AIDS research production from Nigeria between 1987 and 2006, identifying 254 articles in the WoS databases. Our findings, of 679 documents, nearly triple that number, even though the study period is substantially shorter. In South Africa, the production we identified from 2010 to 2017 (n = 6063) is close to that reported by Uthman [9] for the entire period from 1981 to 2009 (n = 8361).

Our results also show a trend toward greater research concentration, with an increase in the relative weight of high-producing countries (particularly South Africa, Uganda, and Kenya), which stand out as the main references for African scientific production on HIV/AIDS. Indeed, these countries now account for over half of all publications from Africa, and their relative contributions are trending upward. Thus, while Uthman [9] reported that South Africa participated in 34% of the HIV/AIDS publications produced by sub-Saharan Africa, in our results this figure stands at 43%. Similarly, the relative weight of Uganda and Kenya (the second and third most productive countries) has risen from 8 and 7% of the total contributions, respectively, to 14 and 11%. Similar observations have been made in other research fields [14] and particularly in the biomedical area [15, 16], demonstrating that economic development and investments in research constitute key factors explaining the rise in scientific productivity [17].

The trend toward a greater concentration of research production in a few countries indicates the need to develop policies that facilitate a greater integration of lower-producing and less-developed countries in research activities. The literature describes some measures to stimulate research in these countries that go beyond economic investments, including training and retaining experienced researchers and fostering long-term partnerships based on equitable collaborative research ties. These strategies can enable researchers from these countries to acquire the methodological skills they need and can favor their leadership in spearheading or directing the research [13].

More specifically to the field of HIV/AIDS, Uthman [9] analyzed the factors associated with scientific productivity on HIV/AIDS in sub-Saharan Africa. His results showed that the number of people living with HIV and the number of indexed journals published in the country were predictive of an increase in publications. Other relevant factors include national scientific policies related to countries’ research agendas for this area, plus the adequate integration and participation in the system for publication and dissemination of scientific knowledge. These variables are more closely associated with scientific productivity on HIV/AIDS than others like the number of higher institutions or the number of physicians. The fact that South Africa is the country with the highest number of HIV-positive people and that this subject area has become a priority on the national research agenda [18] is clearly related to the country’s high research productivity in the field. Its economic growth has complemented this boost; together with other BRICS countries, especially China and Brazil, South Africa has laid the groundwork for development by strengthening its educational, healthcare, and social systems [19, 20]. Increased investments in research go hand in hand with this strategy, including through establishing collaborative links with the most advanced economies at a scientific level [21, 22]. However, as Adams et al. [23] signaled in their study, a myriad of factors affect scientific productivity and collaboration in African countries apart from structural factors like the level of economic growth or population size. For example, countries in the Commonwealth sphere, mostly situated in Eastern and Southern Africa and using English as a second language, generally present a higher level of scientific production and collaborative research than other African countries, like those in the Francophone community [16]. Our results are consistent with this trend: 10 of the 12 most productive countries are linked with the Commonwealth.

Although some countries like Nigeria or Ethiopia have made important research efforts, with corresponding increases in their scientific productivity, different studies have highlighted the need for increasing ties with neighboring countries. This would enable a more fluid exchange of knowledge and experience and foster research in key areas like detection and treatment [11, 24].

The two main bibliometric features we observed to be associated with HIV/AIDS research activity in Africa were: (a) a high degree of international collaboration with countries from other geographical regions, dominated by the USA and Europe (81% of the documents) and (b) a low level of research leadership, as seen through the low participation of African investigators as the first authors of documents produced in collaboration (20 to 38% among the top 10 most productive countries).

These two features may reflect a certain scientific dependence and subordination among African countries in relation to more developed countries. Moreover, the same situation has been observed in other biomedical research fields that are of special importance to the global South, like tropical diseases, infectious diseases, and pediatrics [22, 25, 26]. More specifically, Kelaher et al. [27] analyzed randomized controlled trials in the fields of HIV/AIDS, malaria, and tuberculosis that were undertaken in low- and middle-income countries (LMICs) from 1990 to 2013, identifying three relevant features associated with research leadership. First, there was a much higher proportion of first authors from LMICs in studies funded by LMICs (90%) than in studies funded by the USA (32%). Second, participation as first authors from LMICs was sensibly lower in the field of HIV/AIDS (33%) than for other diseases like malaria (67%). Finally, among first authors from all LMICs worldwide, those from Africa authored fewer papers than those from other regions like Latin America or Asia.

The literature describes different barriers that hinder researchers in LMICs from assuming leadership roles. Some of these are related to the absence of infrastructures or adequate financing [28]. Without an established institutional framework, stable research groups cannot be created or sustained; researchers cannot access the technical and financial support they need to submit research tenders; and coordination and monitoring of research priorities in relation to local research agendas is inadequate [13, 29‐31]. Other barriers have to do with deficits in methodological skills (like research design and statistical interpretation) or language (composition of articles or fluency in English). All of these factors can affect researchers’ capacity to lead studies and authorship [32‐34].

At the same time, there are structural factors related to the hub-and-spoke model that favor the increased recognition and success of countries conducting mainstream research. Economic and human resources are concentrated in North America and Europe, and these regions also establish priority research topics. Editorial bias and the Matthew effect of accumulated advantage cement the structural forces perpetuating the under-representation of researchers from the global South from assuming positions of leadership in scientific publications [26, 32].

The two countries constituting the axis of the collaborative research network on HIV/AIDS are the USA and South Africa. The former stands out for the high number of collaborative links it has established, with its researchers co-authoring papers with most African and Middle Eastern countries (52 countries). In total, 7693 collaborative ties (co-authored papers) were established in the study period, 70% of which were led by researchers in American institutions. Other bibliometric studies have also described the relevance of the USA in collaborative HIV/AIDS research output in Africa [11], Latin America and the Caribbean [35], and Asia [36]. Our own group have highlighted this role in other biomedical research fields [37].

For its part, South Africa is clearly the country of reference for HIV/AIDS research activity on the African continent, with a quantitative weight that is well above that observed in other biomedical areas in which it also exercises leadership. Nachega et al. [16] assessed the participation of African countries in publications on epidemiology and public health in the WoS databases, reporting that South Africa was represented in 22% of the documents, Kenya in 10%, and Nigeria in 9%. In our study, 41% of the documents on HIV/AIDS were authored by researchers in South Africa. This country, along with Ethiopia, is also notable for its leadership, figuring in the affiliations of 38% of the first authors. A similar phenomenon has also been observed in other fields of the health sciences, such as infectious diseases [15, 38].

In addition to maintaining important collaborative ties with the USA and different European countries [39, 40], South Africa has also emerged as a hub for intraregional collaborations within Africa. It has established links with 35 countries—far more than other African countries. Indeed, it is the main collaborator for all the other African countries in the top 10 for HIV/AIDS research productivity, even though these collaborations represent just 12% of the total collaborations in which South Africa participates. In that sense, some papers have called for BRICS countries, including South Africa, to increase their efforts to tackle the challenges primarily affecting the developing world [19]. In the case of South Africa, this could be done by promoting intraregional collaborations in sub-Saharan Africa, as research undertaken at a local level has the most potential to produce benefits, both for population health and socioeconomic development [20, 41]. Hernandez-Villafuerte, Li & Hofman [42] analyzed collaborations among sub-Saharan countries conducting economic evaluations of healthcare interventions, reporting results consistent with ours: researchers in this region tend to collaborate more with Europeans and North Americans than with each other.

The literature highlights specific barriers impeding equitable research collaboration for African researchers, for example the paper by Okeke [43], who pointed to the limited duration of research programs, which should be longer in order to nurture stable collaborations that build hard and leadership capacities. In addition to infrastructure, other aspects mentioned include managerial expertise, administrative capabilities, and the capacity to improvise at African partner institutions. In the same line, Boum II [44] and Boum II et al. [45] discuss the difficulties in harmonizing conflicting interests between Western and African countries, making it essential to prioritize financing for equitable initiatives that lay out specific goals and expectations for partnerships, or which promote initiatives like mentorship programs and investment in Africa-based researchers that strengthen institutional capacity.

Some examples of successful collaborations for promoting equitable research partnerships and African leadership in HIV research include initiatives like the Academic Model Providing Access to Healthcare (AMPATH) in Kenya, the International Epidemiology Databases to Evaluate AIDS (IeDEA) consortium, and different initiatives coordinated and driven by the Africa Centres for Disease Control and Prevention (Africa CDC) or the Joint United Nations Programme on HIV and AIDS (UNAIDS), among others.

HIV/AIDS research produced by solely African countries differed from global research in terms of disciplinary and subject area orientations, with a greater focus on public health, epidemiology, and treatment. This finding indicates the need to consider regional, national, and local specificities and interests when determining research priorities. In fact, numerous studies have already signaled the poor alignment between the priorities laid out in African countries’ national research agendas and the research topics that are actually financed [12, 16, 46‐49].

From a public health perspective, for example, Uthman [11] pointed out the need for further research evidence to inform HIV prevention and control programs. In this field, some countries perform better than others: South Africa is particularly strong in public health research [50], while other African countries and regions, such as French Africa, have made limited contributions [51].

Studies on epidemiology and treatment approaches for HIV/AIDS are very relevant for research produced in Africa, in contrast to what occurs on a global scale, where these orientations have a relatively limited weight. Nachega et al. [16] pointed out that research on HIV/AIDS, tuberculosis, and malaria have become the main research topics addressed in epidemiological and public health publications in African countries. However, these authors argued for moving epidemiology and public health research beyond the limited sphere of communicable disease control in order to address the regional impact of non-communicable diseases, for example in maternal and child health. This is especially relevant in the case of sub-Saharan Africa, where epidemiologists are overwhelmingly deployed to control infectious diseases, especially HIV/AIDS, tuberculosis, and malaria. The study also calls for strengthening regional expertise in epidemiology in order to shed light on the underlying causes of ill health, rather than to merely control infections and outbreaks [16].

In addition to epidemiological studies, African research also reflects an intense interest in drug therapies for HIV/AIDS, illustrating that control of the infection is a priority for research agendas and policies in African countries [12].

More specifically, previous literature on HIV/AIDS research has shown a greater focus on women in studies carried out with the participation of African researchers [10]. Our study confirms this finding: 73 to 77% of the documents investigated women, compared to 55% in the global literature. One possible explanation for this includes the fact that women are more biologically, economically, socially, and culturally vulnerable to infection. Indeed, for every 10 African men who are HIV-positive, there are 12 to 13 infected women; moreover, 55% of adults who acquire HIV are women, with profound implications for mother-to-child transmission [10]. In consonance with this fact, a greater number of women participate and work on HIV care programs in Africa, and a large proportion of the clinicoepidemiological investigations in these settings are based on care program data [52].

The different epidemiological patterns of HIV/AIDS transmission in North America and Western and Central Europe must also be taken into account, that motivate a greater interest of research in these regions on sexual transmission between men and intravenous drug users. These epidemiological patterns are less important in Africa [53]. The presence in the MeSH co-occurrence network of the descriptors “pregnancy” and “sexual behavior” are noteworthy, reflecting how African researchers are investigating aspects like maternal-fetal transmission of HIV [54] or knowledge and prevention of sexual risk, and changing the preconceptions that still persist about the social determinants of transmission [47]. The prominence of topics related to preventing mother-to-child transmission stands in contrast to the near absence of topics related to children and young people. These groups are especially sensitive to the physical and psychosocial impacts of HIV and AIDS, indicating the need for increased research on young people who are at risk of or living with HIV [55].

The greater research attention to topics related to public health, epidemiology, and treatment may also respond to limited laboratory capacity, which is needed for virologic, immunological, and basic research. In that sense, it is essential to promote initiatives that strengthen these research structures and capacities in African countries, rather than only supporting programs and projects on preventive and clinical approaches.

Limitations of the present study include the fact that a considerable portion of HIV/AIDS research in African countries is disseminated using document types and media that we did not consider, such as meeting abstracts and journals that are not indexed in the WoS-CC. Moreover, using the MeSH thesaurus from the field of health sciences could have resulted in an underestimation of research spheres related to our subject area, such as research in the social sciences. In that sense, some papers have indicated that stigma and discrimination still constitute the main barriers to controlling HIV/AIDS [56]. The process used to assign geographic place variables to the papers included in the sample was based on authors’ stated institutional affiliation; this method has the inherent limitation of not being able to measure the author’s origin, nationality, or identification with the country, but rather the institution’s (and the country’s) capacity to generate outputs in the form of scientific publications. Thus, many researchers of African origin who work at institutions in the USA and Europe would be coded as US/European researchers. Furthermore, the use of first author status as a proxy for African leadership may be misleading, as an African senior author may be the last author on a publication or may have played a leadership role in some aspects other than the manuscript preparation.

Our study focused on obtaining macro indicators on scientific collaboration and output by regions and countries. Future lines of research could conduct meso- or microlevel analyses, for example focusing on the participation of institutions or authors in African HIV/AIDS research or on the impact of the publications. It would also be of great interest to identify the organisms or programs that have funded the research inspiring the publications about HIV, measuring resource contributions according to domestic versus international as well as public versus private origins.