Epidemiology of HIV infection in the Middle East and North Africa
Abu-Raddad, Laith Ja,b,c; Hilmi, Nahlad; Mumtaz, Ghinaa; Benkirane, Manale; Akala, Francisca Ayodejid; Riedner, Gabrielef; Tawil, Oussamag; Wilson, Davidh
aWeill Cornell Medical College – Qatar, Cornell University, Qatar Foundation - Education City, Doha, Qatar
bDepartment of Public Health, Weill Cornell Medical College, Cornell University, New York, New York, USA
cVaccine and Infectious Disease Institute, Fred Hutchinson Cancer Research Center, Seattle, Washington, USA
dHuman Development Sector, Middle East and North Africa Region, World Bank, District of Columbia, USA
eAssociation de Lutte Contre le Sida, Marrakesh, Morocco, Egypt
fRegional Office of the Eastern Mediterranean, World Health Organization, Egypt
gJoint United Nations Programme on HIV/AIDS Regional Support Team, Middle East and North Africa, Cairo, Egypt
hGlobal HIV/AIDS Program, World Bank, Washington, District of Columbia, USA.
Correspondence to Laith J. Abu-Raddad, PhD, Weill Cornell Medical College – Qatar, Qatar Foundation – Education City, P.O. Box 24144, Doha, Qatar. Tel: +974 492 8321; fax: +974 492 8333; e-mail: firstname.lastname@example.org
Objective: The Middle East and North Africa (MENA) region continues to be perceived as a region with very limited HIV epidemiological data, raising many controversies about the status of the epidemic in this part of the world. The objective of this review and synthesis was to address the dearth of strategic interpretable data on HIV in MENA by delineating a data-driven overview of HIV epidemiology in this region.
Methods: A comprehensive systematic review of HIV, sexually transmitted infections (STIs) and risk behavior studies in MENA, irrespective of design, was undertaken. Sources of data included Medline for peer-reviewed publications, Google Scholar for other scientific literature published in nonindexed local and regional journals, international organizations reports and databases, country-level reports and database including governmental and nongovernmental organizations publications, as well as various other institutional documents.
Results: Over 5000 sources of data related to HIV and STIs were identified and reviewed. The quality of data and nature of study designs varied substantially. There was no evidence for a sustainable HIV epidemic in the general population in any of the MENA countries, except possibly for southern Sudan. The general pattern in different countries in MENA points towards emerging epidemics in high-risk populations including injecting drug users, men who have sex with men (MSM) and to a lesser extent female sex workers, with heterogeneity between countries on the relative role of each of these high-risk groups. Exogenous HIV exposures among nationals linked to travel abroad appeared to be the dominant HIV transmission pattern in a few MENA countries with no evidence for much epidemic or endemic transmission. The role of bridging populations in bridging the HIV infection to the general population was found to be very limited.
Conclusion: Although they do not provide complete protection against HIV spread, near universal male circumcision and possibly the prevailing sexually conservative cultural norms seemed to have played so far a protective role in slowing and limiting HIV transmission in MENA relative to other regions. If the existing social and epidemiological context remains largely the same, HIV epidemic transmission is likely to remain confined to high-risk populations and their sexual partners, in addition to exogenous exposures. HIV prevention efforts in this region, which continue to be stymied by stigma associated with HIV/AIDS and related risk behaviors, need to be aggressively expanded with a focus on controlling HIV spread along the contours of risk and vulnerability. There is still a window of opportunity to control further HIV transmission among high-risk groups in MENA that, if missed, may entail a health and socioeconomic burden that the region, in large part, is unprepared for.
Despite much progress on understanding HIV epidemiology globally, the Middle East and North Africa (MENA) stands as the only region where knowledge of the epidemic continues to be very limited and subject to much controversy . Despite emerging data revealing low HIV prevalence in the region, some surveys suggest more or less sizable pockets of very high risk . Still, more than 25 years since the discovery of the HIV virus, no scientific study has provided a comprehensive data-driven synthesis of HIV/AIDS spread in this region which continues to be viewed as the anomaly in the HIV/AIDS world map and ‘a real hole in terms of HIV/AIDS epidemiological data’ .
The apparent lack of HIV data has fuelled an intense polemical debate on the status of the epidemic in MENA . Some argue that MENA's cultural values, in terms of strong prohibitions against premarital and extramarital sex, homosexuality and alcohol and drug use, provide ‘sterilizing cultural immunity’ against HIV spread, and that HIV is unlikely to impact MENA societies [4–6]. Interestingly, the same cultural values are held responsible by an opposing viewpoint for slowing, if not freezing, the ability of MENA societies to deal with the epidemic [7,8]. This latter view argues that there is a public health crisis ‘behind the veil’ and that if this crisis is ignored, HIV/AIDS could debilitate or even destabilize some of MENA societies by its drastic effects on morbidity, mortality and economic productivity of the 15–49 years age group [7,8].
Similar to other regions, several vulnerability factors for HIV can be found in different parts of MENA. The process of modernization including mass education and urbanization, which may occur with abandonment of traditional patterns of behavior , continues in MENA at an accelerated pace. Most countries are experiencing diverse influences including changing family structures, exposure to different cultures, and enhanced communication and technology means [5–7]. In many areas of MENA, there appears to be a sociocultural transition leading to more tolerance and acceptance of practices such as premarital and extramarital sex and increased opportunities for sexual partnerships beyond traditional forms . The cultural traditions of balancing premarital chastity with early marriage are no longer the norm in most parts of MENA , and social and gender tensions have been exacerbated by the clashing forces of traditional and modern cultures .
MENA is also distinctively characterized by a massive youth bulge where one-fifth of the population are in the 15–24-year age group [13,14], normally the age of initiation of sexual activities . Complex emergencies such as conflicts and wars are prevalent in the region and can increase vulnerability to HIV by reducing access to HIV prevention services, breaking down of health infrastructure, disrupting social support networks, increasing exposure to sexual violence, and increasing population movement to an area of higher HIV prevalence . Extensive levels of migration, displacement, and mobility exist in MENA, which has the highest number of refugees and internally displaced persons in the world . MENA is flooded as well with inexpensive drugs due to high levels of production of heroin in Afghanistan and major drug trade routes that pass through the region .
The social determinants of health in terms of political conflict, limited resources, and gender inequity continue to challenge many countries in the region . Denial that HIV exists or is an important challenge still persists. High-risk groups are highly stigmatized and lack access to comprehensive and confidential services. Community organizations serving at-risk populations are emerging, but apart from some notable exceptions, are insufficient to meet current needs. Health promotion approaches remain overall didactic and prescriptive, are divorced from behavioral theory, and are nonparticipatory. Most importantly, there is lack of evidence-based policies that can guide effective interventions, and HIV response in MENA continues to be beset by numerous challenges.
With the apparent lack of empirical HIV data to support existing and emerging views on HIV epidemiology in this unique, evolving, and controversial context, the main objective of this investigation was to address the dearth of interpretable data on HIV in MENA by delineating an evidence-based and data-driven overview of HIV epidemiology in this region.
This systematic review summarizes major findings of the MENA HIV/AIDS Epidemiology Synthesis Project whose mandate was to collect and synthesize all available data on HIV, sexually transmitted infections (STIs), and sexual behavior in the MENA region. The project was conducted and funded through a partnership of the World Bank, the MENA Regional Support Team (RST) of the Joint United Nations Programme on HIV/AIDS (UNAIDS), and the Eastern Mediterranean Regional Office (EMRO) of the World Health Organization (WHO) . The following data sources were identified as part of a comprehensive search of relevant studies and databases:
1. Scientific literature search of Medline (PubMed) using a strategy with both free text and MeSH headings, and with no language or year limitations. Although results of some of the searches have not been described in this article, the following set of criteria were used as part of the comprehensive search of the Medline database that was conducted for the Synthesis Project:
a. Studies of HIV infectious spread in its different modes of transmission under the strategy of (‘HIV Seropositivity’ OR ‘HIV’ OR ‘HIV Infections’) AND (‘Middle East’ OR ‘Islam’ OR ‘Arabs’ OR ‘Arab World’ OR ‘Africa, Northern’ OR ‘Mauritania’ OR ‘Sudan’ OR ‘Somalia’ OR ‘Djibouti’ OR ‘Pakistan’).
b. Studies of sexual behavior and levels of risk behavior under the strategy of (‘Sexual Behavior’ OR ‘Sexual Partners’ OR ‘Sexual Abstinence’ OR ‘Unsafe Sex’ OR ‘Sexology’ OR ‘Reproductive Behavior’ OR ‘Safe Sex’ OR ‘Condoms’ OR ‘Sex’) AND (‘Middle East’ OR ‘Islam’ OR ‘Arabs’ OR ‘Arab World’ OR ‘Africa, Northern’ OR ‘Mauritania’ OR ‘Sudan’ OR ‘Somalia’ OR ‘Djibouti’ OR ‘Pakistan’).
c. Studies of herpes simplex virus type two sero-prevalence under the strategy of (‘Herpesvirus 2, Human’ OR ‘Herpes Genitalis’) AND (‘Middle East’ OR ‘Islam’ OR ‘Arabs’ OR ‘Arab World’ OR ‘Africa, Northern’ OR ‘Mauritania’ OR ‘Sudan’ OR ‘Somalia’ OR ‘Djibouti’ OR ‘Pakistan’).
d. Studies of human papillomavirus and cervical cancer under the strategy of (‘HPV’ OR ‘Human papillomavirus’ OR ‘Human papilloma virus’ OR ‘Cervical cancer’) AND (‘Middle East’ OR ‘Islam’ OR ‘Arabs’ OR ‘Arab World’ OR ‘Africa, Northern’ OR ‘Mauritania’ OR ‘Sudan’ OR ‘Somalia’ OR ‘Djibouti’ OR ‘Pakistan’).
e. Studies of bacterial sexually transmitted infections under the strategy of (‘Chlamydia’ OR ‘Chlamydia Infections’ OR ‘Chlamydia trachomatis’ OR ‘Gonorrhea’ OR ‘Neisseria gonorrhoeae’ OR ‘Syphilis’ OR ‘Vaginosis, Bacterial’ OR ‘Pelvic Inflammatory Disease’) AND (‘Middle East’ OR ‘Arabs’ OR ‘Islam’ OR ‘Arab World’ OR ‘Africa, Northern’ OR ‘Mauritania’ OR ‘Sudan’ OR ‘Somalia’ OR ‘Djibouti’ OR ‘Pakistan’).
f. Studies of hepatitis C virus under the strategy of (‘Hepatitis C’ OR ‘Hepatitis C Antibodies’ OR ‘Hepatitis C Antigens’) AND (‘Middle East’ OR ‘Islam’ OR ‘Iran’ OR ‘Arabs’ OR ‘Arab World’ OR ‘Africa, Northern’ OR ‘Mauritania’ OR ‘Sudan’ OR ‘Somalia’ OR ‘Djibouti’ OR ‘Pakistan’).
2. Peer-reviewed publications published in local and regional research journals not indexed in Medline (PubMed), but identified most often through Google Scholar.
3. Country-level reports and databases, governmental and nongovernmental organizations studies and publications, as well as other institutional reports related to HIV and STIs in MENA.
4. International organizations' reports and databases related to HIV and other STIs. Among the organizations from which we obtained reports and data are UNAIDS, WHO, World Bank, United Nations Children's Fund (UNICEF), United Nations Office on Drugs and Crime (UNODC), International Agency for Research on Cancer (IARC), International Organization for Migration (IOM), International Centre for Prison Studies (ICPS), Office of the UN High Commissioner for Refugees (UNHCR), Population Reference Bureau (PRB) and Family Health International (FHI).
5. Demographic and Health Survey (DHS) reports of MENA countries.
6. Consultations with key experts, public health officials, researchers, and academics in the region and beyond.
The review covered all countries included in the MENA definitions of the World Bank, UNAIDS RST and WHO EMRO. These include Afghanistan, Algeria, Bahrain, Djibouti, Egypt, Iran, Iraq, Jordan, Kuwait, Lebanon, Libya, Morocco, Oman, Pakistan, Qatar, Saudi Arabia, Somalia, Sudan, Syria, Tunisia, United Arab Emirates, West Bank and Gaza (Occupied Palestinian Territories), and Yemen. Considering geographic proximity and similarity in the sociocultural context, data were occasionally included on Mauritania, the native Palestinian population in Israel, and Turkey.
In this paper, the MENA population was divided into three classes based on risk of infection. These are high-risk groups, bridging populations, and the general population. As a consequence of the nature of HIV epidemiology in MENA, we focus much of our discussion on the high-risk groups including injecting drug users (IDUs), men who have sex with men (MSM) as well as female sex workers (FSWs) and commercial heterosexual sex networks. Also, for this review, the Results section is primarily structured around summarizing studies on HIV prevalence, risk behavior, and HIV/AIDS knowledge. Findings of other studies, such as those that provide specific context, are presented in relevant parts of the Discussion section.
This review covered over 5000 sources of data. In addition to a large number of unpublished publications, country-level reports, NGOs' studies, international organizations' reports, DHS reports and others, a total of nearly 4000 peer-reviewed scientific sources of literature were identified through the Medline search as of 30 July 2009. More specifically, there were 1036 publications related to HIV infectious spread in its different modes of transmission, 1393 related to sexual behavior and levels of risk behavior, 27 related to herpes simplex virus type two sero-prevalence, 188 related to human papillomavirus and cervical cancer, 523 related to bacterial sexually transmitted infections, and 788 related to hepatitis C virus.
There is considerable evidence on HIV prevalence and risk behavior practices among IDUs, MSM, and FSWs in MENA. Earlier evidence suffered from methodological limitations, but the quality of evidence has increased substantially in recent years. The information reviewed on high-risk groups in MENA includes data originating from integrated biobehavioral surveillance surveys incorporating state-of-the-art surveillance methodologies of hard-to-reach populations such as respondent-driven sampling, from descriptive and qualitative studies such as formative assessments, from HIV testing data, in addition to countries' case notification reports.
Injecting drug users and HIV
Injecting drug use is a key HIV mode of transmission worldwide  and was found to be the dominant mode of transmission in several MENA countries such as Iran  and Libya . HIV has been documented among IDUs in the majority of the MENA countries' case notification surveillance reports . Table 1 describes the results of available HIV point-prevalence surveys among high-risk groups in MENA including IDUs [22–111].
Overall, HIV prevalence among IDUs was in the low to intermediate range compared to global figures , with significant variation across and within MENA countries. Although the prevalence of HIV among this risk group was low in several countries, there was robust evidence for concentrated epidemics among IDUs in at least Iran and Pakistan (Table 1) . Concentrated epidemics are defined as HIV prevalence consistently exceeding 5% in a high-risk group, while remaining below 1% in pregnant women . HIV incidence was found to be at very high levels of 16.8% per person-year among IDUs in a detention center in Iran . High prevalence rates were also documented among IDUs in Libya (up to 59.4%) , Oman (up to 27%) , and Bahrain (up to 21.1%) .
The prevalence of injecting drug use in MENA, at 0.2% of the population, is overall in the intermediate range compared to other regions [25,32,113]. Nevertheless, some MENA countries such as Iran suffer from an extensive IDU problem. Iran has the highest rate of heroin and opium drug dependence (injecting and noninjecting) in the world (one in every 17 people) [114,115] and it is estimated in different studies that there are between about 100 000 and 300 000 IDUs in this country [32,115–119]. Overall, MENA is a major source, route, and destination for the global trade in illicit drugs and is flooded with inexpensive drugs due to record levels of heroin production in Afghanistan .
Substantial levels of risk behavior have been documented among IDUs in MENA. IDUs reported injecting drugs at a rate of about one to two injections per day  and multiple studies documented that about 50% of IDUs in MENA shared injecting equipment . Use of nonsterile injections appeared to be common in MENA and cleaning of syringes with bleach is very limited if at all existent . Other high-risk injecting drug practices have been documented in MENA such as deliberately drawing blood into the syringe during drug injection (‘jerking’) . There was also documented evidence for commercial sale of blood among IDUs , a practice that led to a large number of HIV infections in China through contaminated blood .
Levels of comprehensive HIV knowledge varied across the region, with both high and low levels being documented in different settings . However, despite comprehensive HIV/AIDS knowledge, when available, a large fraction of IDUs do not feel at risk of HIV infection. Only 33.9% , 31.1% , and 35.9%  of IDUs in Pakistan, and 27% of IDUs in Syria , reported self-perception of risk to HIV.
MSM and HIV
Sexual orientation, sexual identity, same sex attraction, and male–male sexual behavior are concepts that are often not clearly defined or distinguished in data collected under the broad topic of ‘MSM’. Moreover, transgendered persons of diverse cultural contexts are often combined with other MSM in many studies despite different identities, patterns of risk, and programmatic needs. Data from MENA are no exception to these limitations. In this review, we conform to the common terminology of ‘MSM’ that is often used in the literature  to refer to the population of men who engage in same-sex sexual activities, namely anal sex.
MSM are the most hidden and stigmatized of all HIV-risk groups in MENA. Although reliable estimates of the number of MSM are scarce, available data indicate that the proportion of the male population engaging in anal sex with males in MENA is comparable to global levels of roughly 2–3% (W. McFarland, 2008, personal communication) [122–124]. In this region of the world, sexual identities are complex and male same-sex behavior may take multiple forms, as is best seen in Pakistan where there is a complex tapestry of MSM and male sex workers (MSWs) including hijras or khusras (transgendered individuals who dress as women), khotkis (biological males who dress as men but have ‘female soul’ and feminized traits), banthas (biological men with a male sex identity) in addition to several other forms [88,125,126].
HIV transmission between MSM has been reported in most MENA countries [62,127,128]. Results of available point-prevalence surveys among MSM including MSWs, hijras, and hijra sex workers (HSWs) are shown in Table 1. Prevalence levels suggest considerable HIV transmission among MSM in MENA. Reported HIV rates among MSM ranged between as low as 0% in certain groups up to 9.8% in Sudan  and 27.6% at one site in Pakistan .
MSM studied in MENA have shown a wide range of high-risk behaviors such as multiple sexual partnerships of different kinds. Over 90% of many MSM populations in different settings reported having multiple partners per year [101,129,130] with large variations in the numbers, ranging from 2 to 42 partners per year [67,131,132]. Also, there was a relatively low rate of condom use, with lack of availability being one of the reported limitations in several settings [83,129,133]. On the contrary, male sex work was found to be prevalent among MSM in MENA who use it possibly to support their living in an environment of stigma and poor support network . Commercial sex work was reported by 42%  and 20%  in Egypt, 36% in Lebanon , and 67%  and 75.5%  in Sudan. It is worth noting that given that MSM are highly hidden in MENA and that representative samples of MSM remain scarce, the relative visibility of MSW may result in biases that overestimate the levels of sex work within the wider MSM population.
Levels of HIV knowledge among MSM in MENA appeared to vary, possibly reflecting the socioeconomic status of each MSM group . However, even in countries with relatively good levels of HIV awareness, many misconceptions were reported [45,136].
Female sex workers and HIV
Although reliable data on the number of FSWs in MENA are limited, available data indicate that commercial sex is fairly prevalent all over MENA with rates ranging between 0.1 and 1% of adult women [22,81,137–141]. These estimates are rather on the low side of the global range [138,142,143], but are consistent with the prevalence of sex work among women in Indonesia and Malaysia, two predominantly Muslim nations, at 0.4%  and 0.9% , respectively. Still, in MENA, the size of the commercial heterosexual sex networks (including FSWs and their clients) is substantially bigger than that of IDUs and MSM risk networks, implying a potentially larger HIV epidemic if HIV establishes itself firmly in commercial sex networks. Social and economic pressure, family disruption, and political conflicts are major drivers of commercial sex in this region .
The prevalence of HIV among FSWs in MENA continues to be at low levels in most countries, although at levels much higher than those in the general population. Although HIV did not appear to be well established among many commercial sex networks in MENA, HIV prevalence has reached high levels among FSWs in at least parts of Djibouti, Somalia, and Sudan (Table 1). For example, in Djibouti, rates of HIV up to 70% [38,39] and 25.6%  have been documented among street-based and bar-based FSWs, respectively. However, even in these three countries, observed rates remain generally at lower levels than those found in hyperendemic HIV epidemics in sub-Saharan Africa .
FSWs in MENA have been shown to engage in multiple sexual risk behaviors. Overall, the number of clients per FSW ranged between one and three clients per working day [82,147–150], which is broadly consistent, but rather on the low side, with global trends [146,151–154]. Nevertheless, higher levels of up to 4.6 clients per working day or 33.7 clients per month per FSW have been reported in Pakistan . There was significant variation in the rates of condom use by FSWs in MENA, although the general trend was on the low end especially in areas of high HIV prevalence among FSWs. For example, in Sudan, 13% of FSWs reported using condoms regularly  and, in another study, only 2% of FSWs clients used condoms during last sex . In many instances, condoms are seen as a contraceptive measure rather than an HIV prevention measure [149,156]. Several studies also documented anal and oral sex practices among FSWs in MENA . Considerable levels of STIs other than HIV have been documented among FSWs in MENA and there is evidence of propagation of these infections between FSWs and their clients . In many countries indeed, STD clinic attendees repeatedly reported acquiring their infection through paid sex [94,157–159].
Levels of comprehensive HIV knowledge among FSWs in MENA varied across the region, with both high and low levels being documented in different settings. However, regardless of the proportion of FSWs who have good knowledge of HIV/AIDS, many misconceptions about its mode of transmission were reported [45,95], and a significant percentage of FSWs reported not feeling at risk of infection [76,108,131].
Overlapping risks among high-risk groups
Considerable levels of risk behavior overlap are noted among the three high-risk groups in MENA. IDUs are mostly sexually active and engage in both heterosexual [2,22,76,160] and male-male sexual contacts [67,73,161]. Multiple sexual partnerships of different kinds, contacting FSWs and exchanging sex for money or drugs, are not uncommon among IDUs in MENA [2,27,63,67,129,162].
Similarly, MSM risk behaviors overlap considerably with heterosexual sex and injecting drug risk behaviors. Overall, 5–17% of MSM were married to females in different studies [45,81,88,136] and a higher proportion reported having sex with females or FSWs [45,48,76,130]. Also MSM in MENA reported somewhat high levels of drug use both in its injecting and noninjecting forms .
Although generally the levels of risk behavior among FSWs in MENA appeared to be on the low side, the subgroups of FSWs engaging in overlapping sexual and injecting risk behaviors may be particularly at high risk of HIV. Several studies have indeed documented injecting drug use among FSWs at a rate of 1–10% [13,45,76,81,150,163], whereas sexual contacts with IDUs as clients, partners or husbands were reported at higher rates of 10–36% [82,88,155,164].
Potential bridging populations and HIV
Bridging populations are defined as the populations that bridge HIV infections from the high-risk groups to the low-risk general population. These conventionally include clients of FSWs and sexual partners of IDUs and MSM, in addition to other groups such as truck and taxi drivers, military personnel, fishermen, sailors, and migrant labor. HIV point-prevalence surveys among potential bridging populations are still scarce in MENA. Main sources of data for this group are limited number of cross-sectional bio-behavioral surveys, HIV testing data, and countries' case notification reports.
Although a sizable segment of MENA populations belong to potentially bridging populations [165–169], a clear dynamical contribution of these groups to HIV transmission in MENA is not evident. This is particularly the case for sexual partners of high-risk populations and partners of clients of FSWs, as these are usually women who rarely engage in nonspousal partnerships , and probably seldom spread the infection further. Furthermore, the low HIV prevalence among FSWs in MENA limits the role of their clients in bridging HIV infection to the general population. Therefore, bridging populations have been labeled here as ‘potential’ bridging populations to highlight the specific nature of their context in MENA.
HIV point-prevalence surveys among potential bridging populations are summarized in Table 2 [171–179].
In most countries, HIV prevalence among selected potential bridging populations was often nil or 1.0% or less, with the exception of Sudan, where rates of 2.9 and 14.0% were reported among military personnel and clients of FSWs, respectively (Table 2). The low HIV prevalence found in available surveys, along with the context of HIV spread in high-risk groups, suggests that HIV transmission may still be limited through bridging populations in MENA, apart from Djibouti, Somalia, and Sudan.
Nevertheless, existing evidence suggests considerable levels of sexual risk behavior among potential bridging populations in MENA . Contact with FSWs appeared to be substantial, with rates sometimes reaching up to 35% such as among urban migrant males in Pakistan [167,169]. Polygamy and having multiple sexual partners also appeared to be common, with a considerable percentage reporting premarital or extramarital sex [163,175,177,180,181]. For example, in Djibouti, 14% of truck drivers and 22.7% of dockers were in polygamous unions ; in Sudan, 57.1% of military personnel had multiple partners ; and in Pakistan, 63.5% of urban migrants ever had sex with one or more nonmarital partners [168,169]. Several studies have also documented male-to-male contacts with men [5,167–169,175] as well as with MSWs or hijras such as in Pakistan [76,167]. Condom use was reported at very low levels of less than 10% in the majority of the countries [76,167,175,177,181].
General population and HIV
HIV prevalence in MENA has been measured in different general population groups, such as pregnant women and blood donors, as well as in few national and population-based surveys. Main sources of data for this group are cross-sectional serological surveys and HIV testing data. Some of the results of these point-prevalence surveys are presented in Table 3 [183–256].
Available data indicate that HIV prevalence in the general population is at very low levels of much less than 1% in all MENA countries apart from Djibouti, Somalia, and Sudan (Table 3). In Djibouti, HIV prevalence was reported to be around 3% nationally among ANC attendees and among blood donors [188,189,191]. Lower rates were observed of about 1% in Somalia, although in one setting, it was at 2.7% among pregnant women . Southern Sudan is of particular concern and could be already in a state of general population HIV epidemic, although conclusive evidence is still lacking. Rates of as low as 0% and as high as 11% have been reported at various locations among ANC attendees and blood donors in southern Sudan [244,245].
Sexual behavioral data among the general population in MENA remain rather limited, with, to our knowledge, no nationwide sexual behavior survey being ever conducted in the region. However, available data from several small-scale investigations indicate that sexual risk behaviors are present but relatively at low levels compared to other regions . Multiple partnerships, premarital and extramarital relationships, casual sex, and contact with FSWs are reported in most countries but with significant variations . Youth appear to engage to some extent in sexual risk behavior but not at levels seen in other regions . Although polygamy is common in MENA, it appears to be in decline with estimates usually ranging between 3 to less than 20% [14,137,229,257–260]. However, nonconventional forms of spousal relationships have been increasingly emerging in MENA such as zawaj al-muta'a (temporary marriage), zawaj urfi (clandestine marriage), and zawaj al misyar (travelers' marriage) . These nonconventional types of marriage possibly could be perceived as legitimization of premarital and extramarital sex and may be increasing the risk of STI transmission among those involved in such marriages [2,261].
Contrary to widely held perception of very limited data, there is a considerable amount of epidemiological data on HIV in MENA. Nevertheless, data are fragmented, lack integration, and are amorphous. The nature of evidence is best exemplified by shattered glass. Numerous studies and point-prevalence surveys are distributed among different disciplines and stakeholders at the local, national, and regional level with no coherent integration, synthesis, and analysis. As part of the systematic search, we have identified hundreds of studies, databases, focused assessments, and reviews that have never been published in scientific publications nor are easily or widely accessible. A large amount of data and studies continue to be disseminated within small circles at the national and regional levels in the form of confidential and nonconfidential reports and unpublished data.
However, the large sums of available data are not necessarily representative and are often not collected using standard accepted surveillance methodologies. A large fraction of data originates from facility-based surveillance on convenient samples of the population. It is often not clear whether internationally accepted ethical guidelines for research on humans were strictly followed in the conduct of studies. Generally speaking, HIV epidemiologic evidence in MENA is highly heterogeneous in terms of quality but, overall, of limited quality. Fortunately, the quality of data has been steadily improving in recent years, although the availability of data and HIV research capacity vary substantially from one country to another. Iran and Morroco, despite many limitations, continue to be a regional leaders in HIV research and HIV/AIDS response, with several countries such as Pakistan and Sudan catching up in building their capacity within the last few years.
Despite the limitations of available data, the diverse sources of data were consistent on the overall epidemiologic picture delineated in this article. There is no evidence for an HIV epidemic in the general population in any of the MENA countries, except possibly for southern Sudan . It is worth noting that south Sudan has sociocultural attributes that are distinct from the rest of MENA countries and the epidemic in this subregion is probably best understood in terms of the context of HIV epidemiology in neighboring sub-Saharan countries such as Kenya and Uganda.
The general pattern in MENA countries points toward growing epidemics in high-risk populations including IDUs, MSM, and, to a lesser extent, FSWs . Table 4 summarizes the current status of the HIV epidemic in MENA countries based on the available and synthesized evidence. The limitations of the surveillance systems in MENA and the scarcity of reliable data are manifest as the status of the epidemic remains unknown in the majority of the risk groups for each country. This testifies to the heterogeneity of available evidence in the region.
Commercial heterosexual sex networks seem to be the major drivers of substantial HIV transmission only in Djibouti, Somalia, and Sudan due to the large size of the commercial sex networks in these settings and to the high levels of risk behavior practiced in these networks. Similar heterogeneities apply to the rest of high-risk groups. Whereas injecting drug use is large in scale in Iran and Pakistan and continues to be the major driver of the HIV epidemics in these countries, it appears to be smaller in scale and have a minor role in other MENA countries. The nature and levels of HIV spread among MSM remains, in relative terms, the least understood in MENA.
HIV epidemic patterns
As can be seen from the description of HIV epidemiology in high-risk groups, there is substantial heterogeneity in HIV spread across MENA, and different risk contexts are present throughout the region. However, the HIV epidemic in MENA can be coarsely classified into two groups based on the extent of HIV spread. The first is the group of somewhat considerable HIV prevalence, which includes the three countries Djibouti, Somalia, and Sudan (mainly southern Sudan). The second group, labeled here as Core MENA Region, is the group of more limited HIV prevalence, which includes the rest of MENA countries. As the latter group consists of most MENA countries, HIV epidemiology here represents the main dynamics found in MENA.
Two main patterns describe HIV epidemiology in the Core MENA Region countries (Fig. 1). The first pattern can be seen in countries' case notification reports of diagnosed cases and is that of exogenous HIV exposures among the nationals of these countries, and HIV acquisition by their sexual partners upon their return. This pattern exists in all MENA countries at varying levels. In fact, there appears to be limited epidemic or endemic transmission of HIV in all population groups, including high-risk populations, in few MENA countries . The number of newly diagnosed HIV infections continues to be rather stable at low frequency, with the majority linked to sexual and injecting exposures abroad [62,262]. For example, in Jordan, 450 out of 501 notified HIV/AIDS cases by 2006 were acquired abroad (Jordan National AIDS Program, 2008, personal communication), whereas in Lebanon, 45.36% of the cases in 2004 were linked to travel abroad . Mobility and migration are drivers of this pattern that has been persistent since the discovery of the epidemic and continues to be seen even among recent HIV acquisitions. This pattern of exogenous HIV exposures is not dissimilar from the pattern of exogenous exposures seen in most countries in the world, but it has importance in some MENA countries as the only observed pattern in absence of sustainable considerable high-risk group or general population HIV epidemics. Still, conclusive evidence as to whether exogenous HIV exposures are the only pattern of HIV transmission in these few MENA countries is still lacking , mainly due to poor surveillance of high-risk populations.
The second pattern of HIV epidemiology in Core MENA Region is that of concentrated HIV epidemics among some of the high-risk groups (HIV prevalence consistently exceeding 5%). There is already documented evidence for concentrated epidemics among IDUs  and suggestive evidence for concentrated epidemics among MSM in some countries such as Egypt , Sudan (north Sudan) , and Pakistan [81–83]. There is no evidence for concentrated HIV epidemics, at the country level, among FSWs in Core MENA Region countries.
Djibouti, Somalia and southern Sudan stand out from the Core MENA Region as having a state, or near state, of generalized HIV epidemics. Yet, most infections in these countries seem to be concentrated in high risk groups and bridging populations, more specifically in commercial heterosexual sex networks (Fig. 1) . There is no evidence of sustainable general population epidemic in these countries (apart from possibly southern Sudan); however the size of the commercial heterosexual networks in these settings is large enough to support an epidemic with a prevalence exceeding 1% in the population as a whole .
Several protective factors appear to have slowed and limited HIV transmission in MENA relative to other regions. A key factor is male circumcision, which has an established 60% efficacy against HIV heterosexual acquisition [263–265]. Male circumcision is nearly universal in MENA . Southern Sudan is the only part of MENA where this practice is not the norm . This could be partially contributing to the considerable spread of HIV in southern Sudan relative to the rest of MENA. The extensive coverage of male circumcision in MENA suggests limited potential for a sustainable HIV epidemic in the general population .
The influence of Islamic cultural traditions on the cultural and social traditions of MENA is another possible limiting factor to the spread of HIV in this region. Although from the available literature, one cannot definitely conclude that Islamic cultural traditions have reduced HIV transmission in the region, several observations, including some quantitative studies, support the protective role of Islamic cultural traditions. Being a Muslim has been repeatedly associated with lower risk behavior [269–274] and lower HIV prevalence [4,270,275–283], in both Muslim-majority countries as well as in Muslim minorities in predominantly non-Muslim nations [4,284]. Islamic cultural traditions have been cited as a protective factor even after adjustment for male circumcision . In fact, in addition to requiring male circumcision, Islam promotes a line of behavior that is in concordance with several themes of HIV/AIDS prevention including prohibitions against premarital and extramarital sex , prohibitions against alcohol consumption with alcohol's strong association with higher risk behavior [278,287,288], closed sexual networks of monogamous or polygamous marriages , among others. It is worth noting though that, despite being heavily influenced by Islamic traditions, parts of the region are experiencing a sociocultural transition at varying pace that is leading to more tolerance and acceptance of practices such as premarital sex and extramarital sex . Counting only on the ‘cultural immunity’ of religious and traditional mores  is, therefore, not enough to prevent an HIV epidemic in the region.
Vulnerability of sexual partners of high-risk group members
A key highlight of HIV epidemiology in MENA is that of the vulnerability of spouses and sexual partners of high-risk group members. Women are especially vulnerable, as most high-risk behaviors in MENA are practiced by men and the majority of infected women acquired the infection through their husbands or sexual partners. For example, 97% of HIV-infected women in Saudi Arabia acquired the infection from their husbands . Similarly, in Iran, 76% of HIV-infected women acquired the infection from their husbands who were predominantly IDUs [291,292]. Also, there appears to be a substantial gap in age in sexual partnerships between men and women in MENA, with women marrying older men. Intergenerational sex puts women at even higher risk of exposure to STI infections, including HIV .
Women who are sexual partners of high-risk group members appear to rarely engage in risk behavior and probably seldom bridge the infection to the rest of the population apart from occasionally to their own children through vertical transmission. Their limited role in HIV transmission dynamics could also be one of the factors behind the consistently very low HIV prevalence in the general population in MENA.
HIV epidemic potential in the Middle East and North Africa
The low HIV prevalence observed in some risk groups in MENA should not be interpreted necessarily as lack of HIV epidemic potential. The extreme within-country variation observed in the prevalence of HIV among different population samples is an indication of existing hidden subepidemics or potential epidemics in certain settings within any one country. Also, the heterogeneity in the availability of well designed studies across population groups and countries could be preventing the identification of hidden epidemics among some hard-to-reach high-risk populations.
The moderate to high prevalence of some proxy biological markers of risk behavior in MENA is another indicator of HIV potential in certain risk groups. For example, hepatitis C infection, which shares the parenteral mode of transmission with HIV, has been documented to be at moderate to high levels among IDUs in most MENA countries  compared to those reported in other regions . Recent rapidly growing HIV epidemics documented among IDUs in Pakistan [76,78,85,295], following many years of low HIV prevalence [41,75,77,296,297] affirms the epidemic potential for at least some of the MENA IDU populations. Similarly, HIV prevalence among hijras in one study in Pakistan was 0.0% in 1998, but syphilis prevalence was 37% [89,298]. This suggests substantial levels of sexual risk behavior and potential for HIV infectious spread in the event HIV is introduced into sexual networks involving this population. This seems to have been confirmed as recent data have shown some rapidly rising epidemics among MSWs and hijras in Pakistan [81–83]. There is also a pattern of increasing HIV prevalence among MSM in other regions with similar socio-cultural background to MENA countries such as in Indonesia in south-east Asia [299,300].
Apart from Djibouti, Somalia, and southern Sudan, the apparently lower levels of risk behavior among FSWs in MENA, in addition to the proven biological efficacy of male circumcision against HIV acquisition with its nearly universal coverage in this region, suggest a limited potential for massive or even concentrated HIV epidemics among FSWs in MENA . This, in turn, limits the role that bridging populations (mainly clients and partners of FSWs and sexual partners of IDUs and MSM) may play in HIV transmission in MENA. As pointed out earlier, a key characteristic of sexual partners of high-risk group members (mainly women) in this region is their vulnerability to HIV, rather than their role in HIV transmission dynamics. With all these factors interplaying, and if the existing social and epidemiological context in the region remains largely the same, it seems unlikely that the MENA region will experience a sustainable HIV epidemic in the general population in at least the foreseeable future, if ever. However, increasing economic pressures affecting, in particular, the large population of young people and ongoing political instability may lead to a rise in risk behavior practices and consequently HIV transmission. In a worst case scenario, the region may face up to a few percentage points prevalence in a few of its countries.
Although HIV prevalence levels in MENA are among the lowest globally, the nature of HIV epidemiology in MENA is no exception to HIV epidemiology in every other region apart from sub-Saharan Africa. HIV in MENA travels along the indigenous contours of risk and vulnerability just as in every other region. The HIV epidemic has not yet reached its epidemic potential in this region and there is an opportunity for prevention that should not be missed to control the epidemic . Missing this window of opportunity may entail a health and socioeconomic cost that the region, in large part, is unprepared for. Stigma associated with HIV/AIDS remains one of the major contributors for the region's unpreparedness to tackle the epidemic and a key barrier towards rational evidence-based policymaking.
The analytical insights drawn from this synthesis of thousands of studies and data sources indicate that there is no escape from the necessity of expanding scientific research on HIV in MENA to address the gaps in our knowledge of the status of the epidemic in different risk groups as manifested in Table 4. In particular, robust surveillance systems need to be developed to monitor HIV transmission, especially among high-risk groups. Effective surveillance of most at-risk populations is essential to detect emerging epidemics at an early stage. This would facilitate targeted prevention at an early phase of an epidemic. Monitoring recent infections and examining the nature of exposures could also be useful in detecting emerging endemic chains of transmission within MENA populations.
Despite many limitations, there is increasingly a political feasibility for implanting and scaling up of interventions including those among high-risk groups . However, current efforts in MENA continue to be focused on awareness-raising activities among the general population, which is the group at the lowest risk of HIV infection. Resources need to be prioritized for interventions among those most at risk, irrespective of whether these groups are ‘culturally safe’ or not [13,303]. Developing creative mechanisms for working with high-risk groups, even if discreetly, need to be explored. A successful formula for HIV efforts could be government organized nongovernmental organizations (GONGOs), where governments fund and support NGOs to discreetly provide services to high-risk populations. NGOs may enable governments to deal with high-risk groups indirectly, thereby avoiding political or cultural sensitivities in explicit outreach efforts among hidden and stigmatized populations [304,305].
Although countries need to address the structural factors that drive risk of exposure to HIV, the priority should be on addressing the direct factors that put individuals at risk of HIV exposure, as tackling structural factors takes time and is beyond the control of the public health community . Access to testing, care, and treatment services need to be expanded substantially. Prevention efforts need to capitalize on the strengths represented by cultural traditions, and be culturally sensitive, while fostering effective responses to the epidemic [1,307,308]. One of the countries in the region, Iran, is already a world leader in harm reduction and has paved the way by showing how HIV prevention can be implemented within the cultural fabric of MENA and in consonance with its sociocultural values.
The MENA HIV/AIDS Epidemiology Synthesis Project was funded through a joint partnership of the World Bank, the MENA Regional Support Team (RST) of United Nations Programme on HIV/AIDS (UNAIDS), and the Eastern Mediterranean Regional Office (EMRO) of the World Health Organization (WHO). LJA and GM are also grateful for the Qatar National Research Fund for supporting this work (NPRP 08–068–3–024).
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