JAIDS Journal of Acquired Immune Deficiency Syndromes:
Epidemiology and Prevention
New Evidence on the HIV Epidemic in Libya: Why Countries Must Implement Prevention Programs Among People Who Inject Drugs
Mirzoyan, Lusine MD, MPH*; Berendes, Sima MD, MPH*; Jeffery, Caroline MA, PhD*; Thomson, Joanna MSc†; Othman, Hussain Ben MD‡; Danon, Leon PhD†; Turki, Abdullah A. MD*; Saffialden, Rabea DipPH*; Valadez, Joseph J. PhD, DSc, MPH*
*Department of International Public Health, Liverpool School of Tropical Medicine, Liverpool, United Kingdom;
†Mathematics Institute, University of Warwick, Coventry, United Kingdom; and
‡National Centre for Diseases Control, National AIDS Program, Tripoli, Libya.
Correspondence to: Sima Berendes, MD, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA, United Kingdom (e-mail: email@example.com).
Supported by the European Commission under the terms of the project “Supporting the development and implementation of a National HIV–AIDS Strategy in Libya.” The sponsor of the study had no role in the study design, data collection, analysis, and interpretation, or writing of the article.
H.B.O. works for the Libyan National Centre for Diseases Control (NCDC), Ministry of Health, which is also responsible for the planning and implementation of the National HIV Strategy informed by the results of this article. The other have no conflicts of interest to disclose.
Authors' contributions: J.J.V. wrote the proposal and obtained funding; J.J.V., L.M. and S.B. designed the study protocol; L.M. led study preparations; J.J.V, L.M., and H.B.O. managed all reporting to Libyan governmental institutions; J.J.V, A.A.T, H.B.O., S.B., and C.J. contributed to the study preparations; L.M., A.A.T., and R.S. predominantly managed data collection;H.B.O., J.J.V., S.B., and C.J. provided technical assistance to the data collection; J.T., L.D., S.B., and C.J. analyzed data; J.J.V., L.M., and R.S. supported the data analysis and all the authors contributed to the interpretation of results;S.B. wrote the first draft of the article; all the authors contributed to the writing of the article, and read and approved the final article.
This publication has been produced with the assistance of the European Commission. The contents of this publication are the sole responsibility of the authors and can in no way be taken to reflect the views of the European Union.
Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal's Web site (www.jaids.com).
Received September 06, 2012
Accepted December 20, 2012
Background: Libya had one of the world's largest nosocomial HIV outbreaks in the late 1990s leading to the detention of 6 foreign medical workers. They were released in 2007 after the Libyan Government and the European Union agreed to humanitarian cooperation that included the development of Libya's first National HIV Strategy and the research reported in this article. Despite the absence of sound evidence on the status and dynamics of Libya's HIV epidemic, some officials posited that injecting drug use was the main mode of transmission. We therefore sought to assess HIV prevalence and related risk factors among people who inject drugs (PWID) in Tripoli.
Methods: We conducted a cross-sectional survey among 328 PWID in Tripoli using respondent-driven sampling. We collected behavioral data and blood samples for HIV, hepatitis C virus, and hepatitis B virus testing.
Results: We estimate an HIV prevalence of 87%, hepatitis C virus prevalence of 94%, and hepatitis B virus prevalence of 5%. We detected injecting drug use–related and sexual risk factors in the context of poor access to comprehensive services for HIV prevention and mitigation. For example, most respondents (85%) reported having shared needles.
Conclusions: In this first biobehavioral survey among PWID in Libya, we detected one of the highest (or even the highest) levels of HIV infection worldwide in the absence of a comprehensive harm-reduction program. There is an urgent need to implement an effective National HIV Strategy informed by the results of this research, especially because recent military events and related sociopolitical disruption and migration might lead to a further expansion of the epidemic.
Sound evidence on the status and dynamics of Libya's HIV epidemic is urgently needed, to inform decision makers and guide the planning and implementation of the country's first national HIV strategy. Limited scientific research on the scale of the HIV epidemic in the Middle East and North Africa constrain HIV-related policies and programs in the region despite a growing awareness of the need to act while the window of opportunity for containing the epidemic is still open.1,2 Such knowledge gaps are particularly profound in Libya, although the nation became aware of the threat of HIV in the late 1990s due to what was purported to be the world's largest documented nosocomial HIV outbreak.3,4 This tragic event and the related detention of 6 foreign medical workers caused an international public and political outcry.5 The case was resolved in 2007 with the release of the detainees and an agreement between the Libyan Government and the European Union on humanitarian cooperation that included the development of Libya's first national HIV strategy and the research reported in this article.6 The development of an effective national strategy based on sound evidence has become all the more relevant due to the recent political military events; warfare, sociopolitical transition, and migration may increase vulnerability of the population to HIV. There is also the risk of the potential bridging of the infection to other high risk groups, such as men having sex with men, female sex workers, and their clients, and spouses of persons engaged in high risk behavior.7,8
No peer-reviewed original publications exist that examine HIV prevalence and risk behaviors in Libya. The fragmented evidence derived from existing national data that had been inaccessible to the international community suggests the “possibility, but no direct empirical evidence,” of a concentrated epidemic among people who inject drugs (PWID) in Libya.3 For example, 90% of reported HIV cases are attributed to injecting drug use (IDU).9 The existing limited data on PWID mainly originate from government facilities, such as hospitals, drug-treatment centers, and prisons. Facility-specific studies capture only a small fraction of the target population, because they do not access those PWID who have not been convicted for drug use and who are not on treatment, or who rather seek treatment in the private sector or abroad due to fear of stigma and persecution. So far, no internationally accepted surveillance methodologies have been applied to measure HIV, hepatitis B virus (HBV), and hepatitis C virus (HCV) prevalence among PWID in Libya.3,10 There are also no published studies on related risk behaviors, such as needle sharing and condom use that estimate PWID vulnerability to HIV infection and the risk of transmission to other vulnerable groups and the general population in Libya.11,12
In collaboration with the National AIDS Program, we conducted the first biobehavior surveillance survey (BBSS) on HIV in Libya. We present findings on the HIV, HBV, and HCV prevalence, and on associated behavioral risk factors among PWID in Tripoli with a view to informing near term policy making.
Study Design and Participants
We implemented a cross-sectional study among PWID in Tripoli, Libya, using respondent-driven sampling (RDS), as an effective method to sample hard-to-reach populations.13–15 Male and female PWIDs were eligible to join the study if they had engaged in injection drug use during the past month, resided, worked or studied in Tripoli, were at least 15 years old, and had a valid referral coupon.
We conducted the study at a single site during July 17–September 19, 2010. Sampling began with 7 initial participants (or seeds) identified during an initial mapping exercise and outreach work. The seeds initiated the recruitment chains by distributing up to 3 recruitment coupons to their peers and referring them to the study site. Upon enrollment, the participants responded to a standardized questionnaire through a face-to-face interview, received pretest counseling, underwent blood draws, were given the opportunity to see a doctor for sexually transmitted infections (STI), and had the option to obtain HIV rapid test results and posttest counseling during the first visit, and HBV and HCV results (available within 2 days) during a second visit. They then received a primary financial compensation (35 LD or 15£) to cover their time and transportation. An additional secondary compensation payment (12 LD or 6.2£) was given at a later stage for each peer they recruited. Participant recruitment continued until the estimated sample size was exceeded.16
Structured questionnaires used IDU- and HIV-related questions based on internationally recognized and standardized indicators and instruments.17,18 RDS-specific questions elicited information on personal network size, and reciprocity of the relationship between recruiter and recruit.13,15,19,20 The questionnaires were translated from English into Libyan colloquial Arabic and French, backtranslated for verification, and refined during pretesting. HIV rapid tests were performed immediately at the study site, and blood samples for HBV and HCV testing were transferred daily to a central reference laboratory.
We used 3 methods (RDSI/DS, RDSII, and RDSII/DA13,21) to estimate population proportion estimates for all variables, and a resampling procedure to estimate confidence intervals in MATLAB (v.2010b).16 We also performed a multivariate logistic regression analysis to identify statistically significant correlates of HIV infection. The analysis was conducted in Stata v.12 using RDSAT-generated survey weights for HIV infection.22
Approval for the study was obtained from ethics committees in the United Kingdom and Libya, and from the Libyan Ministry of Security. All study participants provided oral informed consent.
More details on the study design, procedures, measures, analysis, and ethics are given in Supplemental Digital Content 1 (see http://links.lww.com/QAI/A387).
A total of 328 eligible survey participants were recruited through up to 10 recruitment waves generated by 7 seeds (see Figure S1, Supplemental Digital Content 2, http://links.lww.com/QAI/A387). Equilibrium (the point at which the sample proportion changes only very minimally with continued recruitment) was reached for each reported indicator. The 3 methods for estimating population proportions produced similar results (see Tables S1–5, Supplemental Digital Content 3, http://links.lww.com/QAI/A387). In Tables 1 and 2, we report the RDSII/DA estimates only.21 Results on sociodemographic characteristics are given in Table 1. All study participants were Libyans.
HIV, HBV, and HCV Prevalence
The prevalence of HIV among PWID in Tripoli was 87% (Table 1). Similarly, 94% tested positive for HCV and 83% were HIV/HCV coinfected. In contrast, the HBV prevalence was about 5% with 4% of PWID being HIV/HBV coinfected.
Thirty-four percent of respondents injected for a period of >15 years, 84% used Subutex for injecting and 54% injected at least once a day (Table 2). Eighty-five percent of PWID reported having shared needles in the past, 29% in the past month, and 18% at last injection. More than a third of all PWID reported having shared drugs in a high equipment sharing situation (ie, shooting galleries, prison, or as injection by a dealer) in the past month. Of the 23% of respondents who reported having had sex during the past month (among those who ever had sex) about two-thirds used a condom. Condom use varied with the type of sexual partner, but sample sizes for these indicators were small. Twelve percent of PWID reported having had symptoms of STI and about 5% had experienced sexual and 9% physical violence in the past year.
Access to Services, Knowledge, and Attitudes
Access to HIV prevention services among PWID was limited (see Table S5, SDC3, http://links.lww.com/QAI/A387). Although >90% of PWID indicated that they would always be able to access new needles when needed, the main source of needles was pharmacies (97%) rather than health facilities or outreach workers; About 60% of PWID accessed drug abuse–related treatment or assistance during the past year; however, none of the health or drug-abuse rehabilitation facilities in Libya offered opioid substitution therapy (OST), and the type of treatment received was mostly restricted to detoxification (62.5%).
Most PWID (88%) said they can always access condoms when needed, but few (2.6%) received condoms through outreach services, drop-in centers or health facilities during the past year. Almost all PWID (95%) knew where to get tested for HIV, and about half of them received a test and learned the result in the past year; 29% of PWID confirmed that they got tested voluntarily, meaning that they were not directly forced to be tested.
Only 45% of PWID succeeded in both correctly identifying ways to prevent HIV transmission and rejecting major misconceptions about HIV transmission. STI-related knowledge was poor with only about 5% of PWID being able to name most common STI symptoms. Despite the high HIV prevalence, only 55% of PWID revealed an absence of HIV-related stigma as assessed by a series of standard questions.
Factors Associated with HIV Seropositivity
The adjusted multiple logistic regression analysis revealed that the odds of HIV infection were 7.9 times higher among people injecting for >15 years compared with those injecting for <10 years (P = 0.001), and 3.7 times higher among those who ever shared needles (P = 0.015, Table 3). For details see Table S6, Supplemental Digital Content 3 (http://links.lww.com/QAI/A387).
This first BBSS in Libya not only provides sound evidence for the classification of Libya's HIV epidemic as at least ‘concentrated among PWID’ but also reveals the disturbing scale of the problem by detecting an alarmingly high level of HIV infection.3,23–25 Existing limited evidence puts our results into context. The National AIDS Program reported HIV prevalence among the general population as being below 1%11 and a recent systematic review3 indicated the “possibility, but no direct empirical evidence” for a concentrated epidemic among PWID in Libya. An unpublished report displayed the spread of HIV among PWID over time at a rehabilitation center indicating no cases of HIV among 400 PWID in 1996, but a sudden increase 4 years later, with 50% of 1182 PWID being infected.9 A recent internal report revealed that 84% of 493 PWID from Tripoli admitted to the only drug-treatment center in the country in 2009–2010 were HIV positive.26 Although these data are not necessarily representative of the actively injecting population in the community, they are in line with the HIV prevalence of 87% among PWID in our study.
Results of this shocking scale are comparable only with very few rates in other regions with rates in neighboring countries being substantially lower, for example, 2.6% in Tunis27 and 7.7% in Cairo.28 A recent systematic review23 reported HIV prevalence rates among PWID of >40% for 9 out of 61 countries with the highest midpoint prevalence in Estonia (72.1%).
The behavioral results partly explain the high HIV and HCV prevalence rates among PWID, by revealing a number of risk factors in the context of poor access to comprehensive services for HIV prevention and mitigation. Eighty-five percent of PWID had shared needles in the past, 29% in the past month, and 18% at last injection. Adjusted logistic regression results showed that not only PWID with an experience of needle sharing but also those who injected for >15 years were more likely to be HIV positive. This information suggests a long history for the HIV epidemic in Tripoli. However, the proportion of current sharing of needles and other injection equipment is still far too high and poses an ongoing risk of HIV transmission. Additional sexual risk behavior not only adds to the overall risk but might also lead to the spread of HIV, HCV, and HBV to other subpopulations.8 Although due to low sample sizes our data on condom use are difficult to interpret, other indicators indicate an elevated risk of sexual transmission, such as the level of reported STIs, and history of sexual violence.29
Our results are in line with findings from a qualitative study from 2003 to 2004 showing that 70% of PWID in a rehabilitation program reported previous engagement in risk behaviors.30 It also suggested possible explanations for the explosive elevation of HIV transmission among PWID, including an increase in the number of heroin addicts in the late 1990s, a transition from drug smoking to injection coupled with a lack of HIV awareness,26,30 and reduced availability of syringes in pharmacies since 1997. Although the majority of our study respondents indicated they can access new, unused needles when needed, most of them indicated pharmacies as their only source. However, since the mid-1990s, pharmacists have been reluctant to sell needles to suspected drug addicts due to the perceived or real existence of a law that had been introduced in the mid-1990s restricting the sale of needles.26 Because accounts by different stakeholders on this topic were contradictory, more research is needed to explain this fact. Further clarification is also needed on what respondents perceived as ‘voluntarily’ undergoing HIV testing in the absence of voluntary counseling and testing sites and in the context of mandatory screening for health certificates, required for employment, marriage, and driving licenses.11
So far, prevention efforts in Libya have focused primarily on awareness campaigns among the general public, fear-based education in schools, and training of selected professions.11 Few self-support groups assisted in accessing tools and services for HIV/AIDS prevention and care, and drug rehabilitation treatment. More than half of all PWID in our study had received drug abuse-related treatment in the past, but none of the drug-treatment facilities in the country offered OST. Although the effectiveness of OST and needle exchange programs has been proved,23 they still meet resistance among key stakeholders, so that the country lacks a comprehensive harm-reduction program.11,31
Although we surmounted challenges related to the lack of established links with PWID networks, difficulties remained in identifying female seeds and recruiting female PWID, which is probably related to both, their relatively small number in Tripoli, and greater stigma attached to female PWID. The latter has also been observed in other countries.32 It is interesting that most PWID in our study were >35 years old, which might relate to younger PWID, should they exist in Libya, being less connected and more hidden than older PWID. A more likely alternative explanation could be that the younger generation is less likely to inject drugs due to a positive effect of the education campaigns in schools or due to the higher cost of Buprenorphine, which has replaced Heroin in Tripoli's black market. Future research could shed light on drug use patterns, and on the dynamics of shifting from noninjecting to IDU.12 The fast recruitment into our study indicates good network connectivity and possibly a large number of PWID in Tripoli, but further research is needed to determine the IDU prevalence in Tripoli and other cities, in which so far IDU has been much less frequent. Reports indicate that heroin dealers have recently moved from Tripoli to Benghazi to establish a market place.26 This development and recent conflict-related changes call for an extension of BBSS to other areas and vulnerable groups, including men having sex with men, female sex workers and their clients, sex partners of PWID, and migrant populations.
Our findings constitute a crucial first step to tackle a major crisis. Swift and decisive action is essential, given that in the current postconflict era additional factors may have escalated the epidemic. Increased migration, sexual and gender-based violence, the disruption of infection control and blood safety system, and a nationwide stock-out of antiretroviral drugs raise the specter for an expansion of the epidemic and the development of drug resistance with catastrophic consequences for individuals and the population at large.11 There is an urgent need for the implementation of a National Strategy that is informed by the results of this research, and by existing evidence of the effectiveness of harm-reduction interventions and international recommendations. In 2010, a series of high-impact publications fervently called on countries to abandon the myths and prejudices about HIV in drug users that hamper the role-out of evidence-informed, rights-based combination interventions that could avert as many as two-thirds of HIV infections associated with drug use.33–35 That year, a consensus statement of the Reference Group to the United Nations called for the scale-up of a comprehensive package of 9 harm-reduction interventions as outlined by the World Health Organization.23 For this to be possible, many countries including Libya first need to adapt their policy and legislation and shift from an ineffective approach that is hostile toward PWID, to an effective one that is based on scientific evidence and human rights.23,33
The authors gratefully acknowledge Ms Amal el Karouaoui, Dr Lisa G. Johnston, Prof Mehdi Karkuri, Dr Abdalla Toufik, Dr Simon D.W. Frost, Mr William Vargas, and Prof Patricia Cane for their consultancy work. The authors are also very grateful to Prof Abdulhafid Abudher, then director of the NCDC, Dr. Omar El Ahmar, director of the NCDC laboratory and his team, and to Dr Nabil Abumaer, then head of Department of HIV/AIDS Treatment-Management. The authors express their great appreciation to Mr Abdullah Aljadi, Mr Hussein Rahiel, Mr Owais Al Wahedi, Dr Fannir Abdallah, Ms Sarah Moxon, Dr Gibby Koshy, and all other members of the study team in Tripoli, and the data management teams at the NCDC in Tripoli and at LSTM. Last, but not least, the authors wish to thank all those who participated in this survey for their time and trust.
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HIV; injecting drug use; harm reduction; respondent-driven sampling; North Africa; Libya
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