Overview of HIV molecular epidemiology among people who inject drugs in Europe and Asia

Highlights

• Molecular studies reveal patterns of HIV spread among people who inject drugs (PWID).

• A_FSU, B_FSU (IDU-B), and CRF03_AB produced big epidemics in Former Soviet Union states.

• Subtype G and CRF14_BG caused big epidemics in Portugal/Spain.

• Transmission clusters (B, A, F1, CRF14_BG, CRF35_AD) were observed in Greece/Romania.

• CRF35_AD is the most prevalent clade among PWID in Afghanistan/Iran.

• Recombination hotspots in South-East Asia have been generating several recombinants.

Abstract

HIV strains continuously evolve, tend to recombine, and new circulating variants are being discovered. Novel strains complicate efforts to develop a vaccine against HIV and may exhibit higher transmission efficiency and virulence, and elevated resistance to antiretroviral agents. The United Nations Joint Programme on HIV/AIDS (UNAIDS) set an ambitious goal to end HIV as a public health threat by 2030 through comprehensive strategies that include epidemiological input as the first step of the process. In this context, molecular epidemiology becomes invaluable as it captures trends in HIV evolution rates that shape epidemiological pictures across several geographical areas.

This review briefly summarizes the molecular epidemiology of HIV among people who inject drugs (PWID) in Europe and Asia. Following high transmission rates of subtype G and CRF14_BG among PWID in Portugal and Spain, two European countries, Greece and Romania, experienced recent HIV outbreaks in PWID that consisted of multiple transmission clusters including subtypes B, A, F1, and recombinants CRF14_BG and CRF35_AD. The latter was first identified in Afghanistan. Russia, Ukraine, and other Former Soviet Union (FSU) states are still facing the devastating effects of epidemics in PWID produced by A_FSU (also known as IDU-A), B_FSU (known as IDU-B), and CRF03_AB. In Asia, CRF01_AE and subtype B (Western B and Thai B) travelled from PWID in Thailand to neighboring countries. Recombination hotspots in South China, Northern Myanmar, and Malaysia have been generating several intersubtype and inter-CRF recombinants (e.g. CRF07_BC, CRF08_BC, CRF33_01B etc.), increasing the complexity of HIV molecular patterns.

Introduction

In 1981, unexpected cases of Kaposi sarcoma and Pneumocystis carinii (now known as jirovecii) pneumonia were diagnosed among young men who have sex with men (MSM) (Centers for Disease Control, 1981a, Centers for Disease Control, 1981b, Gottlieb et al., 1981). The United States (US) Centers for Disease Control and Prevention (CDC) carried out detailed investigations and soon defined the acquired immune deficiency syndrome (AIDS) hinting also at a viral etiology of the new disease (Centers for Disease Control, 1982a, Centers for Disease Control, 1982b). Human immunodeficiency virus (HIV), which causes AIDS, was eventually discovered in 1983 (Barré-Sinoussi et al., 1983, Gallo et al., 1984), but the scientific community soon realized that HIV had been spreading globally before the initial recognition of AIDS in the US. As a matter of fact, a stored sample collected in 1959 in Belgian Congo (now Democratic Republic of the Congo) tested positive for HIV (Nahmias et al., 1986, Zhu et al., 1998) and molecular investigations have shown that HIV was the result of cross-species transmissions from different primates that had taken place long before the first diagnoses (Gao et al., 1999, Keele et al., 2006, Sharp and Hahn, 2011, Van Heuverswyn et al., 2006). The most recent ancestor of the pandemic strain was probably circulating in human populations in Central Africa early in the 20th century (Faria et al., 2014, Korber et al., 2000, Worobey et al., 2008).

The toll of HIV has been high with millions of HIV infections and HIV-related deaths since the early 1980s (Faria et al., 2014, Sharp and Hahn, 2011). However, considerable progress has occurred over the years, which transformed HIV from a lethal disease to a chronic condition. Combinations of potent antiretroviral drugs (antiretroviral treatment—ART) in simplified regimens have significantly reduced morbidity and mortality, and people infected today can anticipate an almost normal life expectancy (Mills et al., 2011, Nsanzimana et al., 2015, Samji et al., 2013, The Antiretroviral Cohort Collaboration, 2008). Following intensified efforts by the World Health Organization (WHO) and the United Nations Joint Programme on HIV/AIDS (UNAIDS), around 17 million people worldwide were on ART in 2015 (UNAIDS, 2015, UNAIDS, 2016). In addition, treatment as prevention (TasP) (Cohen et al., 2011a) and pre-exposure prophylaxis (PrEP) (Grant et al., 2010, McCormack et al., 2015, Molina et al., 2015) are promising prevention approaches added to the existing arsenal of effective tools (Giannou et al., 2015) and UNAIDS has thus set an ambitious goal to end the HIV epidemic, as a public health threat, by 2030 (UNAIDS, 2015).

The first important element of a comprehensive strategy to contain HIV transmission and reach UNAIDS targets is public health authorities and other groups in each locale to understand their epidemic (WHO, 2015). Epidemiological input from HIV/AIDS reporting systems, biological surveillance, and behavioral surveys is necessary to get a deep understanding of local epidemics that could then help design, implement, and evaluate appropriate prevention measures (WHO and UNAIDS, 2013). In this context, molecular studies become invaluable as they shed light on parameters that traditional epidemiological techniques fail to capture.

This review summarizes evidence on circulating HIV-1 subtypes in people who inject drugs (PWID) in Europe and Asia. This geographical area includes countries with past or recent PWID-related outbreaks (Nikolopoulos et al., 2015a); countries with mega-epidemics in PWID such as Ukraine, Russia, China, and Malaysia (Wolfe et al., 2010); and hotspots of ongoing recombination processes (Lau and Wong, 2013).