Extremely low and sustained HIV incidence among people who inject drugs in a setting of harm reduction
Iversen, Jennya; Wand, Handanb; Topp, Libbyc; Kaldor, Johnd; Maher, Lisaa
aViral Hepatitis Epidemiology and Prevention Program
bBiostatistics and Databases Program, The Kirby Institute, University of New South Wales
cResearch Strategy Unit, Cancer Council NSW
dPublic Health Interventions Research Group, The Kirby Institute, University of New South Wales, Sydney, New South Wales, Australia.
Correspondence to Jenny Iversen, The Kirby Institute, University of New South Wales, Sydney NSW 2052, Australia. Tel: +61 2 9385 0900; fax: +61 2 9385 0920; e-mail: firstname.lastname@example.org
This study created a retrospective cohort by linking repeat respondents in a large, national, annual cross-sectional sero-survey to estimate HIV incidence among people who inject drugs (PWID) in Australia. The results indicate extremely low and sustained rates of HIV incidence (0.11 per 100 person-years) over almost two decades (1995–2012). The findings demonstrate that sustained prevention of HIV transmission among PWID is possible and suggest that the early establishment and rapid scale-up of needle and syringe programmes, at a time when background prevalence was low, likely contributed to the prevention of an HIV epidemic among Australian PWID.
Globally, an estimated 3 million people who inject drugs (PWID) live with HIV  and injection drug use accounts for around one-third of new infections outside continental Africa . In 2007, HIV prevalence estimates among PWID in 84 countries ranged from less than 0.01% to 72.1% . Although HIV prevalence estimates among at-risk populations are important for planning, implementing and evaluating prevention programmes , incidence is the indicator critical to assessing the current status of an HIV epidemic.
Two previous studies estimated HIV incidence among Australian PWID, with incidence of 0.17 and 0.21 per 100 person-years reported in the early 1990s [4,5]. Although the majority of HIV exposures in Australia are attributed to male-to-male sexual contact , HIV prevalence can escalate rapidly among PWID [7,8] and comprehensive HIV surveillance necessitates periodic examination of incidence in this population. This study utilized serological results of repeat respondents in a large, annual cross-sectional sero-survey of PWID to estimate HIV incidence over the period 1995–2012.
We used a retrospective cohort design, based on linkage of repeat respondents in the Australian Needle Syringe Program Survey (ANSPS). The University of New South Wales Human Research Ethics Committee granted ethical approval. Both ANSPS  and linkage methodologies  are described in detail elsewhere. In brief, the ANSPS is a national cross-sectional sero-survey, conducted annually at approximately 50 needle syringe programmes (NSPs) during a 1–2 week period. Consenting NSP attendees complete a brief self-administered questionnaire and provide a capillary dried blood spot for HIV and hepatitis C antibody testing. HIV antibody (anti-HIV) was detected using Genetic Systems HIV-1 ELISA (until 2010) or Murex 1.2.0 ELISA (Diasorin) (from 2011), with repeatedly reactive specimens subject to western blot confirmatory testing (New LAV Blot 1; Bio-Rad, Marnes-la-Coquette, France).
A deterministic method linked serological results of repeat respondents using a matching key created from partial personal identifying information . The cohort was created from respondents who participated in more than one round of annual ANSPS implementation who were HIV negative at first participation.
The primary outcome was incident HIV infection. Infection date was estimated as the midpoint between the last anti-HIV negative and first anti-HIV positive test. Follow-up time was the difference between this date and date of the initial negative test among those who acquired infection, and the difference between the date of last and first negative tests among respondents who did not acquire infection. HIV incidence rates and 95% confidence intervals (CIs) were calculated using the person-years method and groups compared using the log-rank test. All analyses were conducted using STATA, version 12 (Stata Corporation, College Station, Texas, USA).
Between 1995 and 2012, 34 069 ANSPS records contained anti-HIV test results and sufficient data to create a matching key. Of these, 8873 records (26%) from 3528 individuals were linked (Fig. 1). The proportion of linked respondents in annual samples ranged from 23 to 30% in all years except 1995 (17%). After excluding 38 respondents who tested anti-HIV positive at first participation, the cohort comprised 8763 records from 3490 individuals. The majority (70%) of linked respondents participated twice [interquartile range (IQR) two to three occasions]. The median time between repeat participation was 2 years (IQR 2–3 years). A previously documented comparison between single-occasion and repeat ANSPS respondents demonstrated no substantial differences between the two groups .
Among 3490 anti-HIV negative respondents in our cohort, 17 HIV seroconversions were observed between 1995 and 2012, yielding an incidence rate of 0.11 per 100 person-years (95% CI 0.07–0.17). The majority of incident infections (n = 12; 71%) occurred among MSM, with this group at significantly greater risk of seroconversion than non-MSM (0.83 vs. 0.03 per 100 person-years, respectively, P < 0.001). A minority of incident infections (n = 3) occurred among women. No other demographic or risk behaviours were associated with incident infection.
This is the first study of HIV incidence in a national sample of PWID in Australia. The results indicate an extremely low and sustained HIV incidence over almost two decades. Consistent with HIV transmission patterns among the broader Australian population [6,11], the majority of HIV infections occurred among PWID who identified as MSM. Although recent declines in HIV incidence among PWID have been documented in some industrialized nations, reports of low and sustained HIV incidence at less than 1.0 per 100 person-years are uncommon [12–16].
Australia is internationally recognized as one of the global leaders in harm reduction, with high syringe coverage compared with other countries . In response to the potential emergence of an HIV epidemic among PWID, Australia established free and legal NSPs in the late 1980s. By 1991, 6.3 million syringes  were distributed annually to an estimated 62 000 regular injectors , the equivalent of nearly 100 syringes per annum each. The Australian PWID population is estimated to have doubled in size between 1991 and 1999; however, annual syringe distribution increased five-fold over the same period, to 30.5 million syringes in 1999 .
Study limitations include possible misclassification of newly acquired infections. We also acknowledge that incidence estimates derived from linked records of repeat testers are heavily reliant on underlying testing patterns and inferences with respect to the broader population of interest require careful assessment [20,21]. This study was limited to PWID who attend NSPs; however, there is a substantial overlap between populations who access injecting equipment from NSPs and from other sources, and ANSPS sample characteristics reflect the broader population of NSP attendees . Nevertheless, only a quarter of ANSPS records were included in our cohort.
This study demonstrates that sustained prevention of HIV transmission among PWID over long periods is attainable. Factors contributing to this remarkable prevention effort likely include the early introduction of NSP when background prevalence was very low; rapid scale-up of syringe coverage; restricted population mobility to introduce HIV into Australian PWID networks; and the self-limiting nature of outbreaks where this occurred [23,24]. Serial cross-sectional sero-studies that target PWID should consider inclusion of mechanisms to support linkage of repeat individuals to enable the creation of passive retrospective cohorts to examine HIV incidence at no additional cost.
J.I. coordinated implementation of the study (from 2006), conducted the analyses and led the manuscript writing; H.W. assisted with analyses and study design; L.T. assisted with study implementation and interpretation of results; J.K. helped establish the original surveillance mechanism from which the data are drawn and assisted with data interpretation; L.M. led the study and provided oversight in design, implementation and interpretation of findings. All authors provided significant input into manuscript drafts. All authors declare no conflict of interest.
Conflicts of interest
This study was funded by the Australian Government Department of Health and Ageing. The views expressed in this publication do not necessarily represent the position of the Australian Government. Lisa Maher is supported by an NHMRC Senior Research Fellowship. John Kaldor is supported by an NHMRC Senior Principal Research Fellowship. The Kirby Institute is affiliated with the Faculty of Medicine, University of New South Wales. This work was undertaken on behalf of the ANSPS National Advisory Group and the Australian collaboration of Needle and Syringe Programs. The authors also wish to acknowledge the contribution of management and laboratory staff at St Vincent's Centre for Applied Medical Research and New South Wales State Reference Laboratory for HIV.
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