Since the increased risk of HIV infection for injecting drug users (IDUs) was first recognized in the early 1980s, a high prevalence of HIV has been reported among this group from many parts of the world [1,2]. In many sites HIV prevalence among IDUs has risen to 50% or more within 1 to 2 years of the introduction of the virus [1,2]. Such outbreaks continue to occur, and rapid spread has recently been documented among injectors in the newly independent states of the former Soviet Union . These outbreaks have been associated with increases in injecting drug use and have accompanied major socio-political changes .
A number of northern European countries and Australia have not experienced major outbreaks of HIV infection among IDUs and report either stable or declining trends in prevalence. In Amsterdam, for example, HIV prevalence declined in the 1990s , and in Australia prevalence is low  and may have declined in some areas . In these countries the timely introduction of comprehensive harm reduction measures, particularly needle exchange, is thought to have prevented the rapid spread of HIV . Furthermore, trends in the prevalence of HIV have reversed in a number of sites, for example Northern Italy and New York City, and have been attributed in part to behaviour change, improved access to treatment, and syringe distribution [9,10].
In response to the discovery of high levels of HIV infection among injectors in two Scottish cities , the United Kingdom's first needle exchanges were established through a number of local initiatives in 1986. Following the government-funded pilot programme in 1987 there was a rapid increase in the number and geographical spread of these services, and in 1997 it was estimated that there were almost 1500 outlets in England, 125 in Scotland, and 140 in Wales. These outlets distributed around 25 million syringes in 1997, which constituted a six-fold increase since 1991 . From 1986 onwards there was also an expansion of the prescribing of substitute drugs (mainly methadone) and a wide range of other HIV prevention activities, including outreach and health promotion, which are thought to have prevented a widespread outbreak of HIV among injectors . In the United Kingdom only 7% of the 56 000 HIV infections diagnosed by the end of 2002 were associated with injecting drug use .
Despite this response there have been recent indications of increases in injecting risk behaviour. Data from current injectors in contact with drug agencies indicate that the sharing of needles and syringes increased in the late 1990s , with around one-third reporting sharing between 1998 and 2000 compared with a quarter in earlier years. At the same time there have been reports of increases in the prevalence and incidence of hepatitis C and other infections, such as Group A Streptococci, among IDUs [15,16].
This paper examines whether the HIV epidemic among IDUs in England and Wales continues to be averted by examining time trends in prevalence between 1990 and 2003. It combines, for the first time, data from an ongoing surveillance of injectors in contact with drug agencies with data from a series of community-based surveys, to provide a cross-sectional data set containing almost 28 000 biological specimens.
IDUs in England and Wales were recruited into two complementary voluntary unlinked-anonymous survey programmes between 1990 and 2003.
Since 1990 between 29 and 59 drug agencies (both statutory and non-statutory agencies providing advice, support, harm-reduction or treatment services) from throughout England and Wales have been included in a series of annual surveys of IDUs . Briefly, clients who have ever injected are invited to participate by agency staff, and those who agree provide an oral fluid sample and self-complete a brief behavioural surveillance questionnaire. The questionnaire is available in Spanish, Portuguese and Italian, as well as English and Welsh. Participating drug agencies were selected to reflect the range of services provided for IDUs as well as geographic variations in reports of injecting drug use, and the sampling structure was reviewed on a regular basis.
IDUs who had injected in the last 4 weeks were recruited from community settings in London between 1990 and 1993, and again in 1996 [18,19] in London and seven other cities across England  in 1997/1998, and in London and Brighton in 2001/2002 . IDUs were recruited largely by indigenous fieldworkers [20,21], and recruitment sites included street locations, social venues, participants homes and syringe exchanges (that were not involved in the agency survey) [20,21]. Participants provided an oral fluid specimen and completed an interviewer-administered questionnaire.
The common data items collected by both types of survey in all years were age, gender, age at first injection, recruitment location (London versus elsewhere), and having had a voluntary confidential HIV test. In addition, participants who reported having had a voluntary confidential HIV test were asked for the result of their most recent test in all years of the community surveys and in the agency survey since 1995. Both survey programmes have collected data on injecting equipment sharing (both passing on and receiving of needles and syringes) and the agency survey has done so consistently since 1991. Oral fluid specimens were collected using either the Salivette device (up to 1997 for the agency survey and 1996 for the community surveys) (Starstedt Ltd, Leicester, UK) or EpiScreen device (from 1998 for the agency survey and 1997 for the community survey) (Epitope Inc, Beaverton, Oregon, USA). These specimens were tested for antibodies to HIV (anti-HIV) by HIV-1/2 GACELISA (Murex Diagnostics Ltd, Dartford, UK) by the same laboratory. Reactive specimens underwent further testing according to a proven algorithm that included a second enzyme-linked immunosorbent assay and western blot, and for which sensitivity and specificity approaches 100% .
In both surveys injectors could take part only once in a given year, and only limited demographic information was collected to prevent a theoretical possibility of deductive disclosure. Therefore, as IDUs could participate in more than 1 year, we have referred to results over time as participations rather than individuals. Associations between antibody positivity and covariates were explored by univariable analysis using χ2, and subsequently in a multivariable logistic regression model in which the likelihood ratio test was used to asses statistical significance. Interaction terms were included in the overall model if the P-value from the likelihood ratio test was less than 0.01 . In addition, trends in voluntary confidential anti-HIV testing were explored. All analyses were conducted using SPSS 10.0 (SPSS Inc., Chicago, Illinois, USA) and STATA 7 (Stata Corp, College Station, Texas, USA), and results are restricted to participations for those who had injected in the previous 4 weeks and who were aged between 15 and 49 years.
Force of infection
The force of infection, the rate at which susceptible (that is the sero-negative) IDUs acquire infection , was estimated by fitting a model to prevalence data by calendar year and injecting career length, separately for London and the rest of England and Wales. Thus, we considered that the force of infection (λ) may vary with time (t) and injecting career length (τ). The prevalence P(τ,t) quantifies the expected proportion of individuals with injecting career length τ who were antibody positive at time t. Prevalence in year t for those who have injected for τ years is
Equation (Uncited)Image Tools
where Λ(τ, t) is the cumulative force of infection in year t for those who have injected for τ years and is given by:
Equation (Uncited)Image Tools
This may be expressed relative to a baseline year T
Equation (Uncited)Image Tools
where τ0 = max(0,τ - (t- T)).
As the sample size in 1990 was small 1991 was used as the baseline year. The cumulative force of infection in 1991 Λ(1991,τ), is described by the function f(τ), where
Equation (Uncited)Image Tools
The force of infection from 1992 onwards is modelled as the product of a function describing its trend over time g(t) and a function describing its trend with injecting career length h(τ), where λ(t,τ) = g(t)h(τ).
Between 1990 and 2003, 27 932 specimens were collected from IDUs in England and Wales aged 15 to 49 years who had injected in the previous 4 weeks, of which 3628 (13%) were obtained through the community surveys, and a quarter (27%, 7569) from London. Three-quarters of the samples (76%, 21 125) were from males, 28% (7698) were from injectors aged under 25 years (median age, 28 years), and the median number of years injecting was 7 (range, 0 to 36 years).
The overall prevalence of anti-HIV for the 13 year period was 1.7% (461/27 932). There was a decline in prevalence from 5.9% (67/1132) in 1990 to 0.6% (14/2270) in 1996, a stable period until 2000, and some evidence of an increase to 1.4% (21/1529) in 2003 (Table 1). The decline in prevalence between 1990 and 1996 was seen in all length of injection groups during this period (Fig. 1): from 5.0% (15/298) to 0.2% (1/504) among those injecting less than 3 years, from 3.1% (9/288) to 0.4% (2/482) among those injecting for between 3 and 5 years, from 7.4% (31/420) to 0.2% (1/629) among those injecting for between 6 and 11 years, and from 9.5% (12/126) to 1.5% (10/654) among those injecting for 12 or more years. In all groups prevalence was relatively stable during the late 1990s until the increase in 2001/02 (Fig. 1): in 2003 HIV prevalence was 1.2% (3/260) among those injecting for less than 3 years, 0.3% (1/348) among those injecting between 3 and 5 years, 0.7% (3/437) among those injecting between 6 and 11 years, and 2.9% (14/484) among those injecting for 12 or more years.
Prevalence was higher in London (5.0% compared with 0.4% elsewhere in England and Wales), among those recruited in the community surveys (5.9% compared with 1.0% among those recruited in the agency survey), and among those who had a voluntary confidential HIV test (2.5% compared with 0.7% among those not tested) (Table 1). Prevalence was similar in females (1.8%) and males (1.6%). Prevalence increased with age from 0.8% (64/7698) among those under 25 to 2.4% (143/5907) among those aged 35 and over (data not shown), but as age and length of injecting career were highly correlated (Pearson correlation coefficient = 0.702, P < 0.001) age was not entered in to the multivariable model.
Five factors remained in the multivariable model after adjustment: survey year; recruitment location; length of injecting career; recruitment setting; and having had a voluntary confidential HIV test. For survey year, the univariate finding of increasing odds with earliest survey years remained although it was weakened; so for example, the adjusted odds ratio for anti-HIV positivity in 1990 compared with 1996 was 6.69 after adjustment compared with 10.10 before adjustment. The odds of anti-HIV positivity were higher for the survey years 1990 to 1995 and 2001 to 2003 compared with 1996 (Table 1). Higher odds of anti-HIV positivity were also associated with recruitment in London, longer lengths of injecting career, recruitment in the community survey, and ever having had a voluntary confidential HIV test.
Interaction terms between three variables (survey year; recruitment location; and length of injecting career) were fitted, although only one, between location and survey year, approached significance (P = 0.0247). Results are presented in Figure 2, and suggest that the recent increase in prevalence may be concentrated in London.
Overall 54% (15 066/27 932) of injectors had ever had a voluntary confidential (named) HIV test, and this proportion remained relatively constant over the 13-year period (it was lower in 1990 at 49% [550/1132; odds ratio (OR), 0.81; 95% confidence interval (CI), 0.70-0.94] and higher in 2003 at 60% (920/1529; OR, 1.19; 95% CI, 1.04-1.37) compared with 54% (1235/2270) in 1996 (OR, 1.00) after adjusting for years injecting, gender, recruitment setting, recruited in London, and anti-HIV). Of those testing anti-HIV positive, 81% (371/461) reported having a voluntary confidential HIV test at some time, but as sample sizes for the individual years were small a trend over time could not be discerned. Of those who reported the results of their last HIV test, 75% (193/259) of those with antibodies to HIV reported that they had tested positive and were therefore aware of their infection: in 2002/2003 69% (25/36) reported that their infection was diagnosed.
Force of infection
The force of infection by injecting career length and recruitment location over the period 1992 to 2002 is shown in Figure 3, which suggests that the force of infection is highest in London and among the most recent initiates, those with a duration of injecting under 1 year, and that the force of infection in London has increased over time. In London, the force of infection among new initiates was 0.008 (95% CI, 0.002-0.020) from 1992 to 1997, and 0.028 (95% CI, 0.016-0.045) during the period 1998 to 2003, with the force of infection for IDU injecting careers longer than 1 year being 0.13 times lower across all time periods. Outside London, no trend over time was detected during the period 1992 to 2003, although the force of infection was greatest for new initiates 0.0012 (95% CI, 0.0006-0.0023) compared with more experienced IDUs 0.0001 (95% CI, 0.00001-0.00058).
The increased level of needle and syringe sharing reported previously was sustained through to 2002 ; with 31% (123/399) in London and 29% (311/1,093) elsewhere reporting needle and syringe sharing in the previous 4 weeks.
This analysis indicates that HIV prevalence among IDUs in England and Wales declined during the early part of 1990s before stabilizing between 1996 and 1999. However since then it has increased. Although the current prevalence of around 1.5% is low when compared with many developed, developing and transitional countries [1,2], it is almost twice that during the period 1996 to 2000. This recent increase appears mainly to be concentrated in London, although reported sharing behaviour is uniformly high across the country.
Very few HIV infections were detected among short-term injectors during the period 1994 to 1999 suggesting little ongoing transmission at this time. However, in more recent years prevalence has risen among this group suggesting that incidence may have increased. This is supported by the force of infection modelling which suggests that the rate of infection among susceptible individuals has, in London at least, been higher since 1998. The force of infection among new initiates in London between 1998 and 2003 was approximately 3%, and this compares with findings from a recent cohort study of young injectors in London which indicated an HIV incidence rate of 3.4% per annum in 2001 .
The low HIV prevalence with little evidence of recent transmission during the 1990s probably reflected the continuing benefits of the programme of harm reduction interventions introduced as part of the public health response to HIV in the 1980s. Studies have suggested that countries that have introduced such measures have low or declining HIV prevalence among injectors, in comparison with countries without such measures that show a trend of increasing prevalence . Attendance at needle exchange, a key harm reduction intervention, is typically associated with a reduction in HIV risk behaviours , and declines in prevalence have been associated with changes in injection practices, declines in injecting drug use, or 'saturation' of the injecting population with HIV [26,27]. These explanation are unlikely in the UK as there is no suggestion that during the 1990s the IDU population in the UK was either ageing or in decline, but rather that it was growing .
Since 1997 reported needle and syringe sharing has increased among IDUs participating in the agency survey in England and Wales, with around one in three injectors currently self-reporting sharing compared with around one in five in the mid-1990s. In addition, the proportion of laboratory reports of acute hepatitis B infection associated with injecting drug use increased from around one-quarter in the mid-1990s to over one-third in recent years . Hepatitis C prevalence among injectors in England and Wales is relatively low compared to many other countries , however, recent reports have raised concerns about increased transmission [15,16].
Although the reasons for the increases in these indicators of HIV risk are unknown, there has been a simultaneous shift in the focus of policy and service provision for drug users in England and Wales. Until 1998 there had been a national strategy target for reducing the sharing of needles and syringes . The current national drug strategy , which was launched in 1998, only peripherally mentioned blood-borne viruses and included no specific targets on increasing coverage of syringe distribution or reducing risk behaviour, but focused on wider social harms, in particular drug-related crime . This shift has occurred during a time when there may have been concomitant increases in the overall prevalence of injecting  and in the injection of crack-cocaine , while the coverage of syringe distribution may have fallen or remained unchanged . Further, those injecting in the more recent years of this study would have missed the targeted HIV prevention campaigns and health education of the 1980s and early 1990s.
The geographical difference in HIV prevalence between London and the rest of England and Wales might reflect historical regional variations in past HIV risk. London has traditionally had a higher burden of HIV infection than the rest of England and Wales , and among IDUs this may reflect in part migration to London from, not only other parts of the United Kingdom, but also from other regions of the European Union and globally. Being born outside of the UK has previously been found to be a predictor of HIV infection among IDUs in London , and data on country of birth from clinicians' reports of newly diagnosed HIV infections indicate that two-thirds of HIV-infected IDUs diagnosed in the UK in 2003 were born in another country. Moreover, in those clinician reports in which the probable country of infection was given, for over half this was outside of the UK - mostly in south-western European countries, where HIV prevalence is higher and drug service coverage generally lower [15,35].
Voluntary confidential HIV testing had been taken up by half of the participants in this study overall, suggesting the potential for further development of testing services to increase uptake. However, whereas the majority of those with antibodies to HIV had previously had a voluntary confidential HIV test, and had had their HIV infection diagnosed, around one-fifth remain undiagnosed and unable to access treatment for their infection.
Finally, it is important to consider the generalizability of our findings. The comparative rarity, marginalization and illegal nature of injecting drug use impedes the construction of sampling frames and therefore the representativeness of our sample of injectors is impossible to measure. We aimed to minimize any sampling biases and maximize representativeness by combining two surveys that used complementary and established recruitment strategies, and so the resulting sample is likely to be as representative a sample of injectors as it is practical to obtain. These findings should therefore be generalized cautiously, particularly the force of infection which used only data from the agency survey.
In conclusion, HIV prevalence among current IDUs in England and Wales has recently increased after remaining low in the late 1990s following a decline during the early part of that decade, suggesting increasing incidence. A shift in policy focus from public health to criminal justice issues since the late 1990s may have unintentionally hindered the development and re-invigoration of harm reduction measures in response to evolving patterns of drug use and risk behaviours. This indicates the importance of remaining vigilant in low prevalence settings.
All authors contributed to the writing of the paper, with writing and statistical analyses being led by V.H. The force of infection modelling was undertaken by A.S. The ongoing agency survey is managed by V.H. and O.N.G., while the community surveys were conducted by G.V.S., A.J., and M.H. All laboratory testing was managed by J.P.
We are grateful to all of the injecting drug users who took part in the two survey programmes and to the various services and fieldworkers who assisted with their recruitment. We would like to thank the many staff who have worked on the surveys since 1990 and undertaken the laboratory work. We would also like to thank Peter Madden for his advice in relation to the statistically analyses and Nigel Gay for his advice with the force of infection work. The agency survey is part of the United Kingdom's national Unlinked Anonymous Prevalence Monitoring Programme which is overseen by the Unlinked Anonymous Surveys Steering Group and funded through the Department of Health. The community surveys were also funded by the Department of Health.
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