Increase in diagnosed newly acquired hepatitis C in HIV-positive men who have sex with men across London and Brighton, : is this an outbreak?

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1 1 Health Protetion Ageny (HPA), London, UK; 2 Saint Georges Hospital Medial Shool, London, UK; 3 HPA Centre for Infetions, London, UK; 4 Mortimer Market Centre, London, UK; 5 Brighton and Sussex University Hospitals NHS Trust, Brighton, UK; 6 Ian Charleson Centre, Royal Free Hospital, London, UK; 7 British HIV Assoiation (BHIVA), London UK; 8 British Assoiation for Sexual Health and HIV (BASHH), London, UK Correspondene to: I Giraudon, Health Protetion Ageny, Regional Epidemiology Unit London, 7th Floor, Holborn Gate, 330 High Holborn, London WC1V 7PP, UK; isabelle.giraudon@hpa.org.uk Aepted 8 Otober 2007 Inrease in diagnosed newly aquired hepatitis C in HIV-positive men who have sex with men aross London and Brighton, : is this an outbreak? I Giraudon, 1 M Ruf, 1 H Maguire, 1,2 A Charlett, 3 F Nube, 3 J Turner, 4 R Gilson, 4 M Fisher, 5 S Bhagani, 6 M Johnson, 7 S Barton 8 ABSTRACT Objetives: To determine the inidene of diagnosed newly aquired hepatitis C virus (HCV) in HIV-positive men who have sex with men (MSM) aross London and Brighton in order to inform publi health interventions. Methods: Cases were defined as MSM attending London and Brighton HIV/genitourinary mediine linis from January 2002 to June 2006, with HCV PCR RNA or antibody positive, and a negative HCV test in the previous three years. The yearly number of ases and HCV sreening poliy in MSM were examined. A negative binomial regression model was used to estimate HCV inidene density rate ratio and 95% CI. Results: 20 out of 38 linis provided information, overing 84% of the HIV-positive MSM workload in London and 100% in Brighton. The estimated overall inidene was 9.05 per 1000 HIV-positive MSM patientyears. It inreased from 6.86 per 1000 in 2002 to per 1000 during January June Inidene at linis ranged from 0 to 15.4 (median 6.52) per 1000 HIVpositive MSM patient-years. There was some evidene of differene in the inidene and trend (p = 0.02) in eah lini. The average annual rise in inidene of HCV was 20% (95% CI 4% to 39%, p = 0.001). There was little evidene of suh transmission among MSM with negative or unknown HIV status. Conlusions: HCV inidene learly inreased among HIV-positive MSM in London and Brighton during January 2002 to June Prospetive enhaned surveillane of HCV in MSM, inluding HIV status and behavioural risk fators, is reommended to help inform ontrol measures and better determine the frequeny of transmission in all MSM. Reent reports from genitourinary mediine (GUM) linis in the south east of England suggested a sudden rise in hepatitis C virus (HCV) in HIV-positive men who have sex with men (MSM). 1 4 HCV infetion, whih may lead to symptomati hroni liver disease after many years of asymptomati infetion, has been identified as a major publi health issue in the United Kingdom. 5 Treatment for hroni infetion is available. The effiay for most genotypes remains low, however, with speifi problems in HIV-positive individuals. 6 8 The main risk fator in the United Kingdom is injeting drug use Historially, using data from heterosexual HCV disordant ouples, the risk of sexual transmission was onsidered to be low. Reent lini reports of aute Epidemiology HCV in HIV-positive MSM in the south east of England were mirrored in other European ountries where sexual transmission was being postulated as the primary mode of HCV transmission, in ontrast to onventional routes In the United Kingdom there are several shortomings in the urrent national surveillane systems for HCV Risk fators are poorly reorded (less than a third of the laboratory reports ontain this information) and reports are often inomplete, partiularly in London. 16 The prevalene of HIV/HCV o-infetion in MSM was estimated at the lini level 17 but little is known about the burden of disease at a wider level and about the inidene of HCV infetion. The nature and sale of the observed rise, and whether it was London-wide or extended to Brighton where there is a large MSM ommunity, was therefore unlear. The aim of this investigation was to determine the extent and trends in the inidene of diagnosed newly aquired hepatitis C in MSM in London and Brighton in order to inform publi health interventions. METHODS Diagnosed newly aquired hepatitis C was defined as HCV RNA positive on PCR or HCV antibody positive and a doumented HCV-negative test in the previous three years. A list of all HIV and GUM linis in the London region and Brighton area (East Sussex) was drawn up. It omprised 35 London linis and three major East Sussex linis (ie Brighton, Eastbourne and Hastings). A questionnaire was sent to leading onsultants at eah lini. In HIV-positive MSM, questions were posed about the numbers of new ases of HCV diagnosed eah year between January 2002 and June 2006, liver funtion tests (LFT) and HCV sreening poliies (ie frequeny of sreening and targeted patients). In MSM with negative or unknown HIV status, questions inluded the number of new ases diagnosed eah year between January 2002 and June 2006, and HCV sreening poliy. Estimates of denominators Yearly denominators of HIV-positive MSM patients at eah lini were derived from the Health Protetion Ageny (HPA) Centre for Infetions Survey of Prevalent HIV Infetions Sex Transm Infet 2008;84: doi: /sti

2 Figure 1 Number of ases and estimated inidene of diagnosed newly aquired hepatitis C in HIV-positive men who have sex with men per 1000 patient-years, reported by London and Brighton HIV/ genitourinary mediine linis January 2002 June Diagnosed (SOPHID) data 18 from 2002 to Denominators for the first half of 2006 were derived for eah lini from the 2005 data multiplied by the estimated perentage hange between 2004 and 2005 (+7% on average). Statistial analysis Initially a Poisson regression analysis was performed to assess whether there was an apparent inrease in ases over the time period, ontrolling for the effet of take-up of routine HCV sreening, and whether the inidene differed between London linis. This model did not fit the data, as there was more variation than would be expeted if it had arisen from a Poisson proess. To allow for the extra Poisson variane, a negative binomial regression model was used. Any evidene of nonlinearity was assessed using the likelihood ratio test. To ompare inidene between linis, Chelsea & Westminster Figure 2 HIV/genitourinary mediine linis, aseload of HIV-positive men who have sex with men (MSM) patients (SOPHID 2004 data) and reported diagnosed newly aquired hepatitis C virus (HCV) ases as a proportion of the total. London and Brighton, January 2002 June was hosen as the referene beause it saw the most patients over the years. The natural logarithm of the number of MSM HIV-positive patient-years in eah lini in eah year was used as an offset in the regression model to normalise the results for differenes in the patient-years at risk. It was diffiult to assess the effet of routine HCV sreening as it is intrinsially assoiated with the year and there was a lear temporal trend of HCV inidene. The effet of routine sreening was explored by omparing eah year separately for the inidene aross linis performing and not performing routine HCV sreening. As there was no evidene of a differene, routine sreening was not onsidered as a ovariate in the regression model. RESULTS Response rate Twenty entres out of 38 returned the questionnaire, inluding 17 in London and three in East Sussex. The majority (17 out of 20) provided both HIV and GUM servies; two were exlusively HIV linis (at North Middlesex Hospital and the Ian Charleston Centre at the Royal Free Hospital) and one was exlusively a GUM lini, seeing no HIV patients (Marlborough Clini at the Royal Free Hospital). Seventeen of the 19 HIV linis reported the number of newly aquired HCV ases seen in HIV-positive MSM during the survey time period. Based on SOPHID data these linis ared for 84% of the total number of HIV-positive MSM attending London HIV linis and 100% of HIV-positive MSM attending the Brighton HIV Clini in Thirteen of the 18 GUM linis reported the number of diagnosed newly aquired HCV ases seen in MSM who were HIV negative or of unknown HIV status. Sreening By 2006, routine HCV sreening was arried out in HIV-positive MSM patients in all 19 responding HIV linis, inreasing from five before 2000, to nine before 2003 and 16 before The majority (13 of the 19 responders) repeated HCV sreening annually, two more often and four less often. Regarding HCV sreening in MSM with unknown or negative HIV status, 16 linis responded, of whih five routinely sreened for HCV and two of those started in LFT in HIV-positive MSM were arried out on a quarterly basis in 17 of the 19 HIV linis responding, and less often (four to six-monthly) in the other two linis. One lini reported performing LFT less than one a quarter for HIV-positive MSM patients not on highly ative antiretroviral therapy. Of the 15 linis that speified whih HIV-positive MSM patients had routine LFT, 14 linis responded that testing was arried out on all HIV-positive MSM patients, whereas one lini reported testing only patients on highly ative antiretroviral therapy. Of the nine linis that provided information on the date of introdution of routine LFT testing, all nine did so before Cases among HIV-positive MSM Clinis reported a total of 389 diagnosed newly aquired HCV ases among HIV-positive MSM, inluding 352 in London and 37 in Brighton. Reports inreased from 56 ases in 2002, to 86 in 2004 and 66 in the first six months of 2006 (fig 1). Estimated inidene rate of diagnosed newly aquired HCV infetion in HIV-positive MSM For London and Brighton, 389 diagnosed newly aquired HCV ases arose from a total of HIV-positive MSM patient- 112 Sex Transm Infet 2008;84: doi: /sti

3 Table 1 Reports of diagnosed newly aquired hepatitis C virus infetions and estimated inidene per 1000 patient-years among HIV-positive men who have sex with men, by HIV/genitourinary mediine lini in London and Brighton, January 2002 June 2006 HIV linis years, an overall inidene of 9.05 HCV ases per 1000 patientyears. Inidene inreased from 6.86 per 1000 patient-years in 2002 to per 1000 patient-years during January June The highest inidenes were mainly in entral London and large HIV linis, as well as in Brighton. The estimated inidene aross the linis ranged from 0 to 15.39, the median being 6.52 per 1000 HIV-positive MSM patient-years (table 1). Of the linis that reported numbers of ases, nine reported six or fewer ases (table 1, fig 2). Inidene rate ratio A likelihood ratio test for non-linearity of the time trend was not signifiant, hi square test statisti 0.27 (3 degrees of freedom, p = 0.96), thus a linear time trend was assumed. The Total diagnosed newly aquired HCV infetions in HIV-positive MSM Total patient-years Royal Sussex County Hospital Brighton Eastbourne Hastings Bekenham Hospital Central Middlesex Hospital Charing Cross Hospital Chelsea & Westminster Hospital* Mortimer Market Centre (UCH) North Middlesex Hospital Royal Free Hospital HIV Clini Royal London Hospital St George s Hospital St Mary s Hospital Guys and St Thomas West Middlesex Hospital Queen Elizabeth Woolwih Hospital Total HCV, Hepatitis C virus; MSM, men who have sex with men; UCH, University College Hospital. *Joint two linis. Inidene rate per 1000 patient-years estimate of the annual inrease in inidene of HCV in HIVpositive MSM was 20% eah year (95% onfidene interval 4% to 39%, p = 0.01). The inidene at the Royal Free and Royal London during 2002 to 2006 was more than twie that of the referene lini (Chelsea & Westminster; table 2). There was some evidene that the inidene of HCV differed between linis (p = 0.02). In addition, when linis with two or fewer ases were exluded beause small numbers made the estimated trends unertain, there was strong evidene that the temporal trend of HCV inidene did differ between linis (hi square test statisti 36.3 on 8 degrees of freedom, p,0.0001). There was no differene in inidene between linis with and without routine sreening when eah year was analysed separately. Also, the linis with the greatest estimated annual Table 2 Estimated inidene rate ratio of diagnosed newly aquired hepatitis C virus infetion in HIV-positive men who have sex with men patients by HIV/genitourinary mediine lini, 95% CI and p value estimated from the negative binomial regression model, January 2002 June 2006, London and Brighton Estimated inidene Fator HIV linis rate ratio 95% CI p Value Clini Royal Sussex County Hospital Brighton to Eastbourne 0 Hastings 0 Bekenham Hospital to 8.96 Central Middlesex Hospital to 8.08 Charing Cross Hospital to 1.88 Chelsea & Westminster Hospital* Referene Mortimer Market Centre (UCH) to 3.64 North Middlesex Hospital to 2.83 Royal Free Hospital HIV Clini to 4.49 Royal London Hospital to 4.92 St George s Hospital to 1.83 St Mary s Hospital to 3.09 Guys and St Thomas to 2.93 West Middlesex University Hospital to 4.66 Queen Elizabeth Woolwih Hospital 0 Year to UCH, University College Hospital. *Joint two linis. Sex Transm Infet 2008;84: doi: /sti

4 inrease were those that had routine sreening in plae throughout the study. It would thus appear that the progressive introdution of routine sreening during the study period did not have an undue effet on the observed rise in inidene. Cases with unknown or negative HIV status Only three linis reported ases with unknown or negative HIV status in MSM (total of six ases, inluding three ases at one lini routinely sreening all MSM patients for HCV). DISCUSSION This investigation provides evidene of ongoing and inreasing diagnosed newly aquired HCV infetion in HIV-positive MSM aross most major linis in the London and East Sussex regions sine The doumented inrease does not appear to be assoiated with the progressive implementation of HCV sreening for HIV-positive MSM. We believe that this study provides onfirmation at a regional level that HCV is irulating at high and inreasing levels among HIV-positive MSM and represents a possible outbreak. This adds to the evidene from epidemiologial and moleular studies desribing lusters and suggesting a sustained hain of transmission in the HIV-positive MSM population at the lini level. 2 3 We have not onfirmed individual sexual or other epidemiologial links between ases and further work is needed to onfirm the existene of a London-wide outbreak. Our survey was not designed to ollet individual harateristis (eg timing of any HIV o-infetion) and behavioural information (eg injeting or other drug use or sexual praties inluding number of partners and unproteted sex). There were differenes in inidene and in trends in inidene between linis, possibly related to variations in ase mix, with patients presenting different behavioural risk fators, but we ould not onfirm the ontribution of suh risk fators to the aseload at any lini or their ontribution to the observed differenes. The mehanism of HCV transmission among MSM is not yet fully understood, although it has been postulated that muosal trauma during rough sexual praties (eg fisting) and group sex in onjuntion with rereational drug use may failitate transmission among HIV-positive MSM. Information on risk fators should be onsidered in longer-term prospetive enhaned surveillane. It is possible that response bias ould have led to an overestimation of the inidene as non-responders may have been more likely to have fewer ases. The linis that did respond, however, were major entres overing the large majority of HIV-positive MSM patients under are. We found little evidene to indiate the frequent ourrene of diagnosed newly aquired HCV in MSM with negative or Key messages This study provides evidene of a 20% year on year inrease in the inidene of diagnosed newly aquired HCV infetion in HIV-positive MSM aross major linis in London and Brighton, from January 2002 to June 2006 Little evidene was found on the ourrene of diagnosed newly aquired HCV infetion in MSM with negative or unknown HIV status Enhaned surveillane of diagnosed newly aquired HCV in MSM is reommended to monitor spatial and time trends and to inform publi health interventions unknown HIV status. There have been reports from a study in Brighton suggesting that transmission was not onfined to HIVpositive MSM. 21 In that study, however, HIV-positive men were found to be approximately 13 times more likely to have a new HCV diagnosis ompared with HIV-negative men. It is also possible that the speifiity of our ase definition itself may have led to bias. As doumented evidene of a previously negative test within the past three years was required, HIVpositive MSM may have been more likely to be reported beause they have had previous HCV tests. In addition, although we did not ask if the reported ases were diagnosed through LFT or not, there is a possible detetion bias: HIV-positive MSM patients have routine LFT in all linis, whih may make them more likely to be diagnosed when infeted with HCV. This ould hange should the frequeny of follow-up at linis redue as the number of patients inreases. It was noteworthy, however, that at those London linis where HCV sreening was reportedly being arried out routinely among all MSM patients (inluding those with unknown or negative HIV status), only three ases were reported. Although HIV-positive MSM attending HIV servies do onstitute a well-monitored ohort and may be more likely to be diagnosed if HCV infeted, there are also data from ommunity-based behavioural surveys to show that HIVpositive MSM report more high-risk sexual behaviours and rereational drug use than HIV-negative men Furthermore, sexually transmitted infetions (STI) have been assoiated with more high-risk sexual behaviours in MSM and there have been reent reports of other outbreaks in HIV-positive MSM in the United Kingdom and in London, inluding syphilis, lymphogranuloma venereum and Shigella sonnei outbreaks This suggests a onsiderable and inreasing burden of various STI among HIV-positive MSM, highlighting the need for targeted primary prevention and harm minimisation initiatives. In the era of antiretroviral therapy the number of people living with HIV is steadily inreasing, inluding those ontinuing with high-risk behaviours. The number of HIV-positive MSM who are resident in London and seen for HIV-related healthare inreased by 50% from 6800 in 2000 to in Chroni HCV/HIV o-infetion may ompromise the response to treatment and has important impliations for the prognosis and treatment of both onditions The ongoing transmission of HCV among HIV-positive MSM may have a signifiant impat for health servie provision and osts in the future. The National Institute for Health and Clinial Exellene (NICE) has estimated drug treatment osts for mild hroni HCV of approximately for 48 weeks of treatment. Little ost information is available for the treatment of o-infeted patients 6 and average osts are diffiult to estimate. These are likely to be muh higher as a result of longer treatment yles and greater omplexity; although the lower response rate as well as potential drug interations may also ause more patients to terminate their treatment early. CONCLUSION This survey has shown evidene of ongoing and inreasing transmission of HCV infetions in HIV-positive MSM aross the London and East Sussex regions. Yet there are gaps in our understanding, espeially regarding the relative ontribution of different risk fators and the burden of disease for all MSM. Our findings endorse British HIV Assoiation reommendations for regular HCV testing among HIV-positive patients and among those with unexplained liver transaminase elevation, espeially in patients with potential risk fators (ie MSM with sexual 114 Sex Transm Infet 2008;84: doi: /sti

5 risks). Testing MSM of unknown or negative HIV status should also be reommended when there are speifi risk fators (group sex partiipation, other high-risk sexual behaviours, or rereational drug use). The survey strongly supports the reent researh findings on diagnosed newly aquired HCV infetion in HIV-positive MSM and onfirms the need for better information about new HCV infetions among all MSM. An enhaned surveillane system for newly aquired HCV infetion ould provide useful information on the number of new ases, temporal and spatial trends, as well as risk fators, in order to refine harm minimisation strategies and the publi health response. Aknowledgements: The authors wish to thank the partiipating liniians: Dr Jonathan Ainsworth at North Middlesex Hospital; Dr Guy Baily at Ambrose King Centre, Bart s and the London Hospital; Dr Mihael Brady at Caldeott Centre, Kings College Hospital; Dr Gary Brook at Patrik Clements Clini, Central Middlesex Hospital; Dr David Daniels at West Middlesex University Hospital; Dr Caroline Dimian at Bekenham Hospital; Dr Daniel Ivens at Marlborough Clini, Royal Free Hospital; Dr Babu Kulaseagaram at St Thomas Hospital; Dr Janie Main at St Mary s Hospital; Dr Ken MLean at West London Centre, Charing Cross Hospital; Dr Sue Mithell at Trafalgar Clini, Queen Elizabeth Woolwih Hospital; Dr Nweka Nwokolo at Vitoria Clini, Chelsea & Westminster Hospital; Dr Mark Pakianathan at Courtyard Clini, St George s Hospital; Dr Harish Patel at East Sussex Hospitals; Dr Andrew Shaw at North West London Hospitals; Dr Emma Thomson at St Mary s Hospital. The authors also aknowledge the British Assoiation for Sexual Health and HIV (BASHH) and the British HIV Assoiation (BHIVA) for their support and olleagues at the HPA Centre for Infetions for their ollaboration and advie. They would also like to thank Peter Trail for his ontribution to the launh of the survey, as well as Elizabeth Jaffa and Kathryn Harris, HPA London Region, who helped to ollet the data. Competing interests: The HPA authors, JT, RG, MF, SB, MJ, SB, delared they had no ompeting interests. Contributions: IG designed the questionnaire, organised the data olletion and data management, reviewed the literature and wrote the paper. MR usefully drafted disussion points, failitated the data olletion at some linis and extensively ommented on the drafts. HM led the study and supervised both MR and IG and extensively ommented on drafts. JT, RG, MF and SB provided data and usefully ommented on drafts. 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Antivir Ther 2006;11: Commentary Giraudon et al orroborate that herpes C virus (HCV) is irulating among HIV positive men who have sex with men (MSM) in South East England. 1 Earlier reports noted evidene of aute sexually transmitted infetions among HIV positive men and of HCV infetion among HIV positive men in other ountries. 2-4 Giraudon s study is based on reports of HCV sreening (of people with a history of HCV antibody tests) by 20 of 38 genitourinary linis in London, Brighton and elsewhere in South East England, and an estimated denominator of person years at risk derived from routine surveillane of prevalent HIV infetions from these linis. 1 The linis reported 389 newly aquired HCV infetions over 4.5 years yielding an estimated inidene of 9/1000 person years, whih varied greater than threefold by lini and may have inreased over time. The hypothesis raised by Giraudon et al that inidene has inreased requires further orroboration given that the analysis did not have data on the number of HCV antibody tests onduted in Sex Transm Infet 2008;84: doi: /sti