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Predictors of liver-related death among people who inject drugs in Vancouver, Canada : a 15-year prospective… Hayashi, Kanna; Milloy, M-J; Wood, Evan; Dong, Huiru; Montaner, Julio; Kerr, Thomas Nov 10, 2014

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Short reportPredictors of liver-related death among people who inject drugs inVancouver, Canada: a 15-year prospective cohort studyKanna Hayashi§,1,2, Michael-John Milloy1,3, Evan Wood1,2, Huiru Dong1, Julio SG Montaner1,2 and Thomas Kerr1,2§Corresponding author: Kanna Hayashi, BC Centre for Excellence in HIV/AIDS, 608  1081 Burrard Street, Vancouver BC, Canada V6Z 1Y6. Tel:1 604 682 2344 ext.63210. Fax: 1 604 806 9044. (khayashi@cfenet.ubc.ca)AbstractIntroduction: While HIV/AIDS remains an important cause of death among people who inject drugs (PWID), the potentialmortality burden attributable to hepatitis C virus (HCV) infection among this population is of increasing concern. Therefore,we sought to identify trends in and predictors of liver-related mortality among PWID.Methods: Data were derived from prospective cohorts of PWID in Vancouver, Canada, between 1996 and 2011. Cohort datawere linked to the provincial vital statistics database to ascertain mortality rates and causes of death. Multivariate Coxproportional hazards regression was used to examine the relationship between HCV infection and time to liver-related death.A sub-analysis examined the effect of HIV/HCV co-infection.Results and discussion: In total, 2,279 PWID participated in this study, with 1,921 (84.3%) having seroconverted to anti-HCVprior to baseline assessments and 124 (5.4%) during follow-up. The liver-related mortality rate was 2.1 (95% confidence interval[CI]: 1.53.0) deaths per 1,000 person-years and was stable over time. In multivariate analyses, HCV seropositivity was notsignificantly associated with liver-related mortality (adjusted relative hazard [ARH]: 0.45; 95% CI: 0.151.37), but HIVseropositivity was (ARH: 2.67; 95% CI: 1.275.63). In sub-analysis, HIV/HCV co-infection had a 2.53 (95% CI: 1.185.46) timeshazard of liver-related death compared with HCV mono-infection.Conclusions: In this study, HCV seropositivity did not predict liver-related mortality while HIV seropositivity did. The findingshighlight the critical role of HIV mono- and co-infection rather than HCV infection in contributing to liver-related mortalityamong PWID in this setting.Keywords: injection drug use; hepatitis C virus infection; mortality; Canada.Received 2 June 2014; Revised 22 September 2014; Accepted 10 October 2014; Published 10 November 2014Copyright: – 2014 Hayashi K et al; licensee International AIDS Society. This is an Open Access article distributed under the terms of the Creative CommonsAttribution 3.0 Unported (CC BY 3.0) License (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted use, distribution, and reproduction in anymedium, provided the original work is properly cited.IntroductionPeople who inject drugs (PWID) are at elevated risk of HIV andhepatitis C virus (HCV) infection [1,2].While HIV/AIDS remainsone of the primary causes of death among this populationworldwide [3], a recent study from Australia reported an in-creasing mortality burden of liver disease among opioid users[4]. However, little is known about trends of liver-relatedmortality among PWID in many settings. Further, althoughepidemics of viral hepatitis among PWID are presumed tocontribute to elevated liver-related mortality in this popula-tion [2,4], few studies have examined an independent con-tribution of HCV infection to liver-related deaths among PWID.While a recent study has identified a significant contribu-tion of chronic HCV infection to liver-related deaths amongNorwegian PWID aged 50 years [5], the contribution ofother risk factors, including HIV infection [6] and alcohol use[4,7], has not been fully examined.Vancouver, Canada, has experienced an explosive HIVepidemic among PWID [8]. The estimated HCV prevalence inthis population is also very high at 80% [9]. While previousliterature indicates an increasing coverage of highly activeantiretroviral therapy (HAART) among HIV-positive PWID anddeclining HIV incidence rates among PWID in this setting[10,11], HCV treatment coverage remains very low at B10%[12]. This has led to increasing concerns about the potentialmortality burden attributable to HCV infection among PWID.Therefore, we sought to examine the trend of liver-relateddeaths and the relationship between HCV infection and liver-related death among PWID in Vancouver.MethodsWe pooled participants being followed in two well-characterized, on-going open prospective cohorts of drugusers in Vancouver since 1996: the Vancouver Injection DrugUsers Study (VIDUS) and the AIDS Care Cohort to EvaluateAccess to Survival Services (ACCESS). The cohorts have beendescribed in detail elsewhere [8,13]. Briefly, VIDUS is acohort of HIV-seronegative adult PWID who have injectedan illicit drug in the month prior to baseline assessments.ACCESS is a cohort of HIV-seropositive adult drug users whohave used an illicit drug other than cannabinoids in theprevious month at the baseline interview. The two studiesemployed harmonized recruitment, primarily through snow-ball sampling and street outreach, and data collection tools.Hayashi K et al. Journal of the International AIDS Society 2014, 17:19296http://www.jiasociety.org/index.php/jias/article/view/19296 | http://dx.doi.org/10.7448/IAS.17.1.192961At baseline and semi-annually thereafter, participants answeredan interviewer-administered questionnaire, which elicited dataon demographic characteristics, drug-using behaviours andrelated exposures, and underwent serologic testing for HIVand HCV antibodies. Participants received $20 CAD for eachstudy visit. The University of British Columbia/ProvidenceHealthcare Research Ethics Board approved both studies.We ascertained mortality rates and underlying causes ofdeath among cohort participants through a confidential recordlinkage with the British Columbia Vital Statistics Agency andthrough on-going follow-up with contacts provided by parti-cipants. The specific methods employed have been describedin detail elsewhere [14]. Briefly, all residents in the province ofBritish Columbia have a unique and persistent government-provided identifier, which allows us to perform a semi-annualrecord linkage to the provincial Vital Statistics database withaccuracy. In addition, on-going follow-up with contacts pro-vided by participants have informed us of potential casesof death, for which we reviewed the registry data. The VitalStatistics database recorded causes of death according to theInternational Classification of Diseases, 10th edition (ICD-10).Participants were eligible for the present study if theywere recruited between 1 May 1996 and 31 December 2011and had completed at least one follow-up visit during thestudy period. The sample was further restricted to individualswho reported having injected drugs in the previous six monthsat baseline. To avoid potential bias due to long durationsbetween the last study visit and the date of death, individ-uals who were deceased more than 24 months after the lastfollow-up visit were censored on the last follow-up date.The primary endpoint in this analysis was liver-relateddeath, defined as having any of the following ICD-10 codes:viral hepatitis (B1519), sequelae of viral hepatitis (B942), livercancer (C22), alcoholic liver disease (K70) and non-alcoholicliver disease (K7177). For an unspecified cause of death(ICD-10: R99), we referred to the community follow-up recordfor any indications of a liver-related death. The primaryexplanatory variable of interest was HCV serostatus (positivevs. negative), ascertained at baseline and via semi-annualserologic testing, and was treated as a time-updated variable.Our study protocol did not include HCV RNA testing. Wealso considered a range of secondary explanatory variablesthat might confound the relationship between HCV infectionand time to liver-related death. Time-invariant variablesassessed at baseline included: gender, ethnicity and time sincefirst injection. As we were unable to ascertain timing of HCVinfection, the time since first injection was included in theanalysis as a surrogate measure [5]. Time-updated variablesincluded age, HIV seropositivity and other behaviouralvariables that referred to the previous six months: unstablehousing (i.e., living in single-room occupancy hotels, shelters,other transitional housing, or on the street); daily heroininjection; daily cocaine injection; and daily crack smoking;alcohol consumption (4 drinks per day on average vs.54drinks per day on average); engagement in sex work; andenrolment in methadone maintenance therapy. The cumula-tive number of incarceration events was also included asa time-updated variable. Variable definitions were consistentwith those in our previous studies [9,13,15].First, we examined baseline characteristics of the sampleusing descriptive statistics. Overall mortality rate and a 95%confidence interval [CI] during the study period were calcu-lated using Poisson distribution. Liver-related mortality rateswere calculated for the entire study period as well as atfour-year intervals. Further, we identified an all-cause mor-tality rate and causes of death among HCV-seropositiveparticipants to assess competing mortality risk in this popu-lation. Then, we used Cox proportional hazards regressionto examine bivariate associations between each explanatoryvariable and the time to liver-related death. To fit the mul-tivariate model, we employed a conservative stepwise back-ward selection approach. We included all variables found tobe significantly associated with time to liver-related death inbivariate analyses at pB0.10 in a multivariate model andused a stepwise approach to fit a series of reduced models.After comparing the value of the coefficient associated withHCV serostatus in the full model to the value of the coefficientin each of the reduced models, we dropped the secondaryvariable associated with the smallest relative change. Wecontinued this iterative process until the minimum changeexceeded 5%. Remaining variables were considered as po-tential confounders in a final multivariate model.We also conducted a sub-analysis to examine the effectof HIV/HCVco-infection on the time to liver-related death com-pared with HCV mono-infection. Here, we combined theHCV and HIV serostatus variables into a four-categorical vari-able: HCV-seropositive and HIV-seropositive, HCV-seronegativeand HIV-seropositive, HCV-seronegative and HIV-seronegative,and HCV-seropositive and HIV-seronegative (our referencecategory). We fitted a multivariate Cox proportional hazardsregression model including this new variable and the sameset of covariates included in the final multivariate model inthe primary analysis. All p-values were two-sided. All statisticalanalyses were performed using SAS software version 9.3 (SAS,Cary, NC).ResultsIn total, 2,279 PWID were recruited into this study andfollowed for a median of 60.9 months (interquartile range[IQR]: 34.4113.2). Only one individual was right-censoreddue to a long duration (more than 24 months) between thelast study visit and the date of liver-related death. Table 1shows that 1,519 (66.7%) participants were male, and themedian age at baseline was 37 years (IQR: 2944). The mediantime since first injection at baseline was 14 years (IQR: 624).In total, 1,921 (84.3%) had seroconverted to anti-HCV prior tobaseline assessments, and 124 (5.4%) additionally serocon-verted during follow-up.In total, therewere 487 deaths during the study period, withan overall mortality rate of 33.0 (95% CI: 30.036.1) deathsper 1,000 person-years. A total of 31 liver-related deathswere identified, yielding a liver-related mortality rate of 2.1(95% CI: 1.53.0) deaths per 1,000 person-years. As shown inFigure 1, the rates at four-year intervals were relatively stableover time: 2.5 (95% CI: 1.35.0) in 19961999; 2.1 (95% CI:1.14.3) in 20002003; 1.3 (95% CI: 0.53.1) in 20042007;and 2.3 (95% CI: 1.24.2) in 20082011. The primary under-lying causes of liver-related death were viral hepatitis (n12;Hayashi K et al. Journal of the International AIDS Society 2014, 17:19296http://www.jiasociety.org/index.php/jias/article/view/19296 | http://dx.doi.org/10.7448/IAS.17.1.19296239%), non-alcoholic liver disease (n8; 26%) and liver cancer(n8; 26%). The mortality rates (per 1,000 person-years) dueto viral hepatitis and non-alcoholic liver disease at four-yearintervals appeared to have slightly decreased over time: 1.3(95% CI: 0.53.3) and 1.3 (95% CI: 0.53.3), respectively, in19961999; 0.8 (95% CI: 0.32.5) and 0.5 (0.12.1) in 20002003; 0.8 (95% CI: 0.32.4) and 0.3 (95% CI: 0.041.8) in20042007; and 0.5 (95% CI: 0.11.8) and 0.2 (95% CI: 0.031.6) in 20082011. In contrast, the mortality rates due to livercancer appeared to have increased over time: 0 death in19961999 and 20002003; 0.3 (95% CI: 0.041.8) in 20042007; and 1.6 (95% CI: 0.83.4) in 20082011.Among HCV-seropositive participants (n2045), therewere 465 deaths, and an all-cause mortality rate was 34.2(95% CI: 31.337.4) deaths per 1,000 person-years. Com-mon causes of death among this sample included HIV-related(24.7%), other non-accidental causes (e.g., respiratory andcirculatory diseases, neoplasmas; 24.1%), overdose (23.7%),suicide and other accidental causes (12.3%), and liver related(6.0%).Table 2 shows the results of bivariate and multivariateCox proportional hazards regression analyses. As shown, inmultivariate analysis, HCV seropositivity was not significantlyassociated with liver-related mortality (adjusted relative haz-ard [ARH]: 0.45; 95% CI: 0.151.37), but HIV seropositivitywas independently and positively associated with the out-come (ARH: 2.67; 95% CI: 1.275.63). In sub-analysis,individuals with HIV/HCV co-infection had a 2.53 (95% CI:1.185.46) times hazard of liver-related death comparedwith those with HCV mono-infection.DiscussionOur results demonstrate that liver-related mortality ratesamong our cohorts of PWID in Vancouver were stable between1996 and 2011. We also found that HIV seropositivity ratherthan HCV seropositivity predicted liver-related mortality.Further, we found that HIV/HCVco-infection had a significantlyhigher risk of liver-related mortality than HCVmono-infection.The liver-related mortality rate identified in our studywas slightly higher than a pooled liver-related mortality ratereported in a previous meta-analysis [16]. However, unlikethe previous report from Australia [4], our findings did notindicate an increasing trend of liver-related death over time.Given a very low uptake of HCV treatment in our setting [12],it is unlikely that the trend reflects potential benefits oftherapeutic interventions for HCV. A more plausible explana-tion for the discrepancy may be that competing mortalityrisk was higher in our study population compared with thatin Australia, which was drawn from a registry of patientsreceiving opioid substitution treatment [4]. Further, the lowHIV prevalence among Australian PWID (B2%), compared toour setting (15%), may also explain the discrepancy [17,18].High competing mortality risk among our sample was alsoreflected in the overall mortality rate of 33.0 deaths per 1,000person-years, which was significantly higher than a previouslyreported pooled mortality rate of 23.5 deaths per 1,000person years among PWID worldwide [3]. The low liver-relatedmortality rate among our samplemay also reflect the relativelyshort follow-up time since HCV infection in our study (anestimated 19 years on average). Given that disease progres-sion in chronic HCV would take as long as 15 to 20 years[1921], and considering the increasing rates of death fromliver cancer observed in our study, increases in liver-relatedmortality may follow in this setting. Continued monitoringof rates of liver-related morbidity and mortality among PWID,Table 1. Baseline characteristics of PWID participating in theVIDUS and ACCESS cohorts in Vancouver, Canada, between May1996 and December 2011 (n2,279)Characteristic n (%)Age (median, IQR) 37 (2944)Male gender 1,519 (66.7%)Caucasian ethnicity 1,393 (61.1%)Years since first injection (median, IQR) 14 (624)Unstable housinga 1,602 (70.3%)Daily heroin injectiona 881 (38.7%)Daily cocaine injectiona 711 (31.2%)Daily crack smokinga 545 (23.9%)Alcohol consumption (4 drinks per day on average)a 366 (16.1%)Engagement in sex worka 537 (23.6%)Enrolment in methadone maintenance therapya 514 (22.6%)HIV seropositivity 620 (27.2%)HCV seropositivity 1,921 (84.3%)PWID: people who inject drugs; VIDUS: Vancouver Injection DrugUsers Study; ACCESS: AIDS Care Cohort to Evaluate Access to SurvivalServices; IQR: interquartile range.aDenotes activities during the six months prior to the interview.0.01.02.03.04.05.01996–1999 2000–2003 2004–2007 2008–2011 rate per 1000 person-yearsCalender year Figure 1. Liver-related mortality rates and 95% confidence intervals among PWID in Vancouver, Canada, 19962011.Hayashi K et al. Journal of the International AIDS Society 2014, 17:19296http://www.jiasociety.org/index.php/jias/article/view/19296 | http://dx.doi.org/10.7448/IAS.17.1.192963particularly among individuals infected with HCV at youngerage, is needed in this setting.We found that HIV infection, rather than HCV infection,was an independent predictor of liver-related death. Thisfinding was congruent with recent studies reporting increasingproportions of liver-related mortality among people livingwith HIV/AIDS [6,22]. Our finding that individuals with HIV/HCV co-infection had a greater risk of liver-related mortalitythan those with HCV mono-infection was also consistentwith a meta-analysis showing a higher rate of cirrhosis in HIV/HCV co-infection compared with HCV mono-infection [23].The meta-analysis further suggested that HAART did notimprove the adverse effect of HIV infection on HCV prognosis[23]. Collectively, these findings highlight the importance ofpromoting access to diagnostics and treatment for liverdisease among HIV-positive PWID.Our study has several limitations. First, as the study samplewas not randomly selected, our findings may not be general-izable to other populations of PWID. Second, the self-reporteddata may be affected by reporting biases, including recallbias and socially desirable responding. However, we note thatthis type of data has been commonly utilized in observationalstudies involving PWID and found to be valid [24]. Third,as with all observational studies, the relationships betweenthe explanatory variables and outcome assessed may beunder the influence of unobserved confounding. While wesought to address this bias with multivariate adjustment ofthe key demographic and behavioural predictors of survival,residual confounding may include participants’ clinical char-acteristics, including duration of HCV infection, our relianceon antibody rather than RNA status (e.g., spontaneous HCVclearance was not examined), access to HIV and/or HCVtreatment, and treatment outcomes. Lastly, the liver-relatedmortality rate reported herein may be underestimated dueto potential biases associated with the use of the deathregistry data. For example, approximately 10% of deaths hadunspecified causes. As the registry only records a primarycause of death, liver disease might have been underrepre-sented in the presence of another condition or injury that wasmore directly responsible for the death [25]. Further, deathsoccurring outside of the province were not recorded in theregistry, although we note that migration rates among PWIDhave been shown relatively low in this setting [26]. The lowevent count resulted in wide intervals around some of theestimates reported and made it difficult to undertake addi-tional analyses (e.g., to examine the impact of HAARTon liver-related mortality among HIV-positive PWID).ConclusionsIn summary, HIV seropositivity rather than HCV seropositivitypredicted liver-related mortality among our cohorts of PWIDin Vancouver. The findings highlight the role of HIV mono- andco-infection with HCV rather than HCV infection in contribut-ing to liver-related mortality among PWID. Our results high-light the need to expand efforts to promote access to HCVtesting and treatment, particularly among HIV-positive PWID.Authors’ affiliations1British Columbia Centre for Excellence in HIV/AIDS, Vancouver, Canada;2Division of AIDS, Faculty of Medicine, University of British Columbia,Vancouver, Canada; 3Department of Family Practice, Faculty of Medicine,University of British Columbia, Vancouver, CanadaCompeting interestsJ.S.G.M. is supported by the British Columbia Ministry of Health and throughan Avant-Garde Award (No. 1DP1DA026182) from the National Institute ofDrug Abuse, at the US National Institutes of Health. He has also receivedfinancial support from the International AIDS Society, United Nations AIDSProgram, World Health Organization, National Institutes of Health Research-Office of AIDS Research, National Institute of Allergy & Infectious Diseases,The United States President’s Emergency Plan for AIDS Relief (PEPfAR), UNICEF,the University of British Columbia, Simon Fraser University, Providence HealthCare and Vancouver Coastal Health Authority. He has received grants fromAbbott, Boehringer-Ingelheim, Bristol-Myers Squibb, Gilead Sciences, Janssen,Merck and ViiV Healthcare. The remaining authors have no competinginterests.Table 2. Bivariate and multivariate Cox proportional hazardsregression analysis of factors associated with liver-relatedmortality among PWID in Vancouver, Canada (n2,279)Relative hazard (RH)Characteristic Unadjusted (95% CI) Adjusted (95% CI)AgebPer 10 years older 1.95 (1.362.80) 1.59 (0.902.82)GenderMale vs. female 3.01 (1.187.66) 2.38 (0.866.58)EthnicityCaucasian vs. Others 1.80 (0.823.96)Time since first injectionPer year longer 1.05 (1.011.09) 1.02 (0.981.07)Unstable housinga,bYes vs. no 1.12 (0.552.29)Heroin injectiona,bDaily vs.Bdaily 0.62 (0.241.61)Cocaine injectiona,bDaily vs.Bdaily 1.10 (0.432.82)Crack smokinga,bDaily vs.Bdaily 0.51 (0.201.34)Alcohol consumptiona,b4 drinks per day vs.54 drinks per day1.11 (0.323.90)Engagement in sex worka,bYes vs. no 0.25 (0.031.76)Enrolment in methadone maintenance therapya,bYes vs. no 0.84 (0.421.71)Incarceration eventsb12 times vs. never 1.03 (0.452.32)35 times vs. never 0.68 (0.222.05)5 times vs. never 0.74 (0.192.83)HIV serostatusbPositive vs. negative 2.17 (1.064.43) 2.67 (1.275.63)HCV serostatusbPositive vs. negative 0.85 (0.262.77) 0.45 (0.151.37)PWID: people who inject drugs; CI: confidence interval.aRefers to activities during the six months prior to interview.bDenotes time-updated variables.Hayashi K et al. Journal of the International AIDS Society 2014, 17:19296http://www.jiasociety.org/index.php/jias/article/view/19296 | http://dx.doi.org/10.7448/IAS.17.1.192964Authors’ contributionsK.H., E.W. and T.K. designed the study. H.D. conducted the statistical analyses.K.H. drafted the first manuscript and incorporated suggestions from all co-authors. All authors made significant contributions to the conception of theanalyses, interpretation of the data and drafting of the manuscript. All authorshave read and approved the final version of the article.AcknowledgementsThe authors thank the study participants for their contribution to the research,as well as current and past researchers and staff. The study was supported by theUS National Institutes of Health (VIDUS: R01DA011591, ACCESS: R01DA021525).This research was undertaken, in part, thanks to funding from the CanadaResearch Chairs programme through a Tier 1 Canada Research Chair in InnerCity Medicine, which supports E.W. 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