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Risk factors for developing a cutaneous injection-related infection among injection drug users: a cohort… Lloyd-Smith, Elisa; Wood, Evan; Zhang, Ruth; Tyndall, Mark W; Montaner, Julio S; Kerr, Thomas Dec 9, 2008

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ralssBioMed CentBMC Public HealthOpen AcceResearch articleRisk factors for developing a cutaneous injection-related infection among injection drug users: a cohort studyElisa Lloyd-Smith1,2, Evan Wood1,3, Ruth Zhang1, Mark W Tyndall1,2, Julio SG Montaner1,3 and Thomas Kerr*1,3Address: 1BC Centre for Excellence in HIV/AIDS, St. Paul's Hospital 608-1081 Burrard Street, Vancouver, BC V6Z 1Y6, Canada, 2Department of Health Care and Epidemiology, University of British Columbia, Vancouver, Canada and 3Department of Medicine, University of British Columbia, Vancouver, CanadaEmail: Elisa Lloyd-Smith - esmith@cfenet.ubc.ca; Evan Wood - uhri@cfenet.ubc.ca; Ruth Zhang - rzhang@cfenet.ubc.ca; Mark W Tyndall - mtyndall@cfenet.ubc.ca; Julio SG Montaner - jmontaner@cfenet.ubc.ca; Thomas Kerr* - uhri@cfenet.ubc.ca* Corresponding author    AbstractBackground: Cutaneous injection-related infections (CIRI), such as abscesses and cellulitis, arecommon and preventable among injection drug users (IDU). However, risk factors for CIRI havenot been well described in the literature. We sought to characterize the risk factors for currentCIRI among individuals who use North America's first supervised injection facility (SIF).Methods: A longitudinal analysis of factors associated with developing a CIRI among participantsenrolled in the Scientific Evaluation of Supervised Injecting (SEOSI) cohort between January 1, 2004and December 31, 2005 was conducted using generalized linear mixed-effects modelling.Results: In total, 1065 participants were eligible for this study. The proportion of participants witha CIRI remained under 10% during the study period. In a multivariate generalized linear mixed-effects model, female sex (Adjusted Odds Ratio (AOR) = 1.68 [95% Confidence Interval (CI): 1.16–2.43]), unstable housing (AOR = 1.49 [95% CI: 1.10–2.03]), borrowing a used syringe (AOR = 1.60[95% CI: 1.03–2.48]), requiring help injecting (AOR = 1.42 [95% CI: 1.03–1.94]), and injectingcocaine daily (AOR = 1.41 [95% CI: 1.02–1.95]) were associated with an increased risk of having aCIRI.Conclusion: CIRI were common among a subset of IDU in this study, including females, thoseinjecting cocaine daily, living in unstable housing, requiring help injecting or borrowing syringes. Inorder to reduce the burden of morbidity associated with CIRI, targeted interventions that addressa range of factors, including social and environmental conditions, are needed.BackgroundInjection drug use remains a major public health concernworldwide. While researchers and policy makers have[HIV], hepatitis C virus [HCV]) among injection drugusers (IDU) [1-3], considerably less attention has beendevoted to the problem of bacterial infections of the skinPublished: 9 December 2008BMC Public Health 2008, 8:405 doi:10.1186/1471-2458-8-405Received: 9 May 2008Accepted: 9 December 2008This article is available from: http://www.biomedcentral.com/1471-2458/8/405© 2008 Lloyd-Smith et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.Page 1 of 6(page number not for citation purposes)focused much attention on the transmission of blood-borne viruses (e.g., human immunodeficiency virus[4]. A recent report by the United States Centres for Dis-ease Control and Prevention highlighted the dearth ofBMC Public Health 2008, 8:405 http://www.biomedcentral.com/1471-2458/8/405research on cutaneous injection-related infections (CIRI)among IDU and cited reports of recent and dramaticincreases in CIRI, including abscesses and cellulitis,among IDU in England [5]. In addition, CIRI are the pri-mary reason that IDU seek treatment at an emergencydepartment in some settings [6].The prevalence of CIRI among IDU typically ranges from10% to 30% [7,8]. The variability in prevalence estimatesmay be due to differences in measurement of the occur-rence of CIRI (e.g., reporting current vs. ever having aCIRI), the definition of CIRI (e.g., injection-related vs. anydrug-related) and the fact that there are currently nostandard guidelines with regard to reporting of CIRI basedon severity [4]. Other factors may be the exploration ofdifferent risk factors for developing CIRI across settings,for example differences in types of drugs used (e.g., blacktar heroin in California, United States vs. white heroin inBritish Columbia, Canada), intensity of drug use, andavailability and access to clean injection paraphernalia[9].However, certain factors have been shown to be consist-ently associated with developing a CIRI in particular cit-ies. For example: injecting under the skin (also known as"skin popping") in San Francisco and Glasgow [8,10,11];frequent injection in Amsterdam and Vancouver [12,13];and injection of heroin plus cocaine (i.e. "speedballs") inSan Francisco and Amsterdam [8,13] have been associatedwith CIRI. However, most of these analyses were based oncross-sectional investigations few prospective studiesexist. We conducted the present longitudinal study tocharacterize risk factors of developing a CIRI among IDU.MethodsData source: Scientific Evaluation of Supervised InjectionIn September 2003, a comprehensive evaluation of Insite,North America's first supervised injection facility (SIF),was initiated. Users of the SIF, located in Vancouver'sDowntown Eastside (DTES) neighbourhood, were ran-domly invited to enroll in a prospective cohort studyknown as the Scientific Evaluation of Supervised Injection(SEOSI) and have since been interviewed semi-annually[14]. The methodological details have been describedelsewhere [15]. Briefly, to be recruited into the SEOSIcohort, individuals had to have performed at least twoinjections at the SIF, been at least 19 years old and pro-vided informed consent. Furthermore, the questionnaireis interviewer-administered and elicits a range of informa-tion, including information specific to socio-demo-graphic characteristics, risk behaviours, and involvementin addiction treatment. This is followed by blood testingfor HIV and HCV for those who previously tested negativetion and the types of drug being injected. The SEOSIcohort has received approval from the Providence HealthCare/University of British Columbia Ethics Board.To be eligible for this study, participants must have com-pleted both the interviewer-administered and nurse-administered baseline questionnaires during the studyperiod (January 1, 2004 to December 31, 2005.)Outcome Measure and Explanatory VariablesThe primary outcome for this analysis (dependent varia-ble) was a current CIRI reported to and visually confirmed(e.g., pain, redness, induration, and fluctuation) by thestudy nurse in response to the question "Do you presentlyhave any sores or abscesses from where you have beeninjecting?". Explanatory variables examined in this analy-sis included: age (per year older); sex (female vs. male);unstable housing, defined as living in a single room occu-pancy hotel, shelter, recovery or transition house, jail, onthe street, or having no fixed address as opposed to livingin an apartment or house (yes vs. no); residence in theDTES (yes vs. no); sex trade involvement (yes vs. no); bor-rowing used syringes (yes vs. no); requiring help injecting(yes vs. no); using puddle water for injecting (yes vs. no);injecting cocaine daily (yes vs. no); injecting heroin daily(yes vs. no), injecting crack cocaine daily (yes vs. no);injecting crystal methamphetamine daily (yes vs. no);injecting "speedballs" daily (yes vs. no); the proportion ofall injections at SIF (always vs. < always); HIV serostatus(positive vs. negative); and HCV serostatus (positive vs.negative). Variable definitions were consistent with previ-ous work [16-19]. All variables referred to the six monthsprior to the interview, except for unstable housing and res-idence in the DTES, which referred to resident status at themore recent interview.Statistical AnalysisThe proportion of SEOSI participants who reported hav-ing a CIRI was inspected graphically over time. Univariateand multivariate statistics, including generalized linearmixed-effects modeling, were used to examine factorsassociated with having a CIRI over time. Generalized lin-ear mixed-effects modeling is a longitudinal techniquethat analyzes individual trajectories and produces corre-lates. This analytic technique was chosen because of itsflexibility in variable parameters (e.g., fixed, time-updated, random), its ability to capture heterogeneity ofsubjects and within-subject correlation, and its attempt toidentify individual-level factors [20]. Independent varia-bles were either fixed (e.g., sex) or time-updated (e.g., age,all behavioural variables considered, HIV and HCVserostatus) in this model. Random variation betweenindividuals was accounted for by using random inter-Page 2 of 6(page number not for citation purposes)and a nurse-administered questionnaire on health status.A database in the SIF tracks key events, including utiliza-cepts. Variables significant at the univariate level (p <0.05) were included in the multivariate model. The dataBMC Public Health 2008, 8:405 http://www.biomedcentral.com/1471-2458/8/405were analyzed using SAS version 9.1 (SAS Institute, Cary,NC, USA.) All reported p-values were two-tailed.ResultsOf the 1090 participants recruited into the SEOSI cohortsince November 2003, 1065 (97%) completed both abaseline interviewer-administered questionnaire and anurse-administered questionnaire after recruitment intoSEOSI cohort. Among these participants, 877 (82%)returned for at least one follow-up visit, and 312 (29%)were female. The median age was marginally younger forthose who reported a CIRI at baseline when comparedwith those who did not at baseline (36 [IQR: 31–43] vs.39 [IQR: 33–45], p = 0.095). As shown in Figure 1, theproportion of participants reporting a current CIRI in thisstudy was fairly consistent over the two year study period,ranging from 6% to 10%, although the proportiondeclined slightly between the baseline and first follow-upvisit. At baseline, 106 (10%) of participants reported aCIRI. There were 14 (1%) individuals with missing dataon HIV serostatus and 33 (3%) individuals with missingdata on HCV serostatus at baseline; due to these smallcounts, these individuals were excluded from further anal-yses.Using longitudinal methods, factors associated withreporting a current CIRI at the univariate and multivariatelevel are presented in Table 1. In univariate analyses,being older and reporting use of the SIF for all injectionswas associated with a decreased likelihood of developinga current CIRI. Female sex, living in unstable housing,involvement in the sex trade, borrowing a used syringe,requiring help injecting, injecting cocaine daily, injectingheroin daily, and injecting "speedballs" daily were posi-tively associated with reporting a current CIRI.As displayed in the multivariate model in Table 1, partici-pants who reported a current CIRI were more likely to befemale (Adjusted OR (AOR) = 1.68 [95% ConfidenceIntervals {CI}: 1.16–2.43]); live in unstable housing(AOR = 1.49 [95% CI: 1.10–2.03]); borrow used syringes(AOR = 1.60 [95% CI: 1.03–2.48]); require help injecting(AOR = 1.42 [95% CI: 1.03–1.94]); and inject cocainedaily (AOR = 1.41 [95% CI: 1.02–1.95]).DiscussionIn this study we found that the proportion of IDU report-ing a CIRI remained within the range of six to 10 per centover a median follow-up of 12.6 (IQR: 6.2–17.7) monthsafter SIF recruitment. The level of CIRI is relatively low inthe context of previously reported prevalence (10–30%[7,8]). However, considering that it is based on reportinga current infection, the level in this study is concerning.Proportion of SEOSI participants reporting a CIRI (January 1, 2004 – December 31, 2005, n = 1065)Figure 1Proportion of SEOSI participants reporting a CIRI 0%2%4%6%8%10%12%14%16%18%20%Jan-04Jun-04Jan-05Jun-05Follow-upTable 1: Univariate and multivariate analysis of developing a CIRI among SEOSI participants (n = 1065)Variable OR (95% - CI) AOR (95% - CI)Age(per year older) 0.98 (0.96 – 1.00) 1.00 (0.98 – 1.02)Sex(Female vs. Male) 1.90 (1.39 – 2.58) 1.68 (1.16 – 2.43)Unstable housing(Yes vs. No) 1.56 (1.15 – 2.12) 1.49 (1.10 – 2.03)DTES residence(Yes vs. No) 1.33 (0.96 – 1.85)Sex trade*(Yes vs. No) 1.74 (1.24 – 2.45) 1.02 (0.67 – 1.56)Borrowing syringes*(Yes vs. No) 1.88 (1.22 – 2.88) 1.60 (1.03 – 2.48)Requiring help inject*(Yes vs. No) 1.85 (1.37 – 2.50) 1.42 (1.03 – 1.94)Use puddle to inject*(Yes vs. No) 1.32 (0.83 – 2.11)Cocaine injection*(Daily vs. Not) 1.66 (1.23 – 2.25) 1.41 (1.02 – 1.95)Heroin injection*(Daily vs. Not) 1.53 (1.14 – 2.04) 1.26 (0.93 – 1.72)Crack injection*(Daily vs. Not) 1.54 (0.96 – 2.46)Crystal meth. injection*(Daily vs. Not) 1.48 (0.73 – 3.02)Speedball injection*(Daily vs. Not) 2.00 (1.35 – 2.96) 1.37 (0.89 – 2.11)SIF use(Always vs. Not) 0.47 (0.23 – 0.94) 0.58 (0.29 – 1.19)HIV serostatus(Yes vs. No) 1.23 (0.85–1.77)HCV serostatus(Yes vs. No) 1.35 (0.81 – 2.25)Note: *activity past 6 months, DTES = downtown eastside, meth. = methamphetamine, SIF = supervised injection facilityPage 3 of 6(page number not for citation purposes)Furthermore, our results indicate that being female, livingin unstable housing, borrowing syringes, requiring help(January 1, 2004 – December 31, 2005, n = 1065).BMC Public Health 2008, 8:405 http://www.biomedcentral.com/1471-2458/8/405injecting, and injecting cocaine daily were independentlyassociated with developing a CIRI.The observed associations between female sex, dailycocaine injection, living in unstable housing and an ele-vated risk of having a CIRI are congruent with previousanalyses. The link between being female and having aCIRI echoes the findings of previous studies [10,12,13],and may reflect, in part, the complex gender dynamicsthat exist within injection drug using populations wherewomen are often dependent on men for the attainmentand administration of drugs [21].With regard to the association between cocaine injectionand development of CIRI [12,13], cocaine's anaestheticproperties may make it more difficult for individuals toknow whether or not they are hitting a vein (as opposedto injecting in the surrounding tissue or skin), resulting intrauma through repetitive attempts to access the vein[22,23]. Missing a vein increases vulnerability for CIRIsince injecting into the surrounding tissue creates a nicheenvironment in which bacteria can thrive [9]. Further, dueto cocaine's short half-life in comparison to heroin, it isoften injected many more times than heroin, which alsoincreases the likelihood of CIRI and transmission ofblood-borne viruses such as HIV [16]. Indeed, as indi-cated by our findings and others, intensity of drug useappears to play a role in CIRI development, as individualswho inject at least once daily have been repeatedly identi-fied to be at elevated risk for developing a CIRI [12,13].The association between homelessness and an injectionsite infection has been reported [24]. According to the'risk environment' framework, as proposed by Rhodes etal., structural and environmental factors are important toconsider when assessing risks for drug-related harms asthey shape the context in which individual behaviouroccurs [24]. It may be that those in our study whoreported living in unstable housing may also frequentrisky injecting environments, which in turn lead to rushedinjections (i.e., not taking time to go through every step ofthe injection process to ensure a safer injection) or inject-ing in a high-risk location like the groin for a 'quick fix'[25]. A recent review of homelessness found that between15–50% of homeless individuals inject drugs, and it wasfurther reported that breaks of the skin were commonamong such individuals, often leading to bacterial infec-tions due to a lack of hygiene [26]. In addition, the smallsize, shared facilities and often unhygienic environmentof single room occupancy hotels that are common in theDTES promote disease transmission [27].Among the novel findings in the present study are thesyringes is known to be a strong risk factor for blood-borne viral transmission [28,29]. Our study shows thatthe transmission of CIRI-related bacteria via sharing ofsyringes should also be considered by IDU, health profes-sionals, and public health practitioners. However, it isalso possible that sharing syringes is not the active vectorin this transmission and that this transmission is by otherinjection drug paraphernalia. Requiring help injecting, arisk factor for CIRI in this study, may increase risk of expo-sure to bacteria when the individual who is administeringthe injection injects themselves before injecting the per-son who requires assistance (i.e., "second on the needle").This study has several limitations. Firstly, we were unableto examine "skin popping" as an independent variable inthis study due to a low number of participants reportingthis behaviour. This may be due to the fact that the prac-tice is more commonly associated with injection of "blacktar" heroin, a type rarely used in Vancouver. Given thatour "skin popping" question in the study questionnairepertained to intentional "skin popping" it is also possiblethat participants who injected subcutaneously or intra-muscularly by mistake were not captured. Secondly, ourstudy relies on self-report and therefore is potentially vul-nerable to social desirability bias. However, we know ofno reason to suspect differential reporting between partic-ipants with or without CIRI. Thirdly, it is possible thatindividuals who inject at the SIF are different from thosewho do not. A study by Wood et al. found that IDU thatused the SIF were more likely to be at a higher risk ofblood-borne disease infection and overdose comparedwith IDU who did not use the SIF [30]. Therefore, ourresults may not be generalizable to the broader local IDUpopulation. However, the SEOSI cohort was randomlyrecruited from within the SIF [15]. Therefore, we believethat our sample is representative of SIF users. Fourthly, theexternal validity of this study should be interpreted withcaution, as Vancouver's DTES neighbourhood is uniquedue to its large open drug scene and the high prevalenceof cocaine injection. Finally, this study investigates onlyCIRI related to injection drug use and not other behav-iours for example. However, we feel this is an importantdistinction as it serves to reduce misclassification biasbased on reporting CIRI that may be related to other fac-tors such as picking the skin induced by cocaine psychosis[16].The prevalence of CIRI among IDU in this study suggeststhat a higher priority should be placed on reducing theincidence of these preventable infections. Since a positiveimpact of the SIF on access to assessment, care, and treat-ment of CIRI has been noted [31], it is likely that the rateof CIRI observed here may be lower than the rate observedPage 4 of 6(page number not for citation purposes)associations between CIRI development and borrowingsyringes and requiring help injecting. Borrowing usedin the broader community. Combining harm reduction(e.g., needle exchange programs and supervised injectionBMC Public Health 2008, 8:405 http://www.biomedcentral.com/1471-2458/8/405facilities) and treatment services may be of value to pre-vent and/or reduce the risk for CIRI development. Specif-ically, integrating wound management care into existingharm reduction services, such as needle exchange pro-grams and SIF, in community settings has been found tobe feasible, cost-effective and beneficial for preventingand treating CIRI and other related skin infections such asnecrotizing fasciitis [32]. Expansion of such programsamong harm reduction services may be reasonable, espe-cially as many IDU remain medically underserved [33].ConclusionIn summary, we found that over a two-year period thatbetween six and 10 percent of IDU presented with a CIRI.Risk factors for CIRI development included being female,living in unstable housing, borrowing used syringes,requiring help injecting and injecting cocaine daily. Thesefindings collectively point to the need to develop a rangeof interventions that target the various individual, socialand environmental risks for CIRI development.Competing interestsThe authors declare that they have no competing interests.Authors' contributionsELS conceived and designed the study and drafted themanuscript. ELS and RZ performed the statistical analyses.ELS, TK, RH, EW, MT, contributed to the design and coor-dination of the study and provided assistance with inter-pretation of the results and the draft of the manuscript. Allauthors read and approved the final manuscript.AcknowledgementsThe authors wish to thank the participants in SEOSI and the staff of Insite, the Portland Hotel Society, and Vancouver Coastal Health (Chris Buchner, David Marsh, and Heather Hay.) We also thank the current and past SEOSI staff. We would specifically like to thank Deborah Graham, Tricia Colling-ham, Caitlin Johnston, Steve Kain, and Calvin Lai for their research and administrative assistance. We thank Patrizia Carrieri, Viviane Dias Lima and Karissa Johnstone for their statistical expertise. We thank Drs. Sam Sheps and Robert Hogg for their input and feedback. The evaluation of the super-vised injecting facility was originally made possible through a financial con-tribution from Health Canada, although the views expressed herein do not represent the official policies of Health Canada. The evaluation is currently supported by the Canadian Institutes of Health Research and Vancouver Coastal Health. TK and ELS are supported by the Michael Smith Foundation for Health Research and the Canadian Institutes of Health Research. MT is supported by the Michael Smith Foundation for Health Research.References1. Alter MJ: Epidemiology of Hepatitis C.  Hepatology 1997,26:62-65.2. Holmberg SD: The estimated prevalence and incidence of HIVin 96 large US metropolitan areas.  Am J Public Health 1996,86:642-654.3. Hagan H, Des Jarlais DC: HIV and HCV infection among inject-ing drug users.  Mt Sinai J Med 2000, 67:423-8.5. Irish C, Maxwell R, Dancox M, Brown P, Trotter C, Verne J, et al.:Skin and soft tissue infections and vascular disease amongdrug users, England.  Emerg Infect Dis 2007, 13(10):1510-1511.6. Palepu A, Tyndall MW, Leon H, Muller J, O'Shaughnessy MV, Schech-ter MT, et al.: Hospital utilization and costs in a cohort of injec-tion drug users.  CMAJ 2001, 165:415-20.7. 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Arch Surg 2004, 139:947-953.Pre-publication historyThe pre-publication history for this paper can be accessedhere:http://www.biomedcentral.com/1471-2458/8/405/prepubyours — you keep the copyrightSubmit your manuscript here:http://www.biomedcentral.com/info/publishing_adv.aspBioMedcentralPage 6 of 6(page number not for citation purposes)


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