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Female gender predicts lower access and adherence to antiretroviral therapy in a setting of free healthcare Tapp, Christine; Milloy, M-J; Kerr, Thomas; Zhang, Ruth; Guillemi, Silvia; Hogg, Robert S; Montaner, Julio; Wood, Evan Apr 6, 2011

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RESEARCH ARTICLE Open AccessFemale gender predicts lower access andadherence to antiretroviral therapy in a settingof free healthcareChristine Tapp1, M-J Milloy1, Thomas Kerr1, Ruth Zhang1, Silvia Guillemi1, Robert S Hogg1, Julio Montaner1 andEvan Wood1,2*AbstractBackground: Barriers to HIV treatment among injection drug users (IDU) are a major public health concern.However, there remain few long-term studies investigating key demographic and behavioral factors - and genderdifferences in particular - that may pose barriers to antiretroviral therapy (ART), especially in settings with universalhealthcare. We evaluated access and adherence to ART in a long-term cohort of HIV-positive IDU in a settingwhere medical care and antiretroviral therapy are provided free of charge through a universal healthcare system.Methods: We evaluated baseline antiretroviral use and subsequent adherence to ART among a Canadian cohort ofHIV-positive IDU. We used generalized estimating equation logistic regression to evaluate factors associated with95% adherence to antiretroviral therapy estimated based on prescription refill compliance.Results: Between May 1996 and April 2008, 545 IDU participants were followed for a median of 23.8 months (Inter-quartile range: 8.5 - 91.6), among whom 341 (63%) were male and 204 (37%) were female. Within the six-monthperiod prior to the baseline interview, 133 (39%) men and 62 (30%) women were on ART (p = 0.042). Afteradjusting for clinical characteristics as well as drug use patterns measured longitudinally throughout follow-up,female gender was independently associated with a lower likelihood of being 95% adherent to ART (Odds Ratio[OR] = 0.70; 95% Confidence Interval: 0.53-0.93).Conclusions: Despite universal access to free HIV treatment and medical care, female IDU were less likely to accessand adhere to antiretroviral therapy, a finding that was independent of drug use and clinical characteristics. Thesedata suggest that interventions to improve access to HIV treatment among IDU must be tailored to address uniquebarriers to antiretroviral therapy faced by female IDU.BackgroundDuring the past decade, there have been significantadvances in the treatment of HIV disease with the adventof antiretroviral therapy (ART) [1]. ART has been shownto suppress plasma HIV RNA, contributing to substantialreductions in HIV-related morbidity and mortalityamong people receiving treatment [2,3]. However, effec-tive management of HIV disease requires high levels ofART adherence [4,5], as incomplete adherence can detri-mentally affect virological control and subsequentlydisease progression, as well as contribute to elevatedrates of antiretroviral resistance [5]. Therefore, ensuringthat HIV-positive persons maintain high levels of ARTadherence is of critical clinical importance.Although newer, simplified ART regimens haveenhanced treatment adherence [6], specific HIV-positivepopulations, such as injection drug users (IDU), continueto face barriers to accessing and adhering to ART. Recentinjection drug use is associated with both non-adherenceto ART and HIV disease progression [7,8], and manyIDU live in unstable housing, have undiagnosed oruntreated mental illness, high rates of incarceration,and street-involved survival-lifestyles, which may all com-plicate delivery of HIV-related treatments [9,10].* Correspondence: uhri-ew@cfenet.ubc.ca1British Columbia Centre for Excellence in HIV/AIDS, St. Paul’s Hospital,Vancouver, CanadaFull list of author information is available at the end of the articleTapp et al. BMC Infectious Diseases 2011, 11:86http://www.biomedcentral.com/1471-2334/11/86© 2011 Tapp et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative CommonsAttribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction inany medium, provided the original work is properly cited.In addition, gender is an important and under studiedvariable that may explain barriers to effective HIV care.However, although previous research has assessed factorsassociated with access and adherence to ART amongIDU, there remains a paucity of research investigatingdifferences in adherence between male and female IDUspecifically, as most of the previous research has exploredadherence among either IDU generally or between non-IDU men and women [11-15]. There remain few long-term, prospective studies assessing gender as a factor thataffects adherence conducted within a setting of universalhealthcare.British Columbia, Canada has a universally accessible,publicly funded healthcare system without user fees orother financial barriers to medical services, including allHIV/AIDS care. This allows for investigation of HIV-related outcomes without the potentially confoundingeffect of financial barriers to medical care and HIVtreatment that may be present in other settings. There-fore, we conducted the present study to investigate fac-tors associated with adherence to ART among aCanadian cohort of HIV-positive IDU and specificallyexamined if gender differences in adherence to ARTexisted in this context.MethodsThe AIDS Care Cohort to evaluate Exposure to SurvivalServices (ACCESS) is a prospective observational cohortof HIV-seropositive injection drug users (IDU) in Van-couver, Canada. The cohort has been described in detailpreviously [14,16,17], and was populated through snow-ball sampling and extensive street outreach methods inthe city’s Downtown Eastside. Individuals were eligiblefor ACCESS if they were aged 18 years or older, HIVseropositive, had used injection drugs, and providedwritten informed consent. At baseline and semi-annually, participants answer a standardized interviewer-administered questionnaire and provide blood samplesfor serologic analysis.As previously described [14,16,17], the local settingis somewhat unique in that there is a universal health-care system and a province-wide centralized antiretro-viral dispensation program and HIV/AIDS laboratorywhich enables a complete prospective profile of allpatient CD4 cell count determinations and plasmaHIV-1 RNA levels, as well as a complete prospectiveprofile of antiretroviral therapy use among cohort par-ticipants. This includes the specific antiretroviralagents and the prescribed dose, a validated measure ofpatient adherence derived from prescription refillcompliance, which is described further below [17,18].The study has been approved by the ProvidenceHealth Care/University of British Columbia ResearchEthics Board. Plasma HIV-1 RNA was measured usingthe Roche Amplicor Monitor assay (Roche MolecularSystems, Mississauga, Canada).In the present study, we included all participants whowere recruited and completed at least one interviewbetween May 1996 and April 2008, and excluded onlythose where clinical data were unavailable. As indicatedabove, the primary independent variable of interest wasgender and, to compare rates of ART use at baseline,we evaluated access to ART at the time of recruitmentinto the cohort by examining the proportion of partici-pants who had been on ART in the 6-month periodprior to the baseline interview. Since we had long-termprospective data, we then assessed the longitudinal pat-tern of ART exposure by examining ART adherenceduring the six-month period preceding each semi-annual follow-up visit throughout follow-up. As inprevious studies using this validated and confidentialpharmacy dispensation data [17,18], we measured adher-ence to therapy in each six-month period as a ratio ofthe number of days ART was dispensed over the num-ber of days an individual was eligible for ART anddefined adherence as equal to or greater than 95%adherence to ART during this period.We considered explanatory variables potentially asso-ciated with the dependent variable including: gender(female vs. male); age (<24 yrs vs. ≥24 yrs); ethnicity(Aboriginal ancestry vs. other); daily injection heroin use(yes vs. no); daily cocaine injection (yes vs. no); dailycrack cocaine smoking (yes vs. no); current methadoneuse (yes vs. no); any treatment use (yes vs. no); educa-tion (less than high school vs. other); employment (regjob, temp work, self-emp vs. other); and unstable hous-ing (yes vs. no). Age was defined as a dichotomous vari-able according to the World Health Organization’sdefinition of a ‘young person’, using the upper age limitof 24 as the cut-off [19]. All dichotomous behaviouralvariables referred to the six-month period prior to theinterview. As in our previous work [18], we definedunstable housing as living in a single-room occupancyhotel, shelter or being homeless. Clinical variablesincluded baseline HIV-1 RNA level (per log10copies/mL)and CD4 cell count (per 100 cells/mm3), using the clo-sest measure within one year of the baseline.We began by comparing the rate of ART use at base-line. We then examined univariate associations betweenthe explanatory variables and ART adherence through-out follow-up. Because serial measures for each variablewere available for each subject, we used generalised esti-mating equations (GEE) for the analysis of correlateddata. This approach allows for the identification of fac-tors associated with the outcome over the entire studyperiod. Data from every participant follow-up visit wereconsidered in this analysis. Missing data were addressedthrough the GEE estimating mechanism which uses allTapp et al. BMC Infectious Diseases 2011, 11:86http://www.biomedcentral.com/1471-2334/11/86Page 2 of 7available pairs method to encompass the missing datafrom dropouts or intermittent missing. All non-missingpairs of data are used in the estimators of the workingcorrelation parameters. Standard errors were calculatedusing an exchangeable correlation structure, adjusted bymultiple observations for each individual. GEE modelshave routinely been used to analyse datasets containingrepeated measures, including longitudinal IDU cohorts[20,21].Following examination of the univariate results we fita multivariate GEE logistic regression model using an apriori defined model building protocol whereby weincluded all explanatory variables with a univariate p-value < 0.05. We also ran the models with interactionterms for key independent variables in order to bettercompare rates of adherence between men and women.We conducted additional sub-analyses adjusting for keyclinical or demographic characteristics and for the yearof the baseline interview to account for advances inantiretroviral therapy during the study period. All statis-tical procedures were performed using SAS version 9.1(SAS, Cary, NC, USA). All p-values are two-side.ResultsBetween May 1996 and April 2008, 545 participantswere eligible for the present study, and there was amedian of 23.8 months (Inter-quartile range: 8.5 - 91.6)of prospective follow-up. Of these study participants,341 (63%) were male and 204 (37%) were female. Thecharacteristics of the study population stratified by gen-der are shown in Table 1. As indicated in the table, 133(39%) men and 62 (30%) women were on ART in thesix-month period prior to the baseline interview (p =0.042). There were 1186 (26.6%) periods where indivi-duals were adherent out of 4460 total observations.Overall, 81 (19%) out of 422 males and 83 (29%) out of287 females were excluded from the analysis as a resultof missing baseline CD4 count or viral load.The results of the univariate GEE logistic regressiondemonstrated that methadone use (Odds Ratio [OR] =2.44 [95% CI: 2.01-2.96]; p < 0.001), and accessing anyaddiction treatment (OR = 1.50 [95% CI: 1.26-1.79]; p <0.001) were associated with being 95% adherent to ART,whereas higher baseline viral load (OR = 0.54 [95% CI:0.48-0.60]; p < 0.001), education (OR = 0.56 [95% CI:0.37-0.85; p = 0.007] age less than 24 years (OR = 0.16[95% CI: 0.08-0.31]; p < 0.001), daily heroin injection(OR = 0.38 [95% CI: 0.30-0.48]; p < 0.001), daily cocaineinjection (OR = 0.48 [95% CI: 0.40-0.57]; p < 0.001), andfemale gender (OR = 0.69 [95% CI: 0.52-0.90]; p =0.006) were negatively associated with 95% adherence.Table 2 outlines the results of the univariate GEEanalysis.Multivariate GEE regression demonstrated that metha-done use (OR = 2.35 [95% CI: 1.88-2.94]; p < 0.001) wasindependently associated with 95% ART adherence.Higher baseline viral load (OR = 0.81 [95% CI: 0.68-0.97]; p = 0.018), age less than 24 years (OR = 0.27[95% CI: 0.13-0.57]; p < 0.001), daily heroin injection(OR = 0.56 [95% CI: 0.43-0.73]; p < 0.001), daily cocaineinjection (OR = 0.57 [95% CI: 0.47-0.71]; p < 0.001);Table 1 Baseline socio-demographic, behavioural, andclinical characteristics of ACCESS participants†, stratifiedby genderCharacteristic Malen = 341(63%)Femalen = 204(37%)Odds Ratio(95% CI)pvalueAge≥ 24 years 332 (97) 179 (88) 5.2 (2.4-11.3) <0.001<24 years 9 (3) 25 (12)AboriginalethnicityNo 249 (73) 111 (54)Yes 92 (27) 93 (46) 2.3 (1.6-3.3) <0.001Daily heroin use*No 264 (77) 129 (63)Yes 77 (23) 75 (37) 2.0 (1.4-2.9) <0.001Daily cocaine use*No 227 (67) 126 (62)Yes 114 (33) 78 (38) 1.2 (0.9-1.8) 0.256Daily crack use*No 271 (79) 142 (70) 1.7 (1.1-2.5) 0.009Yes 70 (21) 62 (30)Currentmethadone useNo 251 (74) 125 (61)Yes 90 (26) 79 (39) 1.8 (1.2-2.6) 0.003Any treatmentNo 140 (41) 75 (37)Yes 201 (59) 129 (63) 1.2 (0.8-1.7) 0.320Unstable housingNo 95 (28) 64 (31)Yes 246 (72) 140 (69) 0.8 (0.6-1.2) 0.383On ART at baselineNo 208 (61) 142 (70)Yes 133 (39) 62 (30) 0.7 (0.5-1.0) 0.042Viral load(log10copies/mL)≥ 100,000 66 (19) 32 (16) 1.3 (0.8-2.1) 0.281<100,000 275 (81) 172 (84)CD4+ count (cells/mm3)≥ 200 261 (77) 164 (80) 0.8 (0.5-1.2) 0.294<200 80 (23) 40 (20)†Includes all eligible participants that completed at least one interviewbetween May 1996 and April 2008 and where baseline clinical data wasavailable. *Refers to the six-month period prior to the baseline interview.Tapp et al. BMC Infectious Diseases 2011, 11:86http://www.biomedcentral.com/1471-2334/11/86Page 3 of 7education (OR = 0.65 [95% CI: 0.43-0.98]; p = 0.04);and, female gender (OR = 0.70 [95% CI: 0.53-0.93]; p =0.013) were independently and negatively associatedwith 95% adherence to ART. There were no statisticalinteractions observed in the multivariate GEE analysis.Table 3 and Figure 1 show results of the multivariateGEE logistic regression.We conducted several sub-analyses of behavioural andclinical variables. A sub-analysis was conducted definingdrug use as a 6-level categorical variable using ‘daily inject-ing’ as the reference level showed results that were consis-tent with analyses defining drug use as a dichotomousvariable (data available from the corresponding author).Sub-analyses adjusting for year of the baseline interview,to account for advances in antiretroviral therapy duringthe study period, were consistent with the primary analysis(data available from the corresponding author). Addition-ally, a sub-analysis of time-updated clinical variables todetermine if clinical outcomes affected adherence or drugusing behaviours demonstrated that, although cocaine usewas no longer significant, the gender effect remained(OR = 0.56 [95% CI: 0.43-0.74]; p < 0.001).DiscussionThe present study demonstrates that female IDU areapproximately 30% less likely to adhere to ART, anassociation that persisted after intensive covariateadjustment. To our knowledge this is the first long-termstudy to assess key demographic and behavioural factorsassociated with ART adherence within a community-recruited cohort and within a context of a universalhealthcare system, and implies that barriers to adher-ence among female IDU that are not explained by finan-cial barriers.Although female gender remained significantly asso-ciated with worse adherence in multivariate analyses, itis noteworthy that the strength of the association dimin-ished when we adjusted for drug using and other beha-vioural variables. This implies that drug-usingcharacteristics, which may create barriers to ART adher-ence, were more common among female IDU in oursetting and this was confirmed by our baseline gendercomparisons. These data suggest that women are moreengaged in street-involved, survival activities, and arethereby more marginalized from the healthcare system,which poses a barrier to ART access and adherence.The importance of maintaining high levels of ARTadherence is well established [4,5], and ensuring that vul-nerable and disadvantaged populations have equal accessto HIV treatment is crucial from both an individual andTable 2 Univariate GEE*j analysis of sociodemographic,behavioural and clinical factors associated with ≥ 95%ART adherenceVariable OR (95% CI) p-valueGender(Female vs. Male) 0.69 (0.52-0.90) 0.006Age(<24 yrs vs. ≥ 24 yrs) 0.16 (0.08-0.31) <0.001Ethnicity(Aboriginal vs. other) 0.97 (0.74-1.28) 0.841Heroin use*(Daily vs. not daily) 0.38 (0.30-0.48) <0.001Cocaine use*(Daily vs. not daily) 0.48 (0.40-0.57) <0.001Crack use*(Daily vs. not daily) 0.94 (0.78-1.13) 0.509Methadone treatment(Yes vs. no) 2.44 (2.01-2.96) <0.001Other addiction treatment†(Yes vs. no) 1.50 (1.26-1.79) <0.001Education(less than highschool vs. other) 0.56 (0.37-0.85) 0.007Employment(reg job, temp work, self-emp vs. other) 1.11 (0.87-1.41) 0.401Unstable housing(Yes vs. no) 0.90 (0.76-1.07) 0.239Viral load(per log10copies/mL) 0.54 (0.48-0.60) <0.001CD4+ count(per 100 cells/mm3) 0.95 (0.89-1.00) 0.047*Refers to the previous six-month period. †Defined as drug treatment otherthan methadone in the past six months. jGEE = Generalized EstimatingEquation.Table 3 Multivariate GEE*j analysis of sociodemographic,behavioural and clinical factors associated with ≥ 95%ART adherenceVariable OR (95% CI) p-valueGender(Female vs. Male) 0.70 (0.53-0.93) 0.013Age(<24 yrs vs. ≥ 24 yrs) 0.27 (0.13-0.57) <0.001Heroin use*(Daily vs. not daily) 0.56 (0.43-0.73) <0.001Cocaine use*(Daily vs. not daily) 0.57 (0.47-0.71) <0.001Methadone treatment(Yes vs. no) 2.35 (1.88-2.94) <0.001Education(less than highschool vs. other) 0.65 (0.43-0.98) 0.04Viral load(per log10copies/mL) 0.81 (0.68-0.97) 0.018CD4+ count(per 100 cells/mm3) 0.89 (0.84-0.94) <0.001*Refers to the previous six-month period. †Defined as drug treatment otherthan methadone in the past six months. jGEE = Generalized EstimatingEquation.Tapp et al. BMC Infectious Diseases 2011, 11:86http://www.biomedcentral.com/1471-2334/11/86Page 4 of 7public health standpoint [3,22]. For example, recentresearch from the COHERE cohort in Europe indicatesthat IDU and women, and particularly female IDU, experi-ence higher mortality rates even after achieving optimalCD4 cell counts while on ART, underscoring the urgenthealth needs of this population and the importance ofmaintaining high rates of adherence [23]. However, thereare currently few long term studies pertaining to factorsassociated with ART adherence among IDU, particularlyin settings where HIV care is provided free of charge. Pre-vious research regarding ART adherence across multiplepopulations in the U.S.A. found that, in a post-ART era,socio-demographic and behavioural factors - such as lowereducation status, lower income, lack of medical care cov-erage, a history of frequent drug or alcohol use, African-American race, and female gender - are more frequentlyassociated with access and adherence to ART than clinicalfactors [12,24,25]. Importantly, female gender has beenshown to be associated with lower rates of ART adherenceacross several sub-groups, including both IDU and non-IDU [15,25,26]. Compounding this, a national U.S. studyfound that female IDU were among the most disadvan-taged sub-groups of vulnerable HIV-positive populationsand were about half as likely to receive ART compared tohomosexual males, even after adjusting for other socio-demographic variables [27]. However, because these stu-dies were conducted in the U.S., financial and otherbarriers inherent to the American healthcare system makeit difficult to fully determine whether other factors may beaffecting the association with gender and other socio-demographic characteristics. The present study enhancesthe current body of research by demonstrating that gen-dered barriers to ART adherence persist even in settingswith a universal healthcare system.Research regarding methods to reduce barriers toART are limited, particularly concerning gendered bar-riers, though the need for targeted interventions is clear[23]. Some studies have suggested that health systemchanges such as educating health care providers aboutthe disparities that exist among populations accessingtreatment, anonymous HIV testing and treatment sites,and same-day clinic appointments or extended hours ofoperation, may increase access and adherence to ARTamong vulnerable, marginalized populations [24,27]. Inaddition, providing women-only health and community-based services, increasing efforts to improve self-efficacyamong women in engaging with the healthcare system,as well as education dispelling misinformation and mis-conception about HIV-treatment, may all contribute toimproving access and adherence among women andfemale IDU, specifically [24,28]. However, as our ana-lyses demonstrate, drug using characteristics and thecorollary of more survival-based activities, are also a sig-nificant barrier to ART adherence among women andare likely a first point for interventions that seek toimprove access to healthcare services among IDUwomen.There are some limitations to this study. Most impor-tantly, as this is an observational study, the associationbetween gender and ART adherence should be inter-preted with caution. It is possible that there are otherconfounding factors that were not measured andadjusted for in this study. However, our analysisincluded a large number of explanatory variables and weused a liberal a priori defined model fitting protocol[18]. In addition, our measure of adherence was basedon prescription refill compliance, which measures some-thing different than daily pill taking. With respect toFigure 1 Factors independently associated with 95% ART adherence among HIV-positive injection drug users in GEE* logisticregression. *GEE = Generalized Estimating Equation. Multivariate model fit.Tapp et al. BMC Infectious Diseases 2011, 11:86http://www.biomedcentral.com/1471-2334/11/86Page 5 of 7this concern, we note that our measure of ART adher-ence has been shown to predict virological suppression[29], CD4 response [30], and mortality [17,18] and thusthe differences we observed are likely to be clinically sig-nificant. Lastly, we do not feel that missing data played arole in our results given that all non-missing pairs ofdata are included as a result of using generalized esti-mating equation logistic regression in the statistical ana-lysis when employing generalized estimating equation(GEE) logistic regression.ConclusionsThe current study demonstrates that female gender pre-sents an additional barrier for access and adherence toART among injection drug users, independent of druguse and other socio-behavioural and clinical characteris-tics. This is evidence that even within a context wheremedical care and ART are provided free to HIV-positiveindividuals, there remain important healthcare accessdifferences between male and female IDU. Other socio-structural factors are also critically important in affect-ing equitable access to necessary HIV treatment [31],and women often face barriers derived from their com-paratively lower socio-economic status, and broader, sys-temic inequities that persist even within a context ofuniversal healthcare. In order to improve access andadherence to ART among IDU women, gender-specificinterventions should be developed which recognizethese unique barriers.AcknowledgementsThe authors thank the study participants for their contribution to theresearch, as well as current and past researchers and staff. We wouldspecifically like to thank Deborah Graham, Tricia Collingham, Sandra Niven,Brandon Marshall, Caitlin Johnston, Steve Kain, Benita Yip, and Calvin Lai fortheir research and administrative assistance. The study was supported by theUS National Institutes of Health (R01DA021525) and the Canadian Institutesof Health Research (MOP-79297, RAA-79918). Thomas Kerr is supported bythe Michael Smith Foundation for Health Research and the CanadianInstitutes of Health Research.Author details1British Columbia Centre for Excellence in HIV/AIDS, St. Paul’s Hospital,Vancouver, Canada. 2Department of Medicine, University of British Columbia,Vancouver, Canada.Authors’ contributionsEW, CT, and MJM drafted the manuscript. RZ performed the statisticalanalysis.All authors read and approved the final manuscript.Competing interestsConflict of Interest Disclosure Statement for J MontanerJulio Montaner is supported by the Ministry of Health Services and theMinistry of Healthy Living and Sport, from the Province of British Columbia;through a Knowledge Translation Award from the Canadian Institutes ofHealth Research (CIHR); and through an Avant-Garde Award (No.1DP1DA026182-01) from the National Institute of Drug Abuse, at the USNational Institutes of Health. 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Wood E, Montaner JS, Chan K, Tyndall MW, Schechter MT, Bangsberg D,O’Shaughnessy MV, Hogg RS: Socioeconomic status, access to tripletherapy, and survival from HIV-disease since 1996. AIDS 2002,16(15):2065-2072.Pre-publication historyThe pre-publication history for this paper can be accessed here:http://www.biomedcentral.com/1471-2334/11/86/prepubdoi:10.1186/1471-2334-11-86Cite this article as: Tapp et al.: Female gender predicts lower accessand adherence to antiretroviral therapy in a setting of free healthcare.BMC Infectious Diseases 2011 11:86.Submit your next manuscript to BioMed Centraland take full advantage of: • Convenient online submission• Thorough peer review• No space constraints or color figure charges• Immediate publication on acceptance• Inclusion in PubMed, CAS, Scopus and Google Scholar• Research which is freely available for redistributionSubmit your manuscript at www.biomedcentral.com/submitTapp et al. 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