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Improved adherence to modern antiretroviral therapy among HIV-infected injecting drug users Mann, Bikaramjit; Milloy, M-J; Kerr, Thomas; Zhang, Ruth; Montaner, Julio; Wood, Evan Nov 1, 2012

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Improved Adherence to Modern Antiretroviral Therapy amongHIV Infected Injection Drug UsersBikaramjit Mann1, M-J Milloy2, Thomas Kerr2,3, Ruth Zhang2, Julio Montaner2,3, and EvanWood2,31Department of Medicine, University of Calgary, Calgary, Canada2British Columbia Centre for Excellence in HIV/AIDS, St. Paul’s Hospital, Vancouver, Canada3Department of Medicine, University of British Columbia, Vancouver, CanadaAbstractObjectives—Adherence to antiretroviral therapy (ART) among injection drug users (IDU) isoften sub-optimal, yet little is known about changes in patterns of adherence since the advent ofhighly active antiretroviral therapy in 1996. We sought to assess levels of optimal adherence toART among IDU in a setting of free and universal HIV care.Methods—Data was collected through a prospective cohort study of HIV-positive IDU inVancouver, British Columbia. We calculated the proportion of individuals achieving at least 95%adherence in the year following initiation of ART from 1996 to 2009.Results—Among 682 individuals who initiated ART, the median age was 37 (31–44) years with248 (36.4%) female participants. The proportion achieving at least 95% adherence increased overtime from 19.3% in 1996 to 65.9% in 2009 (Cochrane-Armitage test for trend: p < 0.001). In alogistic regression model examining factors associated with 95% adherence, initiation year wasstatistically significant (Odds Ratio = 1.08, 95% Confidence Interval: 1.03–1.13, p < 0.001 peryear after 1996) after adjustment for a range of drug use variables and other potential confounders.Conclusions—The proportion of IDU achieving at least 95% adherence during the first year ofART has consistently increased over a 13-year period. Although improved tolerability andconvenience of modern ART regimens likely explain these positive trends, by the end of the studyperiod a substantial proportion of IDU still had sub-optimal adherence demonstrating the need foradditional adherence support strategies.INTRODUCTIONIn recent decades, there have been remarkable advances in HIV treatment and care. Inparticular, antiretroviral therapy (ART) has resulted in dramatic reductions in morbidity andmortality for those living with HIV/AIDS (1, 2). However, HIV-positive injection drug users(IDU) have benefited less than other HIV-positive individuals from these advances largelydue to reduced access and adherence to ART (3, 4). This is of particular concern given that,Send correspondence to: Evan Wood, MD, PhD, ABIM, FRCPC, Urban Health Research Initiative, British Columbia Centre forExcellence in HIV/AIDS, 608 - 1081 Burrard Street, Vancouver BC V6Z 1Y6, Canada, Tel: 604 806 9692, Fax: 604 806 9044, uhri-ew@cfenet.ubc.ca.Conflicts of Interest Statement: Dr. Montaner has received educational grants from, served as an ad hoc advisor to or spoken atvarious events sponsored by Abbott Laboratories, Agouron Pharmaceuticals Inc., Boehringer Ingelheim Pharmaceuticals Inc., BoreanPharma AS, Bristol – Myers Squibb, DuPont Pharma, Gilead Sciences, GlaxoSmithKline, Hoffmann – La Roche, Immune ResponseCorporation, Incyte, Janssen – Ortho Inc., Kucera Pharmaceutical Company, Merck Frosst Laboratories, Pfizer Canada Inc., SanofiPasteur, Shire Biochem Inc., Tibotec Pharmaceuticals Ltd. and Trimeris Inc.NIH Public AccessAuthor ManuscriptHIV Med. Author manuscript; available in PMC 2013 November 01.Published in final edited form as:HIV Med. 2012 November ; 13(10): 596–601. doi:10.1111/j.1468-1293.2012.01021.x.NIH-PA Author ManuscriptNIH-PA Author ManuscriptNIH-PA Author ManuscriptThis is the peer reviewed version of the following article: Mann, B., Milloy, M.-J., Kerr, T., Zhang, R., Montaner, J., & Wood, E. (2012). Improved adherence to modern antiretroviral therapy among HIV-infected injecting drug users. HIV Medicine, 13(10), 596-601, which has been published in final form at 10.1111/j.1468-1293.2012.01021.x. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Self-Archiving.during the past two decades, the global HIV epidemic has transitioned from primarily asexually driven epidemic to one in which syringe sharing among illicit IDU contributes to asignificant proportion of infections (5). For instance, while IDU account for approximately5% to 10% of HIV infections globally, this number increases to 30% outside of sub-SaharanAfrica (6).High levels of adherence are required to suppress levels of plasma HIV RNA (7), andincomplete adherence has been associated with virologic rebound and the emergence ofantiretroviral resistance (8). The majority of research on adherence among IDU has focusedon individual-level barriers including illicit drug use,(9) lower self-efficacy,(10, 11) and co-morbid psychiatric conditions;(12–14) however, longer term trends in adherence amongIDU have not been well described. Thus, the present study evaluated long-term adherencepatterns among IDU initiating ART between 1996 and 2009 in a setting of universal accessto HIV care.METHODSData for these analyses were collected through the AIDS Care Cohort to Evaluate access toSurvival Services (ACCESS), an ongoing community-recruited prospective cohort study ofHIV-positive IDU which has been described in detail previously (15, 16). In brief, beginningin May 1996, participants were recruited through self-referral and street outreach fromVancouver’s Downtown Eastside, the local epicenter of drug-related transmission of HIV.At baseline and semi-annually, all HIV-positive participants provided blood samples andcompleted an interviewer-administered questionnaire. The questionnaire elicits demographicdata as well as information about participants’ drug use, including information about type ofdrug, frequency of drug use, involvement in drug treatment and periods of abstinence. Allparticipants provide informed consent and are remunerated $20 CDN for each study visit.The study is somewhat unique in that the province of British Columbia not only delivers allHIV care free of charge through the province’s universal healthcare system but also has acentralized HIV treatment registry. This allows for the confidential linkage of participantsurvey data to the Drug Treatment Program at the BC Centre for Excellence in HIV/AIDS toa complete prospective profile of all HIV-related clinical monitoring and antiretroviraldispensation records. The Providence Health Care/University of British Columbia ResearchEthics Board reviewed and approved the ACCESS study.Participants were eligible for the present analysis if they initiated antiretroviral therapybetween May 1996 and December 2009. The primary outcome in this study was adherenceto antiretroviral therapy based on a previously-validated measure of prescription refillcompliance (22, 23). Specifically, using data from the centralized ART dispensary, wedefined adherence as the number of days for which ART was dispensed over the number ofdays an individual was eligible for ART in the year after ART was initiated. This calculationwas restricted to each patient’s first year on therapy to limit the potential for reversecausation that could occur among patients who cease antiretroviral therapy after they havebecome too sick to take medication (17, 18). We have previously shown this measure ofadherence to reliably predict both virological suppression (19–21) and mortality (22, 23). Asin previous studies, adherence was dichotomized as ≥95% versus <95% (19, 21, 24). As aninitial analysis, we calculated the proportion of individuals achieving at least 95% adherenceto prescribed therapy in the year following initiation of ART during each year from 1996 to2009 and used the Cochrane-Armitage test for trend to assess if rates of adherence changedover time.We then examined factors independently associated with 95% adherence using logisticregression modeling and were specifically interested if year of ART initiation wasMann et al. Page 2HIV Med. Author manuscript; available in PMC 2013 November 01.NIH-PA Author ManuscriptNIH-PA Author ManuscriptNIH-PA Author Manuscriptassociated with adherence after adjustment for potential confounders. We consideredexplanatory variables potentially associated with 95% adherence including: gender (femalevs. male); age (<24 yrs. vs. ≥24 yrs.); ethnicity (Aboriginal ancestry vs. other); daily heroininjection (yes vs. no), daily cocaine injection (yes vs. no); daily crack cocaine smoking (yesvs. no); methadone use (yes vs. no); any other addiction treatment use (yes vs. no); andunstable housing (yes vs. no). Age was defined as a dichotomous variable according to theWorld Health Organization’s definition of a ‘young person’, using the upper age limit of 24as the cut-off (25). All dichotomous behavioural variables referred to the six-month periodprior to the interview. As in our previous work (26), we defined unstable housing as livingin a single-room occupancy hotel, shelter or being homeless. Clinical variables includedbaseline HIV-1 RNA level (per log10copies/mL) and CD4 cell count (per 100 cells/mm3).To estimate the independent relationship between calendar year and likelihood of 95%adherence to prescribed ART, we fit a multivariate logistic regression model using an a-priori defined protocol suggested by Greenland et al (27). First, we fit a full model includingthe primary explanatory variable and all secondary variables with p < 0.20 in univariateanalyses. In a manual stepwise approach we fit a series of reduced models by removing onesecondary explanatory variable, noting the change in the value of the coefficient for theprimary explanatory variable. We then removed the secondary explanatory variableassociated with the smallest absolute change in the primary explanatory coefficient. Wecontinued this process until the maximum change from the full model exceeded 5%. Thistechnique has been used in a number of studies to best estimate the relationship between anoutcome of interest and a primary explanatory variable (28, 29). All statistical procedureswere performed using SAS version 9.1 (SAS, Cary, NC, USA). All p-values are two-sided.ResultsBetween 1996 and 2009, 682 participants initiated ART and were eligible for the presentanalyses. Overall, the median age was 37 years (IQR: 31–44), 243 (36%) were Aboriginaland 248 (36%) were women.As shown in Figure 1, between 1996 and 2009 the proportion of individuals who achieved95% adherence during the first year of ART increased from 19.3% in 1996 to 65.9% in 2009(Cochrane-Armitage test for trend, p < 0.001).As shown in Table 1, in univariate analyses, female participants (Odds Ratio (OR) = 0.62[95% CI: 0.44–0.87]), individuals of Aboriginal ancestry (OR = 0.71 [95% CI: 0.51–0.99]),as well as daily cocaine injection (OR = 0.37 [95% CI: 0.24–0.56]), daily heroin injection(OR = 0.64 [95% CI: 0.42–0.97]) and baseline CD4 count (OR = 0.89 [95% CI: 0.81–0.97])were associated with lower adherence to ART.In the multivariate model, initiation year was significantly associated with the likelihood ofachieving 95% adherence (Adjusted Odds Ratio [AOR] = 1.08 [95% CI: 1.03–1.13] per yearsince 1996) after adjustment for female gender, Aboriginal ancestry, age at baseline,frequent cocaine use, frequent heroin use, receiving treatment for illicit drug or alcohol useand baseline CD4+ cell count.DISCUSSIONIn the present study, adherence to ART during the first year increased significantly from19.3% in 1996 to 65.9% in 2009 among a community recruited cohort of HIV positiveinjection drug users. This trend remained significant even after adjustment for time-updatedpotential confounders including clinical variables, drug use patterns and use of addictiontreatment. We also found that adherence among patients with lower CD4 counts increased,Mann et al. Page 3HIV Med. Author manuscript; available in PMC 2013 November 01.NIH-PA Author ManuscriptNIH-PA Author ManuscriptNIH-PA Author Manuscriptwhich may be related to increased symptoms experienced among participants with lowerCD4 counts.Many studies have found that injection drug use is associated with reduced adherence ofART (30–32). One meta-analysis demonstrated that studies with a lower proportion of IDUare more likely to report a greater proportion of study subjects who are ≥90% adherent toART (33). However, Malta et al. recently demonstrated that IDU tend to be inappropriatelyassumed to be less adherent (34). Our study provides evidence to support improvedadherence during the first year of ART among IDUs in recent years. Adherence among IDUlikely increased due to a variety of variables including decreased toxicity with more modernART regimens and decreased pill burden with simplified once-daily therapy (35–37).Our study has some limitations. First, as no registries of IDU exist, recruiting a randomsample of HIV-seropositive IDU is not possible. However, we used community-basedtechniques to recruit a range of HIV-seropositive IDU both in and out of clinical care.Second, our outcome of interest was based on pharmacy refill activity and might notperfectly reflect daily medication adherence. However, this measure has been usedextensively in previous analyses and has been shown to robustly predict both virologicresponse and survival (19, 23, 38, 39).In the present study, adherence to ART during the first year increased significantly over timeamong a community-recruited cohort of HIV positive injection drug users. This trendremained significant even after adjustment for time-updated measures of potentialconfounders including clinical variables, drug use patterns and use of addiction treatment.IDU in our cohort received free ART with integrated services which has been shown toimprove adherence among HIV-positive IDU and our study demonstrates that this trendincreased over time (40). Although improved tolerability and convenience of modern ARTregimens likely explain these positive trends, by the end of the study period a substantialproportion of IDU still had sub-optimal adherence demonstrating the need additionaladherence support strategies.AcknowledgmentsThe authors thank the study participants for their contribution to the research, as well as current and pastresearchers and staff. We would specifically like to thank Deborah Graham, Tricia Collingham, Carmen Rock,Brandon Marshall, Caitlin Johnston, Steve Kain, Benita Yip, and Calvin Lai for their research and administrativeassistance.Role of Funding Source: The study was supported by the US National Institutes of Health (R01DA021525) andthe Canadian Institutes of Health Research (MOP-79297, RAA-79918). Drs. Kerr and Milloy are supported by theMichael Smith Foundation for Health Research and the Canadian Institutes of Health Research. None of theaforementioned organizations had any further role in study design, the collection, analysis or interpretation of data,in the writing of the report, or the decision to submit the work for publication.References1. Hammer SM, Katzenstein DA, Hughes MD, et al. A Trial Comparing Nucleoside Monotherapy withCombination Therapy in HIV-Infected Adults with CD4 Cell Counts from 200 to 500 per CubicMillimeter. NEJM. 1996; 335:1081–90. [PubMed: 8813038]2. 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Substance Abuse and Medication Adherence AmongHIV-Positive Women with Histories of Child Sexual Abuse. AIDS & Behavior. 2006; 10:279–86.[PubMed: 16501869]12. Arnsten JH, Li X, Mizuno Y, et al. Factors associated with antiretroviral therapy adherence andmedication errors among HIV-infected injection drug users. JAIDS. 2007; 46 (Suppl 2):S64–S71.[PubMed: 18089986]13. Carrieri MP, Chesney MA, Spire B, et al. Failure to maintain adherence to HAART in a cohort ofFrench HIV-positive injecting drug users. IJBM. 2003; 10:1–14.14. Gordillo V, del Amo J, Soriano V, Gonzalez-Lahoz J. Sociodemographic and psychologicalvariables influencing adherence to antiretroviral therapy. AIDS. 1999; 13:1763–9. [PubMed:10509579]15. Palepu A, Tyndall MW, Joy R, et al. Antiretroviral adherence and HIV treatment outcomes amongHIV/HCV co-infected injection drug users: The role of methadone maintenance therapy. DrugAlcohol Depend. 2006; 84:188–94. [PubMed: 16542797]16. 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Intermittent use of triple-combination therapy is predictiveof mortality at baseline and after 1 year of follow-up. AIDS. 2002; 16:1051–8. [PubMed:11953472]25. WHO. World Health Organization, Child and Adolescent Health. Vol. 2011. South-East Asia:WHO;26. Wood E, Hogg RS, Yip B, Harrigan PR, O'Shaughnessy MV, Montaner JS. Effect of medicationadherence on survival of HIV-infected adults who start highly active antiretroviral therapy whenthe CD4+ cell count is 0.200 to 0.350 x 10(9) cells/L. Ann Intern Med. 2003; 139:810–6.[PubMed: 14623618]27. Maldonado G, Grenland S. Simulation study of confounder-selection strategies. Am J Epidemiol.1993; 138:923–36. [PubMed: 8256780]28. Lima V, Fernandes K, Rachlis B, Druyts E, Montaner J, Hogg R. Migration adversely affectsantiretroviral adherence in a population-based cohort of HIV/AIDS patients. Soc Sci Med. 2009;68:1044–9. [PubMed: 19157668]29. Milloy M-J, Kerr T, Buxton J, et al. Dose-response effect of incarceration events on nonadherenceto HIV antiretroviral therapy among injection drug users. J Infect Dis. 2011; 203:1215–21.[PubMed: 21459814]30. Bouhnik A-D, Chesney M, Carrieri P, et al. Nonadherence among HIV-infected injecting drugusers: the impact of social instability. JAIDS. 2002; 31:S149–S53. [PubMed: 12562040]31. Celentano DD, Vlahov D, Cohn S, Shadle VM, Olugbenga O, Moore RD. Self-reportedantiretroviral therapy in injection drug users. JAMA. 1998; 280:544–6. [PubMed: 9707145]32. Chesney MA. Factors affecting adherence to antiretroviral therapy. Clin Infect Dis. 2000;2000:S171–S6. [PubMed: 10860902]33. Ortego C, Huedo-Medina T, Llorca J, et al. Adherence to highly active antiretroviral therapy(HAART): a meta-analysis. AIDS Behav. 2011; 15:1381–96. [PubMed: 21468660]34. Malta M, Magnanini MM, Strathdee SA, Bastos FI. Adherence to antiretroviral therapy amongHIV-infected drug users: a meta-analysis. AIDS Behav. 2010; 14:731–47. [PubMed: 19020970]35. Nachega JB, Mugavero MJ, Zeier M, Vitoria M, Gallant JE. Treatment simplifciation in HIV-infected adults as a strategy to prevent toxicity, improve adherence, quality of life and decreasehealthcare costs. Patient Prefer Adherence. 2011; 5:357–67. [PubMed: 21845035]36. Atkinson MJ, Petrozzino JJ. An evidence-based review of treatment-related determinants ofpatients' nonadherence to HIV medications. AIDS Patient Care STDS. 2009; 23:903–14.[PubMed: 19642921]37. Portsmouth SD, Osorio J, McCormick K, Gazzard BG, Moyle GJ. Better maintained adherence onswitchign from twice-daily to once-daily therapy for HIV: a 24-week randomized trial of treatmentsimplification using stavudine prolonged-release capsules. HIV Med. 2005; 6:185–90. [PubMed:15876285]38. Krusi A, Milloy M-J, Kerr T, et al. Ongoing drug use and outcomes from highly activeantiretroviral therapy among injection drug users in a Canadian setting. Antivir Ther. 2010;15:789–96. [PubMed: 20710061]39. Low-Beer S, Yip B, O'Shaughnessy MV, Hogg RS, Montaner JSG. Adherence to triple therapyand viral load response. JAIDS. 2000; 23:360–1. [PubMed: 10836763]40. Malta M, Strathdee SA, Magnanini MM, Bastos FI. Adherence to antiretroviral therapy for humanimmunodeficiency virus/acquired immune deficiency syndrome among drug users: a systematicreview. Addiction. 2008; 103:1242–57. [PubMed: 18855813]41. Palepu A, Milloy M-J, Kerr T, Zhang R, Wood E. Homelessness and adherence to antiretroviraltherapy among a cohort of HIV-infected injection drug users. J Urban Health. 2011; 88:545–55.[PubMed: 21409604]42. Tapp C, Milloy M-J, Kerr T, et al. Female gender predicts lower access and adherence toantiretroviral therapy in a setting of free healthcare. BMC Infec Dis. 2011;1110.1186/147-2334-11-86Mann et al. Page 6HIV Med. Author manuscript; available in PMC 2013 November 01.NIH-PA Author ManuscriptNIH-PA Author ManuscriptNIH-PA Author ManuscriptFigure 1. Proportion of injection drug users with ≥95% antiretroviral adherence* from 1996 to2009*Adherence defined based on prescription refill compliance.Mann et al. Page 7HIV Med. Author manuscript; available in PMC 2013 November 01.NIH-PA Author ManuscriptNIH-PA Author ManuscriptNIH-PA Author ManuscriptNIH-PA Author ManuscriptNIH-PA Author ManuscriptNIH-PA Author ManuscriptMann et al. Page 8Table 1Socio-demographic, behavioural and clinical characteristics of 682 ACCESS participants stratified by at least 95% adherence to ART in first yearCharacteristic< 95% adherence 450 (66.0%)≥95% adherence 232 (34.0%)Odds Ratio95% Confidence Intervalp-valueART initiation year Per year increase1999 (1997–2004)2003 (1998–2007)1.131.09–1.17< 0.001Gender1 Male270 (60.0)164 (70.7)1.00 Female180 (40.0)68 (29.3)0.620.44–0.870.006Age1 < 24 years21 (4.7)3 (1.3)1.00 ≥ 24 years429 (95.3)229 (98.7)3.741.10–12.660.034Aboriginal ancestry1 No278 (61.8)161 (69.4)1.00 Yes172 (38.2)71 (30.6)0.710.51–0.990.050Heroin use2 < Daily347 (77.1)195 (84.1)1.00 ≥ Daily103 (22.9)37 (15.9)0.640.42–0.970.034Cocaine use2 < Daily320 (71.1)202 (87.1)1.00 ≥ Daily130 (28.9)30 (12.9)0.370.24–0.56< 0.001Crack cocaine use2 < Daily321 (71.3)172 (74.1)1.00 ≥ Daily129 (28.7)60 (25.9)0.880.61–1.260.475Methadone use3 No276 (61.3)150 (64.7)1.00 Yes174 (38.7)82 (35.3)0.870.62–1.210.396Unstable housing3 No155 (34.4)78 (33.6)1.00 Yes295 (65.6)154 (66.4)1.040.74–1.450.830HIV Med. Author manuscript; available in PMC 2013 November 01.NIH-PA Author ManuscriptNIH-PA Author ManuscriptNIH-PA Author ManuscriptMann et al. Page 9Characteristic< 95% adherence 450 (66.0%)≥95% adherence 232 (34.0%)Odds Ratio95% Confidence Intervalp-valuePlasma HIV RNA load Per log10 increase4.9 (4.4–5.1)4.9 (4.4–5.0)0.910.72–1.150.426CD4+ cell count Per 100 cells2.4 (1.4–3.7)1.9 (1.2–3.0)0.890.81–0.970.0081 Time-varying, refers to the six month period prior to baseline2 Time-varying, refers to current statusHIV Med. Author manuscript; available in PMC 2013 November 01.

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