Behavioral Interventions for Tobacco Use in HIV-Infected Smokers: A Meta-Analysis

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1 CLINICAL SCIENCE Behavioral Interventions for Tobacco Use in HIV-Infected Smokers: A Meta-Analysis Asheena Keith, MD,* Yuelei Dong, MD,* Jonathan Shuter, MD, and Seth Himelhoch, MD, MPH* Context: Smoking is responsible for increased morbidity and mortality in HIV-infected smokers. Objective: To assess the efficacy of behavioral interventions for smoking cessation among HIV-infected smokers compared with the standard care. Data sources: PubMed, Cochrane, CINHAL, PsychINFO, and Google Scholar were searched for randomized controlled trials published in English. Study selection: Eligibility criteria were randomized controlled trials with targeted behavioral interventions compared with standard of care (or enhanced standard of care) aimed at promoting abstinence in HIV-infected smokers. A total of 17,384 articles were found and 17,371 were excluded; 13 full text articles were obtained and reviewed, and 8 met the eligibility criteria (Κ =0.94). Data extraction: The primary outcome was expired carbon monoxide verified 7-day point prevalence abstinence rates. Adequate sequence generation and freedom from incomplete or selective outcome reporting was used to assess study quality. Results: A total of 1822 subjects from 8 studies yielded a statistically significant effect of behavioral interventions in increasing abstinence in HIV-infected smokers with a moderate effect size (relative risk: 1.51; 95% confidence interval: 1.17 to 1.95). Those studies with interventions of 8 sessions or more had a large effect size for abstinence (relative risk: 2.88; 95% confidence interval: 1.89 to 4.61). When stratified by the number of sessions, there was no heterogeneity. Conclusions: Targeted behavioral smoking cessation interventions are efficacious. Interventions consisting of 8 sessions or more had the greatest treatment efficacy. Received for publication January 14, 2016; accepted March 14, From the *Department of Psychiatry, University of Maryland School of Medicine, Baltimore, MD; and Department of Medicine, Division of Infectious Diseases, Montefiore Medical Center and the Albert Einstein College of Medicine, New York, NY. Presented in part at the Institute on Psychiatric Service, October 9, 2015 in New York, NY, and are scheduled to be presented at the American Psychiatric Association, May 16, 2016, Atlanta, GA. The authors have no funding or conflicts of interest to disclose. Correspondence to: Seth Himelhoch, MD, MPH, Department of Psychiatry, University of Maryland School of Medicine, 737 West Lombard Street, Suite 560, Baltimore, MD ( shimelho@psych.umaryland.edu). Copyright 2016 Wolters Kluwer Health, Inc. All rights reserved. Key Words: behavioral interventions, HIV smokers, targeted smoking cessation interventions (J Acquir Immune Defic Syndr 2016;72: ) INTRODUCTION Smoking is the leading preventable cause of death and disease in the United States. HIV-infected individuals smoke tobacco at nearly 3 times the rate of the general population. 1 7 These extraordinary smoking rates are associated with greater AIDS-related morbidity, 8,9 greater non-aids related morbidity (including cardiovascular disease, pulmonary disease, and non-aids cancers), 7,10 15 and greater mortality. 16,17 Smoking significantly impacts the progression and outcome of HIV disease, and has been identified as the leading contributor to premature mortality among people with HIV. 18 In fact, a study from Denmark estimated that HIV-positive individuals lose more years from smoking than from HIV infection in and of itself. 19 In our view, shared by others in the field, 4,18,20 24 the single greatest health behavior change that could reduce mortality in this group is smoking cessation. This is well aligned with the personal goals of the target group as surveys have shown that most HIV-infected smokers want to quit. 13,25 27 Thus, establishing the efficacy of interventions for HIV-infected smokers is of critical importance. 28 Although many interventions are effective in helping general population smokers quit, 21 research examining the outcomes of smoking cessation treatments for individuals with HIV is limited. 29,30 Based on the alarming prevalence of smoking and the health-related consequences of smoking among HIV-infected smokers, the 2008 PHS Guideline for Treating Tobacco Use and Dependence specifically called for research that evaluates the efficacy of counseling, and targeted interventions among HIV-infected smokers. 21 To our knowledge, there have been 8 randomized controlled trials evaluating the efficacy of behavioral interventions plus nicotine replacement targeting smoking cessation among people living with HIV/AIDS who smoke. 1,31 37 Some trials demonstrated efficacy 33,38 and several showed no effect. 31,32,34,36,39 The purpose of this meta-analysis was to address the question whether behavioral interventions aimed at smoking cessation led to increased smoking abstinence as measured by expired carbon monoxide (ECO) 7-day point prevalence abstinence () rates compared with control interventions among people living with HIV who smoke. J Acquir Immune Defic Syndr Volume 72, Number 5, August 15,

2 Keith et al J Acquir Immune Defic Syndr Volume 72, Number 5, August 15, 2016 METHODS Eligibility Criteria English language articles from January 1980 through February 2016 were searched. The criteria for inclusion were randomized controlled trials of HIV-infected smokers with or without nicotine replacement therapy with a primary endpoint of carbon monoxide verified 7-day point prevalence. The studies were restricted to smokers of any age with HIV or AIDS with self-reported cigarette use. Studies were excluded if they allowed participants to be enrolled in multiple smoking cessation studies that co-occurred with the study of interest, were not randomized control trials, or used an endpoint of urine nicotine and cotinine. There were no sample size limitations. Information Sources PubMed (1980 to 12/2014), Cochrane (1980 to 12/ 2014), CINHAL ( /2016), PsychINFO ( / 2016), Google Scholar ( /2016), and a literature review through bibliographies of related articles were searched. Search The electronic search strategy was conducted on PubMed,CINHAL,PsychINFO,andCochrane,usingthe following search terms: HIV, AIDS, immune compromised, smokers, behavioral intervention,, nicotine patch, patch treatment, individual therapy, group therapy, motivational interviewing, person counseling, telephone counseling, brief counseling, counseling, behavior. Search filters were used to restrict studies to randomized controlled trials published in English and with human subjects. Google Scholar search included the key phrases such as HIV, randomized controlled trials, and smoking cessation. The bibliographies of included articles were searched for any additional studies. Study Selection Search results were reviewed for any duplicate studies. Two authors (A.K. and Y.D.) independently reviewed all study titles and abstracts for eligibility criteria. If studies met the eligibility criteria through title and abstract, the full article was reviewed. Thirteen full articles were reviewed, and 8 were selected. One study was excluded because the primary endpoint was of urine nicotine and cotinine. Four studies were excluded for not being randomized controlled trials. All the included used ECO-verified 7-day rates for verification of abstinence. Cohen Kappa statistics that assesses the chancecorrected agreement between reviewers was The PRISMA flow diagram (Fig. 1) summarizes the selection process. Data Items The primary endpoint was ECO level verified 7-day. Data Collection Process Two authors (A.K. and Y.D.) independently extracted data from each of the 8 trials. All the data were reviewed for discrepancies. Any disagreement between the 2 reviewers was resolved by consensus. Risk of Bias in Individual Studies All included studies were independently reviewed by 2 reviewers and the validity and reliability were determined according to the Cochrane approach, including adequate sequence generation, allocation concealment, blinding, completeness of outcome data reporting, selective outcome reporting, and presence of other sources of bias. Synthesis of Results We calculated the relative risk (RR) ratios and the weighted pooled RR ratios across studies (Stata 12.0: metan command). We used the DerSimonian and Laird (random effects) model to provide weight estimates for each study (Fig. 2). We chose the random-effects model as it provides a more conservative estimate of weighting than the fixed effect (Mantel Haenszel method) when one is concerned that the fixed-effects assumption, namely that the true effect is the same in each study, may not be met. The Q statistic and I 2 statistic were used to evaluate heterogeneity. The Q statistic quantifies the magnitude of heterogeneity, whereas the I 2 statistic quantifies the total variation due to between-study variance. Publication bias was not formally tested, as tests for publication bias (eg, funnel plot) may be too low to distinguish chance from real asymmetry when using meta-analytic techniques with 10 studies or less. 22,40 RESULTS Study Selection The search of PubMed, Cochrane, CINHAL, PsychINFO, Google Scholar, and a bibliography literature review yielded a total of 17,384 citations after duplicate removal. A total of 17,371 were excluded after review of abstracts indicated eligibility criteria were not met. The remaining 13 full text articles were reviewed for eligibility. Four articles were excluded because they were not randomized controlled trials and 1 for a primary endpoint of urine nicotine and cotinine (Fig. 1). Study Characteristics A total of 8 studies with 1822 subjects were identified for inclusion in the review. All 8 studies were randomized controlled trials in the English language. All studies included nicotine replacement therapy either by prescription, distribution, or referral as a part of the intervention. The study interventions ranged from 4 to 11 sessions, and 5 of the 8 studies had at least 8 sessions. 33,34,36 38 The studies Copyright 2016 Wolters Kluwer Health, Inc. All rights reserved.

3 J Acquir Immune Defic Syndr Volume 72, Number 5, August 15, 2016 Tobacco Use in HIV-Infected Smokers FIGURE 1. Article identification. delivered the behavioral intervention in a range of formats. Three studies used telephone counseling. 36,38,41 Oneusedgroup therapy. 33 Two used computer-based interventions, 31,34 and 3 used individual therapy. 31,32,35 The primary endpoints for all 8 studies were ECO-verified 7-day. All studies compared the intervention group to brief counseling or self-help control conditions (Table 1). Risk of Bias Within Studies All 8 trials were at low risk for bias because of inadequate sequence generation or incomplete data reporting of the primary outcome. There is, however, risk for publication bias. A funnel plot was constructed and by inspection there was no suggestion of publication bias; however, in a meta-analysis with less than 10 studies, funnel plots may not be reliable. 40 Since these were behavioral studies, the nature of the interventions precluded blinding and allocation concealment. Results of Individual Studies Three of the 8 clinical trials reviewed reported treatment efficacy. Wewers et al 37 found statistically significant increase in abstinence at 8 weeks comparing those randomized to the nurse managed, peer led, smoking cessation intervention (n = 8) with the control condition (n = 7) (67.5% vs. 0%). Vidrine et al 38 found a statistically significant increase in abstinence at 3 months among those randomized to the telephone intervention group (n = 48) compared with usual care control (n = 47) (36.8% vs. 10.3%). A larger study conducted by Vidrine et al 36 found a statistically significant increase in abstinence at 3 months for those randomized to the telephone group (n = 236) compared with the control group (n = 238) (11.9% vs. 3.4%). Five of the 8 clinical trials reviewed did not find treatment efficacy Lloyd-Richardson et al 32 found no difference in abstinence at 6 months among those randomized to the motivational enhancement arm (n = 232) compared with those in standard of care (n = 212) (9% vs. 10%). Humfleet et al 31 found no difference in abstinence after 52 weeks among those randomized to individual counseling (n = 69) or computer-based intervention (n = 58) compared with brief counseling control (n = 82) (20.4% vs. 25.6% vs. 19.8%). Shuter et al 34 found no difference in abstinence at 3 months among those randomized to web-based intervention (n = 69) compared with standard-of-care control (n = 69) (10.3% vs. 4.3%). Moadel et al 33 found no difference in abstinence at 3 months among those randomized to group therapy (n = 72) compared with the control condition (n = 73) (19.2 vs. 9.7%). Stanton et al 35 found no evidence that 4 inperson sessions (n = 131) improved cessation rates compared with the standard of care (n = 131) at 3 months (8.5% vs. 9.1%) (Table 1). Synthesis of Results The meta-analysis of the 8 studies evaluating the efficacy of behavioral interventions to increase smoking abstinence among HIV-infected smokers yielded a moderate statistically significant effect size for abstinence Copyright 2016 Wolters Kluwer Health, Inc. All rights reserved

4 Keith et al J Acquir Immune Defic Syndr Volume 72, Number 5, August 15, 2016 FIGURE 2. Forrest plot of efficacy of behavioral interventions for smoking cessation targeting people living with HIV/AIDS who smoke stratified by intervention session number. (RR: 1.51; 95% CI: 1.17 to 1.95). Heterogeneity of the studies was assessed and found to be moderate (I 2 = 43.3%; x 2 = 14.1, d.f. = 8; P = 0.08). When stratified by the number of sessions, those studies with $8 sessions had a large statistically significant effect on abstinence rates (RR: 2.88; 95% CI: 1.89 to 4.61) and no heterogeneity (I 2 =0.0%;x 2 = 1.93; d.f. = 4; P = 0.749). The studies with fewer than 8 sessions or less had nonsignificant results (RR: 1.05; 95% CI:0.77to1.44)andnoheterogeneity(I 2 =0.0%;x 2 = 1.27, d.f. = 3; P = 0.737) (Fig. 2). A sensitivity analysis was conducted to better quantify the effect of the study by Wewer et al on the overall weighted effect of the stratified sample. In the stratified analysis (ie, studies with 8 sessions or more vs. studies with less than 8 sessions), the overall effect including the Wewer s study was RR 2.88 ( ), whereas the overall effect excluding the Wewer s study was an RR 2.70 ( ). DISCUSSION Our systematic review and meta-analysis of the 8 published randomized controlled trials of behavioral tobacco-treatment interventions targeting HIV-infected smokers demonstrated a significant effect in terms of increased abstinence. When stratified by the total number of sessions, studies with 8 or more sessions had a large statistically significant effect size for abstinence, whereas those studies with fewer than 8 sessions yielded nonsignificant results. There was no heterogeneity found with stratification by the total number of sessions. These results suggest that providing a greater number of sessions may be an important determinant of programmatic efficacy. With respect to risk of bias, it is important to note that all the studies in the meta-analysis were deemed to be of high quality. They were all randomized controlled trials with adequate sequence generation and free of selective outcome Copyright 2016 Wolters Kluwer Health, Inc. All rights reserved.

5 J Acquir Immune Defic Syndr Volume 72, Number 5, August 15, 2016 Tobacco Use in HIV-Infected Smokers TABLE 1. Characteristics of Studies for Behavioral Interventions for Smoking Cessation in HIV-Positive Population Investigator Yrs Intervention Demographics Wewers weekly one-on-one 18 yrs or older, 10 cig/d telephone counseling for past year, HIV sessions + offer of vs. self-help Vidrine 38 Vidrine 36 Lloyd- Richardson 32 Moadel 33 Humfleet 31 Shuter 34 Stanton one-on-one telephone counseling sessions + offer of vs. brief counseling + offer of one-on-one telephone counseling sessions + offer of vs. brief counseling + offer of one-one-one motivational interviewing sessions + vs. 2 brief counseling sessions weekly group therapy sessions + offer of vs. brief counseling + offer of one-on-one, in-person counseling sessions vs. 5 web-based sessions vs. brief counseling (all offered ) sessions of web-based treatment programs + offer of vs. brief counseling + offer of in-person sessions of a targeted intervention (Aurora) + vs. 2 in-person sessions of brief advice (enhanced standard care) +, nicotine replacement therapy. 18 yrs or older, HIV, current smoker (.5 cig/d and expired CO.7 ppm), willing to set a quit date within the next 7 days 18 yrs or older, HIV, current smoker (.5 cig/d and expired CO.7 ppm), willing to set a quit date within the next 7 days 18 yrs or older, HIV, current regular smoker (5 cig/d for the past 3 months) Age years $6 on the readiness to quit ladder 18 yrs or older, smoke most days of the month, HIV Self-report smoker, want to quit in next 6 months, HIV 18 yrs or older, current smoker, self-identify as Latino or Hispanic, HIV Total Number Abstinence Rate Intervention Control Endpoint Definition of Abstinence % 0% 8 w 8 ppm ECOverified % 6.4% 3 m 7 ppm ECOverified % 3.4% 3 m 7 ppm ECOverified % 10.0% 2, 4, and 6 m 10 ppm ECOverified % 9.7% 3 m 10 ppm ECOverified 209 IC: 20.4%; CBI: 25.6% 19.7% 52 W 10 ppm ECOverified % 4.3% 3 m 10 ppm ECO verified m: 8% 12 m: 6% 11% 7% 6 and 12 m 10 ppm ECOverified reporting or incomplete outcome reporting in the primary measure The mode of delivery of the behavioral interventions used in these studies differed between trials. Three studies used telephone counseling. 36,38,41 One used group therapy. 33 Two used computer-based interventions, 31,34 and 3 used individual therapy. 31,32,35 Even so, the heterogeneity of the studies was assessed and found to be moderate to low. Although web-based programs have the advantage of flexibility in scheduling, low cost, and the ability to review material as needed, the 2 web-based studies in this metaanalysis had nonsignificant results. Both web-based programs used software that was at the sixth grade reading level. An important difference between the studies was that Shuter et al 34 excluded participants with low literacy scores, whereas Humfleet et al 31 did not. The former study found that a higher educational level was associated with more web pages visited and higher quit rates. This suggests that literacy or perhaps experience using web-based interventions (ie, as a result of the digital divide), which are both associated with higher education, may be important predictors of success with this type of intervention. The advantage of peer-based interventions is that they may bridge potential barriers related to language, culture, and class, and thereby enhance treatment delivery, and they have proved promising in other areas of research. 37,42,43 One of 2 studies that used peer support specialists yielded statistically significant large effect sizes, suggesting that this may be a particularly promising way of delivering targeted behavioral interventions in the future. 33,37 Copyright 2016 Wolters Kluwer Health, Inc. All rights reserved

6 Keith et al J Acquir Immune Defic Syndr Volume 72, Number 5, August 15, 2016 Of note is the finding that the 2 studies that did not assess readiness to quit as a part of their inclusion criteria were also studies that found no treatment effect. 31,32 This may be because of a greater number of participants who were either in precontemplation and/or contemplation and may have negatively contributed to abstinence rates in these trials. The implication of this finding may be that future trials will need to evaluate level of treatment readiness as an eligibility criterion for smoking cessation intervention. Although this meta-analysis was limited to English language articles (ie, Tower of Babel Bias), 44 it still appears that based on these data behavioral interventions targeted at the HIV-infected smokers had a significant effect on increasing smoking abstinence. When stratified by the length of intervention, those studies with interventions of 8 sessions or more had a statistically significant large effect size for abstinence, whereas those studies with interventions consisting of fewer than 8 sessions had nonsignificant results. Future studies may need to include eligibility criteria that emphasize readiness to quit as well and provide $8 intervention sessions. For those studies that are web-based assessment of literacy may be needed. Further study on the utility of peers is an emerging area of research that shows considerable promise. REFERENCES 1. Burkhalter JE, Springer CM, Chhabra R, et al. Tobacco use and readiness to quit smoking in low-income HIV-infected persons. Nicotine Tob Res. 2005;7: Kwong J, Bouchard-Miller K. Smoking cessation for persons living with HIV: a review of currently available interventions. J Assoc Nurses AIDS Care. 2010;21: Lifson AR, Lando HA. Smoking and HIV: prevalence, health risks, and cessation strategies. 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7 J Acquir Immune Defic Syndr Volume 72, Number 5, August 15, 2016 Tobacco Use in HIV-Infected Smokers 38. Vidrine DJ, Arduino RC, Lazev AB, et al. A randomized trial of a proactive cellular telephone intervention for smokers living with HIV/AIDS. AIDS. 2006;20: Manuel JK, Lum PJ, Hengl NS, et al. Smoking cessation interventions with female smokers living with HIV/AIDS: a randomized pilot study of motivational interviewing. AIDS Care. 2013;25: Ioannidis JP, Trikalinos TA. The appropriateness of asymmetry tests for publication bias in meta-analyses: a large survey. CMAJ. 2007;176: Tesoriero JM, Gieryic SM, Carrascal A, et al. Smoking among HIV positive New Yorkers: prevalence, frequency, and opportunities for cessation. AIDS Behav. 2010;14: Napoles AM, Ortiz C, Santoyo-Olsson J, et al. Nuevo Amanecer: results of a randomized controlled trial of a community-based, peerdelivered stress management intervention to improve quality of life in Latinas with breast cancer. Am J Public Health. 2015;105(suppl 3): e Srinivas GL, Benson M, Worley S, et al. A clinic-based breastfeeding peer counselor intervention in an urban, low-income population: interaction with breastfeeding attitude. J Hum Lact. 2015;31: Gregoire G, Derderian F, Le LJ. Selecting the language of the publications included in a meta-analysis: is there a tower of Babel bias? J Clin Epidemiol. 1995;48: Copyright 2016 Wolters Kluwer Health, Inc. All rights reserved