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Clinical Science

Sex Differences in Tobacco Use Among Persons Living With HIV/AIDS: A Systematic Review and Meta-Analysis

Weinberger, Andrea H. PhD*,†; Smith, Philip H. PhD; Funk, Allison P. BA§; Rabin, Shayna*,‖; Shuter, Jonathan MD†,¶

Author Information
JAIDS Journal of Acquired Immune Deficiency Syndromes: April 1, 2017 - Volume 74 - Issue 4 - p 439-453
doi: 10.1097/QAI.0000000000001279
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Abstract

INTRODUCTION

Tobacco use is well known to have numerous, serious health consequences and is a leading cause of mortality in the United States and around the world.1,2 As HIV/AIDS treatment has advanced over time, smoking has had an increasing impact on the health and longevity of persons living with HIV/AIDS (PLWH). Tobacco has emerged as a leading killer among PLWH3 who smoke at 2–3 times the rate of the general adult population in the United States.4 The negative impact of smoking on PLWH includes HIV-related complications (eg, increased viral load, pneumonia), non-HIV medical illnesses (eg, non-HIV/AIDS-related cancers), and greater mortality.5–9 Women with HIV/AIDS face additional sex-specific consequences of smoking including adverse fetal-related outcomes (eg, low birth weight, preterm birth) and early natural menopause.10–12 Quitting smoking reduces HIV-related symptom burden,13 causes of mortality related to HIV and AIDS such as bacterial pneumonia6,14 and cardiovascular morbidity.15

Sex differences in tobacco use exist in the general population. In the United States, men are more likely than women to report current use of cigarettes and other tobacco products16,17 and nicotine dependence.18 Men also report smoking more cigarettes per day (CPD) than women.19,20 Although the prevalence of smoking has decreased over time, women have shown less of a decrease in smoking than men.16 Although men and women do not differ in their interest in quitting smoking,1 there is evidence that women have greater difficulty maintaining smoking abstinence20–23 (see also Ref. 24) especially when quitting “cold turkey.”20,25 When using pharmacotherapy, women seem to be less successful quitting with transdermal nicotine patch26,27 and more successful using varenicline compared with transdermal nicotine patch.28 Furthermore, women metabolize nicotine more quickly,29 experience greater withdrawal symptoms,30–32 and report greater perceived risks of quitting smoking33 than men. Together, men and women in the general population differ in a number of smoking-related behaviors, and it is important to understand whether these differences are similar or different in subgroups of smokers who are disproportionately impacted by smoking such as PLWH.

Smoking has serious health consequences for PLWH, especially for women with HIV/AIDS.10–12 In addition, women in the general population seem to have more difficulty quitting smoking. It is important to identify differences in smoking behaviors for women versus men with HIV/AIDS to understand the best way to target efforts to reduce the consequences of smoking for all PLWH. The purpose of this study was to conduct a systematic literature review to determine what is known about sex differences in smoking behaviors among PLWH. The goals of the review were to synthesize current knowledge, compare sex patterns to what is known in the general population, and identify areas in need of more research.

METHODS

Systematic Review

A MEDLINE search was conducted on February 13, 2016 to identify articles examining sex and smoking among PLWH using search terms related to smoking (“smoking,” “cigarettes,” “tobacco,” “nicotine”) and HIV (“HIV,” “AIDS”). Abstracts from the MEDLINE search were individually examined by at least 2 authors to determine whether they met the inclusion criteria. Full texts were obtained and examined if it was not clear whether the article met the inclusion criteria from the abstract. Additional publications were identified from the reference lists of articles included in the review and review articles on smoking and HIV.4,34,35

To be included in the review, studies had to include (1) persons with HIV and/or AIDS, (2) both men and women, and (3) information about one or more aspects of smoking for men and women separately (eg, smoking prevalence, desire to quit smoking). Exclusion criteria included (1) being published in a language other than English, (2) not having a full text available, (3) study samples that were all or nearly all (ie, >95%) men or women, (4) a small sample size (ie, <30 participants), and (5) a sample where a specific number of smokers and nonsmokers were recruited into the sample (for analysis of smoking prevalence). Information gathered from eligible publications included the country where the study occurred, sample size (overall and by sex), and data on smoking behavior for men versus women including statistics and P values for the comparisons of smoking behavior for men versus women. Smoking behaviors included prevalence of current or lifetime smoking, nicotine dependence, motivation to quit, quit attempts, use of noncigarette tobacco products, and quit outcomes. See Table 1 for a list of data gathered from studies.

T1
TABLE 1.:
Study Characteristics and Smoking Variables That Included Data Presented by Sex
table1-a
TABLE 1-A.:
Study Characteristics and Smoking Variables That Included Data Presented by Sex
table1-b
TABLE 1-B.:
Study Characteristics and Smoking Variables That Included Data Presented by Sex
table1-c
TABLE 1-C.:
Study Characteristics and Smoking Variables That Included Data Presented by Sex

The MEDLINE search yielded 3082 abstracts, and 376 full texts were examined from the abstract list. Abstracts were excluded if the article did not examine smoking behavior of PLWH. The main reasons for excluding full-text articles were that smoking data were not presented for men and women separately, the sample consisted of all or nearly all men or women, and/or there was no full text available (eg, an abstract of a poster conference). Seventy-nine publications met all the inclusion criteria to be included in the review. See Figure 1 for the PRISMA flowchart and Table 1 for a summary of the study characteristics and list of assessed outcomes.

F1
FIGURE 1.:
PRISMA figure for literature search.

Meta-Analysis

We conducted random-effects meta-analyses to estimate meta-analytic prevalence of current smoking among women and men and to summarize odds ratios (ORs) for the comparison of odds between women and men. Studies that included the current smoking prevalence data for men and women were included in the meta-analysis (see Tables 1 and 2). We used the R program Metafor for all analyses,113 and used an inverse variance weighting method. We first conducted the analyses for all studies that documented the prevalence of current smoking for women and men (n = 51). Because the largest number of studies came from the United States, we then limited the sample to studies conducted in the United States (n = 23) and repeated the analyses.

T2
TABLE 2.:
Prevalence of Lifetime Smoking, Current Smoking, Former Smoking, and Never Smoking for Male and Female PLWH
table2-a
TABLE 2-A.:
Prevalence of Lifetime Smoking, Current Smoking, Former Smoking, and Never Smoking for Male and Female PLWH
table2-b
TABLE 2-B.:
Prevalence of Lifetime Smoking, Current Smoking, Former Smoking, and Never Smoking for Male and Female PLWH

RESULTS

Smoking Prevalence

See Table 2 for prevalences of lifetime/ever, current, former, and never smoking for PLWH presented by sex. Across all studies that could be included in the meta-analysis (see Table 1), the prevalence of current smoking among women was 36.3% (95% confidence interval [CI]: 28.0% to 45.4%) and among men was 50.3% (95% CI: 44.4% to 56.2%). For both women and men, the residual heterogeneity of effect sizes was large. For women, Q52 = 2322.94, P < 0.001, and I2 = 99.45%. For men, Q52 = 3604.18, P < 0.001, and I2 = 99.51%. When comparing women and men (referent = women), the meta-analytic OR was 1.78 (95% CI: 1.29 to 2.45), indicating that averaged across investigations men had 78% greater odds of current smoking than women (Fig. 2). Considering the high degree of residual heterogeneity (Q52 = 1508.67, P < 0.001, and I2 = 98.92%), this OR should be interpreted as a weighted expected estimate across studies, without drawing conclusions about its representativeness for any one given study.

F2
FIGURE 2.:
Forest plot for smoking prevalence for PLWH by sex for all eligible studies (referent = women; n = 51).

When selecting for studies conducted in the United States, the meta-analytic prevalence of current smoking among women was 55.1% (95% CI: 47.6% to 62.5%) and among men was 55.5% (95% CI: 48.2% to 62.5%). For both women and men, the residual heterogeneity of effect sizes was large. For women, Q22 = 453.39, P < 0.001, and I2 = 96.52%. For men, Q22 = 931.21, P < 0.001, and I2 = 98.54%. When comparing women and men (referent = women), the meta-analytic OR was 1.04 (95% CI: 0.86 to 1.26), indicating a failure to reject the null hypothesis that across studies, women and men did not differ in their odds of current smoking (Fig. 3). Considering the high degree of residual heterogeneity (Q22 = 110.41, P < 0.001, and I2 = 86.52%), this OR should be interpreted as a weighted expected estimate across studies, without drawing conclusions about its representativeness for any one given study.

F3
FIGURE 3.:
Forest plot for smoking prevalence for PLWH by sex for studies conducted in the United States (referent = women; n = 23).

Among studies that reported the prevalences of smoking for men and women with HIV and men and women in the general population, current smoking prevalences were higher and former smoking prevalences were lower for men and women with HIV (see Table 2). One study99 that included transgender participants also reported a higher current smoking prevalence for transgender PLWH compared with men or women from the general population.

Other Aspects of Smoking or Tobacco Use

Nicotine Dependence/Addiction

Two studies used the Fagerström Test for Nicotine Dependence114 to examine moderate or strong dependence on nicotine in PLWH by sex,46,61 a third study used the Modified Fagerström Tolerance Questionnaire,111 and a fourth study defined dependence by either the time to first cigarette in the morning (<30 minutes) or CPD (>20).94 Although there was no significant sex difference in the report of moderate/strong nicotine dependence in 509 adults in France (men 60.9%; women 58.2%; OR = 1.12; 95% CI: 0.61 to 2.06),46 a lower percentage of women (47.8%) than men (60.0%) reported moderate/strong nicotine dependence in a sample of 1094 US adults (OR = 1.5, 95% CI: 1.0 to 2.2, P < 0.05).61 There was no difference in the average level of nicotine dependence in 167 US adults (men M = 4.8, SD = 2.2; women M = 5.1, SD = 2.0; P = 0.17).111 Finally, among 3019 French adults,94 HIV-infected men who have sex with men were more likely to report strong nicotine dependence than the general population men (63.7% versus 49.0%; OR = 1.37, 95% CI: 1.24 to 1.51). In that study, heterosexual men with HIV and women with HIV were not more likely to report strong nicotine dependence than men or women in the general population, respectively.

Cigarettes per Day

Some studies found no sex differences in CPD,39,40,75,111 whereas other studies reported a greater number of CPD smoked by men compared with women.38,61 In one study of PLWH in New York, more men (25.9%) than women (14.8%) reported smoking ≥20 CPD (P = 0.03).111 Beachler et al68 found that women with and without HIV reported a similar number of CPD (<1 CPD, 54% versus 52%; 1–9 CPD, 31% versus 31%; 10–19 CPD, 13% versus 14%; 20 or more CPD, 2% versus 3%; no significance test reported), whereas more men with HIV, compared with men without HIV, seemed to report smoking high numbers of CPD (<1 CPD, 68% versus 82%; 1–9 CPD, 12% versus 10%; 10–19 CPD, 11% versus 5%; 20 or more CPD, 10% versus 3%; no significance test reported).

Smoking History

There were no sex differences in the age of smoking initiation for 267 PLWH in New York (men M = 16.6 years old, SD = 6.3; women M = 15.9, SD = 4.3; P = 0.34)111 or for 1815 adults from Brazil (men M = 16.9 years old; women M = 16.5; P = 0.61).75 One additional study found no sex difference in pack years (men M = 24.0, SD = 17.6; women M = 24.0, SD = 20.7).58

Change in Smoking After HIV Diagnosis

Three studies examined changes in smoking behavior after an HIV diagnosis with mixed results.36,75,112 There was no sex difference in cutting down or quitting smoking after an HIV diagnosis among 2864 PLWH in the United States36 and no difference in starting smoking after an HIV diagnosis among 966 PLWH in Brazil.75 In a study of 2973 PLWH in China,112 women were more likely than men to report quitting smoking after an HIV diagnosis (30.3% versus 18.4%, P < 0.01). There were no sex differences with regard to increasing smoking or decreasing smoking after their diagnosis.

Motivation to Quit

Studies consistently found no differences in motivation to quit smoking for male and female PLWH.38,46,54,61,62,66,88,111

Abstinence Self-Efficacy and Beliefs About Smoking

Shuter et al found no sex differences in overall abstinence self-efficacy,90,111 abstinence self-efficacy related to specific situations (eg, positive affect/social situations, negative affect),111 or beliefs about smoking-related risks (eg, looking older) and benefits (eg, weight control).73 Tesoriero et al61 also found no sex differences in general smoking knowledge (eg, risk of lung cancer is higher among smokers) and HIV-related smoking knowledge (eg, smoking is a serious health concern for HIV-positive individuals).

Quit Attempts and Outcomes

In a sample of PLWH in San Francisco, CA, a greater proportion of men than women reported a lifetime quit attempt (81% versus 40%; P < 0.001).38 Other studies found no sex differences in the proportion of men versus women who reported a quit attempt over 1,61 2,95 or 5 years.59 There were also no sex differences in the number of past-year or lifetime quit attempts among PLWH in New York.111 Over a 14-year period, a similar number of men and women reported quitting smoking (26.6% versus 24.7%) and relapsing to smoking after quitting (11.8% versus 11.9%).104

Use of Noncigarette Tobacco Products

Two articles examined the use of noncigarette tobacco products by sex among PLWH in the United States entering smoking cessation treatments.81,111 In the first study,81 23.2% of men and 17.7% of women reported polytobacco use (ie, use of cigarettes plus at least one other tobacco product “every day or some days”; P = 0.19). In the second study,111 men and women did not differ in their reported use of pipes (5.8% versus 4.2%, P = 0.78), cigars (18.1% versus 13.2%, P = 0.28), chewing tobacco (2.9% versus 1.7%, P = 0.69), or snuff (0.7% versus 0.0%; P = 1.00).

Smoking Cessation Treatment

Use of Treatments

One study found that women were not significantly more likely than men to report lifetime use of any type of smoking cessation pharmacotherapy (OR = 1.27, 95% CI: 0.71 to 2.28).88 A second study111 found sex differences in the use of some smoking cessation treatments: more women than men reported past use of nicotine replacement therapy (68.3% versus 55.6%, P < 0.05), varenicline (28.5% versus 17.4%, P < 0.05), and acupuncture (24.4% versus 11.8%, P < 0.01), whereas there were no differences in the use of bupropion, quit line, group counseling, individual counseling, or a website.

Treatment Completion and Adherence

In clinical trials of smoking cessation treatment for PLWH, sex was not associated with adherence to study medication (varenicline or nicotine replacement therapy),91,105,107 number of counseling calls completed,107 or number of study appointments completed.72 One study of brief counseling and nicotine replacement therapy reported that women were more likely to complete treatment than men (64.3% versus 25.0%; P = 0.023).78 A trial of transdermal nicotine patch for smoking cessation in 444 PLWH found that sex was not a moderator in the relationship between greater social support and greater adherence to transdermal nicotine patch.108

Treatment Outcomes

Among 5 smoking treatment studies—mostly of pharmacotherapy and counseling—that examined quit outcomes by sex,43,72,84,91,108 none found significant sex differences in abstinence rates. One feasibility pilot study of a web-based intervention and transdermal nicotine patch91 found a trend toward a higher quit rate for women versus men (11.7% versus 2.7%; P = 0.08) and may have been underpowered to find a statistically significant difference. Interestingly, female participants who completed all 8 web-based sessions and who visited all the web pages showed high rates of quitting (30.8% and 40%, respectively).

DISCUSSION

Tobacco use is the most important preventable cause of excess mortality in adults worldwide1,2 with serious additional health risks for PLWH.7,9 Sex differences in smoking behaviors have been found in general population samples,16,20 and women with HIV face sex-specific consequences of smoking.10–12 The purpose of this article was to synthesize published data on sex differences in smoking behaviors for PLWH. A systematic review was conducted to examine a range of smoking behaviors, and a meta-analysis compared the prevalence of current smoking for female versus male PLWH.

The largest amount of data available on sex and smoking for PLWH was for current smoking prevalence. Men and women with HIV/AIDS reported current smoking prevalences that were very high and much higher than men and women in the general population, consistent with other findings.4 Although men reported higher smoking prevalences than women when all global data were considered, the prevalences of current smoking for male PLWH and female PLWH were both greater than 50% and not statistically different from each other when considering US data. Although men are more likely than women to report current smoking in the general US population (men 16.7%; women 13.6%),16 this difference is not manifest in the subsample of US adults with HIV, suggesting that the added relative risk of smoking for people with HIV is greater for women than for men. Whereas there is a continued need for targeted efforts to reduce smoking among all persons with HIV, women with HIV may demonstrate disproportionate health disparities related to smoking because of the greater relative difference in smoking between those with HIV and the general population for women (55.1% versus 13.6%) compared with men (55.5% versus 16.7%).

PLWH report high rates of current and past use of alcohol and other drugs.115,116 Alcohol and substance abuse are related to higher smoking prevalences and lower quit rates for the general population117,118 and for PLWH.39,99,106 In this review, 2 studies examined smoking prevalence in samples of current/past injection drug users74,87 and reported similar smoking rates for men and women (91.3% versus 90.0%74; 73.4% versus 77.9%87). The majority of the other studies (n = 56) reported some aspects of alcohol and/or drug use behavior in their samples; however, no study examined the relationship of alcohol/drug use/abuse to sex differences in smoking behavior. It may be useful for future studies to examine how sex differences in smoking prevalence and other smoking-related behaviors differ for PLWH with and without alcohol and drug use/abuse.

Few studies examined sex differences in smoking-related behaviors other than smoking prevalence, suggesting the need for more research on sex for all aspects of smoking. Mixed results were reported for several smoking variables (eg, CPD, quit attempts). For some of these variables, differences by sex have been found in the general population samples. For example, women in the United States were more likely to report making a quit attempt than men (45.8% versus 41.5%; OR = 1.19, 95% CI: 1.13 to 1.26).119 Because of the small number of studies and the mixed results, it is not clear yet if men and women with HIV demonstrate differences in these smoking variables. Future examinations of smoking behavior by sex will help clarify where sex differences do and do not exist and how strategies tailored by sex may be useful for prevention and intervention programs.

Although some sex differences were suggested for certain smoking variables, no sex differences were found for other variables (eg, quit motivation, use of noncigarette tobacco products). A lack of sex differences have also been found in the general population samples in some cases (eg, motivation to quit smoking120), whereas differences have been reported for other variables. For example, men in the United States are more likely than women in the United States to use noncigarette tobacco products,17 but this difference does not seem to be seen among PLWH, likely because of the higher rates of tobacco use by women with HIV compared with women in the general population. More research on noncigarette tobacco products would be beneficial, especially alternative nicotine-delivery products that have shown recent increases in use (eg, e-cigarettes121).

Successful smoking cessation sustained over time is critical for reducing smoking-related consequences and disease. Whereas no differences in quit outcomes were found for the studies that examined data by sex, overall quit rates were generally very low with the large majority of men and women being unable to abstain from smoking over time. In general, there is a need for more efficacious and effective smoking treatments for PLWH.122–125 More data by sex on smoking variables would help to inform efforts to develop smoking interventions that improve quit outcomes for both men and women. For example, women in the general population are less likely than men to have success when quitting without pharmacotherapy.20,25 In this review, women with HIV were equally or more likely than men to report the use of pharmacotherapies. The greatest number of women reported using nicotine replacement therapy, similar to the general population samples119; however, varenicline shows a greater advantage over transdermal nicotine patch for women compared with men in the general population.28 Women with HIV may benefit from information about the relative efficacy of different pharmacotherapies to quit smoking. No studies were identified that examined a number of smoking-related variables that may impact cessation success (eg, cravings and withdrawal126) and would be additional useful areas of future research.

There are a number of limitations to the current work. First, the criteria for inclusion in the review led to the exclusion of articles in languages other than English, not accessible online, or published in the form of a conference abstract. Second, data on most smoking behaviors came from a small number of studies and from a limited number of countries. Consequently, meta-analysis could only be conducted on current smoking prevalence. As more researchers examine sex differences in other smoking behaviors of PLWH, a clearer picture of these behaviors for men and women will emerge and can then be applied to efforts to help men and women with HIV to quit smoking. Third, very few studies reported data on persons who identified as transgender. More research is needed to examine differences in smoking behaviors of PLWH who identify as transgender compared with PLWH who identify as cisgender.

CONCLUSIONS

PLWH smoke at very high rates compared with the general population, and female sex is associated with a greater difference in smoking prevalence between PLWH and the general population. Little is known about the smoking behavior of transgender PLWH or sex differences in smoking behaviors related to cessation success such as withdrawal symptoms. A more detailed understanding of sex differences among PLWH relating to specific smoking behaviors and not limited to simple prevalence statistics would help to inform smoking cessation interventions for all PLWH. Furthermore, more research on smoking interventions with an emphasis on sex would help to ensure that interventions are optimized for both men and women PLWH.

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          Keywords:

          smoking; tobacco; sex; HIV/AIDS; review; meta-analysis

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