SUMMARY
SETTING
Tuberculosis (TB) health care facilities throughout Georgia.
OBJECTIVE
To describe smoking behaviors among health care workers (HCWs) at TB facilities and determine HCWs’ knowledge and beliefs regarding the impact of tobacco use on anti-tuberculosis treatment.
DESIGN
Cross-sectional survey from May to December 2014 in Georgia. Adult HCWs (age ≥ 18 years) at TB facilities were eligible. We administered a 60-question anonymous survey about tobacco use and knowledge of the effect of smoking on anti-tuberculosis treatment.
RESULTS
Of the 431 HCWs at TB facilities who participated, 377 (87.5%) were female; the median age was 50 years (range 20–77). Overall, 59 (13.7%) HCWs were current smokers and 35 (8.1%) were past smokers. Prevalence of current smoking was more common among physicians than among nurses (18.6% vs. 7.9%, P < 0.0001). Among HCWs, 115 (26.7%) believed smoking does not impact anti-tuberculosis treatment, and only 25.3% of physicians/nurses received formal training in smoking cessation approaches. Physicians who smoked were significantly more likely to believe that smoking does not impact anti-tuberculosis treatment than non-smoking physicians (aOR 5.11, 95%CI 1.46–17.90).
CONCLUSION
Additional education about the effect of smoking on TB treatment outcomes is needed for staff of TB health care facilities in Georgia. Nurses and physicians need more training about smoking cessation approaches for patients with TB.
Keywords: smoking, tobacco, HCW, TB
In 2015, there were an estimated 10.4 million cases of tuberculosis (TB) disease, and 1.5 million deaths due to TB worldwide.1 Globally, there are an estimated 1 billion tobacco smokers, of whom nearly 80% reside in low- and middle-income countries where the TB burden is greatest.2 Smoking tobacco is a well-established risk factor for TB. Meta-analyses estimate that smoking doubles the risk of TB disease and TB mortality and is associated with tuberculous infection and TB relapse.3–5
Among patients without TB, there is substantial evidence to demonstrate that behavioral and pharmacotherapeutic smoking cessation interventions delivered by health care workers (HCWs) are an effective way of reducing smoking-associated morbidity.6,7 Clinical guidelines are widely available to provide HCWs with empirically identified best practices to assist with smoking cessation.8–10 Evidence also suggests that smokers may be more receptive to HCWs’ advice to stop smoking when it is linked to an existing medical condition.11,12 Patients with TB may be highly motivated to quit smoking, given the negative impact of smoke inhalation on TB symptoms.13,14
Although standard TB case management provides a key opportunity for patients to receive smoking cessation support,15,16 little is known about HCW practices at TB facilities with respect to providing smoking cessation recommendations. Despite the recognized need for effective smoking cessation programs tailored to patients with TB,17–19 few interventions have been evaluated,19–21 and to date none have been evaluated using randomized trials.22 Studies that assessed the role of HCWs in assisting patients with TB to cease smoking demonstrated low or no participation in cessation efforts and limited knowledge about smoking cessation options or the impact of smoking on TB outcomes.19,23
In 2015, the country of Georgia (population 3.7 million) had a TB incidence of 99 per 100 000 population.1,24 The 2014 adult prevalence of tobacco smoking in Georgia was estimated at 55.5% among males and 4.8% among females;2 the prevalence of smoking among patients with TB was estimated to be 55.1% among males and 14.2% among females.25 Although Georgia has a high burden of TB and tobacco use, little is known about smoking behaviors or smoking cessation knowledge among HCWs providing care for patients with TB. In the context of limited information on the role of HCWs and provision of smoking cessation assistance for patients with TB, we conducted a study among HCWs at TB treatment facilities in the country of Georgia. The objectives of our study were to measure the prevalence and patterns of smoking among HCWs at TB treatment facilities and to determine the knowledge and beliefs regarding the impact of smoking on TB treatment outcomes.
STUDY POPULATION AND METHODS
Setting and participants
We conducted a cross-sectional study among HCWs at TB treatment facilities in Georgia from May to December 2014. All staff aged ≥ 18 years employed at TB treatment facilities in Georgia, including the National Center for Tuberculosis and Lung Diseases (Tbilisi, Georgia) and affiliated regional clinics that are also part of the Georgian National TB Program, were eligible to participate. Study staff invited HCWs and other treatment facility staff at these TB health care facilities to participate in an anonymous self-administered 60-question survey about tobacco smoking opinions and behaviors. Before enrollment, the participants received information about the study’s objectives and procedures, had the opportunity to ask questions about the study, and provided verbal consent.
Measures
The survey included questions adapted from the Global Adult Tobacco Survey,26 the Global Health Professionals Survey,27 and previously published studies28–30 that assessed smoking behavior and attitudes among health care professionals (see Appendix* for the complete survey). Briefly, the survey asked participants to self-report demographics and employment position at the TB facility, current and past smoking behaviors, and attitudes and beliefs about the role of smoking on anti-tuberculosis treatment. HCWs providing patient care (physicians, nurses and nursing staff) were also asked additional questions about training received, knowledge, and beliefs related to smoking and smoking cessation.
Current smokers were defined as those who self-reported ever smoking a cigarette, who had smoked at least 100 cigarettes, and reported currently smoking tobacco.31 Past smokers were defined as those who self-reported ever smoking a cigarette, who had smoked at least 100 cigarettes, but reported not currently smoking. Participants who self-reported not ever smoking a cigarette were defined as non-smokers. Current smokers were asked additional questions about smoking frequency (cigarettes per day), attempts to cease smoking in the past year, and other questions to characterize their smoking.
Participants were asked if they thought smoking impacts the prognosis for TB and if they thought smoking reduces the effectiveness of anti-tuberculosis treatment; those responding ‘yes’ to either question were defined as believing smoking negatively impacts TB treatment. HCWs responded to multiple Likert scale questions about smoking and smoking cessation related beliefs; those responding ‘agree’ or ‘strongly agree’ were defined as affirming the belief.
Statistical analyses
All study data were collected on a paper survey form, entered into a REDCap32 database (Research Electronic Data Capture, Vanderbilt University, Nashville, TN, USA) by study staff, and analyzed using SAS version 9.4 (Statistical Analysis System, Cary, NC, USA). We used bivariate analyses to examine the associations between 1) participant demographics and current smoking status, 2) specific smoking behaviors and age group and 3) smoking knowledge/beliefs and health care employment position. To determine statistical significance in bivariate analyses, the χ2 test was used for categorical variables and a Kruskal-Wallis or Wilcoxon rank-sum test for continuous variables. We used logistic regression to compare the odds of believing that smoking does not impact anti-tuberculosis treatment by current smoking status. The a priori hypothesis that the effect of current smoking status on the belief that smoking does not impact anti-tuberculosis treatment would differ across health care employment position (physician/nurse) was examined; we assessed this interaction using prevalence differences and logistic models. For interaction assessment, smoking status was dichotomized as current smoker vs. past smoker and non-smoker combined. A two-sided P < 0.05 was considered statistically significant in all analyses.
Ethical review
The study was reviewed and approved by the institutional review boards of Emory University, Atlanta, GA, USA, and the National Center for Tuberculosis and Lung Diseases, Tbilisi, Georgia.
RESULTS
During the study period, 471 HCWs from 11 TB treatment facilities throughout the country of Georgia were invited to participate, of whom 431 (91.5%) were enrolled in the study. Most participants were female (n = 377, 87.5%), reflecting the distribution of HCWs in Georgia; were employed as a nurse or nurse staff (n = 202, 46.9%); and resided in an urban setting (n = 392, 91.0%) (Table 1). The median age was 50 years (interquartile range [IQR] 40–57), and the median years of education was 14 (IQR 12–16).
Table 1.
Smoking status and demographic characteristics among HCWs at tuberculosis treatment facilities from the country of Georgia
| HCW characteristic | Total (n = 431) n (%) |
Current smoker (n = 59, 13.7%) n (%) |
Past smoker (n = 35, 8.1%) n (%) |
Non-smoker (n = 337, 78.2%) n (%) |
P value* |
|---|---|---|---|---|---|
| Sex | |||||
| Male | 54 (12.5) | 25 (46.3) | 11 (20.4) | 18 (33.3) | < 0.0001† |
| Female | 377 (87.5) | 34 (9.0) | 24 (6.4) | 319 (84.6) | |
| Age, years, median [IQR] | 50 [40–57] | 49 [38–56] | 44 [37–57] | 50 [41–58] | 0.30 |
| Residence, urban | 392 (91.0) | 51 (13.0) | 32 (8.2) | 309 (78.8) | 0.43 |
| Employee category | |||||
| Nurse/nurse staff | 202 (46.9) | 16 (7.9) | 9 (4.5) | 177 (87.6) | |
| Physician | 86 (20.0) | 16 (18.6) | 12 (14.0) | 58 (67.4) | < 0.0001† |
| Laboratory/research staff | 45 (10.4) | 6 (13.3) | 5 (11.1) | 34 (75.6) | |
| Administrative staff | 58 (13.5) | 18 (31.0) | 6 (10.3) | 34 (58.6) | |
| Other‡ | 40 (9.3) | 3 (7.5) | 3 (7.5) | 34 (85.0) | |
| Education, years, median [IQR] | 14 [12–16] | 15 [12–16] | 15 [13–17] | 13 [12–16] | 0.0068† |
| Smoking permitted in home | 35 (8.1) | 11 (31.4) | 5 (14.3) | 19 (54.3) | < 0.0001† |
| Smoking permitted in car | 19 (4.4) | 10 (52.6) | 4 (21.1) | 5 (26.3) | < 0.0001† |
| Smoke-free policy at work | 233 (54.1) | 31 (13.3) | 24 (10.3) | 178 (76.4) | 0.19 |
| Public smoke exposure§ | 174 (40.4) | 27 (15.5) | 19 (10.9) | 128 (73.6) | 0.57 |
Two-sided general χ2 P value for categorical variables and two-sided Kruskal-Wallis test for continuous variables.
Statistically significant.
Included medical/nursing student, security staff, or information technology staff.
Self-reported exposure to second-hand smoke on a daily basis.
HCW = health care worker; IQR = interquartile range.
The overall prevalence of current smoking among HCWs at TB facilities was 13.7% (95% confidence interval [CI] 10.7–17.2), and 8.1% (95%CI 5.8–11.0) reported past smoking (Table 1). Current smoking was significantly more common among males than females (46.3% vs. 9.0%), among physicians than nurses (18.6 vs. 7.9%), and among those employed in an administrative position than among all other positions (31.0% vs. 11.0%, P < 0.0001 for all three comparisons). The median years of education was greater among smokers (15, IQR 12–16) than among non-smokers (13, IQR 12–16, P < 0.01). Compared to non-smokers, current smokers were more likely to report that smoking was permitted in their home (18.6% vs. 5.6%) and car (16.9% vs. 1.5%, P < 0.0001).
Among 59 HCWs at TB facilities who reported current smoking, the self-reported median age at first smoking regularly was 22 years (IQR 19–26), and the median number of cigarettes smoked per day was 15 (IQR 8–20). Half (n = 30, 50.9%) of the current smokers reported attempting to quit smoking in the past year; the median number of attempts among those who attempted was two (IQR 1–5). In addition, 56.0% (n = 33) of current smokers reported that they expected to quit in the distant future.
Among 431 HCWs employed at the Georgian TB facilities, 115 (26.7%) reported believing that smoking does not impact TB treatment outcome (Table 2). In multivariable analysis, HCWs aged ≤50 years were significantly more likely to believe that smoking does not impact anti-tuberculosis treatment than those aged ≥51 years (adjusted odds ratio [aOR] 1.66, 95%CI 1.05–2.62). When age was categorized as 20–40 years vs. ≥41 years, the association between age and belief that smoking does not impact anti-tuberculosis treatment increased (aOR 2.11, 95%CI 1.02–4.37, data not shown). Compared to non-smokers, current smokers were non-significantly more likely to believe that smoking does not impact anti-tuberculosis treatment (aOR 1.39, 95%CI 0.71–2.72).
Table 2.
Belief that smoking does not impact anti-tuberculosis treatment among HCWs at TB treatment facilities in the country of Georgia
| Smoking negatively impacts anti-tuberculosis treatment (n = 316, 73.3%) n (%) |
Smoking does not impact anti-tuberculosis treatment (n = 115, 26.7%) n (%) |
OR (95%CI)* | aOR (95%CI)*† | |
|---|---|---|---|---|
| Sex, male vs. female | 38 (70.4) | 16 (29.6) | 1.18 (0.63–2.22) | 1.57 (0.74–3.34) |
| Age, years | ||||
| 20–50 | 164 (68.9) | 74 (31.1) | 1.67 (1.08–2.60)‡ | 1.66 (1.05–2.62)‡ |
| 51–77 | 152 (78.8) | 41 (21.2) | Reference | Reference |
| Residence, urban vs. rural | 287 (73.2) | 105 (26.8) | 1.06 (0.50–2.25) | 1.21 (0.56–2.64) |
| Employee category | ||||
| Nurse/nurse staff | 140 (69.3) | 62 (30.7) | 1.77 (0.77–4.06) | 1.65 (0.65–4.15) |
| Physician | 67 (77.9) | 19 (22.1) | 1.13 (0.45–2.87) | 1.33 (0.51–3.50) |
| Laboratory/research staff | 31 (68.9) | 14 (31.1) | 1.81 (0.67–4.91) | 1.94 (0.70–5.41) |
| Administrative | 46 (79.3) | 12 (20.7) | 1.04 (0.38–2.84) | 0.82 (0.28–2.39) |
| Other§ | 32 (80.0) | 8 (20.0) | Reference | Reference |
| Education, years | ||||
| ≤11 | 53 (71.6) | 21 (28.4) | 1.29 (0.71–2.40) | 1.28 (0.62–2.66) |
| 12–14 | 113 (70.2) | 48 (29.8) | 1.39 (0.86–2.22) | 1.40 (0.74–2.66) |
| ≥15 | 150 (76.5) | 46 (23.5) | Reference | Reference |
| Smoking status | ||||
| Current smoker | 40 (67.8) | 19 (32.2) | 1.37 (0.75–2.48) | 1.39 (0.71–2.72) |
| Past smoker | 26 (74.3) | 9 (25.7) | 1.00 (0.45–2.21) | 0.97 (0.42–2.25) |
| Non smoker | 250 (74.2) | 87 (25.8) | Reference | Reference |
Logistic regression was used to estimate the odds of reporting that smoking does not impact anti-tuberculosis treatment.
Multivariable logistic regression including all variables in the table.
Statistically significant.
Included medical/nursing student, security staff, or information technology staff.
HCW = health care worker; OR = odds ratio; CI = confidence interval; aOR = adjusted OR
In interaction assessment, physicians who were current smokers were significantly more likely than non/past smokers to believe that smoking does not impact anti-tuberculosis treatment (prevalence difference 26.7%, 95%CI 0.7–52.5), while among nurses there was little difference in belief by smoking status (prevalence difference 0.6%, 95%CI −23.1 to 24.3) (Table 3). In multivariable analysis adjusted for age, sex, and years of education, a similar difference in belief that smoking does not impact anti-tuberculosis treatment by smoking status was observed among physicians (aOR 5.11, 95%CI 1.46–17.90) but not nurses (aOR 1.00, 95%CI 0.32–3.08). Statistical tests for heterogeneity of smoking status by employment type in multivariable analysis were non-significant (P = 0.06).
Table 3.
Interaction between current smoking status and employment position with the belief that smoking does not impact anti-tuberculosis treatment
| Prevalence of the belief that smoking does not impact anti-tuberculosis treatment, n/N (%)
|
||
|---|---|---|
| Physician (n = 86) | Nurse (n = 202) | |
| Current smoker | 7/16 (43.8) | 5/16 (31.3) |
| Non/past smoker | 12/70 (17.1) | 57/186 (30.7) |
| Prevalence difference, % (95%CI) | 26.7 (0.7–52.5) | 0.6 (−23.1 to 24.3) |
| aOR (95%CI)* | ||
| Current smoker | 5.11 (1.46–17.90) | 1.00 (0.32–3.08) |
| Non/past smoker | Reference | Reference |
Multivariable model was adjusted for employment position, age, sex, and years of education.
aOR = adjusted odds ratio; CI = confidence interval.
Of the 288 HCWs with patient contact (physicians and nurses), a low proportion (n = 73, 25.3%) had received formal training in smoking cessation approaches (Table 4). Physicians were significantly more likely to be aware of antidepressant pharmacotherapy for smoking cessation than nurses (38.4% vs. 16.8%, P < 0.0001); however, physicians were less likely than nurses to know of community resources available to help patients with TB stop smoking (37.2% vs. 50.5%, P = 0.04). A significantly lower proportion of physicians than nurses believed smoking increases the required duration of anti-tuberculosis treatment (57.0% vs. 76.2%, P = 0.001), but nearly all physicians (95.4%) and nurses (96.0%) believed HCWs should routinely advise patients with TB to cease smoking.
Table 4.
Training experience related to smoking and smoking-related beliefs among HCWs at TB treatment facilities with regular patient contact in the country of Georgia
| Physicians (n = 86, 29.9%) n (%) |
Nurses (n = 202, 70.4%) n (%) |
P value* | |
|---|---|---|---|
| Training received and knowledge related to smoking: | |||
| Taught about dangers of smoking | 47 (54.7) | 84 (41.6) | 0.04† |
| Discussed in training why people smoke | 49 (57.0) | 100 (49.5) | 0.25 |
| Taught to record smoking history in medical record | 62 (72.1) | 124 (61.4) | 0.08 |
| Taught formal smoking cessation approaches | 19 (22.1) | 54 (26.7) | 0.41 |
| Taught to provide smoking cessation materials | 42 (48.8) | 86 (42.6) | 0.33 |
| Aware of nicotine replacement therapy (patch or gum) | 61 (70.9) | 124 (61.4) | 0.12 |
| Aware of antidepressants in tobacco cessation programs | 33 (38.4) | 34 (16.8) | < 0.0001† |
| Know of resources to help patients quit | 32 (37.2) | 102 (50.5) | 0.04† |
| Ever heard of electronic cigarettes | 76 (88.4) | NA | |
| Patients ever asked about using electronic cigarettes to quit | 46 (53.4) | NA | |
| HCWs agree/strongly agree with smoking-related beliefs: | |||
| Smoking increases TB treatment duration | 49 (57.0) | 154 (76.2) | 0.001† |
| Smoking should be banned in TB hospitals | 72 (83.7) | 170 (84.2) | 0.93 |
| HCWs get training on smoking cessation | 70 (81.4) | 170 (84.2) | 0.56 |
| HCWs are role models for their patients | 76 (88.4) | 191 (94.6) | 0.06 |
| HCWs should routinely advise patients to cease smoking | 82 (95.4) | 194 (96.0) | 0.79 |
| HCWs can improve patient’s chance of smoking cessation | 55 (64.0) | 121 (59.9) | 0.52 |
| HCWs who smoke are less likely to advise patients to quit | 46 (53.5) | 83 (41.1) | 0.05 |
Two-sided general χ2.
Statistically significant.
HCW = health care worker; TB = tuberculosis; NA = not available.
DISCUSSION
We found that 13% of HCWs employed at TB treatment facilities in the country of Georgia were current smokers, including nearly half of male physicians. More than 25% of 431 HCWs at 11 TB facilities in Georgia erroneously believed that smoking does not impact TB treatment outcomes, and this belief was significantly more common among younger HCWs. We also found that the effect of smoking status impacted beliefs about TB treatment outcomes. In multivariable analysis, physicians who currently smoked were five times more likely to report that smoking does not impact anti-tuberculosis treatment than non-smoking physicians. Targeted education and smoking cessation programs for HCWs at TB treatment facilities may provide numerous benefits, for preserving the health of HCWs and patients, improving TB treatment outcomes, and increasing quality of life throughout the course of their lives.
The prevalence of current smoking reported by HCWs working at TB treatment facilities in our study was comparable to the estimated national prevalence of smoking in Georgia. For example, 2012–2014 national estimates of smoking prevalence in Georgia were 53–56% among males and 5–6% among females.2,33 In our study of HCWs at TB facilities, 46% of males and 9% of females reported current smoking. It is to be noted that smoking prevalence among HCWs at TB facilities in Georgia was similar to that among patients with TB (55% among males and 14% among females). We suggest that non-smoking HCWs who believe that smoking impacts anti-tuberculosis treatment and serve as role models are likely to be better suited to support smoking cessation efforts of patients with TB.
Studies have not previously surveyed HCWs at TB facilities about smoking behaviors or beliefs about smoking cessation in the context of anti-tuberculosis treatment. Our study enrolled 431 HCWs from TB facilities in various regions of Georgia and surveyed several different types of health care employees. One previous qualitative focus group study of 17 TB physicians from Beijing, China, reported that some TB physicians doubted that smoking affected TB.23 We reported that 22% of TB physicians believed that smoking does not impact anti-tuberculosis treatment and that compared to non-smoking physicians, current smoking physicians were more than five times as likely to believe that smoking does not impact TB treatment. The study from Beijing also reported that physicians who also smoked did not believe smoking cessation to be an integral part of anti-tuberculosis treatment. It is probable that patients with TB who receive care from physicians who do not believe smoking impacts anti-tuberculosis treatment will have a reduced likelihood of smoking cessation during treatment. Because patients with TB who do not cease smoking are at increased risk of TB failure and death,3,5 it is imperative that TB physicians understand the impact of smoking on treatment and support patients to quit smoking.
Our results suggest that training HCWs (specifically physicians and nurses) at these TB facilities about available clinical guidelines for smoking cessation would be beneficial. Previous international recommendations to assign specific HCWs to provide tobacco and smoking cessation interventions as part of TB case management would be a testable and feasible intervention for TB health care facilities in Georgia.15 In addition, our finding that HCWs aged ≤40 years were more than twice as likely to believe smoking does not impact anti-tuberculosis treatment suggests that training related to the negative effects of smoking should be developed to specifically engage younger HCWs. While all HCWs likely need smoking cessation-related training, instruction methods and materials may need to be tailored differently according to the age of the HCWs. Effective training of health care providers on the clinical practice guidelines for smoking cessation may significantly increase rates of patients’ quitting and in turn, improve TB cure rates.34 Preparing a willing and informed health care staff to deliver TB smoking cessation interventions requires that workers view the activity as essential, understand and believe they should provide the cessation intervention, are trained about how to perform the intervention tasks, and have confidence in their ability to deliver the recommended cessation assistance.15,35
Our study was subject to limitations. First, because participation in the survey was anonymous, it was not possible to determine the proportion of HCWs at each TB facility who enrolled. Nonetheless, to our knowledge, our study among 431 physicians, nurses, and other facility staff is the largest to assess smoking behaviors and beliefs among HCWs at TB facilities. Furthermore, our study included 11 geographically diverse TB facilities; we therefore believe our findings are generalizable to HCWs at TB facilities throughout Georgia. Second, as potential participants were informed of the study’s focus on smoking, this may have influenced HCW participation. However, we believe that because the study survey was anonymous, HCWs who smoked were more likely to report their smoking behaviors. Moreover, the reported prevalence of current smoking among TB HCWs was consistent with national estimates of smoking from the country of Georgia.
CONCLUSIONS
Education about the negative impact of smoking on TB outcomes should be provided to all HCWs at TB facilities in Georgia, including physicians and nurses. HCWs at TB facilities with patient contact should receive training about smoking cessation interventions. Such interventions should be offered to patients with TB and to HCWs who smoke.
Supplementary Material
Acknowledgments
This study was supported in part by the National Institutes of Health (NIH) Fogarty International Center (D43TW007124), NIH National Institute of Allergy and Infectious Diseases (K23AI103044), Bethesda, MD, USA, the Atlanta Clinical and Translational Science Institute (NIH/NCATS UL1TR000454), and the Emory Global Health Institute, Atlanta, GA, USA.
The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Conflicts of interest: none declared.
Footnotes
The appendix is available in the online version of this article, at http://www.ingentaconnect.com/content/iuatld/ijtld/2017/00000021/00000009/art00017
References
- 1.World Health Organization. Global tuberculosis report, 2016. Geneva, Switzerland: WHO; 2016. WHO/HTM/TB/2016.13. [Google Scholar]
- 2.World Health Organization. WHO report on the global tobacco epidemic. Geneva, Switzerland: WHO; 2015. [Google Scholar]
- 3.Slama K, Chiang CY, Enarson DA, et al. Tobacco and tuberculosis: a qualitative systematic review and meta-analysis. Int J Tuberc Lung Dis. 2007;11:1049–1061. [PubMed] [Google Scholar]
- 4.Bates MN, Khalakdina A, Pai M, Chang L, Lessa F, Smith KR. Risk of tuberculosis from exposure to tobacco smoke: a systematic review and meta-analysis. Arch Intern Med. 2007;167:335–342. doi: 10.1001/archinte.167.4.335. [DOI] [PubMed] [Google Scholar]
- 5.Lin HH, Ezzati M, Murray M. Tobacco smoke, indoor air pollution and tuberculosis: a systematic review and meta-analysis. PLOS Med. 2007;4:e20. doi: 10.1371/journal.pmed.0040020. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Stead LF, Buitrago D, Preciado N, Sanchez G, Hartmann-Boyce J, Lancaster T. Physician advice for smoking cessation. Cochrane Database Syst Rev. 2013;(5):CD000165. doi: 10.1002/14651858.CD000165.pub4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Stead LF, Koilpillai P, Fanshawe TR, Lancaster T. Combined pharmacotherapy and behavioural interventions for smoking cessation. Cochrane Database Syst Rev. 2016;(3):CD008286. doi: 10.1002/14651858.CD008286.pub3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Schnoll RA, Rukstalis M, Wileyto EP, Shields AE. Smoking cessation treatment by primary care physicians: an update and call for training. Am J Prev Med. 2006;31:233–239. doi: 10.1016/j.amepre.2006.05.001. [DOI] [PubMed] [Google Scholar]
- 9.West R, McNeill A, Raw M. Smoking cessation guidelines for health professionals: an update. Health Education Authority Thorax. 2000;55:987–999. doi: 10.1136/thorax.55.12.987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Clinical Practice Guideline Treating Tobacco Use and Dependence 2008 Update Panel, Liaisons, and Staff. A clinical practice guideline for treating tobacco use and dependence: 2008 update. A US Public Health Service report. Am J Prev Med. 2008;35:158–176. doi: 10.1016/j.amepre.2008.04.009. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Butler CC, Pill R, Stott NC. Qualitative study of patients’ perceptions of doctors’ advice to quit smoking: implications for opportunistic health promotion. BMJ. 1998;316:1878–1881. doi: 10.1136/bmj.316.7148.1878. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Carlos RC, Fendrick AM. Improving cancer screening adherence: using the ‘teachable moment’ as a delivery setting for educational interventions. Am J Managed Care. 2004;10:247–248. [PubMed] [Google Scholar]
- 13.Aryanpur M, Masjedi MR, Mortaz E, et al. Intention to quit smoking and associated factors in smokers newly diagnosed with pulmonary tuberculosis. Tanaffos. 2016;15:17–24. [PMC free article] [PubMed] [Google Scholar]
- 14.Melzer AC, Feemster LC, Crothers K, et al. Respiratory and bronchitic symptoms predict intention to quit smoking among current smokers with, and at risk for, chronic obstructive pulmonary disease. Ann Am Thorac Soc. 2016;13:1490–1496. doi: 10.1513/AnnalsATS.201601-075OC. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Slama K, Chiang CY, Enarson DA. Introducing brief advice in tuberculosis services. Int J Tuberc Lung Dis. 2007;11:496–499. [PubMed] [Google Scholar]
- 16.Schneider NK, Novotny TE. Addressing smoking cessation in tuberculosis control. Bull World Health Organ. 2007;85:820–821. doi: 10.2471/BLT.07.043794. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Wang J, Shen H. Review of cigarette smoking and tuberculosis in China: intervention is needed for smoking cessation among tuberculosis patients. BMC Public Health. 2009;9:292. doi: 10.1186/1471-2458-9-292. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Pradeepkumar AS, Thankappan KR, Nichter M. Smoking among tuberculosis patients in Kerala, India: proactive cessation efforts are urgently needed. Int J Tuberc Lung Dis. 2008;12:1139–1145. [PubMed] [Google Scholar]
- 19.Ng N, Padmawati RS, Prabandari YS, Nichter M. Smoking behavior among former tuberculosis patients in Indonesia: intervention is needed. Int J Tuberc Lung Dis. 2008;12:567–572. [PubMed] [Google Scholar]
- 20.Lin Y, Wang LX, Qiu LX, et al. A smoking cessation intervention among tuberculosis patients in rural China. Public Health Action. 2015;5:183–187. doi: 10.5588/pha.15.0025. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Siddiquea BN, Islam MA, Bam TS, et al. High quit rate among smokers with tuberculosis in a modified smoking cessation programme in Dhaka, Bangladesh. Public Health Action. 2013;3:243–246. doi: 10.5588/pha.13.0051. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Jeyashree K, Kathirvel S, Shewade HD, Kaur H, Goel S. Smoking cessation interventions for pulmonary tuberculosis treatment outcomes. Cochrane Database Syst Rev. 2016;(1):CD011125. doi: 10.1002/14651858.CD011125.pub2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Shin SS, Xiao D, Cao M, et al. Patient and doctor perspectives on incorporating smoking cessation into tuberculosis care in Beijing, China. Int J Tuberc Lung Dis. 2012;16:126–131. doi: 10.5588/ijtld.11.0044. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.World Bank. Population estimates and projections. Washington DC, USA: World Bank; 2015. [Google Scholar]
- 25.Gegia M, Magee MJ, Kempker RR, et al. Tobacco smoking and tuberculosis treatment outcomes: a prospective cohort study in Georgia. Bull World Health Organiz. 2015;93:390–399. doi: 10.2471/BLT.14.147439. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Global Adult Tobacco Survey Group. Tobacco questions for surveys: a subset of key questions from the Global Adult Tobacco Survey (GATS) 2. Atlanta, GA, USA: Centers for Disease Control and Prevention; 2011. [Google Scholar]
- 27.Centers for Disease Control and Prevention. Tobacco use and cessation counseling—global health professionals survey pilot study, 10 countries, 2005. MMWR Morb Mortal Wkly Rep. 2005;54:505–509. [PubMed] [Google Scholar]
- 28.Prochaska JO, DiClemente CC, Norcross JC. In search of how people change. Applications to addictive behaviors. Am Psychol. 1992;47:1102–1114. doi: 10.1037//0003-066x.47.9.1102. [DOI] [PubMed] [Google Scholar]
- 29.Movsisyan NK, Varduhi P, Arusyak H, Diana P, Armen M, Frances SA. Smoking behavior, attitudes, and cessation counseling among healthcare professionals in Armenia. BMC Public Health. 2012;12:1028. doi: 10.1186/1471-2458-12-1028. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30.Biener L, Abrams DB. The contemplation ladder: validation of a measure of readiness to consider smoking cessation. Health Psychol. 1991;10:360–365. doi: 10.1037//0278-6133.10.5.360. [DOI] [PubMed] [Google Scholar]
- 31.Ryan H, Trosclair A, Gfroerer J. Adult current smoking: differences in definitions and prevalence estimates—NHIS and NSDUH, 2008. J Environ Public Health. 2012;2012:918368. doi: 10.1155/2012/918368. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32.Harris PA, Taylor R, Thielke R, Payne J, Gonzalez N, Conde JG. Research electronic data capture (REDCap)—a metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform. 2009;42:377–381. doi: 10.1016/j.jbi.2008.08.010. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Roberts B, Gilmore A, Stickley A, et al. Changes in smoking prevalence in 8 countries of the former Soviet Union between 2001 and 2010. Am J Public Health. 2012;102:1320–1328. doi: 10.2105/AJPH.2011.300547. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.El Sony A, Slama K, Salieh M, et al. Feasibility of brief tobacco cessation advice for tuberculosis patients: a study from Sudan. Int J Tuberc Lung Dis. 2007;11:150–155. [PubMed] [Google Scholar]
- 35.Elford RW, Yeo M, Jennett PA, Sawa RJ. A practical approach to lifestyle change counselling in primary care. Patient Educ Couns. 1994;24:175–183. doi: 10.1016/0738-3991(94)90011-6. [DOI] [PubMed] [Google Scholar]
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