Examination of the variability in study effect sizes for correlates reported in terms of I2 in Table 3 indicate low heterogeneity for sex (I2 = 24.42%) and history of cardiovascular disease (I2 = 0%); moderate heterogeneity for BMI (I2 = 50.12%); and high levels of heterogeneity for age (I2 = 71.55%), hypertension (I2 = 72.94%), and diabetes (I2 = 97.56%). In particular, the directions of the ORs for hypertension and diabetes were inconsistent across the studies (ie, ORs >1 and <1).
Outcomes of Posttransplant Smoking
Included studies examined 24 outcomes of posttransplant smoking, of which 20 were studied less than 5 times (Figure 8). There was only 1 study investigating the association with health-related quality of life and no studies investigating economic outcomes.
Average effect size estimates could be calculated for 4 outcomes (Table 3, Figure 7). Across 9 studies, our meta-analysis showed that the odds of having cardiovascular disease (ie, new onset disease not present at time of transplantation) were 1.41 times higher than that of nonsmokers (OR, 1.41; 95% CI, 1.02-1.95; P = 0.036). Based on 6 studies, the odds ratio for the association between posttransplant smoking and nonskin malignancies was 2.58 (95% CI, 1.26-5.29; P = 0.01). The pooled results from 5 and 8 studies showed a statistically significant association of posttransplant smoking with patient survival time (OR, 0.59; 95% CI, 0.44-0.79; P < 0.001) and patient mortality (OR, 1.74; 95% CI, 1.21-2.48; P = 0.003), respectively.
Assessment of heterogeneity of study effect sizes for outcomes yields a low I2 value of 38.77% for cardiovascular disease, moderate I2 value of 50.59% for patient survival time, and high I2 values of 73.68% and 83.38% for nonskin malignancies and patient mortality, respectively (Table 3). Except for 1 study on nonskin malignancies and 1 study on patient mortality, the directions of the associations across studies were consistent.
This systematic review and meta-analysis comprehensively summarized the state of the art on correlates of pos-transplant smoking for the first time. It is also the first investigation that synthesized study findings on the association of posttransplant smoking with various clinical outcomes in single adult lung, heart, liver, and kidney transplant patients. This is useful given the continued challenge to identify modifiable risk factors to improve posttransplant outcomes. The results of this meta-analysis may inform transplant clinicians which patients are more likely to smoke posttransplant and provide some recommendations for future research in this area.
Surprisingly enough, of the 90 correlates abstracted from the included papers, we could only calculate pooled effect sizes for 6 of them. More specifically, we revealed that male patients, younger patients, and patients with a lower BMI were more likely to be smokers. Hypertension, diabetes mellitus, and a history of cardiovascular disease were not significantly associated with posttransplant smoking. However, it is important to be cautious about drawing conclusions for hypertension and diabetes, because the directions of the ORs were inconsistent across the studies, in addition to high I2 values.
The finding that male patients are more likely to smoke posttransplant is in line with the World Health Organization findings showing that men smoke at 5 times the rate of women (the average rates are 36% and 7%, respectively).56 Globally, however, the gap between men's and women's smoking rates is becoming smaller. As society became more tolerant of women who smoke and women's economic resources are increasing, the tobacco industry has been targeting women through advertisements promoting cigarettes as a symbol of freedom, emancipation, beauty, and prestige.57,58 So also in transplantation, despite men being more prone to posttransplant smoking, the rise of smoking among women needs to be carefully followed.
From our results, it also appeared that older patients were less likely to smoke than younger patients. A hypothesis might be that older transplant patients experience more health problems, including smoking-related illnesses, and therefore are more likely to stop smoking, yet this merits further investigation. Another possibility is that older patients already died because of smoking-related illnesses and were subsequently not included in the analyses (ie, survival bias).
For BMI, we found that patients with a higher BMI were significantly less likely to smoke. On the one hand, this is not surprising because smokers tend to be leaner than nonsmokers and concerns over weight gain are often a reason why individuals are reluctant to stop smoking.59,60 On the other hand, one would expect that unhealthy behaviors, such as smoking, unhealthy eating, and physical inactivity, go hand in hand. Also, in the general population, the association between BMI and smoking is complex and not completely understood, and published studies yielded conflicting results.61 More studies are needed to explore possible causal mechanisms.
Hypertension was not significantly associated with posttransplant smoking. This should come as no surprise because although smoking can cause acute blood pressure elevation through the stimulation of the sympathetic nervous system,62 chronic smoking has not been conclusively shown to cause high blood pressure in the general population.63 The lack of an association between diabetes mellitus and posttransplant smoking, on the other hand, contradicts evidence in other populations, showing that smokers are 30% to 40% more likely to develop type 2 diabetes than nonsmokers.64 It might be that an association in this meta-analysis was not found because intensity and duration of smoking (including pretransplant smoking) were not taken into account. As indicated earlier, it must also be noted that there was a significant degree of heterogeneity among the studies for hypertension and diabetes, making it difficult to draw any firm conclusions. When comparing these different studies, differences can be observed, with a wide variety between study designs used, smoking definitions, and smoking assessment methods, possibly explaining the observed heterogeneity. For 3 of the 7 studies on diabetes, it was also not clear whether diabetes was already present at time of transplantation or newly developed after transplantation.
Having a history of cardiovascular disease was also not significantly associated with posttransplant smoking. In contrast to hypertension and diabetes, there was no heterogeneity among the studies. The lack of a significant association is difficult to explain. One would assume that patients who have a history of cardiovascular disease are probably more likely to be the ones who smoked pretransplant, and 3 studies included in this review showed that pretransplant smoking was associated with posttransplant smoking (Figure 4). On the other hand, it is possible that having a history of cardiovascular disease is a good motivator to maintain smoking abstinence. Additional research examining the association between having a history of cardiovascular disease and posttransplant smoking is needed.
For the remaining 89 correlates, no effect sizes could be calculated. Most of these factors were investigated only once or twice and focused largely on condition-related factors, whereas healthcare team and system-related factors were not studied at all. Yet, smoking is a behavioral process strongly influenced by the environment in which the patient lives, including the healthcare practices and systems. Thus, from a behavioral perspective, healthcare team and system-related factors should be studied more. The general paucity of studies examining relevant factors is probably due to a lack of theoretical underpinnings in the included studies. Nevertheless, theoretical or conceptual models, like “the Integrated Model of Behavioral Prediction of Fishbein”65 or “the conceptual framework of the International Tobacco Control Policy Evaluation Project”66 are valuable in developing more targeted research questions, in identifying variables to study, and in interpreting research results.
Of the 24 outcomes abstracted from the included papers, we could only calculate pooled effect sizes for 4 of them, that is, cardiovascular disease, nonskin malignancies, patient survival time, and patient mortality. Our results suggest that posttransplant smoking is statistically significantly associated with all 4 outcomes, which is in line with the wide acknowledgment that cigarette smoking is a major risk factor for cardiovascular disease, cancer, and mortality in the general population. However, given that smoking globally contributes to the burden of over 200 diseases, it is remarkable that few studies (ie, less than 5 studies) explored the effects of posttransplant smoking on other outcomes, such as graft loss, stroke, pulmonary diseases, kidney function, osteoporosis, skin problems, and so on. On the other hand, the fact that 73 studies examined correlates/outcomes of posttransplant smoking indicates that not only pretransplant smoking but also smoking after transplantation is increasingly recognized as being important. For a long time, it was assumed that transplant patients did not smoke after having received the precious gift of life. However, we should not forget that smoking is an addiction, hence relapse after transplantation is always possible.67 Smoking relapse after smoke-free periods is not typical for transplant patients, but reflects the cyclic process of smoking-quitting relapse also observed in the general population.
Apart from the fact that few pooled effect sizes could be calculated for both correlates and outcomes, despite the multitude of factors having been explored, some results from the quality assessment also merit some further reflection. First, most studies did not provide a definition of smoking, and for those that did, the definition was not consistent. For example, some defined smoking as “smoking 7 or more cigarettes per week,”40 while others simply defined it as current smoking, regardless of the intensity or duration of smoking.68 Future research should specify the type and “dose” of smoking over a specific time period (eg, posttransplant or lifetime). Second, 47 studies (64.4%) did not use a prospective observational design, hence conclusions cannot be made about causality. Third, most studies used self-reporting with its inherent limitations to determine the prevalence of smoking, with only a few using biological measures. Some of the inconsistent correlations may be attributed to the use of these different smoking definitions and measurements. Fourth, although there are some articles on smoking before lung transplantation, there was only 1 article on correlates or outcomes of posttransplant smoking in lung transplant patients.29 Although relapse numbers are lower for lung transplant patients, probably reflecting the strict nonsmoking policy and regular assessment of a patient's smoking status pretransplant and posttransplant, they do not equal zero. More specifically, a recent study of Ruttens and colleagues69 demonstrated that 12% of lung transplant patients resumed smoking posttransplant. Thus, we believe that more studies are needed to better understand the correlates and outcomes of posttransplant smoking, especially in this vulnerable transplant patient group. Fifth, there were studies that only permitted the effect size estimate to be approximated from less than optimal statistical information (eg, only the sample size, information on the direction of the association, and a P value less than or greater than a specified value), leading to less precise estimates of the effect sizes. Moreover, some studies could not be included because the data reported did not permit the calculation of an effect size, probably causing some bias in our review. Although some authors were contacted in case of missing data, we did not receive the information needed to calculate the effect sizes.
This systematic review and meta-analysis might have some methodological shortcomings as well. First, despite the extensive and rigorous systematic review process used, it is possible that relevant papers were missed, bearing in mind that searching for literature is not an exact science. Second, although we included papers in 7 different languages, we had to exclude 10 articles due to a foreign language nobody of the research team could understand. Third, our review is limited to the occurrence of posttransplant smoking, and we did not take into account the severity or duration of posttransplant smoking. Also, by focusing on posttransplant smoking only, we are aware that we did not look at total lifetime exposure to cigarette smoke (ie, both pretransplant and posttransplant), which might be important when investigating impact on outcomes. However, most authors do not clearly distinguish pretransplant versus posttransplant smoking, making it impossible to run separate analyses according to the patients' pretransplant smoking history. These studies were strictly excluded. Moreover, in case that 3 groups were reported (nonsmokers, past smokers, and current smokers), we considered past smokers as nonsmokers, although we did not know whether these patients quit smoking before or after transplantation.
Implications for Clinical Practice
Despite the limitations of this review, it seems reasonable to conclude that abstinence from cigarette smoking should be strongly encouraged after transplantation, taking into account the association with cardiovascular disease, nonskin malignancies, a shorter patient survival time, and mortality.
Transplant teams have a key role to play in this important area of prevention. They should be encouraged to focus on smoking abstinence as a central theme to discuss with the patient at least at the yearly follow-up check-up. In patients with higher odds for smoking posttransplant (ie, male patients, younger patients, patients with a lower BMI), smoking status may need to be assessed more frequently (every 1 to 3 months).9
Smoking status can be assessed by self-report and/or biological measures (eg, cotinine measures derived from saliva, urine, and blood or exhaled carbon monoxide). Although cotinine measurements are more objective methods and preferred over self-reported smoking exposure to assess relation of smoking with outcomes in epidemiological studies,30 self-report is probably the most accessible and cost-effective method to implement in daily clinical practice. Moreover, it has been shown in nontransplant populations that self-reporting of smoking can be a valid measurement method, when used under nonthreatening and open circumstances between healthcare providers and their patients.70 At the same time, one must be aware that some patients may not admit smoking, because smoking after transplantation remains an ethical issue, and it might be considered ethically justified to deny active smokers a second transplant. Therefore, self-report screening tools must be validated in transplant populations, and where possible, combined with cotinine measurements.71
Both the inpatient and the outpatient setting provide an opportunity to promote smoking cessation to active smokers and to encourage continued smoking cessation to past and never smokers. It is important for transplant clinicians to assess patients' motivation to quit smoking or continue smoking cessation and to realize that many patients often make repeated attempts to stop before succeeding in breaking their habit. If motivated patients have difficulties to stop smoking, they can be referred to community smoking cessation services for more intensive behavioral support.
Further, the Institute of Medicine recommends including the behavioral assessment and interventions in the electronic health record, because this has great potential to improve quality, coordination, safety, health outcomes, and overall efficiency in healthcare.72
Implications for Future Research
The findings of the current systematic review and meta-analysis also reveal several important implications for future research. First, it is important to emphasize the importance of good and complete reporting. For example, authors should better define smoking, and report important smoking details, such as smoking intensity, duration, and number of pack-years. We also recommend to do separate analyses for pretransplant and posttransplant smoking because correlates and outcomes might be different. Authors also need to report sufficient information to allow calculation of effect sizes. At a minimum, they need to report the sample size, exact P value, and information on the direction of the association. In addition, future research needs to pay attention to several issues related to the research methodology. For example, studies should be guided by theoretical models to examine the mechanism of how pretransplant and posttransplant factors influence posttransplant smoking and how posttransplant smoking, in turn, may affect outcomes. That way, the relationship of posttransplant smoking with more targeted factors at the patient level, health care system–related factors (eg, higher tobacco taxes, antismoking education, bans on tobacco advertising and promotion, policies designed to prevent smoking in public spaces or workplaces), quality of life, and economic outcomes could be explored more. Furthermore, future studies should also use a prospective study design whenever possible to establish a meaningful causal relationship between posttransplant smoking and its correlates and outcomes. Interventions could then be tailored to those at highest risk for smoking posttransplant. Third, given the paucity of data, more studies are needed on correlates and outcomes of posttransplant smoking in lung transplant patients. Fourth, although not the scope of the current review, it would also be helpful to evaluate possible additional risks of electronic cigarette smoking, secondhand smoking, and smokeless tobacco in the transplant population. And fifth, future studies should examine whether smoking withdrawal or cessation after solid organ transplantation has a protective effect against the development of cardiovascular disease.
In conclusion, posttransplant smoking is associated with cardiovascular disease, nonskin malignancies, a shorter patient survival time, and mortality. The association of posttransplant smoking with other outcomes (clinical, economic, and quality of life outcomes) remains to be evaluated. Male patients, younger patients, and patients with a lower BMI are more likely to be smokers. Transplant teams play an important role in routinely assessing patients' smoking status during transplant follow-up by using self-report and/or cotinine measurements, assessing patients' motivation to quit smoking, promoting smoking cessation, and referring motivated patients to community smoking cessation services when necessary.
B-SERIOUS consortium (in alphabetical order): Berben Lut, MSN, PhD, Institute of Nursing Science, University of Basel, Switzerland; Binet Isabelle, MD, Nephrology and Transplantation Medicine, Cantonal Hospital St. Gallen, Switzerland; Burkhalter Hanna, RN, PhD, Centre of Sleep Medicine, Hirslanden Group Zürich, Switzerland; De Geest Sabina, PhD, RN, Institute of Nursing Science, University of Basel, Switzerland & Academic Centre for Nursing and Midwifery, KU Leuven–University of Leuven, Belgium; De Simone Paolo, MD, PhD, Hepatobiliary surgery and liver Transplantation, University of Pisa Medical School Hospital, Italy; Denhaerynck Kris, PhD, RN, Institute of Nursing Science, University of Basel, Switzerland; Dobbels Fabienne, MSc, PhD, Academic Centre for Nursing and Midwifery, KU Leuven–University of Leuven, Belgium & Institute of Nursing Science, University of Basel, Switzerland; Drent Gerda, RN, PhD, Department of Gastroenterology and Hepatology, University Medical Center Groningen, Groningen, the Netherlands; Duerinckx Nathalie, MSN, Academic Centre for Nursing and Midwifery, KU Leuven–University of Leuven, Belgium & Heart Transplantation Program, University Hospitals Leuven, Belgium; Engberg Sandra J., RN, PhD, School of Nursing, University of Pittsburgh, United States; Glass Tracy, PhD, Department of Biostatistics, Swiss Tropical and Public Health Institute, University of Basel, Switzerland; Gordon Elisa, MPH, PhD, Center for Healthcare Studies and Comprehensive Transplant Center, Northwestern University Feinberg School of Medicine, Chicago, United States; Kirsch Monika, RN, PhD, Department of Anesthesiology, University Hospital of Basel, Switzerland; Klem Mary Lou, MLIS, PhD, Health Sciences Library System, University of Pittsburgh, United States; Kugler Christiane, RN, PhD, Nursing Science, University of Witten/Herdecke, Germany; Lerret Stacee, RN, PhD, Department of Pediatric Gastroenterology and Transplant Surgery, Medical College of Wisconsin, United States; Rossmeissl Anja, MD, Department of Sports, Exercise and Health, University of Basel, Switzerland; Russell Cynthia, RN, PhD, School of Nursing and Health Studies, University of Missouri-Kansas City, United States; Schmidt-Trucksäss Arno, MD, PhD, Department of Sports, Exercise and Health, University of Basel, Switzerland; Scalso de Almeida Samira, MSN, Transplantation program, Hospital Israelita Albert Einstein, Sao Paulo, Brazil; Sereika Susan M., MPH, PhD, School of Nursing, University of Pittsburgh, United States.
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