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© 2003 American Society for Clinical Oncology Brief Physician-Initiated Quit-Smoking Strategies for Clinical Oncology Settings: A Trial Coordinated by the Eastern Cooperative Oncology GroupFrom the Fox Chase Cancer Center, Philadelphia, PA; Dana-Farber Cancer Institute, Boston, MA; Duluth Clinic, Duluth, MN; Park Nicollet Health Services, St. Louis Park, MN; and AMC Research Center, Denver, CO. Address reprint requests to Robert A. Schnoll, PhD, Psychosocial and Behavioral Medicine Program, Fox Chase Cancer Center, 510 Township Line Rd, Cheltenham, PA 19012; email: RA_Schnoll{at}fccc.edu.
Purpose: Although tobacco use by cancer patients increases the risk of relapse, diminishes treatment efficacy, and worsens quality of life, about one third of patients who smoked before their diagnosis continue to smoke. Because patients have regular contact with oncologists, the efficacy of a physician-based smoking cessation treatment was evaluated. Methods:Cancer patients (n = 432) were randomly assigned to either usual care or a National Institutes of Health (NIH) physician-based smoking intervention. The primary outcome was 7-day point prevalence abstinence at 6 and 12 months after study entry. Results: At the 6-month follow-up, there was no significant difference in quit rates between the usual care (11.9%) and intervention (14.4%) groups, and there was no significant difference between the usual care (13.6%) and intervention (13.3%) groups at the 12-month follow-up. Patients were more likely to have quit smoking at 6 months if they had head and neck or lung cancer, began smoking after the age of 16, reported at baseline using a cessation self-help guide or treatment in the last 6 months, and showed greater baseline desire to quit. Patients were more likely to have quit smoking at 12 months if they smoked 15 or fewer cigarettes per day, had head and neck or lung cancer, tried a group cessation program, and showed greater baseline desire to quit. Finally, there was greater adherence among physicians to the NIH model for physician smoking treatment for patients in the intervention versus the usual care group. Conclusion: While training physicians to provide smoking cessation treatment to cancer patients can enhance physician adherence to clinical practice guidelines, physician smoking cessation interventions fail to yield significant gains in long-term quit rates among cancer patients.
THE RANGE of adverse health consequences of tobacco use are well documented and widely acknowledged. However, there is generally less awareness of the important ways that continued tobacco use by cancer patients can further compromise the patients health. Studies with cancer patients show that continued smoking after diagnosis and treatment reduces survival time,13 increases the risk of a recurrence or a second primary tumor,46 reduces treatment efficacy,7 and exacerbates and prolongs treatment-induced complications such as mucositis, dry mouth, loss of taste and voice, impaired pulmonary function and wound healing, and tissue and bone necrosis.812 Despite the significant increase in risk for these negative health effects, upwards of one quarter to one third of cancer patients who smoked before their diagnosis continue to do so after diagnosis.1319 Such findings lend strong support for the need to integrate formal smoking cessation clinical services within Comprehensive Cancer Centers. Over the last 20 years, there has been a steady accumulation of research on the efficacy of smoking cessation interventions provided in a medical context.20,21 One treatment approach that has received a sizable amount of research attention is physician-based intervention.22 This approach, whereby the physician is trained to deliver cessation advice and assistance, yields abstinence rates of 10% to 11%.2224 The effectiveness of this intervention approach may be attributable to the fact that hospitalizations or visits to physicians represent a "window of opportunity" during which patients are particularly motivated to quit smoking and are especially receptive to smoking cessation treatments.20,21,25 Indeed, patients highly respect physicians opinions and recommendations, and they enter a medical encounter with a focus on their health and a readiness to engage in actions relevant to improving their well-being, such as quitting smoking.26 The growth of physician-based smoking interventions has been spurred by a number of additional factors as well, including the finding that more than 90% of smokers who are able to achieve abstinence have not used formal clinical programs to do so27 and the observation that this approach to treating nicotine addiction can reach a substantial number of smokers, because more than 80% of smokers visit a physician at least once each year.28 When considering the recent emphasis on assessing the effectiveness of smoking treatments in terms of their impact value (ie, the abstinence rate yielded by the intervention multiplied by the participation rate),29,30 physician-based smoking interventions represent a relatively potent way to address the epidemic of tobacco use in the United States. In light of accumulated data supporting the effectiveness of physician-based smoking interventions, public health agencies have urged physicians to implement smoking interventions by providing treatment guidelines and training manuals.31 One model for physician-based smoking treatments, referred to as the "5 As," was devised by the Agency for Healthcare Research and Quality:32 Ask (screen for tobacco use), Advise (provide a personalized and strong quit message), Assess (evaluate the smokers readiness to quit), Assist (provide cessation counseling, pharmacotherapy, and self-help guides), and Arrange (appraise cessation progress). Because use of this model can yield a 10% to 11% quit rate and upwards of 80% of smokers could be reached by this treatment approach, physician-based smoking treatments have the potential to yield sizable reductions in the overall population rate of tobacco use. To date, however, the potential effectiveness of this model for reducing continued tobacco use by cancer patients has yet to be explored. A review of the literature33 uncovered only five studies of smoking treatments with cancer patients.3438 Further, the studies that have been conducted have used small samples and/or have failed to maintain sufficient internal validity.33 As such, despite the need to provide cancer patients with formal cessation assistance,39 cancer patients who smoke remain a group of smokers for whom smoking interventions have yet to be adequately evaluated. Thus, in this study, we examined the effectiveness of a 5 As, physician-based smoking cessation intervention for promoting long-term abstinence among cancer patients. We expected that patients who smoke and who are randomly chosen to receive a physician-based smoking intervention would show higher quit rates at 6-month and 12-month follow-up time points, versus patients who smoke who receive usual care. In addition, we explored whether sociodemographic (eg, age, sex), medical (eg, cancer site or stage), and behavioral (ie, desire to quit, expectations about quitting) factors, along with smoking history (eg, level of nicotine addiction, number of years smoked), predict long-term abstinence. With few exceptions,13,40 there has not been sufficient assessment of factors predictive of long-term tobacco use among cancer patients, although such analyses can provide important information for the design of smoking cessation interventions with this population.33 Finally, we explored the degree to which the physician-based intervention enhanced physician adherence to the 5 As model (eg, improved the rate at which physicians assessed smoking behavior) to provide a possible explanation for an effect of the physician-based intervention on patient quit rates.
Participants This study was originally conducted by Fox Chase Cancer Center (Philadelphia, PA) outside a cooperative. From December 1990 to May 1991, institutions that were members of the Eastern Cooperative Oncology Group (ECOG), the Southwestern Oncology Group, and the Cancer and Leukemia Group B participated in the study (see Table 1
Procedure Participating physicians at the recruitment sites identified potentially eligible patients, using standard intake evaluation forms. Eligible patients had the study objectives explained to them, and they were presented with an informed consent form. Consenting patients then completed a baseline assessment, which included an evaluation of their smoking history and certain behavioral factors that are strongly related to the ability to quit smoking (eg, desire to quit). Sociodemographic and medical data were recorded from medical charts or self-report. Random assignment to the usual care condition or the physician-based intervention was conducted using permuted blocks with dynamic balancing within the recruitment sites. Patients randomly assigned to the usual care arm (n = 218) received standard care after recruitment. Because physicians, from an ethical standpoint, could not withhold quit advice and prevent the patient from seeking cessation treatment outside the study, patients in the usual care arm might have been provided with physician quit advice and/or may have sought assistance with quitting. At the end of the study, patients in this arm who were smoking were instructed to call 1800-4-CANCER for assistance and/or referral to a cessation program. Patients randomly assigned to the physician-based intervention (n = 217) received quit advice and assistance during a physician visit in accordance with the National Institutes of Health guidelines for physician-based smoking interventions;31 all patients, regardless of the site of their tumor, received the same intervention. For the intervention, the physician provided brief (< 5 minutes) quit advice, which emphasized the overall benefits of quitting (eg, improved general health) and the specific health benefits for cancer patients (eg, lower chance for recurrence); tried to convince the patient to set a quit date and worked with the patient to identify the quit date; discussed nicotine replacement therapy (NRT) with the patient and provided a prescription if indicated (ie, for patients who exhibited high nicotine dependence); provided the patient with a self-help smoking cessation guide (ie, Freedom from Smoking for You and Your Family)41 and the 1800-4-CANCER telephone number for additional assistance and/or referral to a cessation program; and assessed cessation progress during subsequent medical visits. ECOG-trained data coordinators assisted physicians with standardizing intervention components at each site. All patients were contacted by telephone to complete a 6-month and a 12-month assessment, which contained the same information as the baseline assessment and questions (at the 6-month assessment only) to assess physician adherence to the smoking cessation treatment model (eg, whether or not the physician discussed the patients smoking habits).
Measures Medical data. Data on the patients diagnosis and health were collected from the medical chart or from the patient. These included cancer site, time since diagnosis (ie, the duration from diagnosis to baseline assessment), cancer stage, ECOG performance status, and physical symptoms (eg, trouble breathing, pain or tightness in chest) and diseases or conditions (ie, diabetes, high blood pressure, heart trouble/attack, emphysema, chronic bronchitis, or asthma). Smoking history. Participants indicated age of smoking initiation; average number of cigarettes smoked per day in the past 7 days; how soon they smoke after they wake (to assess level of nicotine addiction); whether others in the household smoke; number of lifetime 24-hour quit attempts; whether or not they had tried to quit in the past year; whether they had been advised to quit by a health care worker; whether they had ever tried individual counseling, group counseling, or NRT to quit smoking; whether, in the past 6 months, they had tried to reduce the amount they smoked, tried to quit, or used a quit-smoking guide; whether they used other forms of tobacco besides cigarettes (eg, cigars); and whether they are seriously contemplating quitting smoking in the next 6 months. Behavioral data. Two attitudinal variables were assessed as potential predictors of quitting, because in previous studies these have been linked to the ability to quit smoking.40 First, using six Likert-type questions, which ranged from 0 (not at all) to 4 (very much), desire to quit smoking was assessed (eg, "How much, if at all, do you want to quit smoking?"). Second, using six Likert-type questions, ranging from 0 (not at all) to 4 (very much), negative expectations about quitting were assessed (eg, "How much of a problem do you think being irritable, angry, or tense might be for you when you quit smoking?"). For each of these, a sum score was formed and used as a predictor variable in the analyses; higher scores on each composite variable represent, respectively, greater desire to quit or greater negative expectations about quitting. Smoking status. This variable, which served as the primary outcome measure, was assessed using 7-day point prevalence abstinence, as has been done in previous studies.14 The patient was considered abstinent if he or she reported not smoking for at least 1 week before the interview (ie, 7-day point prevalence abstinence). This measure of smoking status is as reliable and valid as other common measures of smoking status, such as 24-hour point prevalence, 30-day prolonged abstinence, and 6-month prolonged abstinence.42 All nondeceased nonrespondents were considered to be smokers at the follow-up assessments. Physician adherence to the 5 As model. At the 6-month follow-up, patients reported physician adherence to the physician-based smoking cessation clinical guidelines (ie, the 5 As). A yes or no format was used to assess whether physicians discussed smoking with the patient, suggested that the patient quit smoking, reviewed with the patient the benefits of quitting, helped the patient to set a quit date, sent a follow-up letter about the patients quitting plans, provided the patient with quit-smoking materials, and provided a prescription for NRT.
Statistical Analyses
Second, a Bayesian model was used to assess baseline predictors of long-term abstinence at the follow-up, including all participants regardless of missing data in the covariates. A Bayesian approach was used because this would allow for including all the subjects in the model, even those that have missing data in the covariates. There was a fairly high level of missing data (see Table 2
Finally, to explore the degree to which the intervention affected physician adherence to the 5 As model, we calculated the proportions across the study arms of patients who indicated that the physician assisted them with quitting smoking. Because this aim was primarily exploratory in nature, we restrict these analyses to descriptive analysis.
Descriptive sociodemographic, medical, and smoking history data for the sample are shown in Tables 2
The Effect of Physician-Based Smoking Intervention on Long-Term Quit Rates
The quit rates at 12 months are shown in the bottom of Table 4 Finally, there were no significant differences in quit rates at 6 months and at 12 months when the results were stratified by sex. At 6 months, the quit rates for males were 12.5% in the usual care arm and 15.0% in the physician-based intervention arm (P = .34); at 12 months, the quit rates for males were 13.6% in the usual care arm and 14.8% in the physician-based intervention arm (P = .46). For females, the 6-month quit rates were 11.0% in the usual care arm and 13.1% in the physician-based intervention arm (P = .45); the 12-month quit rates were 13.6% in the usual care arm and 9.8% in the physician-based intervention arm (P = .34).
Examination of Predictors of Long-Term Smoking Cessation
Table 5
The Bayesian multiple regression model of 12-month quitting is shown in Table 5
Physician Adherence to Smoking Cessation Treatment Guidelines
When taken together, our analyses yield several important findings. First, contrary to our hypothesis, we did not find that the provision of a physician-based smoking intervention increased long-term quit rates among cancer patients. This finding is consistent with a study by Gritz et al,36 which reported no significant difference in the rates of quitting between patients provided with a physician-based cessation treatment and patients randomly assigned to a control comparison group. However, our finding contradicts the general literature concerning the effect of physician-based smoking interventions, which indicates that brief physician-based interventions yield upwards of a 10% to 11% increase in quit rates (versus usual care).22
There are several possible explanations for our null finding. First, our finding may be the result of methodological confounding that was caused by the inability to use a "true" control group for this study (ie, an arm that received no active treatment). Although our findings indicated greater adherence to the 5 As model among the physicians in the intervention condition (Table 6 A second possible explanation for our null finding is that the brief, relatively low-intensity, physician-based intervention evaluated here was not sufficient to increase long-term quit rates among cancer patients, who may be considered "hard-core" smokers because they continue to smoke despite their diagnosis. The relatively low overall rate of long-term quitting across both conditions (13.2% and 13.4% at the 6-month and 12-month follow-ups, respectively), when compared with previous intervention studies with cancer patients, lends support for this explanation. For example, in a study that evaluated the benefits of a nurse-managed, 5 As modelbased smoking intervention for lung cancer patients, Browning et al34 found that 10 of 14 (71%) patients in the intervention condition were abstinent at a 6-month follow-up, versus six of 11 (55%) patients in the usual care group. Compared with the quit advice and self-help literature provided in the usual care condition, the intervention condition in the study by Browning et al34 consisted of eight structured clinical sessions involving quit advice, guidance in the establishment of a quit date, teaching of behavioral and cognitive strategies to manage stress, provision of support and encouragement, use of self-help guides, recommendation to use NRT and bupropion, and follow-up telephone booster contacts. That the regression models in the present study found that patients who used more-intensive forms of smoking treatment (ie, group counseling, NRT) were more likely to have quit smoking in the long term supports this explanation as well. Thus, future studies in this area may need to assess higher-intensity interventions (ie, physician-based intervention plus adjunctive behavioral and pharmacologic treatment), with the understanding that the brief, low-impact, physician-based intervention that may be sufficient for initiating quitting among healthy smokers (even in a medical context) is not adequate for smokers diagnosed with cancer. A third possible explanation for a lack of statistical impact of the intervention relates to the inclusion of patients whose primary cancer was not linked to tobacco use (eg, breast or testicular cancer, lymphoma), because the intervention, in large part, relies on the high level of quit motivation among the individuals diagnosed with a tobacco-related illness. The inclusion of such patients, who may have lower levels of desire to quit because they do not necessarily perceive their current health problem as linked to their tobacco use, may have contributed to the low cessation rates across the two conditions and created a scenario from the beginning of the study that was to make a treatment effect unlikely. Supporting this explanation is the higher cessation rate demonstrated in prior smoking intervention studies that used either head and neck or lung cancer patients.34,36,37 In addition, the present analyses found that cancer site was a strong predictor of long-term quit rates, with patients who have head and neck or lung tumors (whose etiology is strongly linked to tobacco use) exhibiting significantly higher quit rates than patients diagnosed with other forms of cancer. Thus, it may be the case that physician-based interventions such as the one tested here are effective only with patients manifesting a tobacco-related illness. A final possible explanation for the null findings concerns the outcome measure selected. In this study, we did not assess immediate quit rates after cessation advice but, rather, focused on long-term abstinence. It may be that the physician intervention yielded a significant increase in initial quitting after the provision of cessation advice but was not effective at promoting long-term maintenance of abstinence. (However, we did not assess immediate quit rates after quit advice.) This distinction between initial quitting and long-term abstinence is important to consider, because if a physician-based treatment can motivate initial cessation but fail to promote long-term abstinence, low-cost relapse prevention techniques, rather than incorporating more intensive interventions at the outset, may be a useful adjunct to a physicians quit advice. A second important finding from this study concerns the results from the prediction models of long-term quitting. These models identified several medical, smoking, and behavioral factors (assessed at baseline) that are linked to the patients ability to quit smoking in the long term. As mentioned, the tumor site has an effect on the likelihood of quitting; patients diagnosed with head and neck or lung cancer were substantially more likely to be abstinent at the 6-month and 12-month follow-up, versus patients with tumors at other sites. This finding may be attributable to the awareness among patients that the etiology of head and neck and lung tumors is strongly linked to tobacco use. This recognition, in turn, may spark greater quit motivation. Indeed, a study with head and neck cancer patients found that attributing the cause of the disease to tobacco use predicted the ability to quit smoking after diagnosis.44 Alternatively, smoking rates may be lower among head and neck cancer patients because of the greater likelihood of physical disability from treatments for this cancer type, which makes it impossible to smoke. Regardless, to boost quit motivation and eventual cessation, more-intensive interventions may need to be targeted toward patients with tumors that are not traditionally linked with tobacco use. In addition, interventions may need to be targeted to patients with a longer time since diagnosis, because these patients were less likely to have been abstinent at the 12-month follow-up, as reported previously.38,40 After the diagnosis, risk of smoking may increase over time because, initially, debilitating medical treatments or symptoms make it impossible for patients to smoke. Alternatively, once sufficient time has elapsed, and treatments have been completed, patients may minimize the seriousness of their diagnosis, and they might be, thus, less committed to maintaining abstinence from tobacco use. Finally, smoking rates may be lower at the outset as a result of a strong message from a physician requiring that the patient abstain from smoking during treatment, but as time elapses, the effect of this message fades. Regardless of the explanation, this finding highlights the need for relapse prevention for patients. Four variables, assessed at baseline, related to the patients smoking history predicted long-term quitting in the regression models. Patients who started smoking before the age of 16 (ie, smoked for a greater number of years) and patients who smoked 15 cigarettes per day or more (ie, heavier smokers) were less likely to quit at follow-up. The link between smoking duration and the amount smoked, on the one hand, and the ability to quit smoking, on the other hand, has been shown in large prospective studies with noncancer populations.45,46 In addition, patients who reported using a quit-smoking guide or treatment in the past 6 months or who tried a group cessation program were more likely to have quit smoking in the long term. This finding is also supported by literature that has demonstrated the benefits of such treatments.32,47 These results replicate those previously found concerning smoking history and the ability to quit, and they indicate that patients who start smoking at a younger age or patients that are heavy smokers require more intensive cessation treatments and that methods for promoting use of cessation interventions should be explored to increase the likelihood that patients will abstain from tobacco use in the long term. Finally, patients who showed a strong desire to quit smoking at baseline were more likely to be abstinent in the long term. Prospective studies show that the desire to quit smoking (often referred to as quit motivation, readiness to change, or stage of change) is a consistent predictor of smoking cessation.36,48 Further, treatment studies show that initial motivation to quit smoking predicts success in a smoking intervention.49 Quit motivation predicted a better outcome in treatment studies with cancer patients, as well.36,38 Such data sparked the development of behavior change theories, such as the Transtheoretical model,50 and clinical approaches, such as motivational interviewing.51 One important contribution of this research has been the matching of clinical techniques to the individuals level of quit motivation.52 For instance, although action-oriented techniques (eg, NRT, behavioral counseling) can promote quitting among those motivated to quit, such methods may be met with resistance by those with low quit motivation. Instead, unmotivated smokers require a unique set of techniques designed to boost motivation and prepare the person for engaging in action-oriented strategies.52 Thus, as seen in the general population of smokers, interventions for cancer patients who smoke may also need to be tailored to the persons level of readiness to quit to maximize the impact of treatment. A third important finding concerns the effect of the intervention on physician adherence to the 5 As model. Despite the potential benefits of physician-based smoking interventions, only 20% to 25% of U.S. smokers receive smoking cessation counseling from their physician.53 One explanation for the low rate of physician adherence to the 5 As model is the lack of training in smoking cessation counseling for physicians. Ferry et al54 surveyed 120 U.S. undergraduate medical programs and found that only 2.4% of those schools require students to complete a course in tobacco education. Because our study found that physicians in the intervention condition showed greater adherence to the 5 As model, providing physicians with basic training in conducting smoking interventions may improve physician practice. One caveat to highlight is sources of bias in patient recall of physician practices, which may yield unreliable measures of physician behavior. First, because these measures were taken 6 months after physician intervention, patients may have forgotten that physicians had provided such treatment, thereby artificially lowering the rate of adherence. Second, patients recall may have been influenced by whether they had made a quit attempt and failed; these patients may be reluctant to report physician attempts to encourage their cessation because they want to provide a rationale for their inability to maintain abstinence. Our findings should be viewed in the context of additional limitations. First, because the use of self-reporting, versus biochemical verification, to determine smoking status can be unreliable,55 a certain number of patients may have been incorrectly classified at the follow-ups. It is important to note that large studies have shown false reporting rates to be about 3% to 5%,56,57 which indicates that, if deception occurred in this study, the rate was small. Nevertheless, future studies that evaluate smoking interventions with cancer patients should use biochemical verification of smoking status. Second, the external validity of this study is limited by the samples lack of ethnic diversity. Even though patient ethnicity has not been found to be associated with the patients ability to quit smoking after diagnosis, future studies in this area should use samples that better approximate the ethnic distribution of U.S. cancer patients. Third, as mentioned, a "true" control group was not used. Thus, confounding the content of from exposure to smoking cessation treatment among patients in the usual care arm may have undermined the studys internal validity. Fourth, practical constraints required that patients be randomly assigned, rather than physicians. Thus, the same physicians implemented the usual care as well as the physician-based intervention. If this methodological approach affected the data, it would be expected to yield a type I error (ie, declaring the physician-based intervention to be effective when it is not), because physicians knowledge of which treatment condition the patients are in could influence their treatment approach in favor of the study hypothesis. With a null finding for treatment condition, this cannot be the case (indeed, only a type II error is plausible). Thus, although we acknowledge the methodological shortcoming of having the same physician provide both treatments, we do not believe that this would explain the null findings. Finally, the eligibility criteria used allowed recent quitters to be included in the study. This procedure can artificially increase quit rates. However, as a product of the random assignment procedures, the proportion of these individuals in each condition could be reasonably expected to be equivalent. With these limitations acknowledged, this study makes an important contribution to the literature on smoking treatments for cancer patients, because only one previous study36 tested a physician-based smoking cessation with cancer patients. As the recognition for the need to address tobacco use among cancer patients grows, studies such as this can help guide the implementation of clinical initiatives. It is important that this study suggests the need for more intensive smoking interventions for this population than basic physician-based treatments, as well as the need for the development of relapse prevention strategies. Although the provision of physician advice and basic assistance (eg, self-help guides, referral for NRT) should be seen as the standard of care (and likely to be effective in a primary care setting), a substantial proportion of cancer patients (especially those with non-tobacco-related neoplasms and those in latter stages of recovery) are likely to need more intensive cessation treatment, which could include the use of antidepressants and formal behavioral counseling tailored to the patients quit motivation,33 or long-term relapse prevention in the form of quit lines or support groups. The seamless integration of more intensive smoking interventions or relapse prevention approaches within the oncologic context represents an important priority for Comprehensive Cancer Centers and potentially a promising approach to assisting patients to achieve a better quality of life.
This ECOG-coordinated study (E1Y92; Robert L. Comis, MD) was supported by the National Cancer Institute, National Institutes of Health, Department of Health and Human Services grants CA23318, CA66636, CA21115, CA27525, and CA13650. Its contents are the authors responsibility and do not necessarily represent the views of the National Cancer Institute.
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