Content uploaded by Mary E Cooley
Author content
All content in this area was uploaded by Mary E Cooley on Feb 17, 2021
Content may be subject to copyright.
Smoking cessation is challenging even for patients recovering
from lung cancer surgery with curative intent
Mary E. Cooley, PhD, RN,
Dana Farber Cancer Institute, Phyllis F. Cantor Center, Research in Nursing and Patient Care
University of Massachusette-Boston College of Nursing and Health Sciences Boston, MA, USA
Linda Sarna, DNSc, RN, FAAN,
University of California, Los Angeles, School of Nursing, Los Angeles, CA, USA
Jenny Kotlerman, MS,
University of California, Los Angeles, David Geffen School of Medicine, Los Angeles, CA, USA
Jeanne M. Lukanich, MD,
Brigham and Women’s Hospital, Department of Thoracic Surgery, Boston, MA, USA
Michael Jaklitsch, MD,
Brigham and Women’s Hospital, Department of Thoracic Surgery Boston, MA, USA
Sarah B. Green, and
Dana Farber Cancer Institute, Phyllis F. Cantor Center, Research in Nursing and Patient Care
Boston, MA, USA
Raphael Bueno, MD
Brigham and Women’s Hospital, Department of Thoracic Surgery, Boston, MA, USA
Mary E. Cooley: mary_cooley@dfci.harvard.edu; Linda Sarna: lsarna@sonnet.ucla.edu; Jenny Kotlerman:
jkotlerman@mednet.ucla.edu; Jeanne M. Lukanich: jlukanich@partners.org; Michael Jaklitsch: Mjaklitsch@partners.org;
Raphael Bueno: rbueno@partners.org
Abstract
Background—Although it is recommended that smokers undergoing surgery for lung cancer
quit smoking to reduce post-operative complications, few studies have examined patterns of
smoking in the peri-operative period. The goals of this study were to determine: 1) patterns of
smoking during post-operative recovery, 2) types of cessation strategies used to quit smoking, and
3) factors related to smoking after lung cancer surgery.
Methods—Data were collected from 94 patients through chart review, tobacco, health-status, and
symptom questionnaires at 1, 2, and 4-months after surgery. Smoking status was assessed through
self-report and urinary cotinine measurement.
Results—Eighty-four patients (89%) were ever-smokers and 35 (37%) reported smoking at
diagnosis. Thirty-nine (46%) ever-smokers remained abstinent, 13 (16%) continued smoking at all
© 2009 Elsevier Ireland Ltd. All rights reserved.
Corresponding Author: Mary E Cooley, 44 Binney Street, CP 302, Boston, MA, 02115, Phone: 617-632-4653, Fax: 617-632-5636,
mary_cooley@dfci.harvard.edu.
Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our
customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of
the resulting proof before it is published in its final citable form. Please note that during the production process errors may be
discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Conflict of Interest Statement
:
All of the authors have no conflicts of interest to declare
NIH Public Access
Author Manuscript
Lung Cancer
. Author manuscript; available in PMC 2013 October 22.
Published in final edited form as:
Lung Cancer
. 2009 November ; 66(2): 218–225. doi:10.1016/j.lungcan.2009.01.021.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
time-points, and 32 (38%) relapsed. Ten (46%) of those who relapsed were former-smokers and
had not smoked for at least 1-year. Sixteen (46%) of those who were smoking at diagnosis
received cessation assistance with pharmacotherapy being the most common strategy. Factors
associated with smoking during recovery were younger age and quitting smoking ≤ six-months
before the diagnosis of lung cancer. Factors that were marginally significant were lower
educational level, male gender, lower number of comorbidities, and the presence of pain
Conclusion—Only half of those who were smoking received assistance to quit prior to surgery.
Some patients were unable to quit and relapse rates post-surgery were high even among those who
quit more than 1-year prior. Innovative programs incorporating symptom management and relapse
prevention may enhance smoking abstinence during post-operative care.
Keywords
lung cancer; thoracic surgery; smoking cessation; symptom management
INTRODUCTION
Evidence suggests that smoking cessation is associated with a better perceived health status,
improved survival and decreased cancer recurrence among patients with early stage non-
small cell lung cancer (NSCLC)1–3. Therefore, patients with potentially curative lung cancer
who are smoking at the time of diagnoses are advised to quit smoking pre-operatively in
order to reduce post-operative complications4–6.
Although several studies have examined smoking behaviors in patients with varied stages of
lung and head and neck cancer7–9, only two studies have examined smoking behaviors after
surgical treatment for early stage lung cancer10, 11. Gritz and colleagues followed 840
patients who underwent surgical resection for NSCLC for four-years and examined their
smoking patterns. Sixty-percent of the patients reported smoking at the time of diagnosis. It
took two-years for smoking cessation rates to stabilize after surgery. By then, approximately
40% of the patients who smoked at diagnosis quit smoking. Dresler and colleagues11
followed 363 patients undergoing surgery for NSCLC to determine the patterns of smoking
before and after surgery. Ninety-five percent of patients had a smoking history. Nineteen
percent of patients reported smoking up until their surgery, 12% quit 2-weeks prior to
surgery, 15% quit between 2-weeks and 3-months prior to surgery, 6% quit between 3-
months and I-year prior to surgery, 42% quit smoking at least 1-year prior to surgery, and
the smoking status of 6% were unknown. Only 13% of smokers reported smoking within 1
year post-operatively.
A number of investigators have examined factors associated with smoking relapse among
patients receiving surgery for NSCLC12, 13. Walker and colleagues12 followed patients with
NSCLC who were smoking within 3-months of their surgery for 12-months after surgery to
assess smoking status and predictors of smoking relapse. At some point after surgery, 43%
of patients smoked; at 12- months after surgery, 37% were smoking. Sixty-percent of
patients who relapsed did so within 2-months after surgery. Smoking at follow-up was
associated with shorter quit duration before surgery, more intense cravings, lower income,
and higher education. Among those who relapsed, greater delay before the relapse was
associated with abstinence at 12-months. In a smaller study, Walker et al13 found that
younger age and lower education were associated with smoking and shorter time to smoking
relapse. Dresler and colleagues11 noted that shorter quit duration before surgery was
associated with continued smoking and return to smoking after surgery. Of the 13% who
smoked after their surgery, the majority (61%) had never stopped smoking pre-operatively,
only 3% of patients who quit smoking > 3-months before surgery returned to smoking.
Cooley et al. Page 2
Lung Cancer
. Author manuscript; available in PMC 2013 October 22.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
Little information is available about smoking cessation strategies used by patients
undergoing lung cancer surgery. Dresler and colleagues noted that only 59% of smokers
reported that a physician told them to quit smoking pre-operatively11. However, 89% of
patients who continued smoking post-operatively reported physician advice to quit
smoking11. Recommended evidence-based methods for cessation include the use of
pharmacotherapy (nicotine replacement medications, buproprion, or varenicline) and
behavioral counseling14. Although counseling and medication are effective when used by
themselves for treating tobacco dependence, the combination of counseling and medication
is more effective than either alone and is the recommended standard by the Public Health
Service Tobacco Dependence Treatment Guideline15. Several studies have demonstrated
that the majority of smokers attempt to quit “cold turkey”, which is abruptly, on their own
and without the use of proven cessation aides16, 17. It is important to recognize that the use
of proven cessation aides doubles the rate of success in maintaining smoking abstinence15.
In summary, the data that describe smoking behaviors and factors related to smoking after
surgery for lung cancer, or cessation strategies used prior to surgery are limited and
incomplete. This type of information is crucial to provide the basis for future development
and testing of effective smoking cessation interventions. Our study extends previous studies
by focusing specifically on patients recovering from curative surgery for lung cancer.
Sanderson-Cox and colleagues18 note that the majority of studies examining smoking
behavior in cancer patients have been conducted in heterogeneous groups of patients and
that further research is needed to clarify to what degree smoking behavior may be related to
a specific type of cancer, stage of disease and type of treatment. In addition, this study adds
several unique variables such as the number of comorbidities and post-operative symptoms
within the context of surgical recovery that haven’t been examined in previous studies as
factors that may influence smoking relapse. The presence of these variables may influence
cessation either positively or negatively. The purposes of our study are to determine: 1)
patterns of smoking during post-operative recovery, 2) types of cessation strategies used to
quit smoking, and 3) factors (demographic, tobacco-related, health status and post-operative
symptoms) related to smoking after lung cancer surgery.
METHODS
Ninety-seven patients were recruited and gave written consent to participate in this
Institutional Review Board-approved prospective clinical study. Entry criteria included:
patients with stage I, II, IIIA NSCLC who underwent potentially curative surgical treatment,
were ≥18 years of age, and able to read and understand English. Three patients were
excluded from analysis because they did not meet study criteria. Ninety-four patients
provided data at entry to the study (1-month after surgery); 92 at 2-months after surgery; and
86 at 4-months after surgery.
This study was part of a larger multi-site study that described symptom patterns during
recovery from lung cancer surgery, which was an exploratory study conducted between
2002 and 2006 targeted to recruit 90 patients.19 A convenience sample was obtained from
four data collection sites located in the western (University of California, Los Angeles),
eastern (Dana-Farber/Brigham and Women’s Cancer Center and University at Buffalo, State
University of New York), and southern US (Medical College of Georgia). Potential
participants were recruited through letters sent from physicians and advertising through
brochures and flyers. Because of restrictions imposed by the Institutional Review Board,
patients were required to approach us; therefore, we cannot determine the exact number of
participants who met the inclusion criteria and who were not interested in participating at
each site. Participants were given a small stipend ($25.00) for their time and efforts after
each interview.
Cooley et al. Page 3
Lung Cancer
. Author manuscript; available in PMC 2013 October 22.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
DATA COLLECTION
Demographic information was collected at baseline using a self-report questionnaire and
included: age, gender, marital status, race, living situation, and level of education.
Tobacco variables—Tobacco use questions were based on items from the Behavioral
Risk Factor Survey15, 20 and the Fagerstrom Test for Nicotine Dependence.21 These items
included: age at initiation, number of years smoked, methods used for cessation, level of
nicotine dependence, smoking status of household members, and exposure to environmental
tobacco smoke (ETS). Methods used for cessation were defined as counseling, information,
nicotine replacement, or other medication used for smoking cessation (i.e. bupropion,
varenicline). Participants could select more than one method used for cessation. Time to
smoke the first cigarette in the morning, an item on the Fagerstrom Test for Nicotine
Dependence, was used as a measure of nicotine dependence in this study. High levels of
nicotine dependence were defined as smoking the first cigarette in the morning within 30
minutes of awakening. This question has been found to be the best single item predictor of
nicotine dependence22.
Smoking status—Smoking status was determined through self-report and biochemical
verification with urinary cotinine (Nic-alert, Jant Corporation). Current smokers were
defined as patients who responded “yes” to smoking now or responded “no” to smoking
now but had a urine positive for a cotinine level of ≥ 3 on the dipstick23. If patients
responded, “no” to smoking now and reported current use of nicotine replacement
medications, they were classified as non-smokers. Smoking status was classified as current
(at the time of the first interview), recent-quitter (quit < 1 year prior to diagnosis), former-
quitter (quit ≥ 1 year prior to diagnosis), and never-smoker. Smoking status among the ever
smokers was re-assessed at each subsequent time point as smoking or not smoking. Smoking
status was assessed at 1, 2 and 4 months after surgery, this time period is consistent with
recommendations from the Society for Research in Nicotine and Tobacco for short-term
follow-up (≤ 3 months) of smoking abstinence24, 25. The primary goal of this study was to
understand smoking behaviors and factors associated with return to smoking after surgery
for lung cancer in order to develop effective smoking cessation interventions in the future.
Therefore, short-term follow-up of smoking status was the most appropriate outcome
measure for use in this study. Longer-term follow-up such as 6 or 12 months is
recommended as abstinence measures for smoking cessation intervention clinical trials24.
Health status—The health status variables included comorbidities measured with the
Charlson Comorbidity Index self-report26. This instrument has been previously validated as
reliable in lung cancer patients27.
Post-operative symptoms—The post-operative symptoms including pain, dyspnea,
fatigue, and depressed mood were assessed at each time period.
Post-operative pain was measured with the Brief Pain Inventory (BPI) short-form, which is a
9-item self-report questionnaire. It has been used extensively in patients with cancer28. Two
single items (pain presence and worst pain) and the two subscales (pain severity and
interference with activities “during the last 24 hours”) were used in this analysis.
Post-operative dyspnea was measured with the American Thoracic Society Dyspnea
Index29. This is a five-item self-report questionnaire that describes breathlessness according
to level of activity. Higher scores indicate more severe respiratory problems.
Cooley et al. Page 4
Lung Cancer
. Author manuscript; available in PMC 2013 October 22.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
Post-operative fatigue was measured by the Schwartz Cancer Fatigue Scale30, 31, a
previously validated, six-item self-report questionnaire.
Depressed mood was measured by the Center for Epidemiological Studies— Depression
scale32. This 20-item self-report questionnaire, with a score of >15 representing depressed
mood, has been used extensively in adults with cancer.
Clinical variables were collected through a medical chart review and included histology,
stage of cancer, type of resection, and receipt of adjuvant therapy. The American Joint
Committee on Cancer Staging Manual was used to classify stage33.
DATA ANALYSIS
Data analyses were performed using SAS 9.1.3. Distributions of certain characteristics are
presented using frequencies and percents or means with standard deviations. Univariate
logistic regressions were used to calculate the odds-ratios for predictors of smoking at any
time after lung cancer surgery among participants who ever smoked prior to surgery. A
stepwise multiple logistic regression model was used to identify which covariates remained
significant when considered in combination.
RESULTS
Patient Cohort
As displayed in Table-1, the mean age of the patients was 63 years (s.d 9.9). Most were
white, female, married and had a high school education or higher. The majority had Stage I
or II adenocarcinoma and underwent a lobectomy.
Patterns of smoking during surgical recovery
Thirty-five patients (35/94) were smokers at the diagnosis of lung cancer making the
frequency of smoking prevalence 37%. Eighty-four patients (89%) were ever-smokers and
10 (11%) were never-smokers. As Table-2 shows, among ever-smokers, most (n=47/84,
56%) had quit smoking prior to their diagnosis, 21/84 (25%) patients reported that they quit
after their diagnosis, and 11/84 (13%) reported that they were smoking at 1-month after their
surgery. However, 5 additional (total n=16/84; 19%) patients were identified as smokers at 1
month after surgery based on positive urine cotinine analysis. In addition, after they were
diagnosed with lung cancer 18/69 (26%) patients had household members who continued to
smoke. Forty-six/ninety-three (49%) patients reported exposure to environmental tobacco
smoke (ETS) less than once a week, 14/93 (15%) reported exposure to ETS several times a
week and 33/93 (36%) reported exposure to ETS everyday.
The mean time interval between quitting and cancer diagnosis was 8 years (sd 12). Smokers
who continued smoking post-operatively were highly nicotine-dependent as 9/11 (86%)
current-smokers reported smoking within 30 minutes of waking up in the morning (Table 2).
Of the 84 ever-smokers, only 46% (39/84) did not smoke at all throughout the study.
Patterns of smoking showed that by 1-month after surgery, 18% (16/84) of ever-smokers
had relapsed back to smoking, by two-months after surgery, 33.3% (28/84) relapsed back to
smoking and at 4-months 42% (34/84) had relapsed back to smoking (see Figure 1).
We also examined patterns of smoking for those who had quit before their diagnosis and
those who were smoking at their diagnosis (see Figures 2 and 3). The majority of ever-
smokers (n= 49/84, 58%) had quit smoking prior to their diagnosis. However, ten of those
who quit smoking before their diagnosis (n=10/49, 20%) relapsed to smoking after their
Cooley et al. Page 5
Lung Cancer
. Author manuscript; available in PMC 2013 October 22.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
surgery (see Figure 2). Surprisingly, eight (n=8/10, 80%) of those who relapsed had quit ≥ 1
year prior to their diagnosis. In fact, their mean time since quitting was 8.5 (sd=6.5) years.
Thirty-five (n= 35/84, 42%) ever-smokers were smoking at the time of cancer diagnosis.
Although the majority of those who were smoking at diagnosis attempted to quit smoking,
only ten (n=10/35, 29%) smokers were able to maintain cessation throughout the study
(Figure 3). Some patients returned to smoking as early as 1-month after surgery, however,
most patients who ultimately returned to smoking did so within 2-months after their surgery.
A substantial portion of smokers (n=13/35, 37%) who were smoking at the time of diagnosis
continued to smoke at each time point throughout the study period.
Strategies used to assist in cessation
Among patients who were smoking at the time of their diagnosis, 16 (46%) received
assistance with cessation. Treatment with medication (nicotine replacement or bupropion)
was the most commonly used strategy (Table 4). Medications were given alone, in
combination with other tobacco dependence medications or in combination with smoking
cessation information. In this cohort, only 1 (6%) lung cancer patient received combined
treatment with counseling and pharmacotherapy.
Factors (demographic, tobacco-related, health status and post-operative symptoms)
correlated with smoking during surgical recovery
Potential factors related to smoking during surgical recovery were examined at entry to the
study using logistic regression (Table-4 and Table-5). Age, education, time since smoking
cessation and pain were significant in the univariate models. Younger patients were more
likely to be have smoked after surgery as compared with older patients, those with less than
a high school education were more likely to smoke after surgery as compared to those with a
high school or higher education, those who quit smoking within 6-months prior to diagnosis
were more likely to smoke after surgery as compared with those who had quit for a longer
period of time, and those who had significant pain were more likely to smoke after surgery
as compared to those who didn’t have pain. The presence of post-operative pain was
significantly correlated with smoking after surgery across three different variables. Patients
who reported the presence of pain, worse pain during the last 24 hours and increased
severity of pain were more likely to smoke after surgery compared to those without pain (see
Table-4).
Factors associated with smoking during recovery in a multiple logistic model were younger
age and quitting smoking less than six months before the diagnosis of lung cancer. Factors
that showed a trend toward significant difference were lower educational level, male gender,
lower number of comorbidities, and the presence of pain (see Table-5).
DISCUSSION
The most recent smoking prevalence rates among US adults showed a decline in smoking
from 24.7% in 1997 to 18.6% in early 200734. For both sexes combined, the percentage of
smoking adults was lower among those 65 years and over (7.5%) than among those in the
18–44 (20.6%) and 45–64 (20.9%) age groups. Our study provides current information
about smoking patterns after surgery for patients who underwent surgery for NSCLC. We
discovered that 37% of patients in this study were smoking at the time of their diagnosis. In
addition, 26% of household members continued to smoke after their family member was
diagnosed with lung cancer. Thus, the frequency of smoking prevalence for both patients
and their family members in our study were much higher than the general population even
when compared by age group. However, when compared with previous studies of patients
Cooley et al. Page 6
Lung Cancer
. Author manuscript; available in PMC 2013 October 22.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
with newly diagnosed surgical lung cancer, our study’s frequency of smoking prevalence are
lower than the 60% reported by Gritz and colleagues10 and higher than the 19% reported by
Dresler and colleagues11. Reasons for differences in frequency of smoking prevalence may
be related to a time lag between the various studies and use of different methodologies to
assess smoking status (i.e. self-report versus use of self-report and biochemical verification).
In this study, 51% of lung cancer patients were exposed to ETS after their surgery. Of these
patients, 15% were exposed to ETS several times a week while more than one-third (36%)
of patients were exposed to ETS every day. The frequency of ETS exposure in this patient
cohort (51%) is higher than other samples of early stage lung cancer patients reported in the
literature (28% and 45%)35, 36. Exposure to ETS in early stage NSCLC patients has been
associated with a threefold increase in respiratory symptoms and worse survival, especially
for ETS at work35, 36. Given the high rates of ETS exposure within this cohort, future
studies are needed which seek to understand the location and duration of exposure to ETS so
that interventions can be developed to decrease exposure.
Of the patients who were still smoking at the time of their diagnosis, 16 (46%) received
smoking cessation interventions consisting of counseling, information, and/or
pharmacotherapy. This finding is similar to that of Schnoll and colleagues who assessed the
smoking cessation interventions that cancer patients in a smoking cessation program used in
their previous quit attempts37. Many patients quit “cold turkey” and didn’t use any cessation
aides in their quit attempt. Similar to our study, Schnoll and colleagues found that a-third to
half of patients used proven cessation aides such as nicotine replacement or bupropion. An
additional finding from our study is that only one (6%) smoker received combined treatment
with counseling and medication, the recommended intervention for tobacco dependence
treatment. Thus, we find in our study that the vast majority of lung cancer patients did not
receive optimum treatment for nicotine dependence14.
The majority of smokers in our study made a quit attempt at the time of their diagnosis and
approximately 50% were able to quit and not return to smoking during the 4-months after
surgery. Twardella and colleagues38 examined the relationship between the diagnosis of a
smoking-related disease and smoking cessation among older adults (aged 50–74 years) in a
primary care setting and found that when individuals experience the personal health effects,
many permanently quit; in the year of the diagnosis of cancer, the rate of cessation increased
five-fold. It is important to recognize, however, that quitting smoking is a difficult process
for most smokers and often requires repeated attempts in order to be successful15. Smoking
relapse can occur even after a lengthy period of abstinence. In our study, ten out of forty-
nine (20%) former smokers who had quit ≥ 1-year prior to their diagnosis experienced
smoking relapse after their diagnosis. This finding is similar to that from a study by Krall et
al who examined rates of late smoking relapse among aging men who were followed in the
VA Normative Aging Study 39. Among this cohort, smokers who had been abstinent for
two-years were followed for twenty additional years. Approximately 20% relapsed after
two-years. Most of the smoking relapse was in years 3–10. After 10-years of abstinence,
however, smoking relapse rates were less than 1% per year. In another study, Gilpin and
colleagues estimated the probability of future smoking relapse for different durations of
abstinence at baseline but they weren’t able to find any one duration of abstinence after
which former smokers had no risk of smoking relapse40. However, if three-years was used
as a criterion, 97% of participants remained abstinent. Thus, even former-smokers require
ongoing support to maintain cessation.
Despite the diagnosis of lung cancer, a sizable proportion (n=13/35, 37%) of smokers
enrolled in our trial continued smoking at all time points. Emery and colleagues defined
individuals who are heavy smokers, have a weak quitting history and may never quit
Cooley et al. Page 7
Lung Cancer
. Author manuscript; available in PMC 2013 October 22.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
smoking as “hard core” smokers41. This subgroup of smokers requires innovative
approaches to enhance cessation. A growing body of evidence suggests that genetic factors
influence smoking initiation, progression to nicotine dependence and persistent smoking17.
Thus, a promising direction for future smoking cessation treatments is the use of
pharmacogenetic approaches to individualize treatments. Pharmacogenetics research can
potentially improve treatment by identifying genetic variants that are predictive of
therapeutic response. In turn, the selection of treatment can be optimized by matching
treatment modality to genetic profile42. Further study is needed to determine if people with
tobacco-related cancers have these genetic variants.
We also found that a shorter time since quit appeared to be a risk factor for smoking after
surgery. Similar to other studies, our study identified that shorter time since quit was
associated with smoking after surgery11, 13. Smokers who quit smoking ≤ six-months before
the diagnosis of lung cancer were nine-times more likely to return to smoking as compared
to those who quit smoking > then six-months before diagnosis. Given that most smokers
find it difficult to quit and remain abstinent, more innovative therapies may be needed to
address tobacco dependence, especially in patients with lung cancer who are often highly
dependent smokers. Steinberg and colleagues43 have recently suggested that tobacco
dependence should be treated as a chronic disease. The optimal duration of therapy is not
known and some smokers may require extended therapy given as long as is necessary to
enhance successful outcomes43.
Male gender, lower educational level, lower number of comorbidities and presence of pain
were marginally associated with smoking during recovery. Gritz and colleagues also found
that women were more likely to quit smoking and stay quit after lung cancer surgery44.
Studies that have examined gender differences in the general population have had mixed
results45–47. Some studies have shown that women have a more difficult time quitting
smoking, whereas other have found no differences exist. Few studies have examined gender
differences in smoking cessation among medically ill populations. It is not clear whether
there is an interaction between gender, illness, and smoking cessation. Further studies are
needed to clarify whether gender differences in smoking cessation exist among those with
medical conditions.
Lower education was associated with return to smoking after surgery. This finding is similar
to other studies in the general population that have found education to be one of the most
potent sociodemographic predictors of cessation. Less educated persons have higher
smoking prevalence rates and lower rates for cessation. Although it is not clear how or why
educational level influences smoking cessation outcomes48, 49 contextual factors such as
having a greater prevalence and acceptance of smoking as a social norm among those who
are less educated may influence the dynamics of smoking50.
A lower number of comorbidities were marginally associated with smoking during recovery.
This finding suggests that healthier smokers may not be compelled to quit in the same way
that those smokers who are symptomatic. Thus, they may have a more difficult time quitting
and staying quit. Further studies to replicate this finding are needed since even smoking
cessation at the time of diagnosis is associated with improved clinical outcomes.
The presence of significant pain was marginally associated with smoking during recovery.
To our knowledge, no other studies have reported the relationship between post-operative
pain and smoking after surgery. Another study examined changes in symptom burden in
smokers with AIDS/HIV who enrolled in a smoking trial51. Results from Vidrine et al’s
study identified that increased days of smoking abstinence were associated with a decrease
Cooley et al. Page 8
Lung Cancer
. Author manuscript; available in PMC 2013 October 22.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
in HIV-related symptom burden; this finding underscores the importance of maintaining
smoking abstinence in a medically ill population51.
The findings from our study provide direction for future smoking cessation interventions.
Smoking relapse rates are high after lung cancer surgery even among those who quit ≥ 1-
year prior. Similar to Walker et al’s findings, our study found that most smokers had
relapsed by 2-months after their surgery12, 13. Smokers were highly dependent and many
didn’t receive optimal smoking cessation interventions. Although the diagnosis of lung
cancer provides a window of opportunity to promote cessation, many challenges exist for
patients and health care providers. First, patients undergoing lung cancer surgery have little
time to adequately prepare for their cessation attempt. In addition, the diagnosis of lung
cancer and subsequent treatment is often accompanied by cancer or treatment-related
symptoms. Moreover, patients may be reluctant to disclose their smoking behaviors because
of the stigma and embarrassment of continued smoking after a cancer diagnosis52. As a
result, clinicians may not be aware of relapse issues. Smoking cessation interventions need
to be tailored to this population. Ideally, smoking cessation interventions (medications and
behavioral counseling) should begin prior to surgery and continue for at least 2-months after
surgery. A longer duration of treatment may be needed, however, to enhance success rates43.
Given that former-smokers are at high risk for smoking relapse, they should be included in
smoking cessation interventions that incorporate the opportunity for repeat tobacco
dependence treatment if needed, adequate symptom management and smoking relapse
prevention53.
There were several limitations of the study that must be considered in interpreting the
findings, including the use of convenience sampling and the relatively small sample size.
This study did not include pre-operative data collection, a challenging time because of the
short window from diagnosis to surgery in many situations. Future studies are needed that
include a baseline assessment as well as a longer follow-up period to follow relapse. The
strengths of the study are that we used biochemical verification to confirm self-report
smoking status.
In summary, it is essential to promote smoking cessation both before and after lung cancer
surgery in order to improve clinical outcomes. Only half of smokers received an appropriate
smoking cessation intervention prior to surgery. Further study is needed to understand
patient interest in participating in smoking cessation interventions and what type of
programs they prefer so that programs can be tailored to meet their needs. Despite a
diagnosis of potentially curable lung cancer, some patients were unable to quit prior to
surgery and relapse rates post-surgery were high even among those who quit more than 1-
year prior. Innovative cessation programs incorporating symptom management and relapse
prevention are needed to enhance quitting prior to surgery and to maintain abstinence during
post-operative care.
Acknowledgments
Funding from the National Cancer Institute 1 K07 CA92696-02 and James B. Gillen Thoracic Oncology Research
Fund, Dana-Farber Cancer Institute (Mary E. Cooley) and Oncology Nursing Foundation Center for Leadership,
Information, and Research (#018652) (PI: Linda Sarna).
References
1. Sardari Nia P, Weyler J, Colpaert C, Vermeulen P, Van Marck E, Van Schil P. Prognostic value of
smoking status in operated non-small cell lung cancer. Lung Cancer. 2005; 47:351–357. [PubMed:
15713518]
Cooley et al. Page 9
Lung Cancer
. Author manuscript; available in PMC 2013 October 22.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
2. Davison G, Duffy M. Smoking habits of long-term survivors of surgery for lung cancer. Thorax.
1982; 37:331–333. [PubMed: 7112468]
3. Evangelista L, Sarna L, Brecht M, Padilla G, Chen J. Health perceptions and risk behaviors of lung
cancer survivors. Heart & Lung: Journal of Critical Care. 2003; 32(2):131–139.
4. Moller AM, Villebro N, Pedersen T, Tonnesen H. Effect of preoperative smoking intervention on
postoperative complications: A randomized clinical trial. Lancet. Jan 12; 2002 359(9301):114–117.
[PubMed: 11809253]
5. Bluman LG, Mosca L, Newman N, Simon DG. Preoperative smoking habits and postoperative
pulmonary complications. Chest. Apr; 1998 113(4):883–889. [PubMed: 9554620]
6. Vaporciyan A, Merriman K, Ece F, et al. Incidence of major pulmonary morbidity after
pneumonectomy:Association with timing of smoking cessation. Annals of Thoracic Surgery. 2002;
73:420–426. [PubMed: 11845853]
7. Ostroff J, Jacobsen P, Moadel A, et al. Prevalence and predictors of continued tobacco use after
treatment of patients with head and neck cancer. Cancer. 1995; 75:569–576. [PubMed: 7812925]
8. Schnoll R, Malstrom M, James C, et al. Correlates of tobacco use among smokers and recent
quitters diagnosed with cancer. Patient Education and Counseling. 2002; 46:137–145. [PubMed:
11867244]
9. Schnoll R, James C, Malstrom M, et al. Longitudinal predictors of continued tobacco use among
patients diagnosed with cancer. Annals of Behavioral Medicine. 2003; 25:214–222. [PubMed:
12763716]
10. Gritz E, Nisembaum R, Elashoff R, Holmes E. Smoking behaviors following diagnosis of patients
with stage I non-small cell lung cancer. Cancer Causes and Control. 1991; 2:105–112. [PubMed:
1651777]
11. Dresler C, Bailey M, Roper C, Patterson G, Cooper J. Smoking cessation and lung cancer
resection. Chest. 1996; 110:1199–1202. [PubMed: 8915221]
12. Walker MS, Vidrine DJ, Gritz ER, et al. Smoking relapse during the first year after treatment for
early-stage non-small-cell lung cancer. Cancer Epidemiology Biomarkers and Prevention. Dec;
2006 15(12):2370–2377.
13. Walker M, Larsen R, Zona D, Govindan R, Fisher E. Smoking urges and relapse among lung
cancer patients: Findings from a preliminary retrospective study. Preventative Medicine. 2004;
39:449–457.
14. Fiore MC, Jaen CR. A clinical blueprint to accelerate the elimination of tobacco use. Journal of the
American Medical Association. May 7; 2008 299(17):2083–2085. [PubMed: 18460668]
15. Fiore, M.; Jaen, C.; Baker, T.; Bailey, W.; Benowitz, N.; Curry, S. Treating Tobacco Use and
Dependence: 2008 Update. Clinical Practice Guideline. Rockville, MD: US Department of Health
and Human Services. Public Health Services; 2008.
16. Fiore M, Novotny T, Pierce J. Methods used to quit smoking in the United States: Do cessation
programs help? Journal of the American Medical Association. 1990; 263:2760–2765. [PubMed:
2271019]
17. Schnoll RA, Johnson TA, Lerman C. Genetics and smoking behavior. Current Psychiatry Reports.
Oct; 2007 9(5):349–357. [PubMed: 17915073]
18. Cox LS, Africano NL, Tercyak KP, Taylor KL. Nicotine dependence treatment for patients with
cancer. Cancer. Aug 1; 2003 98(3):632–644. [PubMed: 12879483]
19. Sarna L, Cooley M, Brown J, et al. Comparison of quality of life and health status of family
members and women with lung cancer. Oncology Nursing Forum. 2006; 33(6):1109–1116.
[PubMed: 17149394]
20. CDC. State-and sex-specific prevalence of selected characteristics-Behavioral Risk Factor
Surveillance System, 1996 and 1997. Washington, DC: US Government Printing Office; 2000.
21. Heatherton T, Kozlowski L, Frecker R, Fagerstrom K. The Fagerstrom test for nicotine
dependence: A revision of the Fagerstrom Tolerance Questionnaire. British Journal of Addiction.
1991; 86:1119–1127. [PubMed: 1932883]
22. Baker TB, Piper ME, McCarthy DE, et al. Time to first cigarette in the morning as an index of
ability to quit smoking: implications for nicotine dependence. Nicotine Tobacco Research. Nov;
2007 9(Suppl 4):S555–S570. [PubMed: 18067032]
Cooley et al. Page 10
Lung Cancer
. Author manuscript; available in PMC 2013 October 22.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
23. Parker E, Lasater T, Windsor R, Wilkins J, Upegui D, Heimdal J. The accuracy of self-reported
smoking status assessed by cotinine test strips. Nicotine and Tobacco Research. 2002; 4:305–309.
[PubMed: 12215239]
24. Hughes JR, Keely JP, Niaura RS, Ossip-Klein DJ, Richmond RL, Swan GE. Measures of
abstinence in clinical trials: issues and recommendations. Nicotine Tobacco Research. Feb; 2003
5(1):13–25. [PubMed: 12745503]
25. Hughes JR, Benowitz N, Hatsukami D, Mermelstein RJ, Shiffman S. Clarification of SRNT
workgroup guidelines for measures in clinical trials of smoking cessation therapies. Nicotine Tob
Res. Oct; 2004 6(5):863–864. [PubMed: 15700922]
26. Charlson ME, Pompei P, Ales KL, MacKenzie CR. A new method of classifying prognostic
comorbidity in longitudinal studies: development and validation. Journal of Chronic Disease.
1987; 40(5):373–383.
27. Sarna L, Cooley ME, Brown JK, et al. Quality of Life and Meaning of Illness of Women With
Lung Cancer. Oncology Nursing Forum. 2005; 32(1):E9–E19. [PubMed: 15660139]
28. Tittle MB, McMillan SC, Hagan S. Validating the brief pain inventory for use with surgical
patients with cancer. Oncology Nursing Forum. Mar-Apr;2003 30(2):325–330. [PubMed:
12692666]
29. Speizer F, Comstock G. Recomended respiratory disease questionnaires for use with adults and
children with epidemiologic research. Epidemiology standardization project. American Review of
Respiratory Disease. 1978; 118:117–153.
30. Schwartz AL. The Schwartz Cancer Fatigue Scale: testing reliability and validity. Oncology
Nursing Forum. May; 1998 25(4):711–717. [PubMed: 9599354]
31. Schwartz AL, Meek PM, Nail LM, et al. Measurement of fatigue. determining minimally important
clinical differences. Journal of Clinical Epidemiology. Mar; 2002 55(3):239–244. [PubMed:
11864794]
32. Radloff L. The CES-D scale: as self report depression scale for research in the general population.
Applied Psychology Measurement. 1977; 1:385–401.
33. Greene, F.; Page, DL.; Fleming, ID., et al. AJCC Cancer Staging Handbook. Sixth Edition.
Springer; 2002.
34. Prevalence of current smoking among adults aged 18 years and over: United States, 1997-March
2007. United States; Mar. 2007 www.cdc.giv/Nchs/data/nhis/earlyrelease/200709_08.pdf
35. Sarna L, Evangelista L, Tashkin D, et al. Impact of respiratory symptoms and pulmonary function
on quality of life of long-term survivors of non-small cell lung cancer. Chest. Feb; 2004 125(2):
439–445. [PubMed: 14769722]
36. Zhou W, Heist RS, Liu G, et al. Second hand smoke exposure and survival in early-stage non-
small-cell lung cancer patients. Clinical Cancer Research. Dec 1; 2006 12(23):7187–7193.
[PubMed: 17145845]
37. Schnoll R, Rothman R, Newman H, et al. Characteristics of cancer patients entering a smoking
cessation program and correlates of quit motivation: Implications for the development of tobacco
control programs for cancer patients. Psycho-Oncology. 2004; 13:346–358. [PubMed: 15133775]
38. Twardella D, Loew M, Rothenbacher D, Stegmaier C, Ziegler H, Brenner H. The diagnosis of a
smoking related disease is a prominent trigger for smoking cessation in a retrospective cohort.
Journal of Clinical Epidemiology. 2006; 59:82–89. [PubMed: 16360565]
39. Krall EA, Garvey AJ, Garcia RI. Smoking relapse after 2 years of abstinence: findings from the
VA Normative Aging Study. Nicotine Tobacco Research. Feb; 2002 4(1):95–100. [PubMed:
11906685]
40. Gilpin E, Pierce JP, Farkas AJ. Duration of Smoking Abstinence and Success in Quitting. Journal
of the National Cancer Institute. Apr 16.1997 89:572–576. [PubMed: 9106646]
41. Emery S, Gilpin EA, Ake C, Farkas AJ, Pierce JP. Characterizing and identifying "hard-core"
smokers: implications for further reducing smoking prevalence. American Journal of Public
Health. Mar; 2000 90(3):387–394. [PubMed: 10705856]
42. Patterson F, Schnoll R, Wileyto E, et al. Toward Personalized Therapy for Smoking Cessation: A
Randomized Placebo-controlled Trial of Bupropion. Clinical Pharmacological Therapies. Apr
2.2008
Cooley et al. Page 11
Lung Cancer
. Author manuscript; available in PMC 2013 October 22.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
43. Steinberg MB, Schmelzer AC, Richardson DL, Foulds J. The case for treating tobacco dependence
as a chronic disease. Annals of Internal Medicine. Apr 1; 2008 148(7):554–556. [PubMed:
18378950]
44. Gritz E, Nielsen I, Brooks L. Smoking cessation and gender: The influence of physiological,
psychological amd behavioral factors. Journal of American Medical Women's Association. 1996;
51:35–42.
45. Audrain J, Gomez-Caminero A, Robertson A, Boyd R, Orleans C, Lerman C. Gender and ethnic
differences in readiness to change smoking behavior. Womens Health. 1997; 3(2):139–150.
[PubMed: 9332155]
46. Etter J, Prohorov A, Perneger T. Gender differences in the psychological determinents of cigarette
smoking. Addiction. 2002; 97(6):733–743. [PubMed: 12084143]
47. Garvey A, Bliss R, Hitchcock J, Heinrold J, Rosner B. Predictors of smoking relapse among self-
quitters: A report from the Normative Aging Study. Addictive Behaviors. 1992; 17:367–377.
[PubMed: 1502970]
48. Wetter DW, Cofta-Gunn L, Irvin JE, et al. What accounts for the association of education and
smoking cessation? Preventative Medicine. Apr; 2005 40(4):452–460.
49. Escobedo LG, Peddicord JP. Smoking prevalence in US birth cohorts: the influence of gender and
education. American Journal of Public Health. Feb; 1996 86(2):231–236. [PubMed: 8633741]
50. Christakis NA, Fowler JH. The collective dynamics of smoking in a large social network. New
England Journal of Medicine. May 22; 2008 358(21):2249–2258. [PubMed: 18499567]
51. Vidrine DJ, Arduino RC, Gritz ER. The effects of smoking abstinence on symptom burden and
quality of life among persons living with HIV/AIDS. Aids Patient Care STDS. Sep; 2007 21(9):
659–666. [PubMed: 17919093]
52. Chapple A, Ziebland S, McPherson A. Stigma, shame, and blame experienced by patients with
lung cancer: qualitative study. British Medical Journal. Jun 19.2004 328(7454):1470. [PubMed:
15194599]
53. Fu SS, Partin MR, Snyder A, et al. Promoting repeat tobacco dependence treatment: are relapsed
smokers interested? American Journal of Managed Care. Apr; 2006 12(4):235–243. [PubMed:
16610925]
Cooley et al. Page 12
Lung Cancer
. Author manuscript; available in PMC 2013 October 22.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
Figure 1.
Pattern of SR over time
Cooley et al. Page 13
Lung Cancer
. Author manuscript; available in PMC 2013 October 22.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
Figure 2.
Pattern of SR: Quit before surgery
Cooley et al. Page 14
Lung Cancer
. Author manuscript; available in PMC 2013 October 22.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
Figure 3.
Pattern of SR: Smoking at diagnosis (n=35)
Cooley et al. Page 15
Lung Cancer
. Author manuscript; available in PMC 2013 October 22.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
Cooley et al. Page 16
Table 1
Demographic and Clinical Characteristics of the Sample at 1-month after surgery (n=94)
Characteristic N (%) Mean Value (SD)
Age 63.3 years (9.9)
Gender
Male 40 (42.5%)
Female 54 (57.5%)
Race
White 84 (89%)
Black 9 (10%)
Asian 1 ( 1%)
Education
Less than High School 24 (26%)
High School 35 (37%)
Greater than High School 35 (37%)
Marital Status
Married/partnered 57 (61%)
Live alone 37 (39%)
Stage at Diagnosis
I 64 (69%)
II 23 (24%)
III A 7 ( 7%)
Type of Lung Cancer
Adenocarcinoma 49 (52%)
Squamous Carcinoma 25 (27%)
Bronchioalveolar 6 ( 6%)
Large Cell 3 ( 3%)
Other 11 (12%)
Type of Surgical Procedures
Lobectomy 74 (79%)
Pnemonectomy 8 ( 9%)
Wedge Resection 12 (13%)
Lung Cancer
. Author manuscript; available in PMC 2013 October 22.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
Cooley et al. Page 17
Table 2
Tobacco and nicotine dependence history Tobacco history at baseline (1 month after surgery) (n=94)
Smoking status N (%)
Never smoker 10 (11%)
Ever smoker 84 (89%)
Former smoker 68 (81%)
Quit smoking before diagnosis 47 (56%)
Quit smoking after diagnosis 21 (25%)
Current smoker 16 (19%)
Continued smoking in household members 18/69 (26%)
Exposure to ETS
Less than one day/week 46/93 (49%)
Several days/week 14/93 (15%)
Every day 33/93 (36%)
Tobacco history for ever-smokers Mean (sd)
Age at initiation 17 years (5)
Number of years smoked 37 years (13)
Number of years since quit 8 years (12)
Number of cigarettes smoked per day 17 (14)
Dependence history for current smokers at baseline (self-report) (n=11)
Time to smoke the first cigarette in the morning n (%)
Within 5 minutes
+
5 (45%)
Between 6–30 minutes
+
4 (36%)
Between 31–60 minutes 0 (0%)
After 60 minutes 2 (18%)
+
highly nicotine dependent smoker
Lung Cancer
. Author manuscript; available in PMC 2013 October 22.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
Cooley et al. Page 18
Table 3
Cessation strategies used to quit at diagnosis (among 35 who smoked at diagnosis)
N %
Assistance 16 46
Type of assistance provided
Counseling only 1 6
Bupropion only 4 24
Nicotine replacement 4 24
Bupropion and Nicotine replacement 1 6
Bupropion and Information 1 6
Information and Nicotine replacement 3 18
Information and counseling 1 6
Combined treatment with counseling and Pharmacotherapy
*
1 6
*
recommended standard for tobacco dependence treatment.
Lung Cancer
. Author manuscript; available in PMC 2013 October 22.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
Cooley et al. Page 19
Table 4
Table of unadjusted logistic regressions for ever-smokers who smoked after lung cancer surgery (n= 84)
Variable Referent Quitters SR OR*CI P-value
Quit Status
1 year + since quit 36(73%) 10(29%) 1.00 - -
6 months to 1 year since quit 2(4%) 1(3%) 1.80 0.15,21.94 0.72
Less than 6 mos since quit 11(22%) 24(69%) 7.86 2.89,21.35 0.0001
Age 67±9 58±9 0.90 0.84,0.95 0.0004
Comorbidity 1.7±1.2 1.2±1.1 0.72 0.49,1.07 0.11
Gender Female 28(57%) 16(46%) 1.00 - -
Male 21(43%) 19(54%) 1.58 0.66,3.79 0.30
Dyspnea None 17(35%) 13(37%) 1.00 - -
Present 32(65%) 22(63%) 0.90 0.36,2.22 0.82
SCFS 11.4±5.5 13.4±5.7 1.06 0.98,1.15 0.12
BPI- Presence of pain None 24(50%) 6(18%) 1.00 - -
Present 24(50%) 27(82%) 4.50 1.58,12.86 0.005
Education <HS 8(16%) 14(40%) 1.00 - -
HS 41(84%) 21(60%) 0.29 0.11,0.81 0.02
CESDtotal 11±10 15±12 1.03 0.99,1.08 0.12
Depression Not Depressed 30(71%) 20(61%) 1.00 - -
Depressed 12(29%) 13(39%) 1.63 0.62,4.28 0.33
BPI- Worst pain over last 24 hours 3.7±2.6 5.4±2.5 1.28 1.06,1.55 0.01
BPI- Pain Interference with activities 19.5±20.2 23.7±19.1 1.01 0.99,1.04 0.37
BPI Severity of pain 10±8 14±9 1.06 1.00,1.12 0.05
Family smoker No 42(86%) 25(71%) 1.00 - -
Bold text= factors significantly related to smoking relapse (SR)
*
Odds Ratio is measuring the odds of ever-smokers relapsing after lung surgery versus those who did not relapse
Lung Cancer
. Author manuscript; available in PMC 2013 October 22.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
Cooley et al. Page 20
Table 5
Multivariate logistic regression for factors related to smoking relapse (n=84)
Variable Referent OR (CI) P-value
When quit <6 mo vs. 1+ yr 9.36 (2.43, 36.05) 0.001
6–12 mo vs. 1+ yr 1.30 (0.06, 26.81) 0.86
Gender M vs. F 2.96 (0.79, 11.06) 0.11
Number of comorbidities 0.55 (0.30, 1.01) 0.05
Age 0.92 (0.85, 0.99) 0.04
Education HS+ vs. <HS 0.23 (0.05, 1.03) 0.05
Presence of Pain Yes vs. No 3.24 (0.80,13.11) 0.10
Bold text= factors significantly related to smoking relapse (SR)
*
Odds Ratio is measuring the odds of ever-smokers relapsing after lung surgery versus those who did not relapse
Lung Cancer
. Author manuscript; available in PMC 2013 October 22.