Smoking, Cessation, and Cessation Counseling in Patients With Cancer: A Population-Based Analysis
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1 Smoking, Cessation, and Cessation Counseling in Patients With Cancer: A Population-Based Analysis Apoorva T. Ramaswamy MD 1 ; Benjamin A. Toll PhD 2,3 ; Anees B. Chagpar MD 3,4 ; and Benjamin L. Judson MD 3,4 BACKGROUND: Smoking is known to be carcinogenic and an important factor in the outcome of cancer treatment. However, to the authors knowledge, smoking habits and smoking cessation counseling in patients with cancer have been poorly studied. The authors sought to analyze smoking habits among Americans diagnosed with cancer in a nationally representative dataset. METHODS: The cancer supplement of the National Health Interview Survey (NHIS) in 2010 was used to obtain information regarding self-reported smoking behavior in a representative sample of the US population. Cancer history, smoking history, quitting behavior, cessation counseling, cessation approaches, and sociodemographic variables were analyzed. RESULTS: A total of 27,157 individuals were interviewed for the NHIS in 2010, representing 216,052,891 individuals, 7,058,135 of whom had ever smoked and 13,188,875 of whom had been told that they had cancer. Approximately 51.7% of individuals diagnosed with cancer and who were active smokers reported being counseled to quit smoking by a health professional within the previous 12 months. Cancer survivors were no more likely to quit smoking than individuals in the general population. Those diagnosed with a tobacco-related cancer were found to be no more likely to report quitting smoking than those with other types of cancers. Rates of quitting did not appear to vary based on the type of smoking cessation method used (P 5.50). CONCLUSIONS: Patients with cancer, including those diagnosed with a tobacco-related cancer, do not appear to be more likely to quit smoking than the general population. Only approximately one-half of patients with cancer who smoke are counseled to quit. Smoking cessation in patients with cancer is an important area for intervention and investigation. Cancer 2016;122: VC 2016 American Cancer Society. KEYWORDS: cancer, cancer survivors, smoking, smoking cessation. INTRODUCTION The detrimental effects of smoking have become widely known since the US Surgeon General first published the report on smoking in 1964, associating it with lung cancer. In the 50th anniversary edition of the Surgeon General s report, the causal role of smoking was expanded to include colon and liver cancers. 1 Other cancers in which smoking has been implicated include head and neck, esophageal, pancreatic, gastric, gallbladder, breast, bladder, and kidney cancers. In addition to decreasing the risk of malignancy, smoking cessation is considered an important step toward a reduction in the risks of stroke, myocardial infarction, chronic obstructive pulmonary disease, and a host of other ailments. As more people survive the initial diagnosis of cancer, the beneficial effects of smoking cessation particular to this population are becoming clearer. 2 It is estimated that in 2010, the United States spent $125 billion on cancer therapies that have considerably changed the prognosis of many patients. 3 Nevertheless, patients with cancer who continue to smoke receive fewer benefits from these therapies. Smoking has been associated with increased postoperative complications, with decreased wound healing and pulmonary complications. 4,5 It also has been shown to worsen the side effects of radiation and chemotherapy, 4 and to decrease the efficacy of radiotherapy on malignancies. 6 There has also been a question of the decreased efficacy of certain chemotherapeutic agents due to increased hepatic metabolism secondary to smoking. 7 These differences in treatment have translated into significantly decreased survival in patients with cancer who continue to smoke, with studies performed in patients with lung, head and neck, prostate, and cervical cancer. 6,8-10 Data regarding the beneficial effects of smoking cessation have been encouraging. Perioperative pulmonary and wound healing complications are reported to decrease after just 4 weeks of preoperative smoking cessation. 5,11 Cessation within 12 weeks of a cancer diagnosis decreases mortality by 40%, whereas cessation for >1 year decreases mortality by Corresponding author: Benjamin L. Judson, MD, Department of Surgery, Yale University School of Medicine, PO Box , 333 Cedar St, New Haven, CT 06520; Fax: (203) ; Benjamin.judson@yale.edu 1 Department of Otolaryngology, New York-Presbyterian University Hospital of Columbia and Cornell, New York City, New York; 2 Department of Public Health Sciences, Medical University of South Carolina, Charleston, South Carolina; 3 Department of Surgery, Yale University School of Medicine, New Haven, Connecticut; 4 Yale Cancer Center, New Haven, Connecticut. DOI: /cncr.29851, Received: September 28, 2015; Revised: November 17, 2015; Accepted: November 19, 2015, Published online February 16, 2016 in Wiley Online Library (wileyonlinelibrary.com) Cancer April 15,
2 TABLE 1. Sociodemographic Characteristics of Cancer Survivors Versus Those With No History of Cancer Cancer Cohort Noncancer Cohort Characteristic Percentage Weighted No. No. Percentage Weighted No. No. Total 13,188, ,052,891 25,482 Region Northeast ,404, ,116, Midwest ,361, ,870, South ,737, ,906, West ,685, ,159, Age, y < ,802, ,722,601 12, ,561, ,101, > ,824, ,228, Sex Male ,311, ,503,275 11,382 Female ,877, ,549,616 14,100 Education <Grade ,947, ,950, High school graduate ,719, ,722, Some college/associatedegree ,046, ,518, Bachelor s degree ,000, ,659, Master s degree 7.7 1,012, ,657, Professional/doctorate , ,634, Insurance None , ,189, Medicare ,690, ,469, Medicaid , ,780, Military , ,011, Private ,460, ,489,922 12,231 Employment status Working ,536, ,696,543 14,285 Looking for work , ,497, Not working and not looking ,875, ,509, Race White ,810, ,335,913 14,370 Black 9.1 1,195, ,171, Asian , ,503, Hispanic , ,284, Other , ,757, Marital status Married ,633, ,596,457 11,294 Widowed ,015, ,629, Divorced/separated ,951, ,051, Never married 7.7 1,008, ,173, Living with partner , ,332, Type of cancer NA NA NA Head and neck , Breast ,718, Cervix 8.8 1,154, Ovary , Uterus , Prostate ,060, Bladder , Kidney , Thyroid , Colorectal 8.0 1,042, Esophagus ,615 9 Leukemia/lymphoma , Liver , Pancreas , Stomach , Lung , Melanoma ,348, Other , Tobacco-related cancer NA NA NA Yes ,090, No ,013, Cancer April 15, 2016
3 Smoking in Patients With Cancer/Ramaswamy et al TABLE 1. Continued Cancer Cohort Noncancer Cohort Characteristic Percentage Weighted No. No. Percentage Weighted No. No. Smoking history Never smoked ,961, ,460,946 10,018 Ever smoked ,058, ,319,695 15,308 Current smoker ,360, ,699, Former smoker ,697, ,745, Abbreviation: NA, not applicable. 70%. 6 In the head and neck cancer population, 2 years of smoking cessation are reported to reduce mortality levels of former smokers down to the level of patients who have never smoked. 12 Moreover, smoking cessation has been shown to decrease the likelihood of a second primary malignancy and to improve quality of life. 13 In 2000, the US Department of Health and Human Services issued a clinical practice guideline for all physicians regarding treating tobacco use and dependence that subsequently was updated in ,15 This document encouraged all health care providers to identify and provide smoking cessation counseling to their patients who use tobacco products. Acknowledging the significance of smoking on cancer outcomes and treatment efficacy, the American Association for Cancer Research published a policy statement highlighting the necessity of documenting smoking status among patients with cancer and subsequent counseling for this population. 2 Given the importance of smoking in the outcomes of patients with cancer, we sought to investigate smoking behaviors and smoking cessation counseling in cancer survivors, using a nationally representative, population-based survey. MATERIALS AND METHODS The National Health Interview Survey (NHIS) is a crosssectional, population-based, face-to-face survey conducted annually by the National Center for Health Statistics. Survey participation is voluntary, and the US Census Bureau implements data collection using approximately 400 trained interviewers. The weighted sample is designed to reflect the noninstitutionalized civilian population of the United States. The final weights are adjusted according to age, sex, race, and ethnicity classes based on population estimates produced by the US Census Bureau. The sample is reevaluated every 10 years, using the most recent census information. The sample is chosen such that each person in the population has a known non-zero probability of selection, and the sample is representative of the noninstitutionalized civilian population in the United States. The 2010 NHIS included a cancer supplement, which provided information regarding self-reported history of cancer and smoking habits. The final response rate for individuals reporting these data was 60.8%. The total sample size of the cancer supplement was 27,157 individuals, representing 216,052,891 individuals, 7,058,135 of whom had ever smoked and 13,188,875 of whom had been told that they had cancer. In addition to evaluating patients who had been told they had any cancer diagnosis, we also specifically analyzed tobacco-related cancers, which were defined according to the American Cancer Society s list, and consisted of lung, laryngeal, oral cavity, nose/sinus, pharyngeal, esophageal, gastric, pancreatic, cervical, kidney, bladder, ovarian, and colorectal cancer as well as acute myeloid leukemia. However, acute myeloid leukemia was not included in the current analysis because the NHIS did not provide information concerning the type of leukemia diagnoses. We classified individuals who were ever-smokers as those who reported having smoked 100 cigarettes. In addition, we evaluated whether cancer survivors had tried to quit smoking, defining this as current smokers who stopped smoking at least 1 day within the past 12 months because they were trying to quit. We further evaluated various types of smoking cessation therapies, including nicotine replacement therapy, which we defined as the use of a nicotine patch, nicotine gum/lozenge, or nicotine nasal spray/inhaler. Eversmoking was defined as ever having smoked 100 cigarettes. Tried to quit smoking was defined as those current smokers who stopped smoking at least 1 day within the past 12 months because they were trying to quit. Statistical Analysis Statistical analysis was performed using SAS (version 9.1.3; SAS Institute Inc, Cary, NC) and SUDAAN (RTI International, Research Triangle Park, NC) statistical software. Univariate analysis of meeting Centers for Cancer April 15,
4 Disease Control and Prevention guidelines and selfreported quality of life was conducted using chi-square analysis. The Taylor series was chosen as the method of variance estimation. Multivariate analyses were conducted using logistic regression. The Taylor series was used for variance estimation and robust standard error method calculation was used. 16 RESULTS In the 2010 NHIS, 27,157 individuals were surveyed, representing 216,052,891 individuals in the population. Of these, 5.75% had been told that they had cancer (excluding nonmelanomatous skin cancer). The sociodemographic factors, including smoking history, of cancer survivors versus those who did not have a history of cancer is shown in Table 1. Smoking rates were higher in the cancer population, with 54.2% of those having been diagnosed with cancer having ever smoked compared with 40.3% of those who had never been diagnosed with cancer (P<.001). On bivariate analysis, comparing those with a cancer diagnosis with the general population, cancer survivors were more likely to have reported quitting smoking than ever-smokers in the general population (66.6% vs 51.8%; P<.01). We then focused our attention on respondents who had ever smoked and who reported having been diagnosed with cancer to determine factors associated with quitting smoking. In this population, age, sex, educational level, insurance status, employment status, marital status, type of cancer (all P<.01), and having been diagnosed with a tobacco-related cancer (P 5.03) were all found to be significantly associated with rates of individuals identifying as former smokers (Table 2). Older smokers were more likely to have quit (83.2% of those aged > 60 years), as were men (76.5%); more highly educated individuals (79.9% of those with a professional degree); those with Medicare (78.7%), military (64.4%), or private insurance (65.6%); and those who were not working and not looking for a job (71.0%). However, those who had been diagnosed with a tobacco-related cancer (62.0%) were not found to be more likely to have quit smoking compared with those with a non-tobacco-related cancer (69.9%). On multivariate analysis, age (P<.01), insurance status (P 5.01), and type of cancer (P 5.04) remained significant predictors of having quit smoking among cancer survivors whereas marital status (P 5.05) and educational level (P 5.06) were not found to be significant (Table 3). When asked about any smoking cessation counseling they may have received, only 51.7% of cancer survivors who currently smoke recalled having been counseled TABLE 2. Factors Associated With Successfully Quitting Smoking Among Cancer Survivors Variable Current Smoker Former Smoker Age, y <.01 < > Sex <.01 Male Female Education level <.01 <Grade High school graduate Some college/associate degree Bachelor s degree Master s degree Professional/doctorate Insurance status <.01 None Medicare Medicaid Military Private Employment status <.01 Working Looking for work Not working and not looking Race.63 White Black Asian Hispanic Other Marital status <.01 Married Widowed Divorced/separated Never married Living with partner Type of cancer <.01 Head and neck Breast Cervix Ovary Uterus Prostate Bladder Kidney Thyroid Colorectal Testicular Lymphoma/leukemia Lung Melanoma Other Tobacco-related cancer.27 Yes No Types of smoking cessation.50 methods Nicotine replacement Prescription (bupropion or varenicline) Counseling/support P 1250 Cancer April 15, 2016
5 Smoking in Patients With Cancer/Ramaswamy et al TABLE 3. Multivariate Analysis of Successfully Quitting Smoking Among Cancer Survivors OR (95% CI) Age, y <.01 < ( ) > ( ) Education level.06 <Grade ( ) High school graduate Some college/associate degree 0.91 ( ) Bachelor s degree 0.38 ( ) Master s degree 0.34 ( ) Professional/doctorate 0.60 ( ) Insurance status.01 None 2.94 ( ) Medicare 2.13 ( ) Medicaid 4.08 ( ) Military 1.80 ( ) Private Employment status.37 Working Looking for work 0.62 ( ) Not working and not looking 0.74 ( ) Marital status.05 Married Widowed 1.44 ( ) Divorced/separated 1.37 ( ) Never married 1.17 ( ) Living with partner 4.06 ( ) Type of cancer Head and neck.04 Breast 6.58 ( ) Cervix ( ) Ovary 6.72 ( ) Uterus 9.36 ( ) Prostate 2.87 ( ) Bladder 2.65 ( ) Kidney 2.75 ( ) Thyroid 4.51 ( ) Colorectal 4.05 ( ) Testicular ( ) Lymphoma/leukemia 6.37 ( ) Lung 2.66 ( ) Melanoma 5.51 ( ) Other 4.31 ( ) Sex.49 Male Female 1.21 ( ) Abbreviations: 95% CI, 95% confidence interval; OR, odds ratio. to quit smoking by any health professional within the past 12 months. It is interesting to note that only 55.9% of patients with a tobacco-related cancer recalled being counseled to quit smoking, whereas 56.8% of those diagnosed with a non-tobacco-related cancer had been counseled to quit. The only factor that was found to be significantly associated with being counseled to quit smoking was educational level (P 5.03), with those with higher levels of education being less likely to report having been counseled to quit (Table 4). Of those who had been diagnosed with a tobacco-related cancer, 55.9% recalled P TABLE 4. Factors Associated With Receiving Counseling to Quit Smoking Variable Counseled to Quit Not Counseled Age, y.92 < > Sex.28 Male Female Education level.03 <Grade High school graduate Some college/ associate degree Bachelor s degree Master s degree Professional/ doctorate Insurance status.66 None Medicare Medicaid Military Private Employment status.77 Working Looking for work Not working and not looking Race.74 White Black Asian Hispanic Other Marital status.72 Married Widowed Divorced/ separated Never married Living with partner Type of cancer.80 Head and neck Breast Cervix Ovary Uterus Prostate Bladder Kidney Thyroid Colorectal Testicular Lymphoma/ leukemia Lung Melanoma Other Tobacco-related cancer.64 Yes No Tried to quit smoking.15 Yes No P Cancer April 15,
6 being counseled to quit smoking whereas 56.8% of those diagnosed with a non-tobacco-related cancer had been counseled to quit. On multivariate analysis of the relationship between level of education, diagnosis of a tobaccorelated cancer, and being counseled to quit smoking, only educational level was found to be statistically significant (P<.05). Those with Bachelor s degrees had an odds ratio of 0.26 (95% confidence interval, ) of being counseled to quit compared with those who had gone no further after graduating high school. To understand the sociodemographics of attempting to quit, we evaluated factors associated with trying to quit smoking among current smokers who had been diagnosed with cancer. In total, approximately 50.1% had stopped smoking for at least 1 day in an attempt to quit. Only level of education (P 5.03) and type of cancer (P 5.04) were found to be significantly correlated with trying to quit on univariate analysis. DISCUSSION Greater than 50% of Americans diagnosed with cancer have smoked, and of those, greater than one-third are current smokers, suggesting that despite the knowledge that smoking is deleterious to their general health, many cancer survivors continue to smoke. Previous studies have suggested that 86% of patients with lung cancer 17 and 84% of patients with head and neck cancer 18 attempt to quit smoking, especially at the time of diagnosis, 19 although estimates of the rate of relapse range from 13% to 60%. 17,20-22 However, we found that a diagnosis of cancer is not associated with a higher quit rate compared with the general population. In 2012, Park et al examined smoking rates in patients with lung and colorectal cancer at the time of diagnosis and 5 months afterward. 23 As in the current study, Park et al found that having public or no insurance was correlated with an increased likelihood of continuing to smoke after a cancer diagnosis. However, in the current study, diagnosis with a tobacco-related cancer was not found to be a significant predictor of quitting smoking. Contrary to the findings of the current study, Park et al found that for patients with colorectal cancer, older age and male sex were correlated with an increased likelihood of continuing smoking. They also found that patients diagnosed with lung cancer were more likely to quit smoking after diagnosis than those diagnosed with colorectal cancer. 23 However, the study by Park et al evaluated smoking status only 5 months after the original diagnosis of cancer, whereas the current study includes a more diverse population. Studies by Gritz et al 17 and Davison and Duffy 21 have reported a 48% relapse rate within 1 year and a 60% relapse rate within 2 years, respectively. Counseling regarding smoking cessation and support for smoking cessation have become an important measure for improvement in the oncology community. 2 The American College of Chest Physicians includes this in their list of 7 quality indicators for the treatment of lung cancer. 24 However, the findings of the current study suggest that only approximately one-half of those diagnosed with cancer have been advised to quit smoking by a health professional within the past year. Those with tobacco-related cancers were counseled at the same rate as their counterparts who had been diagnosed with a cancer not related to tobacco. Patients with head and neck cancer were most likely to have been counseled to quit (77.5%), and patients with ovarian cancer were the least likely to have been so advised (20.3%). Highly educated smokers also were the least likely to be counseled to quit, with only 20.8% of those with a professional degree being counseled to quit. This may be due to the fact that health care providers assume that such individuals are aware of the risks of their behavior. Potential reasons for the lack of reported counseling by healthcare professionals include ignorance of the patients smoking status, lack of time during an appointment, and perceived inefficacy of counseling in changing patient behavior. The US Centers for Medicare and Medicaid Services requires healthcare providers to document smoking status for at least 80% of their patients of 13 years as a basic measure of quality of care. In response, the intake forms of many healthcare providers now include a section regarding smoking status. Time is also a significant issue for healthcare providers. In an attempt to decrease the time burden of counseling on nonspecialists, quitlines as well as smoking cessation referrals have been established so that busy clinicians can guide patients to proper interventions for smoking cessation. The last issue of efficacy is also potentially the most difficult to argue against and will be addressed below. In the current study, patients who were counseled to quit smoking by a health professional were not found to be more likely to have tried to quit smoking within the past year (P 5.15). Indeed, a 2013 systematic review and meta-analysis by Nayan et al 25 suggested that tobacco cessation interventions in the oncology population do not significantly affect cessation rates. However, a study of smokers in the United Kingdom found that not having been advised to quit by a health professional was predictive of never trying to quit smoking. 26 Another Cochrane review from 2008 of 41 trials of healthcare provider-based smoking interventions in the general smoker population found that brief advice regarding cessation increased the rate of quitting over no advice, with 1252 Cancer April 15, 2016
7 Smoking in Patients With Cancer/Ramaswamy et al a relative risk of Perhaps the population of smokers who develop cancer are a more inveterate group who are more resistant to advice regarding smoking cessation. Nevertheless, the benefits of smoking cessation are much better established and represent the strongest argument for counseling regarding cessation. 27 An important advantage of this population-based survey analysis of the NHIS is its geographic, socioeconomic, and racial diversity. It is less subject to the selection biases of institution-based surveys. However, the current study is subject to significant weaknesses, including the fact that it is a cross-sectional survey and therefore it is not possible to establish causality. As a self-report survey without official diagnostic or treatment-specific data, questions regarding diagnosis or time since treatment cannot be verified further. In addition, questions regarding counseling to quit smoking by a health professional within the past 12 months are necessarily subject to recall bias. The finding that greater than one-third of Americans who are diagnosed with cancer continue to smoke, and only approximately one-half of those have been counseled to quit smoking do in fact quit is a call to action for all health care providers. As has been recommended previously, the smoking status should be assessed for all patients, especially those with cancer diagnoses, and the responsibility for encouraging smoking cessation lies in the hands of all those who are engaged in working toward their patients well-being. Indeed, given all of the benefits of smoking cessation for patients with cancer, it is crucial that all health care providers counsel their patients with cancer to quit smoking. FUNDING SUPPORT No specific funding was disclosed. CONFLICT OF INTEREST DISCLOSURES Benjamin Toll has received an investigator-initiated grant from Pfizer for medicine only for work performed outside of the current study. REFERENCES 1. US Department of Health and Human Services. The Health Consequences of Smoking-50 Years of Progress: A Report of the Surgeon General. Atlanta, GA: US Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health; Toll BA, Brandon TH, Gritz ER, Warren GW, Herbst RS; AACR Subcommittee on Tobacco and Cancer. Assessing tobacco use by cancer patients and facilitating cessation: an American Association for Cancer Research policy statement. Clin Cancer Res. 2013;19: Yabroff KR, Lund J, Kepka D, Mariotto A. Economic burden of cancer in the United States: estimates, projections, and future research. Cancer Epidemiol Biomarkers Prev. 2011;20: Gritz ER, Vidrine DJ, Lazev AB. 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The influence of nicotine abuse and diabetes mellitus on the results of primary irradiation in the treatment of carcinoma of the cervix. Cancer. 1987;60: Gritz ER, Fingeret MC, Vidrine DJ, Lazev AB, Mehta NV, Reece GP. Successes and failures of the teachable moment: smoking cessation in cancer patients. Cancer. 2006;106: Stevens MH, Gardner JW, Parkin JL, Johnson LP. Head and neck cancer survival and life-style change. Arch Otolaryngol. 1983;109: Gritz ER, Carmack CL, de Moor C, et al. First year after head and neck cancer: quality of life. J Clin Oncol. 1999;17: Fiore MC, Bailey WC, Cohen SJ, et al. Treating Tobacco Use and Dependence. Rockville, MD: US Department of Health and Human Services Public Health Service; Tobacco Use and Dependence Guideline Panel. Treating Tobacco Use and Dependence: 2008 Update. Rockville, MD: US Department of Health and Human Services; Binder DA. On the variances of asymptotically normal estimators from complex surveys. Int Stat Rev. 1983;51: Gritz ER, Nisenbaum R, Elashoff RE, Holmes EC. Smoking behavior following diagnosis in patients with stage I non-small cell lung cancer. Cancer Causes Control. 1991;2: Ostroff JS, Jacobsen PB, Moadel AB, et al. Prevalence and predictors of continued tobacco use after treatment of patients with head and neck cancer. Cancer. 1995;75: Vander Ark W, DiNardo LJ, Oliver DS. Factors affecting smoking cessation in patients with head and neck cancer. Laryngoscope. 1997; 107: Dresler CM, Bailey M, Roper CR, Patterson GA, Cooper JD. Smoking cessation and lung cancer resection. Chest. 1996;110: Davison AG, Duffy M. Smoking habits of long-term survivors of surgery for lung cancer. Thorax. 1982;37: Walker MS, Larsen RJ, Zona DM, Govindan R, Fisher EB. Smoking urges and relapse among lung cancer patients: findings from a preliminary retrospective study. Prev Med. 2004;39: Park ER, Japuntich SJ, Rigotti NA, et al. A snapshot of smokers after lung and colorectal cancer diagnosis. Cancer. 2012;118: Mazzone PJ, Vachani A, Chang A, et al. Quality indicators for the evaluation of patients with lung cancer. Chest. 2014;146: Nayan S, Gupta MK, Strychowsky JE, Sommer DD. Smoking cessation interventions and cessation rates in the oncology population: an updated systematic review and meta-analysis. Otolaryngol Head Neck Surg. 2013; 149: Sharma A, Szatkowski L. Characteristics of smokers who have never tried to quit: evidence from the British Opinions and Lifestyle Survey. BMC Public Health. 2014;14: Stead L, Bergson G, Lancaster T. Physician advice for smoking cessation. Cochrane Database Syst Rev. 2008;(2):CD Cancer April 15,
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