The association between tobacco smoking and colorectal cancer: A meta analysis

The objective of this study was to conduct a systematic review and analyze the association between tobacco smoking and CRC from published papers during the previous five years. All published cohort studies within the last five years using specific keywords were reviewed. The title and abstract of all available papers were reviewed and considered for eligibility inclusion.

JOURNAL OF MEDICAL RESEARCH THE ASSOCIATION BETWEEN TOBACCO SMOKING AND COLORECTAL CANCER: A META ANALYSIS Nguyen Thi Nga, 2Pham Phuong Lien, 3Khanpaseuth Sengngam, 4,5Le Tran Ngoan Vinh Medical University, Vietnam; 2Hanoi University of Public Health, Vietnam; National Institute of Public Health, Lao PDR; International University of Health and Welfare, Japan; 5Hanoi Medical University, Vietnam Cigarette smoking is recognized as the cause of a number of diseases including cancer, however, previous findings of its relation to colorectal cancer (CRC) are inconsistent The objective of this study was to conduct a systematic review and analyze the association between tobacco smoking and CRC from published papers during the previous five years All published cohort studies within the last five years using specific keywords were reviewed The title and abstract of all available papers were reviewed and considered for eligibility inclusion The ln(HR) and se(ln(HR)) were estimated from the multivariable adjusted HR and the 95% confidence interval (CI) was derived from published studies The random pooled multivariable adjusted HR and 95%CI was analyzed using STATA 10 There were 20 studies included for pooled analysis The test for heterogeneity yielded Q = 128.044 on 22 degrees of freedom (p = 0.000) Moment-based estimate of between studies variance = 0.021 HR = 1.16; CI (1.08 - 1.27), statistically significant, p < 0.01 We observed a significant positive association between tobacco smoking and the risk of colorectal cancer Key words: CRC, cigarette smoking, cohort study, meta-analysis I INTRODUCTION Cigarette smoking has been recognized as communicable diseases such as cardiovascular diseases, cancers, chronic respiratory the cause of a number of diseases including diseases and diabetes Despite these negative cancer [1] Annually, while active smoking kills health effects, the prevalence of tobacco more than five million people, secondhand smoking has been increasing globally in smoking (SHS) causes the death of over recent years, particularly among youth in low 600,000 people worldwide [2] If the situation and middle income countries [4 - 6] Colorectal is not controlled, deaths due to tobacco use cancer incidence and mortality has been the will reach eight million per year by 2030 The fifth vast majority of these deaths are projected to approximately 1.4 million new cases and occur in the developing world, including 694,000 deaths were estimated to have Vietnam [3] Tobacco use was also associated occurred in 2012 alone [7] Although the with a high burden of diseases from non- involvement of cigarette smoking in the most common cancer worldwide; development of colorectal cancer has been reported in some studies, evidence of the Corresponding author: Le Tran Ngoan, Hanoi Medical University Email: letngoan@hmu.edu.vn Received: 15/4/2018 Accepted: 22/11/2018 JMR 116 E3 (7) - 2018 association between tobacco smoking and colorectal cancer risk is still unclear [8; 9] To our knowledge, no literature review has been conducted on the association between 87 JOURNAL OF MEDICAL RESEARCH tobacco smoking and colorectal cancer since our earlier review in 2013 We aim to review the association between tobacco smoking and CRC from published papers during the previous five years • At least one of the outcomes (colon, rectal, or CRC) was reported Inclusion criteria - Patients were prospectively recruited and followed up II METHODS - Studies reported relative risk (RR) or To further investigate the controversial hazard ratios (HR) and their corresponding relationship between cigarette smoking and 95% confidence intervals (95% CIs) of CRC or CRC, we conducted a review of all published some other factors effecting CRC status by cohort studies within the last five years The different smoking categories search process was conducted in January through August of 2017 using PubMed with the keywords: (smoke OR cigarette OR tobacco OR smoking) AND (Colon cancer OR Rectum cancer OR colo-rectal cancer OR colorectal cancer OR colorectum cancer OR colon rectum cancer) AND cohort studies) The studies were collected and handled in two stages In the first stage, the title and abstract of all collected researches were - At least one of the outcomes (colon, rectal, or CRC) was reported Exclusion criteria - Case-control design - Studies that included hereditary CRC syndromes, chronic inflammatory bowel disease, history of colorectal cancer, or previous bowel resection - Full publication not written in English reviewed Studies not related to cigarette Data of all studies were extracted and smoking and CRC were excluded Studies arranged into a formation for analyzing and matching the selection criteria were stored as evaluating full text and were moved to the second stage include: At this stage, we proceeded to read and check the results and methodology of the studies Studies related to the association of cigarette smoking and CRC published from 2013 until the present were selected For studies that The characteristics extracted - Basic information: Name of author, conducted year, published year, setting - Detailed information: Subject, gender, person at risk, type of CRC published data from the same cohort, we - Research results: Incidence or mortality, chose only the most recent and complete smoking category, cigarettes per day, smoking report for analysis duration, pack-year, initiate age, RR, HR - Patients were prospectively recruited and followed up adjusted The primary outcome of this study was the - Studies reported relative risk (RR) or incidence of CRC (International Classification hazard ratios (HR) and their corresponding of Disease [ICD] versions - 9: 153 - 154; ICD 95% confidence intervals (95% CIs) of CRC or 10: C18 - 21) Secondary outcomes included some other factors effecting CRC status by incidence of colonic cancer (ICD - 9: 153; different smoking categories ICD 10: C18 - 19) and rectal cancer (ICD - 9: 88 JMR 116 E3 (7) - 2018 JOURNAL OF MEDICAL RESEARCH 154; ICD 10: C20 –21) The cancer diagnosis (Figure 1) All studies were conducted and was records, followed up between 1972 and 2013 Most of pathology reports, or cancer registry All the articles were published in regional or world studies used were published and data can be cancer magazines In 2016 and 2017, only used the one study was published while four were information collected was kept confidential and published in 2014 Six studies were published was only available for research purposes in 2015 and eight were published in 2013 identified for through researching hospital purposes All Sixteen studies included CRC, three studies Data synthesis and analysis included colon cancer only and one included The ln(HR) and se(ln(HR)) were estimated only rectal cancer (Table 1) Five studies from the multivariable adjusted HR, 95% CI indicated cases of CRC deaths but only four derived from published prospective studies studies described hazard ratios of colorectal The random pooled multivariable adjusted HR, cancer mortality for current smokers (Table 2) 95% CI was analyzed using STATA 10 In two studies of Ahmadi et al and Tao L et al, III RESULTS current smoking was associated with colorectal cancer-specific mortality [10; 28] We identified eligible 400 abstracts from whereas two studies were not associated with the initial literature search After screening and colorectal cancer specific mortality [10; 15] In excluding duplicate abstracts, 20 articles were a study of Jang B et al, multivariable-adjusted considered of interest and full texts were Cox proportional hazards regression models retrieved for detailed evaluation The present showed that smoking before diagnosis was study included 20 cohort studies with data associated from a total of 6.302.836 participants Six mortality (RR, 2.14; 95% CI, 1.50 to 3.07) and studies post-diagnosis smoking was associated with were populations, conducted eight in the in American Asian Pacific populations and six in European populations JMR 116 E3 (7) - 2018 with colorectal cancer-specific colorectal cancer-specific mortality (RR, 1.92; 95% CI, 1.15 to 3.21) [12] 89 Identification JOURNAL OF MEDICAL RESEARCH Records identified through database searching, (n = 643) Screening Records after duplicates removed (n = 243) Records screened (n = 400) Included Eligibility Full-text articles assessed Records excluded (n = 362) Full-text articles excluded, Studies included in qualitative synthesis (n = 20) Studies included in quantitative synthesis (Metaanalysis), (n = 18) Figure Flowchart of systematic literature search and review for eligible studies Table The title and author in included studies Number Name of studies and [source] Author Behavioural and Metabolic Risk Factors for Mortality from Colon and Rectum Cancer: Analysis of Data from the Asia- Morrison DS et al Pacific Cohort Studies Collaboration [10] 90 Active smoking and mortality among colorectal cancer survivors: the Cancer Prevention Study II nutrition cohort [11] Yang B et al Weight change later in life and colon and rectal cancer risk in participants in the EPIC-PANACEA study [12] Steins Bisschop BN et al JMR 116 E3 (7) - 2018 JOURNAL OF MEDICAL RESEARCH Number Name of studies and [source] Author Risk of colorectal cancer associated with active smoking among female teachers [13] Susan Hurley et al Fruit and vegetable intake and the risk of colorectal cancer: Results from the Shanghai Men's Health Study [14] VogtmannE et al Lifestyle factors associated with survival after colorectal cancer diagnosis [15] Boyle Tat et al Smoking and survival of colorectal cancer patients: population -based study from Germany [16] Walter V et al The Increased Risk of Colon Cancer Due to Cigarette Smoking May Be Greater in Women than Men [17] Parajuli R et al Proportion of Colon Cancer Attributable to Lifestyle in a Cohort of US Women [18] Erdrich J et al 10 Combined impact of healthy lifestyle factors on colorectal cancer: a large European cohort study [19] Aleksandrova K et al 11 Does active smoking induce hematogenous metastatic spread in colon cancer? [20] Ahmadi A et al 12 Association of body mass index and smoking on outcome of Chinese patients with colorectal cancer [21] Liu D et al 13 Risk factors for Colorectal Cancer in Thailand [22] 14 Associations between Environmental Exposures and Incident Colorectal Cancer by ESR2 Protein Expression Level in a Population-Based Cohort of Older Women [23] Tillmans LS et al 15 Smoking increases rectal cancer risk to the same extent in women as in men: results from a Norwegian cohort study [24] Parajuli R et al 16 Mortality determinants in colorectal cancer patients at different grades: a prospective, cohort study in Iran [25] Ahmadi A et al 17 Hypertension is an important predictor of recurrent colorectal adenoma after screening colonoscopy with adenoma polypectomy [26] Lin CC et al 18 Heterogeneity of colorectal cancer risk by tumour characteristics: Large prospective study of UK women [27] BurónPust A et al 19 Impact of postdiagnosis smoking on long-term survival of cancer patients: the Shanghai cohort study [28] Tao L et al 20 A Prospective Study of Duration of Smoking Cessation and Colorectal Cancer Risk by Epigenetics-related Tumor Classification[29] Nishihara R et al JMR 116 E3 (7) - 2018 Poomphakwaen K et al 91 JOURNAL OF MEDICAL RESEARCH Table Hazard ratio of colorectal cancer mortality for smoking status Smoking status Reference HR (Multivariate Adjusted)* Never smokers = [10] Current smoker 1.08 (0.72 - 1.62) [11] Current smoker - [15] Current smoker 1.31 (0.82 - 2.09) [25] Current smoker 1.55(1.03 - 2.34) [28] Male Current smoker 2.31 (1.40 - 3.81) *HR adjusted by many variables depending on the research including age, BMI, physical activity, height, drink, smoke, cholesterol, diabetes and education were included in the sex and study stratified model Table HR of Colorectal Cancer Incidence for smoking status Reference [12] [13] 92 Smoking status Adjusted HR Never, current, former - Never, current, former Current smokers: HR = 1.28, (1.00 - 1.63) Former smokers: HR = 1.10, (0.97 - 1.24) [14] Ever smokers, never smokers - [17] Never, former, current, ever [18] Cigarette smoking pack years [19] Current, never, former [22] Non-smoker, ex-smokers, current smokers [23] Never, ever, former, current smokers [24] Never, former, current, [27] Current, never - [28] Non-smokers, current smokers - [29] Current smokers - Female ever-smokers: HR =1.19, (1.09 - 1.32) Male ever-smoker: HR = 1.08, (0.97 - 1.19) Ex-smokers: HR = 1.34(0.52 - 3.46) Current smokers: HR = 0.51(0.18 - 1.38) Male ever-smoker: HR = 1.27, ( 1.11 - 1.45) Female ever-smokers: HR = 1.28, (1.11 - 1.48) JMR 116 E3 (7) - 2018 JOURNAL OF MEDICAL RESEARCH There were 12 studies which indicated the female and males) such that 23 variables were incidence of CRC but only studies described analyzed together In these 23 variables, there HR indicator for different types of smoking were two relatively low risk and statistically status (Table 3) significant outcomes while there were seven Our study included 20 studies that met the results for no statistically significant criteria, including 18 studies showing the asso- relationship Fourteen results suggested that ciation of smoking and colorectal cancer with smoking increases the risk of colorectal cancer HR and RR, although each study presented These results were inconsistent and the data many indicators was put into the Stata analysis table This result Therefore, the author conducted a selection of evaluated the dispersion of data sets and it can the lowest correlation indicators the be seen that the studies had a high dispersion combined study Of the 18 studies, 15 studies (p < 0.000) (Figure 2) Specifically, the results included HR for both colorectal cancer in of the analysis by the random method was general; one for colon (colon, proximal, distal); included in pooled estimation, odds ratio one for result of three types of CRC (colon, (hazard ratio) = 1.16; CI (1.08 - 1.27) and p < rectal and CRC) and one for gender (both for 0.000, (Figure 2, Table 4) different RR and HR for Table Combined analyses results of fixed and random methods Method Random Pooled estimation 95% confidence interval 1.16 1.08 1.27 Asymptotic z-value 4.131 p-value 0.000 Number of analyses 23 Test for heterogeneity: Q = 128.044 on 22 degrees of freedom (p = 0.000) Moment-based estimate of between studies variance = 0.021 Although the degree of dispersion was high when selecting 23 indices from 18 studies, the pooled estimation from the Random methods were similar (statistically significant) After a meta-analysis of 23 indicators of 18 studies, it was concluded that smoking increases the risk of colorectal cancer JMR 116 E3 (7) - 2018 93 JOURNAL OF MEDICAL RESEARCH Figure Combined estimation of 23 studies IV DISCUSSION The research of David Stewart Morrison et tal cancer survival and the first study to al and T Boy et al found no convincing prospectively collect both pre- and post- relationship between smoking and colorectal diagnosis smoking information In this cohort cancer mortality [10] and the remaining three study of colorectal cancer survivors, smoking studies found no association between current before or after cancer diagnosis was associ- smoking and survival in colorectal cancer ated with higher risk of mortality resulting from patients [30 - 32] A recent meta-analysis of colorectal cancer [34] According to a recent Liang et al reported that current smokers had meta-analysis from Walter et al, smoking is higher colorectal cancer mortality compared associated with poorer long-term prognosis with never-smokers, but the absence of any after colorectal cancer diagnosis Specifically, significant association between former smok- the risk of all-cause mortality was higher for ers and colorectal cancer mortality or between current smoking at all time points (HR, 1.26; smoking and site specific cancer mortality 95% CI, 1.15 to 1.37) [35] We found a greater suggested that further research was needed than two-fold risk of all-cause mortality for both [33] The research of Baiyu Yang et al is one pre- and post-diagnosis smoking compared of the largest studies of smoking and colorec- with never smoking and lower though still sta- 94 JMR 116 E3 (7) - 2018 JOURNAL OF MEDICAL RESEARCH tistically significant associations with both risk estimate for former smokers in the current pre- and post- diagnosis former smoking This study is likely a reflection of the fact that nearly result is similar to the research of Tao L et al half of the former smokers in our study popula- [28] Only six other studies have examined the tion quit smoking more than 20 years before association between smoking and colorectal joining the cohort, by which time their risk ap- cancer–specific mortality[15; 36 - 40]; of these, pears to no longer be elevated Interestingly, two studies with sample sizes comparable to the most recent and one of the largest studies ours [37; 38] found current smoking to be as- conducted to date reported no association sociated with significantly higher colorectal between age at smoking initiation and colorec- cancer–specific mortality, consistent with our tal cancer risk among members of the EPIC results However, the previous RRs were cohort [46] In a recent meta-analysis, Liang lower than the RRs in our study, with pre- reported that for each 10-year delay in smok- diagnosis smoking associated with an RR of ing initiation, there was a 4.4% reduction in 1.30 in a study of patients with colorectal can- risk ratios for colorectal cancer [33] cer in Washington state and an RR of 1.46 The degree to which smoking-related colo- among patients with colon cancer in a large rectal cancer risks are similar among men and US cohort [37; 38] Another study found a women has been a matter of debate Initially, greater than two-fold higher risk of colorectal the preponderance of data seemed to suggest cancer–specific mortality comparing current that the effect of smoking was either limited to, smokers with former or never-smokers com- or at least stronger, among men than among bined, and the remaining three studies found women [47] Explanations offered for this ap- no post- parent difference have included both limita- diagnosis current and ever smoking with colo- tions in exposure potential (given the apparent rectal however, long latency) as well as real sex-related bio- these analyses were based on relatively logic differences potentially arising from differ- smaller sample sizes [15; 36; 39; 40] The ential interactions between smoking and pro- study of Ali Ahmadi et al illustrated that smok- tective endogenous estrogens, body mass ing increased the risk of death in these pa- index, and/or abdominal adiposity [42] Two tients, which is consistent with a study in the recent meta-analyses of prospective cohort United States that reported smoking increased studies on this topic reported that risks for cur- the mortality risk after CRC diagnosis [37] rent smoking continued to be higher among association between cancer–specific pre- mortality; and The colorectal cancer risk estimated for men than among women [42; 43], although smoking status from the study of Hurley et al only one found these differences to be statisti- (HR = 1.28 for current smokers; HR = 1.10 for cally significant at the 0.05 level [42] In con- former smokers) [13] is consistent with find- trast, a meta-analyses that included both co- ings from a number of recently published meta hort and case–control studies published during -analysis on this topic in which summary the same time period reported no evidence for measures of risk have ranged from 1.12 to differences in risk by sex [41] More recent 1.26 for current smokers and 1.18 to 1.20 for findings from the European Prospective Inves- former smokers [41 - 45] The marginally lower tigation Into Cancer [46]and the Cancer Pre- JMR 116 E3 (7) - 2018 95 JOURNAL OF MEDICAL RESEARCH vention Study II [9], both of which reported no ated with a significant increased risk of colo- differences in risk by sex, were not included in rectal cancer [44] but the meta-analysis of these meta-analyses Regardless of whether Constance M Johnson et al in 2013 indicated risks are higher in men than in women, there that cigarette smoking was associated with is now convincing evidence that risks are ap- moderately increased risk of CR (RR = 1.06, parent in women Along with the elevated risks 95% CI: 1.03 - 1.08 for pack- years) [51] found in this study and those reported among the female participants in the EPIC and CPS-II Limitations cohorts, elevated risks also have been re- To our knowledge, no literature review has ported among members of the Norwegian been conducted on the association between Women and Cancer Study [48] and the tobacco smoking and colorectal cancer since Women's Health Initiative [49], both large well- our earlier review in 2013 The confidence in conducted prospective cohort studies among the effects estimates in review is affected by a women The Norwegian study, however, only number of limitations Indeed, we only de- observed an effect for rectal but not colon can- scribed the results of the selected studies by cer, a finding that also was reported among using a sensitive search strategy in Pub Med members of the Canadian Breast Screening and conducting screening and data extraction Study over 10 years ago [50] independently and in duplicate Most studies The meta-analysis of Botteri et al in 2008 not give a precise percentage of the num- which analyzed one hundred and six observa- ber of smokers, and the groupings of smoking tional studies found that cigarette smoking is status are different and depend on the re- significantly associated with colorectal cancer search questions asked by the authors incidence and mortality but the association was stronger for cancer of the rectum than of the colon [41] Some of the studies that produce the HR index have been calibrated but are corrected by different factors so we were not able to The meta-analysis of Tsoi et al included 28 conduct a meta-analysis for all outcomes One prospective cohort studies in 2009 showing reason was the high level of heterogeneity, as that smoking was associated with a signifi- was the case for the quality of life outcome cantly increased risk of CRC Current smokers Another reason was that we could not pool had a modestly higher risk of CRC than never several outcomes derived from the same smokers and former smokers still carried a study, different smoking status, duration and higher CRC risk than never smokers In addi- type of CRC The study results not cover tion, the associated risk was higher for men other life style factors and information on mo- and rectal cancers and the increased risk of lecular subtypes Additional studies of our find- CRC was related to cigarettes per day, longer ings include the need for further research on years of smoking, or larger pack years [42] this topic by conducting more cohort studies to Another meta-analysis including 103 co- clearly determine the effects of smoking status hort studies of Huxley et al in 2009 indicated on the types and stages of colorectal cancer that smoking may be a lifestyle factor associ- and the factors that can be combined 96 JMR 116 E3 (7) - 2018 JOURNAL OF MEDICAL RESEARCH V CONCLUSION Patterns of Tobacco Smoking and Tobacco Control Policies European Association of In conclusion, this meta-analysis demonstrates that smoking shows a statistically significant risk of CRC Male smokers and current smokers had a higher colorectal cancer mortality compared with never smokers ACKNOWLEDGMENTS Urology, - 16 Bray F Torre LA, Siegel RL (2015) Global cancer statistics, 2012 65, 87 Ho JW1, Lam TH, Tse CW et al (2004) Smoking, drinking and colorectal cancer in HongKong Chinese: a case-control study Int J Cancer, 109, 587 - 597 The present work was the part of a mas- Hannan LM1, Jacobs EJ, Thun MJ et ter’s thesis of the course named “One Health” al (2009) The association between cigarette at Hanoi Medical University The protocol and smoking and risk of colorectal cancer in a completed thesis was approved by a scientific large prospective cohort from the United committee of the university States American association for cancer research REFERENCES 10 Morrison DS., Lam TH (2013) Behavioural and metabolic risk factors for mortal- World Health Organization (2011) WHO REPORT on the Global Tobacco Epidemic, 2011 Warning about the dangers of tobacco Centers for Disease Control and Prevention U.S Department of Health and Human Services (2010) Surgeon General Report How tobacco smoke causes disease World Health Organization (2008) WHO report on the global tobacco epidemic: The MPOWER package, Geneva, Switzerland, WHO Library Cataloguing-in-Publication Data World Health Organization (2014) Global health estimates: deaths by cause, age, sex, and country, 2000-2012, World Health Organization, Geneva ity from colon and rectum cancer: analysis of data from the Asia-Pacific Cohort Studies Collaboration Asian Pac J Cancer Prev, 14(2), 1083 - 1087 11 Yang B, Susan M Gapstur, Victoria Stevens et al (2015) Active Smoking and Mortality Among Colorectal Cancer Survivors: The Cancer Prevention Study II Nutrition Cohort JOURNAL OF CLINICAL ONCOLOGY, 33(8), 952 12 Steins Bisschop Phòng Cơng nghệ thơng tin., Emaus MJ (2014) Weight change later in life and colon and rectal cancer risk in participants in the EPIC-PANACEA study Am J Clin Nutr, 99(1), 139 - 47 13 Susan Hurley., Debbie Goldberg., David O et al (2013) Risk of colorectal can- World Health Organization (2017) cer associated with active smoking among WHO REPORT ON THE GLOBAL TOBACCO female teachers Cancer Causes Control, 24 EPIDEMIC, 2017 Monitoring tobacco use and (7), 1291 - 1304 prevention policies, Geneva, Switzerland 14 Vogtmann E., Hong-Lan Li (2013) Michal Stoklosa., Farhad Islami., Jef- Fruit and vegetable intake and the risk of colo- frey Drope et al (2015) Global and Regional rectal cancer: Results from the Shanghai JMR 116 E3 (7) - 2018 97 JOURNAL OF MEDICAL RESEARCH Men's Health Study Cancer Causes Control, rectal Cancer by ESR2 Protein Expression 24(11), 1935 - 1945 Level in a Population-Based Cohort of Older 15 Boyle T., Platell C(2013) Lifestyle factors associated with survival after colorectal cancer diagnosis Br J Cancer, 109(3), 814 – 822 Women Cancer Epidemiol Biomarkers Prev, 24(4), 713 - 719 24 Parajuli R., Eivind Bjerkaas., Aage Tverdal et al (2014) Smoking increases rec- 16 Walter V., Hoffmeister M (2015) tal cancer risk to the same extent in women as Smoking and survival of colorectal cancer pa- in men: results from a Norwegian cohort study tients: population-based study from Germany BMC Cancer, 14, 321 Int J Cancer, 137(6), 1433 - 1445 25 Ahmadi A., Mosavi-Jarrahi A., Pour- 17 Parajuli R., Bjerkaas E., Tverdal A hoseingholi MA et al (2015) Mortality deter- at al (2013) The Increased Risk of Colon minants in colorectal cancer patients at differ- Cancer Due to Cigarette Smoking May Be ent grades: a prospective, cohort study in Iran Greater in Women than Men Cancer Epide- Asian Pac J Cancer Prev, 16(3), 1069 - 1072 miol Biomarkers Prev, 22(5), 862 - 71 26 Lin CC., Kuang-Wei Huang., Jiing- 18 Erdrich J., Xuehong Zhang, Edward Chyuan Luo et al (2014) Hypertension is an Giovannucci et al (2016) Proportion of Colon important predictor of recurrent colorectal ade- Cancer Attributable to Lifestyle in a Cohort of noma after screening colonoscopy with ade- US Women Cancer Causes Control, 26(9), noma polypectomy J Chin Med Assoc, 77 1271 - 1279 (10), 508 - 512 19 Aleksandrova K., Tobias Pischon., 27 Burón Pust A., Rupert Alison., Mazda Jenab (2014) Combined impact of Roger Blanks et al (2017) Heterogeneity of healthy lifestyle factors on colorectal cancer: a colorectal cancer risk by tumour characteris- large European cohort study, BMC Med, 12, tics: Large prospective study of UK women Int 168 J Cancer, 140(5), 1082 - 1090 20 Amri R., Bordeianou LG., Sylla P et 28 Tao L., Renwei Wang., Yu-Tang Gao al (2015) Does active smoking induce he- et al (2013) Impact of postdiagnosis smoking matogenous metastatic spread in colon can- on long-term survival of cancer patients: the cer? Am J Surg, 210(5), 930 - 932 Shanghai cohort study Cancer Epidemiol Bio- 21 Liu D.,Li Q., Yang Z et al (2013) As- markers Prev, 22(12), 2404 – 2411 sociation of body mass index and smoking on 29 Nishihara R., Morikawa T., Kuchiba outcome of Chinese patients with colorectal A et al (2013) A Prospective Study of Dura- cancer World J Surg Oncol, 11, 271 tion of Smoking Cessation and Colorectal 22 Poomphakwaen K,Promthet S, Su- Cancer Risk by Epigenetics-related Tumor wanrungruang K et al (2015) Risk Factors Classification Am J Epidemiol, 178(1), 84 -100 for Colorectal Cancer in Thailand Asian Pac J Cancer Prev, 16(14), 6105 - 6109 30 McCleary NJ., Niedzwiecki D., Donna Hollis D et al (2010) Impact of smok- 23 Tillmans LS., Robert A., Vierkant., ing on patients with stage III colon cancer: Alice H et al (2015) Associations between Results from CALGB 89803 Cancer, 116(4), Environmental Exposures and Incident Colo- 957 - 966 98 JMR 116 E3 (7) - 2018 JOURNAL OF MEDICAL RESEARCH 31 Nordenvall C., Nilsson PJ., Ye W et 39 Richards CH., Leitch EF., Horgan al (2013) Tobacco use and cancer survival: a PG et al (2010) The relationship between cohort study of 40,230 Swedish male con- patient physiology, the systemic inflammatory struction workers with incident cancer Int J response and survival in patients undergoing Cancer, 132(1), 155 - 161 curative resection of colorectal cancer Br J 32 Park SM., Lim MK., Shin SA et al Cancer, 103(9),1356 - 1361 (2006) Impact of prediagnosis smoking, alco- 40 Munro AJ., Bentley AH., Ackland C hol, obesity, and insulin resistance on survival at al (2006) Smoking compromises cause- in male cancer patients: National Health Insur- specific survival in patients with operable colo- ance Corporation Study J Clin Oncol, 24(31), rectal cancer Clin Oncol , 18(6), 436 - 440 5017 - 5024 33 Liang PS., Chen T-Y., Giovannucci E et al (2009) Cigarette smoking and colorec- 41 Botteri E1., Iodice S., Bagnardi V et al (2008) Smoking and colorectal cancer: a meta-analysis JAMA, 300, 2765 - 2778 tal cancer incidence and mortality: systematic 42 Tsoi KK., Pau CY., Wu WK et al review and meta-analysis Int J Cancer, 124, (2009) Cigarette smoking and the risk of colo- 2406 - 2015 rectal cancer: a meta-analysis of prospective 34 Yang B., Jacobs EJ., Gapstur SM at al (2015) Active smoking and mortality among cohort studies Clin Gastroenterol Hepatol, (6), 682 - 688 colorectal cancer survivors: the Cancer Pre- 43 Huxley RR1., Ansary-Moghaddam A., vention Study II nutrition cohort J Clin Oncol, Clifton P et al (2009) The impact of dietary 33(8), 885 - 893 and lifestyle risk factors on risk of colorectal 35 Walter V., Jansen L., Hoffmeister et al (2014) Smoking and survival of colorectal cancer patients: systematic review and metaanalysis Ann Oncol, 25(8),1517 - 1525 36 Warren GW., Kasza KA., Reid ME et cancer: a quantitative overview of the epidemiological evidence Int J Cancer, (125), 171 - 180 44 Huxley RR., Ansary-Moghaddam A., Clifton P et al (2009) The impact of dietary and lifestyle risk factors on risk of colorectal al (2013) Smoking at diagnosis and survival cancer: a quantitative overview of the in cancer patients Int J Cancer, 132(2), epidemiological evidence Int J Cancer, 125 401 - 410 (1), 171 - 180 37 Phipps AI., Baron J., Newcomb PA 45 Gong J., Hutter C., Baron JA et al (2011) Prediagnostic smoking history, alcohol (2012) A pooled analysis of smoking and co- consumption, and colorectal cancer survival: lorectal cancer: timing of exposure and inter- the Seattle Colon Cancer Family Registry actions with environmental factors Cancer Cancer, 117(21), 4948 - 4957 Epidemiol Biomarkers Prev, 21(11),1974 - 85 38 Pelser C., Arem H., Pfeiffer RM et al 46 Leufkens AM, Van Duijnhoven FJ, (2014) Prediagnostic lifestyle factors and sur- Siersema PD et al (2011) Cigarette smoking vival after colon and rectal cancer diagnosis in and colorectal cancer risk in the European the National Institutes of Health (NIH)-AARP Prospective Investigation into Cancer and Nu- Diet and Health Study Cancer, 120(10), 1540 trition study Clin Gastroenterol Hepatol, - 1547 (2):137 - 144 JMR 116 E3 (7) - 2018 99 JOURNAL OF MEDICAL RESEARCH 47 Giovannucci E (2001) An updated ing and colorectal cancer in the Women’s review of the epidemiological evidence that Health Initiative J Natl Cancer Inst, 99(22), cigarette smoking increases risk of colorectal 1729 - 1735 cancer Cancer Epidemiol Biomarkers Prev, 50 Terry PD., Miller AB., Rohan TE (10), 725 - 731.Hepatol, 2009 7(6), 682 - 688 (2002) Prospective cohort study of cigarette 48 Gram IT., Braaten T., Lund E (2009) smoking and colorectal cancer risk in women Cigarette smoking and risk of colorectal cancer among Norwegian women Cancer Causes Control, 20(6), 895 - 903 49 Paskett ED., Reeves KW., Rohan TE (2007) Association between cigarette smok- 100 Int J Cancer, 99(3), 480 - 483 51 Johnson CM1., Wei C., Ensor JE et al (2013) Meta-analyses of Colorectal Cancer Risk Factors Cancer Causes Control, 24(6), 1207 - 1222 JMR 116 E3 (7) - 2018 ... incidence and mortality: systematic 42 Tsoi KK., Pau CY., Wu WK et al review and meta- analysis Int J Cancer, 124, (2009) Cigarette smoking and the risk of colo- 2406 - 2015 rectal cancer: a meta- analysis. .. with smoking increases the risk of colorectal cancer HR and RR, although each study presented These results were inconsistent and the data many indicators was put into the Stata analysis table... T-Y., Giovannucci E et al (2009) Cigarette smoking and colorec- 41 Botteri E1., Iodice S., Bagnardi V et al (2008) Smoking and colorectal cancer: a meta- analysis JAMA, 300, 2765 - 2778 tal cancer