Gastroenterology
Volume 134, Issue 2 , Pages 388-395.e3, February 2008

Cigarette Smoking and Adenomatous Polyps: A Meta-analysis

  • Edoardo Botteri

      Affiliations

    • Division of Epidemiology and Biostatistics, European Institute of Oncology, Milan, Italy
    • Corresponding Author InformationAddress requests for reprints to: Edoardo Botteri, MD, Division of Epidemiology and Biostatistics, European Institute of Oncology, Via Ripamonti 435, 20141, Milan, Italy. fax: (39) 02-57489922.
    • ,
  • Simona Iodice

      Affiliations

    • Division of Epidemiology and Biostatistics, European Institute of Oncology, Milan, Italy
    • ,
  • Sara Raimondi

      Affiliations

    • Division of Epidemiology and Biostatistics, European Institute of Oncology, Milan, Italy
    • ,
  • Patrick Maisonneuve

      Affiliations

    • Division of Epidemiology and Biostatistics, European Institute of Oncology, Milan, Italy
    • ,
  • Albert B. Lowenfels

      Affiliations

    • Department of Surgery and Department of Community and Preventive Medicine, New York Medical College, Valhalla, New York

Received 31 August 2007; accepted 25 October 2007. published online 05 November 2007.

Article Outline

Background & Aims: Through the past 2 decades, a consistent association between cigarette smoking and colorectal adenomatous polyps, recognized precursor lesions of colorectal cancer, has been shown. We performed a meta-analysis to provide a quantitative pooled risk estimate of the association, focusing on the different characteristics of the study populations, study designs, and clinical feature of the polyps. Methods: We performed a comprehensive literature search of studies linking cigarette smoking and adenomas. We used random effects models to evaluate pooled relative risks and performed dose-response, heterogeneity, publication bias, and sensitivity analyses. Results: Forty-two independent observational studies were included in the analysis. The pooled risk estimates for current, former, and ever smokers in comparison with never smokers were 2.14 (95% confidence interval [CI], 1.86–2.46), 1.47 (95% CI, 1.29–1.67), and 1.82 (95% CI, 1.65–2.00), respectively. The association was stronger for high-risk adenomas than for low-risk adenomas. Studies in which all controls underwent full colonoscopy showed a higher risk compared with studies in which some or all controls underwent partial colon examination. Conclusions: This meta-analysis provides strong evidence of the detrimental effect of cigarette smoking on the development of adenomatous polyps. Smoking is important for both formation and aggressiveness of adenomas.

Abbreviations used in this paper: CI, confidence interval, CRC, colorectal cancer, RR, relative risk

 

See editorial on page 617; See Gupta S et al on page 220 in CGH.

Colorectal cancer (CRC) is the third most common form of cancer and the fourth most frequent cause of cancer deaths worldwide. More than 1 million new cases of CRC occur annually, and nearly 530,000 individuals die from CRC every year.1 Similar to other epithelial malignancies, CRC is a heterogeneous disease with respect to tumor phenotype, risk factors, genetic predisposition, response to treatment, and outcome. Identifying genetic and environmental risk factors for CRC might improve our understanding of its etiology, and thereby contribute to its prevention by targeting screening and other preventive measures to high-risk individuals.

Tobacco use is known to cause many types of cancers, including some in organs not directly in contact with smoke.2 Tobacco contains a large number of carcinogens that may bind to DNA and form adducts, potentially causing irreversible genetic damage to the normal colorectal mucosa. In addition, tobacco smoke contains many procarcinogens, which require metabolic activation to form DNA adducts, induce mutations, and initiate carcinogenesis.3, 4 Evidence of a role for tobacco smoking in the development of CRC still is debatable, and so far it is not considered as an established risk factor for CRC by the International Agency for Research on Cancer.5

Cigarette smoking has been more consistently associated with colorectal adenomatous polyps,6 which are recognized precursor lesions of CRC,7, 8, 9, 10 than with CRC itself. Two possible explanations for this paradox are as follows: (1) the association between cigarette smoking and polyps may be stronger with nonprogressing adenomas, such as those that are smaller and less villous; and (2) the latency period to uncover an association between cigarette smoking and CRC is longer than the follow-up duration of several cohort studies.11, 12

Despite the apparent evidence of an association between smoking and adenomas, we performed an exhaustive meta-analysis combining the evidence published in the past 2 decades to provide a summary risk estimate and to emphasize the consistency of the studies. Another aim of the study was to assess whether or not the risk varied according to different characteristics of the study populations, study designs, or clinical features of the polyps. A final aim of the study was to establish whether the type of examination performed (full vs partial colonoscopy) in the individual studies could have influenced the single risk estimates.

Back to Article Outline

Materials and Methods 

Definition of Exposure and Outcome 

We studied the effect of current and past cigarette smoking on the risk of adenomatous polyps, limiting our analysis to histologically confirmed adenomatous polyps (adenomas) arising from the mucous membrane of either the colon or the rectum.

Search Strategy, Inclusion Criteria, and Data Abstraction 

We made a preliminary literature search for the following terms using PubMed: ([smoke OR cigarette OR tobacco OR smoking] AND [(adenomatous polyps OR adenoma OR polyps) AND (colon OR rectum OR colorectal OR colorectum OR colon rectum)]) OR (“adenomatous polyps”[MeSH major topic] AND “epidemiologic studies”[MeSH terms]). No restrictions were applied. In addition, we performed a manual review of references from all articles and reviews of interest on the topic to identify additional relevant studies. Only reports complying with the following inclusion criteria were included in the meta-analysis.

First, studies should contain the minimum information necessary to estimate the relative risk (RR) associated with tobacco smoking and a corresponding measure of uncertainty (ie, 95% confidence interval [CI], standard error, variance, or P value of the significance of the estimate).

Second, studies should be independent. In case of multiple reports on the same population or subpopulation, we considered the estimates from the most recent or most informative report.

Third, study populations should be as homogeneous as possible, and not be affected by a particular disease that could have affected the smoking-related adenoma risk. In particular, we excluded studies conducted in patients with any hereditary colorectal cancer syndromes, chronic inflammatory bowel disease, history of colorectal polyps or cancer, or previous bowel resection.

Fourth, if cases of hyperplastic polyps, malignant polyps, or CRC were reported in the study, the report should present separate information for adenomatous polyps.

When available, we used adjusted estimates and estimates based on population-based controls. All articles were reviewed independently and cross-checked by 3 investigators (E.B., S.I., and S.R.). Disagreements were resolved by consensus among the 3 reviewers.

Data Analysis 

We used random effects models with restricted maximum likelihood estimate to evaluate summary relative risks. Homogeneity of effects across studies was assessed using the χ2 statistic. Subgroup analyses and meta-regressions were performed to investigate between-study heterogeneity, which we considered statistically significant when the P value was .10 or less. Sensitivity analysis was performed to evaluate whether results were influenced by a single or a group of studies.

We ignored the distinction between various measures of RR (ie, odds ratio and RR) on the assumption that tobacco-related adenomas are sufficiently rare.13 When several risk estimates were retrieved from a single study (ie, separate estimates for proximal and distal colon), we adjusted the pooled estimates for intrastudy correlation when several risk estimates were retrieved from a single study (ie, separate estimates for proximal and distal colon).14

In the dose-response analysis, we considered doses expressed in pack-years and we used a linear model according to the method proposed by Greenland and Longnecker.15 For the highest open categories, we considered 60 pack-years as the maximum consumption.

Publication bias was evaluated by funnel plots and quantified by the Egger’s test.16

All analyses were performed with SAS (version 8.02; SAS Institute, Cary, NC) and STATA software (version 8.2; Statacorp LP, College Station, TX).

Back to Article Outline

Results 

From PubMed we identified and screened 783 abstracts. Only 125 articles were considered of interest and full text was retrieved for detailed evaluation. References of all 125 articles were reviewed, but no additional relevant studies were identified. Forty-two independent case-control or nested case-control, population-based studies that met the inclusion criteria were included in the final analysis (Table 1). For 4 studies, the risk estimates for the main and subgroup analyses were retrieved from 2 separate publications.17, 18, 19, 20, 21, 22, 23, 24 Overall, 15,354 cases and 100,011 controls were analyzed.

Table 1. Description of the Included Studies
StudyYear of publicationAreaSmoking classesCases/controls
Demers et al391988United StatesC94/1134
Kikendall et al401989United StatesC,F,E98/87
Kato et al411990JapanC,F525/578
Cope et al421991EuropeC66/86
Monnet et al431991EuropeC,F,E103/108
Shahangian et al441991United StatesC,F,E22/47
Zahm et al451991United StatesC,F,E31/470
Kune et al351992AustraliaC29/348
Lee et al321992United StatesE271/457
Clark et al461993United StatesC,F,E28/20
Olsen and Kronborg471993EuropeC,F,E171/362
Giovannucci et al341994United StatesE,C499/7968
Giovannucci et al331994United StatesE,C498/11,645
Boutron et al251995EuropeE362/427
Honjo et al17a1992JapanC,F116/930
Honjo et al181995JapanE504/3101
Martinez et al481995United StatesC,F,E157/480
Lubin et al491997IsraelC,F196/196
Terry and Neugut111998United StatesE270/508
Nagata et al501999JapanC,F,E242/26,365
Almendingen et al272000EuropeC,F,E87/35
Breuer-Katschinski et al262000EuropeC,F,E182/182
Hoshiyama et al512001JapanC,F,E105/84
Ulrich et al522001United StatesC,F,E530/649
Cardoso et al532002South AmericaC,F,E123/212
Erhardt et al542002EuropeC,F,E207/223
Voskuil et al552002EuropeC,F,E57/65
Anderson et al302003United StatesE408/654
Sparks et al562004United StatesC,F,E513/606
Inoue et al19a2000JapanC,F205/220
Toyomura et al202004JapanE754/1547
Gong et al572005United StatesC163/212
Jiang et al582005JapanE224/230
Kim et al592005South KoreaE98/468
Tranah et al23a2004United StatesE654/947
Tranah et al242005United StatesE901/1239
Tiemersma et al21a2004EuropeC,F431/432
van den Donk et al222005EuropeE768/709
Ji et al312006United StatesC,F,E2225/30,848
Larsen et al292006EuropeC,F,E443/3436
Mitrou et al602006EuropeC,F,E809/873
Otani et al612006JapanE777/729
Reid et al622006United StatesC,F,E160/882
Skjelbred et al282006EuropeE827/332
Stern et al632006United StatesC,F,E804/845
Ashktorab et al642007United StatesC,F,E23/35

C, current; F, former; E, ever.

aThe study is not independent from the following one, but it provides additional information for subgroup analysis.

Studies were published between 1988 and June 2007; 20 were conducted in the United States, 12 in Europe, 8 in Asia, 1 in South America, and 1 in Australia. Forty-one were written in English, and 1 was written in Korean with the abstract and tables in English.

The procedure for colorectal examination varied among studies. It was complete in 26 studies (total colonoscopy in 25, and sigmoidoscopy combined with barium edema and a radiograph of the entire colorectum in 1) and partial in 16 studies (only sigmoidoscopy in all or some patients).

Quantitative Data Synthesis 

The pooled risk estimate for current vs never smokers, based on 33 studies, was 2.14 (95% CI, 1.86–2.46; Table 2, supplementary Figure 1; see supplementary material online at www.gastrojournal.org). The pooled risk estimate for former vs never smokers, based on 27 studies, was 1.47 (95% CI, 1.29–1.67; Table 2, supplementary Figure 2; see supplementary material online at www.gastrojournal.org). The pooled risk estimate for ever vs never smokers, based on 36 studies, was 1.82 (95% CI, 1.65–2.00; Table 2; Figure 1). We found significant heterogeneity among the studies for all classes of smoking (P < .001).

Table 2. Pooled Estimates of the Association Between Cigarette Smoking and Adenomas
StrataRRa (95% CI)No. of studiesP value heterogeneityI2
Smoking status
Current2.14(1.86–2.46)33<.00158%
Former1.47(1.29–1.67)27<.00157%
Ever1.82(1.65–2.00)36<.00177%
Dose response (ever smoker) per 10 packs-yearsb1.13(1.09–1.18)19<.00170%

I2, percentage of total variation across studies that is attributable to heterogeneity rather than to chance.

aReferences category “never smokers.”

bRisk for an individual who has smoked 10 pack-years.

  • View full-size image.
  • Figure 1. 

    Forest plot for ever smokers vs never smokers. The partial endoscopy group is composed of studies in which some or all controls underwent partial colon examination. The full colonoscopy group is composed of studies in which all controls underwent complete colon examination. *Estimates for men; **estimates for women.

We report the dose-response analysis in Table 2. Assuming a linear increase of the risk with increasing smoking, ever smokers had a 13% (95% CI, 9%–18%) increasing risk of presenting adenomatous polyps for every additional 10 pack-years smoked in comparison with never smokers. For example, an individual who smoked 1 pack of cigarettes per day for 50 years or 2 packs per day for 25 years has almost twice the probability of having an adenoma (RR, 1.88) in comparison with an individual who never smoked.

Geographic areas for which only 1 report was available (Australia, Israel, and South America) were excluded from the subgroup analysis on geographic areas (Table 3). The risk of adenoma for ever vs never smokers was lower in the United States (RR, 1.65; 95% CI, 1.44–1.89), intermediate in Europe (RR, 1.80; 95% CI, 1.53–2.13), and higher in Asia (RR, 2.18; 95% CI, 1.79–2.66), with indication of heterogeneity between geographic areas (P = .073). These differences were not observed for current and former smokers.

Table 3. Heterogeneity Analysis
FactorsStratificationCurrent vs never smokersFormer vs never smokersEver vs never smokers
RR(95% CI)No.P valueRR(95% CI)No.P valueRR(95% CI)No.P value
SexFemale2.06(1.60–2.66)6.8681.10(0.80–1.52)4.2091.91(1.54–2.35)8.489
Male2.02(1.64–2.50)131.41(1.15–1.73)91.80(1.50–2.16)14
Geographic areaEurope2.09(1.61–2.72)10.9741.54(1.23–1.93)9.5511.80(1.53–2.13)11.073
United States2.18(1.75–2.70)151.33(1.08–1.63)111.65(1.44–1.89)17
Asiaa2.17(1.54–3.04)51.56(1.14–2.12)72.18(1.79–2.66)7
Type of adenomaLow-risk adenoma1.52(1.22–1.90)6.0241.05(0.93–1.19)4.3451.82(1.58–2.10)9.099
High-risk adenoma2.04(1.56–2.66)61.17(0.97–1.42)32.10(1.79–2.47)8
Size of adenoma<10 mm1.69(0.51–5.55)5.3601.01(0.74–1.38)3.3521.93(1.64–2.27)6.682
≥10 mm2.02(0.62–6.56)41.17(0.77–1.79)32.02(1.73–2.36)6
Examination in controlsFull colonoscopy2.22(1.86–2.67)19.5751.61(1.37–1.89)17.0882.06(1.79–2.38)23.090
Partial endoscopy2.05(1.68–2.51)141.31(1.11–1.56)101.68(1.40–2.03)13
Type of controlSymptomatic2.10(1.63–2.70)12.9231.57(1.28–1.93)11.2861.78(1.48–2.14)11.942
Asymptomatic2.13(1.78–2.55)171.37(1.17–1.60)141.79(1.59–2.02)20
Site of adenomaProximal colon1.53(0.87–2.72)2.9331.23(0.70–2.16)2.7871.65(1.25–2.19)4.993
Distal colon1.68(1.23–2.30)71.13(0.80–1.59)41.64(1.37–1.96)7
Rectum1.72(0.92–3.22)21.39(0.75–2.60)21.68(1.10–12.57)3
Adjustment of estimatesAdjusted2.07(1.73–2.49)17.5971.32(1.17–1.49)17.0051.71(1.42–2.05)13.125
Not adjusted2.23(1.82–2.74)151.84(1.51–2.24)102.05(1.77–2.37)22

NOTE. P value tests between-study heterogeneity. Bold text indicates statistical significance.

aAsia includes Japan and South Korea.

Eleven studies21, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34 reported stratification for high-risk and low-risk adenomas. From 1 study29 it was possible to obtain only the estimate for low-risk adenomas (defined as tubular adenomas, size ≤10 mm, and without severe dysplasia) because advanced adenoma patients were analyzed together with CRC patients. One additional study35 reported data for high-risk adenomas only. Although the definition of high-risk adenoma differed from one report to another, the diameter size of the adenoma was a point in common: 10 mm or greater in 9 studies; 10 mm or greater and/or with villous or tubulovillous components and/or showing severe dysplasia in 2 studies; and 10 mm or greater and/or with villous or tubulovillous components and/or 3 or more adenomas in 1 study. The risk of high-risk adenoma was greater than the risk of low-risk adenomas for all 3 smoking classes, reaching a statistical significance for current smokers (RR, 2.04; 95% CI, 1.56–2.66; and 1.52; 95% CI, 1.22–1.90, respectively; P = .024) and for ever smokers (RR, 2.10; 95% CI, 1.79–2.47; and 1.82; 95% CI, 1.58–2.10, respectively; P = .099). The dimension of adenomas alone was not a source of heterogeneity, even if the pooled risk estimates for adenomas with a diameter of 10 mm or greater were consistently higher than those for adenomas with a diameter of less than 10 mm in all 3 smoking classes.

Studies in which all subjects (cases and controls) underwent full colonoscopy showed a higher risk compared with studies in which some or all controls underwent partial examination, with statistical significance for former smokers (RR, 1.61; 95% CI, 1.37–1.89; and 1.31; 95% CI, 1.11–1.56, respectively; P for heterogeneity = .088) and ever smokers (RR, 2.06; 95% CI, 1.79–2.38; and 1.68; 95% CI, 1.40–2.03, respectively; P for heterogeneity = .090).

Adjusted estimates were consistently lower than nonadjusted ones, this result being statistically significant for former smokers (RR, 1.32; 95% CI, 1.17–1.49; and 1.84; 95% CI, 1.51–2.24, respectively; P for heterogeneity = .005).

Presence/absence of symptoms or signs (diarrhea, bloating, abdominal pain, and fecal occult blood) in the control population, anatomic site of colon, publication year, and sex were not sources of heterogeneity.

Publication Bias and Sensitivity Analysis 

A funnel plot did not show evidence of publication bias for current smokers (P = .32; supplementary Figure 3; see supplementary material online at www.gastrojournal.org) whereas evidence of publication bias was present for former and for ever smokers (P < .001 for both; Figure 2; supplementary Figure 4; see supplementary material online at www.gastrojournal.org). In one single study,31 the largest in our meta-analysis, adjusted risks for former and ever smokers (RR, 1.1; 95% CI, 1.0–1.2; and RR, 1.2; 95% CI, 1.1–1.3, respectively) were much lower than the corresponding pooled risk estimates. After the exclusion of this study, there was no evidence of publication bias for any smoking class and the revised pooled risk estimates were higher: RR was 2.17 (95% CI, 1.87–2.51), 1.50 (95% CI, 1.32–1.72), and 1.84 (95% CI, 1.68–2.02) for current, former, and ever smokers, respectively.

Because some studies reported risk estimates for current and not for former smokers, to allow an unbiased comparison between the 2 smoking classes we also computed RR for current smokers in the 27 studies reporting both estimates: 2.12 (95% CI, 1.80–2.50).

Back to Article Outline

Discussion 

During the past 2 decades, several studies have suggested that cigarette smoking has a marked effect on the development of adenomatous polyps. The results from this meta-analysis, based on 42 independent studies, support and strengthen this evidence, showing pooled risk estimates of 2.1 (95% CI, 1.9–2.5) and 1.8 (95% CI, 1.7–2.0) for current vs never smokers and ever vs never smokers, respectively.

In contrast, the association between cigarette smoking and CRC has been more controversial. The usual explanation for this paradox is that the latency period to uncover an association between cigarette smoking and CRC, which may be more than 30 years,33, 34, 36 is longer than the follow-up times of several cohort studies. Another explanation, the so-called dilution effect, is that only a small subset of adenomas progress to cancer, and the effect of cigarette smoking may be stronger on nonprogressing adenomas, such as those that are small, solitary, and less villous. Two studies reporting higher estimates for low-risk adenomas than for high-risk adenomas support this hypothesis,21, 27 many others20, 25, 28, 30, 31, 34, 37 do not. In particular, a recent study by Toyomura et al20 showed a clear higher risk for large and multiple adenomas in every anatomic site of the colon in a dose-response fashion. In our meta-analysis the pooled estimate for high-risk adenomas was greater than the one for low-risk adenomas, with a statistically significant difference for current and ever smokers, refuting the dilution effect explanation of the paradox.

Terry and Neugut11 mentioned a third possibility: the inclusion of a high proportion of subjects with adenomas in the unscreened control groups of most CRC case-control studies. Given the consistent association found between smoking and adenoma, the misclassification of controls might have biased the estimates toward the null hypothesis of no association. Our subgroup analysis on the type of examination performed on controls indirectly supports this third hypothesis of the paradox: we showed that the risk of having an adenoma associated with cigarette smoking is significantly higher in studies in which controls underwent total colon examination in comparison with studies in which some or all controls underwent incomplete examination (sigmoidoscopy). In the latter studies there could be a misclassification of controls, resulting in a reduction of the risk estimates. The less complete the examination, the more significant the misclassification.

This third hypothesis also would help to explain the evidence of publication bias in our meta-analysis. One single study31 clearly influenced the result. It was by far the largest study (it counted more than 26% of all controls of the entire meta-analysis) and it reported much lower risk estimates for former and ever smokers than the corresponding pooled risk estimates. In this study endoscopic examination was stopped at the distal colon, allowing possible misclassification of controls and reduction of the true relative risk. After its exclusion there was no evidence of publication bias for any smoking class.

The risk of adenoma for ever vs never smokers was lower in the United States, intermediate in Europe, and higher in Asia. These differences were not observed for current and former smokers. Although the statistically significant heterogeneity for ever smokers could be owing to chance, it might depend on differential smoking cessation patterns in the various continents.

Although the deleterious health effects of tobacco smoking are abundant, smoking has not been considered so far in the stratification of subjects for CRC screening by the public authorities. Although some investigators38 have proposed lowering the age threshold for CRC screening in men because of the higher detection rate of advanced neoplasia as compared with women, others34 have suggested lowering the age threshold among long-term smokers regardless of sex. The results from this meta-analysis show that smokers are at higher risk, which should be considered in developing screening policies.

The large number of studies, and the consequent possibility of subgroup analyses, permitted us to better understand the effect of smoking on different types of adenomas in different subgroups, and to make some inferences in regards to the adenoma-CRC sequence.

A possible limitation of our study was the heterogeneity of the studies in regard to methodologies of diagnosis of polyps and adjustments of the estimates for potential confounders, which limits the generalization of the results. We tried to overcome this problem by providing subgroup analyses in more homogeneous subsets of studies.

In conclusion, this meta-analysis provides strong evidence for the detrimental effect of cigarette smoking on the development of adenomatous polyps. Because risk was significantly greater for high-risk adenomas, smoking may be important for both the formation and aggressiveness of adenomas.

Back to Article Outline

 

The authors would like to thank Cristiano Crosta for his helpful comments and William Russell-Edu for his valuable library assistance.

Back to Article Outline

References 

  1. Parkin DM, Bray F, Ferlay J, et al. Global cancer statistics, 2002. CA Cancer J Clin. 2005;55:74–108
  2. Gandini S, Botteri E, Iodice S, et al. Tobacco smoking and cancer: a meta-analysis. Int J Cancer. 2008;1:155–164
  3. Wogan GN, Hecht SS, Felton JS, et al. Environmental and chemical carcinogenesis. Semin Cancer Biol. 2004;14:473–486
  4. Hecht SS. Tobacco carcinogens, their biomarkers and tobacco-induced cancer. Nat Rev Cancer. 2003;3:733–744
  5. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Tobacco smoke and involuntary smoking. IARC Monogr Eval Carcinog Risks Hum. 2004;83:1–1438
  6. Giovannucci E. An updated review of the epidemiological evidence that cigarette smoking increases risk of colorectal cancer. Cancer Epidemiol Biomarkers Prev. 2001;10:725–731
  7. Fearon ER, Vogelstein B. A genetic model for colorectal tumorigenesis. Cell. 1990;61:759–767
  8. Hill MJ, Morson BC, Bussey HJ. Aetiology of adenoma—carcinoma sequence in large bowel. Lancet. 1978;1:245–247
  9. Hill MJ. European Organization for Cooperation in Cancer Prevention: research and policy for primary prevention of colorectal cancer and background of intervention trial. In:  Rozen P,  Reich CB,  Winawer SJ editor. Frontiers of gastrointestinal research. Volume 18. Large bowel cancer policy, prevention, research and treatment. Basel: Karger; 1991;p. 38–59
  10. Neugut AI, Jacobson JS, De V, et al. Epidemiology of colorectal adenomatous polyps. Cancer Epidemiol Biomarkers Prev. 1993;2:159–176
  11. Terry MB, Neugut AI. Cigarette smoking and the colorectal adenoma-carcinoma sequence: a hypothesis to explain the paradox. Am J Epidemiol. 1998;147:903–910
  12. Neugut AI, Terry MB. Cigarette smoking and microsatellite instability: causal pathway or marker-defined subset of colon tumors?. J Natl Cancer Inst. 2000;92:1791–1793
  13. Greenland S. Quantitative methods in the review of epidemiologic literature. Epidemiol Rev. 1987;9:1–30
  14. van Houwelingen HC, Arends LR, Stijnen T. Advanced methods in meta-analysis: multivariate approach and meta-regression. Stat Med. 2002;21:589–624
  15. Greenland S, Longnecker MP. Methods for trend estimation from summarized dose-response data, with applications to meta-analysis. Am J Epidemiol. 1992;135:1301–1309
  16. Egger M, Davey SG, Schneider M, et al. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315:629–634
  17. Honjo S, Kono S, Shinchi K, et al. Cigarette smoking, alcohol use and adenomatous polyps of the sigmoid colon. Jpn J Cancer Res. 1992;83:806–811
  18. Honjo S, Kono S, Shinchi K, et al. The relation of smoking, alcohol use and obesity to risk of sigmoid colon and rectal adenomas. Jpn J Cancer Res. 1995;86:1019–1026
  19. Inoue H, Kiyohara C, Marugame T, et al. Cigarette smoking, CYP1A1 MspI and GSTM1 genotypes, and colorectal adenomas. Cancer Res. 2000;60:3749–3752
  20. Toyomura K, Yamaguchi K, Kawamoto H, et al. Relation of cigarette smoking and alcohol use to colorectal adenomas by subsite: the self-defense forces health study. Cancer Sci. 2004;95:72–76
  21. Tiemersma EW, Bunschoten A, Kok FJ, et al. Effect of SULT1A1 and NAT2 genetic polymorphism on the association between cigarette smoking and colorectal adenomas. Int J Cancer. 2004;108:97–103
  22. van den Donk M, Buijsse B, van den Berg SW, et al. Dietary intake of folate and riboflavin, MTHFR C677T genotype, and colorectal adenoma risk: a Dutch case-control study. Cancer Epidemiol Biomarkers Prev. 2005;14:1562–1566
  23. Tranah GJ, Giovannucci E, Ma J, et al. Epoxide hydrolase polymorphisms, cigarette smoking and risk of colorectal adenoma in the Nurses’ Health Study and the Health Professionals Follow-up Study. Carcinogenesis. 2004;25:1211–1218
  24. Tranah GJ, Giovannucci E, Ma J, et al. APC Asp1822Val and Gly2502Ser polymorphisms and risk of colorectal cancer and adenoma. Cancer Epidemiol Biomarkers Prev. 2005;14:863–870
  25. Boutron MC, Faivre J, Dop MC, et al. Tobacco, alcohol, and colorectal tumors: a multistep process. Am J Epidemiol. 1995;141:1038–1046
  26. Breuer-Katschinski B, Nemes K, Marr A, et al. Alcohol and cigarette smoking and the risk of colorectal adenomas. Dig Dis Sci. 2000;45:487–493
  27. Almendingen K, Hofstad B, Trygg K, et al. Smoking and colorectal adenomas: a case-control study. Eur J Cancer Prev. 2000;9:193–203
  28. Skjelbred CF, Saebo M, Wallin H, et al. Polymorphisms of the XRCC1, XRCC3 and XPD genes and risk of colorectal adenoma and carcinoma, in a Norwegian cohort: a case control study. BMC Cancer. 2006;6:67
  29. Larsen IK, Grotmol T, Almendingen K, et al. Lifestyle as a predictor for colonic neoplasia in asymptomatic individuals. BMC Gastroenterol. 2006;6:5
  30. Anderson JC, Attam R, Alpern Z, et al. Prevalence of colorectal neoplasia in smokers. Am J Gastroenterol. 2003;98:2777–2783
  31. Ji BT, Weissfeld JL, Chow WH, et al. Tobacco smoking and colorectal hyperplastic and adenomatous polyps. Cancer Epidemiol Biomarkers Prev. 2006;15:897–901
  32. Lee WC, Neugut AI, Garbowski GC, et al. Cigarettes, alcohol, coffee, and caffeine as risk factors for colorectal adenomatous polyps. Ann Epidemiol. 1993;3:239–244
  33. Giovannucci E, Colditz GA, Stampfer MJ, et al. A prospective study of cigarette smoking and risk of colorectal adenoma and colorectal cancer in U.S. women. J Natl Cancer Inst. 1994;86:192–199
  34. Giovannucci E, Rimm EB, Stampfer MJ, et al. A prospective study of cigarette smoking and risk of colorectal adenoma and colorectal cancer in U.S. men. J Natl Cancer Inst. 1994;86:183–191
  35. Kune GA, Kune S, Watson LF, et al. Smoking and adenomatous colorectal polyps. Gastroenterology. 1992;103:1370–1371
  36. Heineman EF, Zahm SH, McLaughlin JK, et al. Increased risk of colorectal cancer among smokers: results of a 26-year follow-up of US veterans and a review. Int J Cancer. 1994;59:728–738
  37. Longnecker MP, Chen MJ, Probst-Hensch NM, et al. Alcohol and smoking in relation to the prevalence of adenomatous colorectal polyps detected at sigmoidoscopy. Epidemiology. 1996;7:275–280
  38. Regula J, Rupinski M, Kraszewska E, et al. Colonoscopy in colorectal-cancer screening for detection of advanced neoplasia. N Engl J Med. 2006;355:1863–1872
  39. Demers RY, Neale AV, Demers P, et al. Serum cholesterol and colorectal polyps. J Clin Epidemiol. 1988;41:9–13
  40. Kikendall JW, Bowen PE, Burgess MB, et al. Cigarettes and alcohol as independent risk factors for colonic adenomas. Gastroenterology. 1989;97:660–664
  41. Kato I, Tominaga S, Matsuura A, et al. A comparative case-control study of colorectal cancer and adenoma. Jpn J Cancer Res. 1990;81:1101–1108
  42. Cope GF, Wyatt JI, Pinder IF, et al. Alcohol consumption in patients with colorectal adenomatous polyps. Gut. 1991;32:70–72
  43. Monnet E, Allemand H, Farina H, et al. Cigarette smoking and the risk of colorectal adenoma in men. Scand J Gastroenterol. 1991;26:758–762
  44. Shahangian S, Fritsche HA, Hughes JI. Carcinoembryonic antigen in serum of patients with colorectal polyps: correlation with histology and smoking status. Clin Chem. 1991;37:651–655
  45. Zahm SH, Cocco P, Blair A. Tobacco smoking as a risk factor for colon polyps. Am J Public Health. 1991;81:846–849
  46. Clark LC, Hixson LJ, Combs GFJ, et al. Plasma selenium concentration predicts the prevalence of colorectal adenomatous polyps. Cancer Epidemiol Biomarkers Prev. 1993;2:41–46
  47. Olsen J, Kronborg O. Coffee, tobacco and alcohol as risk factors for cancer and adenoma of the large intestine. Int J Epidemiol. 1993;22:398–402
  48. Martinez ME, McPherson RS, Annegers JF, et al. Cigarette smoking and alcohol consumption as risk factors for colorectal adenomatous polyps. J Natl Cancer Inst. 1995;87:274–279
  49. Lubin F, Rozen P, Arieli B, et al. Nutritional and lifestyle habits and water-fiber interaction in colorectal adenoma etiology. Cancer Epidemiol Biomarkers Prev. 1997;6:79–85
  50. Nagata C, Shimizu H, Kametani M, et al. Cigarette smoking, alcohol use, and colorectal adenoma in Japanese men and women. Dis Colon Rectum. 1999;42:337–342
  51. Hoshiyama Y, Kono S, Sasaba T, et al. Relation of cigarette smoking, alcohol use, and dietary habits to colon adenomas: a case-control study in Saitama, Japan. Asian Pac J Cancer Prev. 2000;1:139–146
  52. Ulrich CM, Bigler J, Whitton JA, et al. Epoxide hydrolase Tyr113His polymorphism is associated with elevated risk of colorectal polyps in the presence of smoking and high meat intake. Cancer Epidemiol Biomarkers Prev. 2001;10:875–882
  53. Cardoso MA, Maruta LM, Kida AA, et al. Micronutrients and the risk of colorectal adenomas: a case-control study in Sao Paulo, Brazil. IARC Sci Publ. 2002;156:361–363
  54. Erhardt JG, Kreichgauer HP, Meisner C, et al. Alcohol, cigarette smoking, dietary factors and the risk of colorectal adenomas and hyperplastic polyps—a case control study. Eur J Nutr. 2002;41:35–43
  55. Voskuil DW, Kampman E, Grubben MJ, et al. Meat consumption and meat preparation in relation to colorectal adenomas among sporadic and HNPCC family patients in The Netherlands. Eur J Cancer. 2002;38:2300–2308
  56. Sparks R, Bigler J, Sibert JG, et al. TGFbeta1 polymorphism (L10P) and risk of colorectal adenomatous and hyperplastic polyps. Int J Epidemiol. 2004;33:955–961
  57. Gong Z, Xie D, Deng Z, et al. The PPAR{gamma} Pro12Ala polymorphism and risk for incident sporadic colorectal adenomas. Carcinogenesis. 2005;26:579–585
  58. Jiang J, Suzuki S, Xiang J, et al. Plasma carotenoid, alpha-tocopherol and retinol concentrations and risk of colorectal adenomas: a case-control study in Japan. Cancer Lett. 2005;226:133–141
  59. Kim CS, Kim MC, Cheong HK, et al. [The association of obesity and left colonic adenomatous polyps in Korean adult men.]. J Prev Med Pub Health. 2005;38:415–419
  60. Mitrou PN, Watson MA, Loktionov AS, et al. MTHFR (C677T and A1298C) polymorphisms and risk of sporadic distal colorectal adenoma in the UK Flexible Sigmoidoscopy Screening Trial (United Kingdom). Cancer Causes Control. 2006;17:793–801
  61. Otani T, Iwasaki M, Ikeda S, et al. Serum triglycerides and colorectal adenoma in a case-control study among cancer screening examinees (Japan). Cancer Causes Control. 2006;17:1245–1252
  62. Reid ME, Duffield-Lillico AJ, Sunga A, et al. Selenium supplementation and colorectal adenomas: an analysis of the nutritional prevention of cancer trial. Int J Cancer. 2006;118:1777–1781
  63. Stern MC, Siegmund KD, Conti DV, et al. XRCC1, XRCC3, and XPD polymorphisms as modifiers of the effect of smoking and alcohol on colorectal adenoma risk. Cancer Epidemiol Biomarkers Prev. 2006;15:2384–2390
  64. Ashktorab H, Begum R, Akhgar A, et al. Folate status and risk of colorectal polyps in African Americans. Dig Dis Sci. 2007;52:1462–1470

PII: S0016-5085(07)01997-X

doi:10.1053/j.gastro.2007.11.007

Refers to article:

  • Cigarette Smoking and the Colorectal Adenoma-Carcinoma Sequence

    Julian A. Abrams, Mary Beth Terry, Alfred I. Neugut
    Gastroenterology February 2008 (Vol. 134, Issue 2, Pages 617-619)

Gastroenterology
Volume 134, Issue 2 , Pages 388-395.e3, February 2008

Article Tools

* Image Usage & Resolution