Cited by 622Cancer Risks and FactorsColorectal Cancer Screening and DetectionObesity, Physical Activity, Diet

Obesity and Risk of Colorectal Cancer: A Systematic Review of Prospective Studies

Open access
Ma, Yanlei, Yang, Yongzhi, Wang, Feng, Zhang, Peng, Shi, Chenzhang, Zou, Yang, Qin, Huanlong·2013·PLoS ONE

Abstract

BACKGROUND: Mounting evidence indicates that obesity may be associated with the risk of colorectal cancer (CRC). To conduct a systematic review of prospective studies assessing the association of obesity with the risk of CRC using meta-analysis. METHODOLOGY/PRINCIPAL FINDINGS: Relevant studies were identified by a search of MEDLINE and EMBASE databases before January 2012, with no restrictions. We also reviewed reference lists from retrieved articles. We included prospective studies that reported relative risk (RR) estimates with 95% confidence intervals (CIs) for the association between general obesity [measured using body mass index (BMI)] or central obesity [measured using waist circumference (WC)] and the risk of colorectal, colon, or rectal cancer. Approximately 9, 000, 000 participants from several countries were included in this analysis. 41 studies on general obesity and 13 studies on central obesity were included in the meta-analysis. The pooled RRs of CRC for the obese vs. normal category of BMI were 1.334 (95% CI, 1.253-1.420), and the highest vs. lowest category of WC were 1.455 (95% CI, 1.327-1.596). There was heterogeneity among studies of BMI (P<0.001) but not among studies of WC (P=0.323). CONCLUSIONS: Both of general and central obesity were positively associated with the risk of CRC in this meta-analysis.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1371/journal.pone.0053916

Cites

5 of 5 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 65

  1. [1]Jemal A, Siegel R, Ward E, Hao Y, Xu J, et al (2008) Cancer statistics, 2008. CA Cancer J Clin 58: 71– 96. 18287387
  2. [2]Sung JJ, Lau JY, Goh KL, Leung WK (2005) Increasing incidence of colorectal cancer in Asia: implications for screening. Lancet Oncol 6: 871– 876. 16257795
  3. [3]Bianchini F, Kaaks R, Vainio H (2002) Overweight, obesity, and cancer risk. Lancet Oncol 3: 565– 574. 12217794
  4. [5]Terry P, Giovannucci E, Michels KB, Bergkvist L, Hansen H, et al (2001) Fruit, vegetables, dietary fiber, and risk of colorectal cancer. J Natl Cancer Inst 93: 525– 533. 11287446
  5. [6]Parr CL, Batty GD, Lam TH, Barzi F, Fang X, et al (2010) Body-mass index and cancer mortality in the Asia-Pacific Cohort Studies Collaboration: pooled analyses of 424,519 participants. Lancet Oncol 11: 741– 752. 20594911 PMC4170782
  6. [7]Park JY, Mitrou PN, Keogh RH, Luben RN, Wareham NJ, et al. (2011) Self-reported and measured anthropometric data and risk of colorectal cancer in the EPIC-Norfolk study. Int J Obes (Lond). 21427695
  7. [8]Odegaard AO, Koh WP, Yu MC, Yuan JM (2011) Body mass index and risk of colorectal cancer in Chinese Singaporeans: the Singapore Chinese Health Study. Cancer 117: 3841– 3849. 21815135 PMC3151024
  8. [9]Matsuo K, Mizoue T, Tanaka K, Tsuji I, Sugawara Y, et al. (2011) Association between body mass index and the colorectal cancer risk in Japan: pooled analysis of population-based cohort studies in Japan. Ann Oncol. 21597097
  9. [10]Levi Z, Kark JD, Barchana M, Liphshitz I, Zavdi O, et al. (2011) Measured Body Mass Index in Adolescence and the Incidence of Colorectal Cancer in a Cohort of 1.1 Million Males. Cancer Epidemiol Biomarkers Prev. 22056504
  10. [11]Hughes LA, Simons CC, van den Brandt PA, Goldbohm RA, van Engeland M, et al (2011) Body Size and Colorectal Cancer Risk After 16.3 Years of Follow-up: An Analysis From the Netherlands Cohort Study. Am J Epidemiol 174: 1127– 1139. 21984660
  11. [12]Oxentenko AS, Bardia A, Vierkant RA, Wang AH, Anderson KE, et al (2010) Body size and incident colorectal cancer: a prospective study of older women. Cancer Prev Res (Phila) 3: 1608– 1620. 20719902 PMC3005991
  12. [13]Bassett JK, Severi G, English DR, Baglietto L, Krishnan K, et al (2010) Body size, weight change, and risk of colon cancer. Cancer Epidemiol Biomarkers Prev 19: 2978– 2986. 20870733
  13. [14]Wang Y, Jacobs EJ, Patel AV, Rodriguez C, McCullough ML, et al (2008) A prospective study of waist circumference and body mass index in relation to colorectal cancer incidence. Cancer Causes Control 19: 783– 792. 18322811
  14. [16]Rapp K, Klenk J, Ulmer H, Concin H, Diem G, et al (2008) Weight change and cancer risk in a cohort of more than 65,000 adults in Austria. Ann Oncol 19: 641– 648. 18056917
  15. [17]Wang Y, Jacobs EJ, Teras LR, Pavluck AL, Rodriguez C, et al (2007) Lack of evidence for effect modification by estrogen of association between body mass index and colorectal cancer risk among postmenopausal women. Cancer Causes Control 18: 793– 799. 17619155
  16. [18]Reeves GK, Pirie K, Beral V, Green J, Spencer E, et al (2007) Cancer incidence and mortality in relation to body mass index in the Million Women Study: cohort study. BMJ 335: 1134. 17986716 PMC2099519
  17. [19]Lundqvist E, Kaprio J, Verkasalo PK, Pukkala E, Koskenvuo M, et al (2007) Co-twin control and cohort analyses of body mass index and height in relation to breast, prostate, ovarian, corpus uteri, colon and rectal cancer among Swedish and Finnish twins. Int J Cancer 121: 810– 818. 17455257
  18. [20]Adams KF, Leitzmann MF, Albanes D, Kipnis V, Mouw T, et al (2007) Body mass and colorectal cancer risk in the NIH-AARP cohort. Am J Epidemiol 166: 36– 45. 17449892
  19. [21]Samanic C, Chow WH, Gridley G, Jarvholm B, Fraumeni JF Jr (2006) Relation of body mass index to cancer risk in 362,552 Swedish men. Cancer Causes Control 17: 901– 909. 16841257
  20. [22]Pischon T, Lahmann PH, Boeing H, Friedenreich C, Norat T, et al (2006) Body size and risk of colon and rectal cancer in the European Prospective Investigation Into Cancer and Nutrition (EPIC). J Natl Cancer Inst 98: 920– 931. 16818856
  21. [23]MacInnis RJ, English DR, Hopper JL, Gertig DM, Haydon AM, et al (2006) Body size and composition and colon cancer risk in women. Int J Cancer 118: 1496– 1500. 16187280
  22. [24]MacInnis RJ, English DR, Haydon AM, Hopper JL, Gertig DM, et al (2006) Body size and composition and risk of rectal cancer (Australia). Cancer Causes Control 17: 1291– 1297. 17111261
  23. [25]Lukanova A, Bjor O, Kaaks R, Lenner P, Lindahl B, et al (2006) Body mass index and cancer: results from the Northern Sweden Health and Disease Cohort. Int J Cancer 118: 458– 466. 16049963
  24. [26]Larsson SC, Rutegard J, Bergkvist L, Wolk A (2006) Physical activity, obesity, and risk of colon and rectal cancer in a cohort of Swedish men. Eur J Cancer 42: 2590– 2597. 16914307
  25. [27]Bowers K, Albanes D, Limburg P, Pietinen P, Taylor PR, et al (2006) A prospective study of anthropometric and clinical measurements associated with insulin resistance syndrome and colorectal cancer in male smokers. Am J Epidemiol 164: 652– 664. 16877536
  26. [28]Ahmed RL, Schmitz KH, Anderson KE, Rosamond WD, Folsom AR (2006) The metabolic syndrome and risk of incident colorectal cancer. Cancer 107: 28– 36. 16721800
  27. [29]Rapp K, Schroeder J, Klenk J, Stoehr S, Ulmer H, et al (2005) Obesity and incidence of cancer: a large cohort study of over 145,000 adults in Austria. Br J Cancer 93: 1062– 1067. 16234822 PMC2361672
  28. [30]Otani T, Iwasaki M, Inoue M (2005) Body mass index, body height, and subsequent risk of colorectal cancer in middle-aged and elderly Japanese men and women: Japan public health center-based prospective study. Cancer Causes Control 16: 839– 850. 16132794
  29. [31]Oh SW, Yoon YS, Shin SA (2005) Effects of excess weight on cancer incidences depending on cancer sites and histologic findings among men: Korea National Health Insurance Corporation Study. J Clin Oncol 23: 4742– 4754. 16034050
  30. [32]Kuriyama S, Tsubono Y, Hozawa A, Shimazu T, Suzuki Y, et al (2005) Obesity and risk of cancer in Japan. Int J Cancer 113: 148– 157. 15386435
  31. [33]Engeland A, Tretli S, Austad G, Bjorge T (2005) Height and body mass index in relation to colorectal and gallbladder cancer in two million Norwegian men and women. Cancer Causes Control 16: 987– 996. 16132807
  32. [34]Wei EK, Giovannucci E, Wu K, Rosner B, Fuchs CS, et al (2004) Comparison of risk factors for colon and rectal cancer. Int J Cancer 108: 433– 442. 14648711 PMC2903217
  33. [35]Moore LL, Bradlee ML, Singer MR, Splansky GL, Proctor MH, et al (2004) BMI and waist circumference as predictors of lifetime colon cancer risk in Framingham Study adults. Int J Obes Relat Metab Disord 28: 559– 567. 14770200
  34. [36]MacInnis RJ, English DR, Hopper JL, Haydon AM, Gertig DM, et al (2004) Body size and composition and colon cancer risk in men. Cancer Epidemiol Biomarkers Prev 13: 553– 559. 15066919
  35. [37]Lin J, Zhang SM, Cook NR, Rexrode KM, Lee IM, et al (2004) Body mass index and risk of colorectal cancer in women (United States). Cancer Causes Control 15: 581– 589. 15280637
  36. [38]Shimizu N, Nagata C, Shimizu H, Kametani M, Takeyama N, et al (2003) Height, weight, and alcohol consumption in relation to the risk of colorectal cancer in Japan: a prospective study. Br J Cancer 88: 1038– 1043. 12671701 PMC2376385
  37. [39]Terry PD, Miller AB, Rohan TE (2002) Obesity and colorectal cancer risk in women. Gut 51: 191– 194. 12117878 PMC1773328
  38. [40]Terry P, Giovannucci E, Bergkvist L, Holmberg L, Wolk A (2001) Body weight and colorectal cancer risk in a cohort of Swedish women: relation varies by age and cancer site. Br J Cancer 85: 346– 349. 11487263 PMC2364077
  39. [41]Kaaks R, Toniolo P, Akhmedkhanov A, Lukanova A, Biessy C, et al (2000) Serum C-peptide, insulin-like growth factor (IGF)-I, IGF-binding proteins, and colorectal cancer risk in women. J Natl Cancer Inst 92: 1592– 1600. 11018095
  40. [42]Schoen RE, Tangen CM, Kuller LH, Burke GL, Cushman M, et al (1999) Increased blood glucose and insulin, body size, and incident colorectal cancer. J Natl Cancer Inst 91: 1147– 1154. 10393723
  41. [43]Ford ES (1999) Body mass index and colon cancer in a national sample of adult US men and women. Am J Epidemiol 150: 390– 398. 10453815
  42. [44]Singh PN, Fraser GE (1998) Dietary risk factors for colon cancer in a low-risk population. Am J Epidemiol 148: 761– 774. 9786231
  43. [46]Chyou PH, Nomura AM, Stemmermann GN (1996) A prospective study of colon and rectal cancer among Hawaii Japanese men. Ann Epidemiol 6: 276– 282. 8876837
  44. [47]Giovannucci E, Ascherio A, Rimm EB, Colditz GA, Stampfer MJ, et al (1995) Physical activity, obesity, and risk for colon cancer and adenoma in men. Ann Intern Med 122: 327– 334. 7847643
  45. [48]Bostick RM, Potter JD, Kushi LH, Sellers TA, Steinmetz KA, et al (1994) Sugar, meat, and fat intake, and non-dietary risk factors for colon cancer incidence in Iowa women (United States). Cancer Causes Control 5: 38– 52. 8123778
  46. [49]Lee IM, Paffenbarger RS Jr (1992) Quetelet's index and risk of colon cancer in college alumni. J Natl Cancer Inst 84: 1326– 1331. 1495102
  47. [50]Moghaddam AA, Woodward M, Huxley R (2007) Obesity and risk of colorectal cancer: a meta-analysis of 31 studies with 70,000 events. Cancer Epidemiol Biomarkers Prev 16: 2533– 2547. 18086756
  48. [51]Dai Z, Xu YC, Niu L (2007) Obesity and colorectal cancer risk: a meta-analysis of cohort studies. World J Gastroenterol 13: 4199– 4206. 17696248 PMC4250618
  49. [52]Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, et al (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 283: 2008– 2012. 10789670
  50. [53]Stang A (2010) Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 25: 603– 605. 20652370
  51. [55]Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315: 629– 634. 9310563 PMC2127453
  52. [56]Ezzati M, Lopez AD, Rodgers A, Vander Hoorn S, Murray CJ (2002) Selected major risk factors and global and regional burden of disease. Lancet 360: 1347– 1360. 12423980
  53. [57]Bergstrom A, Pisani P, Tenet V, Wolk A, Adami HO (2001) Overweight as an avoidable cause of cancer in Europe. Int J Cancer 91: 421– 430. 11169969
  54. [58]Clayton PE, Banerjee I, Murray PG, Renehan AG (2011) Growth hormone, the insulin-like growth factor axis, insulin and cancer risk. Nat Rev Endocrinol 7: 11– 24. 20956999
  55. [59]Renehan AG, Painter JE, Atkin WS, Potten CS, Shalet SM, et al (2001) High-risk colorectal adenomas and serum insulin-like growth factors. Br J Surg 88: 107– 113. 11136321
  56. [60]Renehan AG, Zwahlen M, Minder C, O'Dwyer ST, Shalet SM, et al (2004) Insulin-like growth factor (IGF)-I, IGF binding protein-3, and cancer risk: systematic review and meta-regression analysis. Lancet 363: 1346– 1353. 15110491
  57. [61]Renehan AG, Frystyk J, Flyvbjerg A (2006) Obesity and cancer risk: the role of the insulin-IGF axis. Trends Endocrinol Metab 17: 328– 336. 16956771
  58. [62]Larsson SC, Orsini N, Wolk A (2005) Diabetes mellitus and risk of colorectal cancer: a meta-analysis. J Natl Cancer Inst 97: 1679– 1687. 16288121
  59. [63]Chung YW, Han DS, Park YK, Son BK, Paik CH, et al (2006) Association of obesity, serum glucose and lipids with the risk of advanced colorectal adenoma and cancer: a case-control study in Korea. Dig Liver Dis 38: 668– 672. 16790371
  60. [64]Amemori S, Ootani A, Aoki S, Fujise T, Shimoda R, et al (2007) Adipocytes and preadipocytes promote the proliferation of colon cancer cells in vitro. Am J Physiol Gastrointest Liver Physiol 292: G923– 929. 17170030
  61. [65]Ogino S, Kawasaki T, Ogawa A, Kirkner GJ, Loda M, et al (2007) Fatty acid synthase overexpression in colorectal cancer is associated with microsatellite instability, independent of CpG island methylator phenotype. Hum Pathol 38: 842– 849. 17350669
  62. [66]Renehan AG, Roberts DL, Dive C (2008) Obesity and cancer: pathophysiological and biological mechanisms. Arch Physiol Biochem 114: 71– 83. 18465361
  63. [67]Stattin P, Lukanova A, Biessy C, Soderberg S, Palmqvist R, et al (2004) Obesity and colon cancer: does leptin provide a link? Int J Cancer 109: 149– 152. 14735482
  64. [68]Stattin P, Palmqvist R, Soderberg S, Biessy C, Ardnor B, et al (2003) Plasma leptin and colorectal cancer risk: a prospective study in Northern Sweden. Oncol Rep 10: 2015– 2021. 14534736
  65. [69]Yin L, Grandi N, Raum E, Haug U, Arndt V, et al (2009) Meta-analysis: longitudinal studies of serum vitamin D and colorectal cancer risk. Aliment Pharmacol Ther 30: 113– 125. 19392870

Cited by

Sorted by citations

Authors
Ma, Y., Yang, Y., Wang, F., Zhang, P., Shi, C., Zou, Y., & Qin, H.
Affiliations
  • Tongji University (CN)
  • Shanghai Jiao Tong University (CN)
Corresponding author
  • Ma, Yanlei
  • Qin, Huanlong
Venue
PLoS ONE
Published
2013-01-17
Volume
8
Issue
1
Pages
e53916
ISSN
1932-6203 (ISSN-L)
OpenAlex
W1990436525
Cited by
622
References
5
Citations by year
2026: 25 · 2025: 35 · 2024: 45 · 2023: 55 · 2022: 68 · 2021: 55 · 2020: 64 · 2019: 62 · 2018: 49 · 2017: 37 · 2016: 35 · 2015: 34 · 2014: 37 · 2013: 20
FWCI
4.44
Type
journal article
Language
en
Open access
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
Funders
  • Shanghai Science and Technology Development Foundation (12140902300, 12410707400)
  • National Natural Science Foundation of China (81001069)
  • Shanghai Rising-Star Program (11QA1404800)
Topics
  • Health Sciences › Medicine › Oncology › Cancer Risks and Factors
  • Health Sciences › Medicine › Oncology › Colorectal Cancer Screening and Detection
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Obesity, Physical Activity, Diet
Keywords
obesity, colorectal cancer, body mass index, waist circumference, abdominal obesity, colon cancer, rectal cancer, cancer risk factors
MeSH terms
Humans, Obesity, Prospective Studies, Risk Factors, Colorectal Neoplasms, Body Mass Index, Risk Assessment, Waist Circumference

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review