Abstract
Insulin-like growth factor peptides, play an important role in regulating cell growth, differentiation, and apoptosis, which has been demonstrated to promote the development of cancer. The purpose of our study is to assess the association between circulation insulin-like growth factor peptides and colorectal cancer (CRC) risk. We searched Medline, EMBASE, OVID and Web of Science and picked up epidemiological studies that satisfied our inclusion criteria. A meta-analysis of 19 epidemiological studies containing 5,155 cases and 9,420 controls related with the association of circulation insulin-like growth factor peptides and CRC risk was carried out. Meta-analysis showed that high level IGF-I and IGF-II significantly increased CRC risk, (OR = 1.25, 95 % CI: 1.08–1.45 for IGF-I; OR = 1.52, 95 % CI: 1.16–2.01 for IGF-II; OR = 0.85, 95 % CI: 0.70–1.03 for IGFBP-1; OR = 0.77, 95 % CI: 0.41–1.43 for IGFBP-2 and OR = 0.88, 95 % CI: 0.71–1.10 for IGFBP-3). Subgroup analysis showed that the increased cancer risk by IGF-I was more distinguished in colon cancer (OR = 1.35, 95 % CI: 1.04–1.75) and Caucasian (OR = 1.32, 95 % CI: 1.12–1.56). Our meta-analysis provides comprehensive support for a role of circulation IGF-I and IGF-II in the etiology of CRC.
Similar content being viewed by others
References
Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM (2010) Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 127(12):2893–2917
de la Chapelle A (2004) Genetic predisposition to colorectal cancer. Nat Rev Cancer 4(10):769–780
Jemal A, Siegel R, Xu J, Ward E (2010) Cancer statistics. CA Cancer J Clin 60(5):277–300
Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D (2011) Global cancer statistics. CA Cancer J Clin 61(2):69–90
Sandhu MS, Dunger DB, Giovannucci EL (2002) Insulin, insulin-like growth factor-I (IGF-I), IGF binding proteins, their biologic interactions, and colorectal cancer. J Natl Cancer Inst 94(13):972–980
Khandwala HM, McCutcheon IE, Flyvbjerg A, Friend KE (2000) The effects of insulin-like growth factors on tumorigenesis and neoplastic growth. Endocr Rev 21(3):215–244
Jerome L, Shiry L, Leyland-Jones B (2003) Deregulation of the IGF axis in cancer: epidemiological evidence and potential therapeutic interventions. Endocr Relat Cancer 10(4):561–578
Pollak MN, Schernhammer ES, Hankinson SE (2004) Insulin-like growth factors and neoplasia. Nat Rev Cancer 4(7):505–518
LeRoith D, Baserga R, Helman L, Roberts CT Jr (1995) Insulin-like growth factors and cancer. Ann Intern Med 122(1):54–59
Baserga R (1995) The insulin-like growth factor I receptor: a key to tumor growth? Cancer Res 55(2):249–252
Ma J, Pollak MN, Giovannucci E, Chan JM, Tao Y, Hennekens CH, Stampfer MJ (1999) Prospective study of colorectal cancer risk in men and plasma levels of insulin-like growth factor (IGF)-I and IGF-binding protein-3. J Natl Cancer Inst 91(7):620–625
Manousos O, Souglakos J, Bosetti C, Tzonou A, Chatzidakis V, Trichopoulos D, Adami HO, Mantzoros C (1999) IGF-I and IGF-II in relation to colorectal cancer. Int J Cancer 83(1):15–17
Probst-Hensch NM, Yuan JM, Stanczyk FZ, Gao YT, Ross RK, Yu MC (2001) IGF-1, IGF-2 and IGFBP-3 in prediagnostic serum: association with colorectal cancer in a cohort of Chinese men in Shanghai. Br J Cancer 85(11):1695–1699
Nomura AM, Stemmermann GN, Lee J, Pollak MN (2003) Serum insulin-like growth factor I and subsequent risk of colorectal cancer among Japanese-American men. Am J Epidemiol 158(5):424–431
Ollberding NJ, Cheng I, Wilkens LR, Henderson BE, Pollak MN, Kolonel LN, Le Marchand L (2012) Genetic variants, prediagnostic circulating levels of insulin-like growth factors, insulin, and glucose and the risk of colorectal cancer: the Multiethnic Cohort study. Cancer Epidemiol Biomarkers Prev 21(5):810–820
Giovannucci E, Pollak MN, Platz EA, Willett WC, Stampfer MJ, Majeed N, Colditz GA, Speizer FE, Hankinson SE (2000) A prospective study of plasma insulin-like growth factor-1 and binding protein-3 and risk of colorectal neoplasia in women. Cancer Epidemiol Biomarkers Prev 9(4):345–349
Otani T, Iwasaki M, Sasazuki S, Inoue M, Tsugane S (2007) Plasma C-peptide, insulin-like growth factor-I, insulin-like growth factor binding proteins and risk of colorectal cancer in a nested case–control study: the Japan public health center-based prospective study. Int J Cancer 120(9):2007–2012
Rinaldi S, Cleveland R, Norat T, Biessy C, Rohrmann S, Linseisen J, Boeing H, Pischon T, Panico S, Agnoli C, Palli D, Tumino R, Vineis P, Peeters PH, van Gils CH, Bueno-de-Mesquita BH, Vrieling A, Allen NE, Roddam A, Bingham S, Khaw KT, Manjer J, Borgquist S, Dumeaux V, Gram IT, Lund E, Trichopoulou A, Makrygiannis G, Benetou V, Molina E, Suarez ID, Gurrea AB, Gonzalez CA, Tormo MJ, Altzibar JM, Olsen A, Tjonneland A, Gronbaek H, Overvad K, Clavel-Chapelon F, Boutron-Ruault MC, Morois S, Slimani N, Boffetta P, Jenab M, Riboli E, Kaaks R (2010) Serum levels of IGF-I, IGFBP-3 and colorectal cancer risk: results from the EPIC cohort, plus a meta-analysis of prospective studies. Int J Cancer 126(7):1702–1715
Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21(11):1539–1558
Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327(7414):557–560
Andrel JA, Keith SW, Leiby BE (2009) Meta-analysis: a brief introduction. Clin Transl Sci 2(5):374–378
Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315(7109):629–634
Begg CB, Mazumdar M (1994) Operating characteristics of a rank correlation test for publication bias. Biometrics 50(4):1088–1101
Wei EK, Ma J, Pollak MN, Rifai N, Fuchs CS, Hankinson SE, Giovannucci E (2005) A prospective study of C-peptide, insulin-like growth factor-1, insulin-like growth factor binding protein-1, and the risk of colorectal cancer in women. Cancer Epidemiol Biomarkers Prev 14(4):850–855
Kaaks R, Toniolo P, Akhmedkhanov A, Lukanova A, Biessy C, Dechaud H, Rinaldi S, Zeleniuch-Jacquotte A, Shore RE, Riboli E (2000) Serum C-peptide, insulin-like growth factor (IGF)-I, IGF-binding proteins, and colorectal cancer risk in women. J Natl Cancer Inst 92(19):1592–1600
Hunt KJ, Toniolo P, Akhmedkhanov A, Lukanova A, Dechaud H, Rinaldi S, Zeleniuch-Jacquotte A, Shore RE, Riboli E, Kaaks R (2002) Insulin-like growth factor II and colorectal cancer risk in women. Cancer Epidemiol Biomarkers Prev 11(9):901–905
Palmqvist R, Hallmans G, Rinaldi S, Biessy C, Stenling R, Riboli E, Kaaks R (2002) Plasma insulin-like growth factor 1, insulin-like growth factor binding protein 3, and risk of colorectal cancer: a prospective study in northern Sweden. Gut 50(5):642–646
Palmqvist R, Stattin P, Rinaldi S, Biessy C, Stenling R, Riboli E, Hallmans G, Kaaks R (2003) Plasma insulin, IGF-binding proteins-1 and -2 and risk of colorectal cancer: a prospective study in northern Sweden. Int J Cancer 107(1):89–93
Pollak MN (1998) Endocrine effects of IGF-I on normal and transformed breast epithelial cells: potential relevance to strategies for breast cancer treatment and prevention. Breast Cancer Res Treat 47(3):209–217
Jenkins PJ, Bustin SA (2004) Evidence for a link between IGF-I and cancer. Eur J Endocrinol 151(Suppl 1):S17–S22
LeRoith D, Roberts CT Jr (2003) The insulin-like growth factor system and cancer. Cancer Lett 195(2):127–137
Reinmuth N, Liu W, Fan F, Jung YD, Ahmad SA, Stoeltzing O, Bucana CD, Radinsky R, Ellis LM (2002) Blockade of insulin-like growth factor I receptor function inhibits growth and angiogenesis of colon cancer. Clin Cancer Res 8(10):3259–3269
Wolpin BM, Michaud DS, Giovannucci EL, Schernhammer ES, Stampfer MJ, Manson JE, Cochrane BB, Rohan TE, Ma J, Pollak MN, Fuchs CS (2007) Circulating insulin-like growth factor axis and the risk of pancreatic cancer in four prospective cohorts. Br J Cancer 97(1):98–104
Pham TM, Fujino Y, Kikuchi S, Tamakoshi A, Yatsuya H, Matsuda S, Yoshimura T (2007) A nested case–control study of stomach cancer and serum insulin-like growth factor (IGF)-1, IGF-2 and IGF-binding protein (IGFBP)-3. Eur J Cancer 43(10):1611–1616
Peeters PH, Lukanova A, Allen N, Berrino F, Key T, Dossus L, Rinaldi S, van Gils CH, Bueno-de-Mesquita HB, Boeing H, Schulz M, Chang-Claude J, Linseisen J, Panico S, Sacerdote C, Palli D, Tumino R, Trichopoulou A, Trichopolos D, Bamia C, Larranaga N, Ardanaz E, Pera G, Quiros JR, Martinez-Garcia C, Navarro C, Bingham SA, Khaw KT, Clavel F, Tjonneland A, Olsen A, Overvad K, Tetsche MS, Lund E, Lundin E, Berglund G, Riboli E, Kaaks R (2007) Serum IGF-I, its major binding protein (IGFBP-3) and epithelial ovarian cancer risk: the European Prospective Investigation into Cancer and Nutrition (EPIC). Endocr Relat Cancer 14(1):81–90
Hernandez W, Grenade C, Santos ER, Bonilla C, Ahaghotu C, Kittles RA (2007) IGF-1 and IGFBP-3 gene variants influence on serum levels and prostate cancer risk in African-Americans. Carcinogenesis 28(10):2154–2159
Rinaldi S, Peeters PH, Berrino F, Dossus L, Biessy C, Olsen A, Tjonneland A, Overvad K, Clavel-Chapelon F, Boutron-Ruault MC, Tehard B, Nagel G, Linseisen J, Boeing H, Lahmann PH, Trichopoulou A, Trichopoulos D, Koliva M, Palli D, Panico S, Tumino R, Sacerdote C, van Gils CH, van Noord P, Grobbee DE, Bueno-de-Mesquita HB, Gonzalez CA, Agudo A, Chirlaque MD, Barricarte A, Larranaga N, Quiros JR, Bingham S, Khaw KT, Key T, Allen NE, Lukanova A, Slimani N, Saracci R, Riboli E, Kaaks R (2006) IGF-I, IGFBP-3 and breast cancer risk in women: The European Prospective Investigation into Cancer and Nutrition (EPIC). Endocr Relat Cancer 13(2):593–605
Aksoy Y, Aksoy H, Bakan E, Atmaca AF, Akcay F (2004) Serum insulin-like growth factor-I and insulin-like growth factor-binding protein-3 in localized, metastasized prostate cancer and benign prostatic hyperplasia. Urol Int 72(1):62–65
Harman SM, Metter EJ, Blackman MR, Landis PK, Carter HB (2000) Serum levels of insulin-like growth factor I (IGF-I), IGF-II, IGF-binding protein-3, and prostate-specific antigen as predictors of clinical prostate cancer. J Clin Endocrinol Metab 85(11):4258–4265
Muti P, Quattrin T, Grant BJ, Krogh V, Micheli A, Schunemann HJ, Ram M, Freudenheim JL, Sieri S, Trevisan M, Berrino F (2002) Fasting glucose is a risk factor for breast cancer: a prospective study. Cancer Epidemiol Biomarkers Prev 11(11):1361–1368
London SJ, Yuan JM, Travlos GS, Gao YT, Wilson RE, Ross RK, Yu MC (2002) Insulin-like growth factor I, IGF-binding protein 3, and lung cancer risk in a prospective study of men in China. J Natl Cancer Inst 94(10):749–754
Renehan AG, Zwahlen M, Minder C, O’Dwyer ST, Shalet SM, Egger M (2004) Insulin-like growth factor (IGF)-I, IGF binding protein-3, and cancer risk: systematic review and meta-regression analysis. Lancet 363(9418):1346–1353
Duan QH, Wang ZG, Zhu GB, Lu ZX, Shi LY, Nie SF (2005) Study on the relations between serum insulin-like growth factor-1, insulin-like growth factor binding protein-3 and colorectal cancer: a meta-analysis. Zhonghua Liu Xing Bing Xue Za Zhi 26(2):132–134
Morris JK, George LM, Wu T, Wald NJ (2006) Insulin-like growth factors and cancer: no role in screening. Evidence from the BUPA study and meta-analysis of prospective epidemiological studies. Br J Cancer 95(1):112–117
Cui H, Cruz-Correa M, Giardiello FM, Hutcheon DF, Kafonek DR, Brandenburg S, Wu Y, He X, Powe NR, Feinberg AP (2003) Loss of IGF2 imprinting: a potential marker of colorectal cancer risk. Science 299(5613):1753–1755
Bertucci F, Salas S, Eysteries S, Nasser V, Finetti P, Ginestier C, Charafe-Jauffret E, Loriod B, Bachelart L, Montfort J, Victorero G, Viret F, Ollendorff V, Fert V, Giovaninni M, Delpero JR, Nguyen C, Viens P, Monges G, Birnbaum D, Houlgatte R (2004) Gene expression profiling of colon cancer by DNA microarrays and correlation with histoclinical parameters. Oncogene 23(7):1377–1391
Conflict of interest
There is no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Chi, F., Wu, R., Zeng, Yc. et al. Circulation insulin-like growth factor peptides and colorectal cancer risk: an updated systematic review and meta-analysis. Mol Biol Rep 40, 3583–3590 (2013). https://doi.org/10.1007/s11033-012-2432-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11033-012-2432-z