Serum C-peptide levels and breast cancer risk: Results from the European Prospective Investigation into Cancer and Nutrition (EPIC)

International Journal of Cancer

Volumn 119, Issue 3, 2006, Pages 659-667

  Verheus, Martijn ^a,b   Peeters, Petra H M ^b   Rinaldi, Sabina ^a   Dossus, Laure ^a   Biessy, Carine ^a   Olsen, Anja ^c   Tjønneland, Anne ^c   Overvad, Kim ^d   Jeppesen, Majbritt ^e   Clavel Chapelon, Françoise ^f   Téhard, Bertrand ^f   Nagel, Gabriele ^g   Linseisen, Jakob ^g   Boeing, Heiner ^h   Lahmann, Petra H ^h   Arvaniti, Athina ⁱ   Psaltopoulou, Theodora ⁱ   Trichopoulou, Antonia ⁱ   Palli, Domenico ^j   Tumino, Rosario ^k   Panico, Salvatore ^l   Sacerdote, Carlotta ^m   Sieri, Sabina ⁿ   Van Gils, Carla H ^b   Bueno De Mesquita, Bas H ^o   González, Carlos A ^p   Ardanaz, Eva ^q   Larranaga, Nera ^r   Garcia, Carmen Martinez ^s   Navarro, Carmen ^t   Quirós, J Ramón ^u   Key, Tim ^v   Allen, Naomi ^v   Bingham, Sheila ^w   Khaw, Kay Tee ^x   Slimani, Nadia ^a   Riboli, Elio ^a   Kaaks, Rudolf ^a   more..

^a INTERNATIONAL AGENCY FOR RESEARCH ON CANCER   (France)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c INSTITUTE OF CANCER EPIDEMIOLOGY   (Denmark)

^d AALBORG UNIVERSITY HOSPITAL   (Denmark)

^e AARHUS UNIVERSITY   (Denmark)

^f INSTITUT GUSTAVE ROUSSY   (France)

^g GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^h GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

ⁱ UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

^j CANCER RESEARCH AND PREVENTION INSTITUTE ISPO   (Italy)

^k CIVILE M P AREZZO HOSPITAL   (Italy)

^l UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^m UNIVERSITY OF TURIN   (Italy)

ⁿ NATIONAL CANCER INSTITUTE   (Italy)

^o NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^p CATALAN INSTITUTE OF ONCOLOGY   (Spain)

^q INSTITUTO DE SALUD PÚBLICA DE NAVARRA   (Spain)

^r Basque Government   (Spain)

^s ANDALUSIAN SCHOOL OF PUBLIC HEALTH   (Spain)

^t DEPARTMENT OF EPIDEMIOLOGY   (Spain)

^u Public Health and Health Planning Directorate   (Spain)

^v UNIVERSITY OF OXFORD   (United Kingdom)

^w UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^x ADDENBROOKE S HOSPITAL   (United Kingdom)

more..

Author keywords

Breast cancer; C peptide; Cohort; EPIC; Prospective

Indexed keywords

C PEPTIDE; ESTRADIOL; INSULIN; SEX HORMONE; SEX HORMONE BINDING GLOBULIN; TESTOSTERONE;

ADULT; AGED; AGING; ARTICLE; BREAST CANCER; CANCER INCIDENCE; CANCER RISK; COHORT ANALYSIS; CONTROLLED STUDY; CORRELATION COEFFICIENT; ESTRADIOL BLOOD LEVEL; EUROPE; FEMALE; HUMAN; HYPERINSULINEMIA; INSULIN RELEASE; LOGISTIC REGRESSION ANALYSIS; MAJOR CLINICAL STUDY; OBESITY; PHYSICAL ACTIVITY; POSTMENOPAUSE; PREMENOPAUSE; PRIORITY JOURNAL; PROSPECTIVE STUDY; PROTEIN BLOOD LEVEL; RISK ASSESSMENT; TESTOSTERONE BLOOD LEVEL;

ADULT; AGED; BODY MASS INDEX; BREAST NEOPLASMS; C-PEPTIDE; CASE-CONTROL STUDIES; EUROPE; FEMALE; HUMANS; INCIDENCE; LOGISTIC MODELS; MIDDLE AGED; MULTIVARIATE ANALYSIS; ODDS RATIO; POSTMENOPAUSE; PREMENOPAUSE; RISK FACTORS;

EID: 33745464228     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.21861     Document Type: Article

References (54)

1. van den Brandt PA, Spiegelman D, Yaun SS, Adami HO, Beeson L, Folsom AR, Fraser G, Goldbohm RA, Graham S, Kushi L, Marshall JR, Miller AB, et al. Pooled analysis of prospective cohort studies on height, weight, and breast cancer risk. Am J Epidemiol 2000;152:514-27.
2. Lahmann PH, Hoffmann K, Allen N, Van Gils CH, Khaw KT, Tehard B, Berrino F, Tjonneland A, Bigaard J, Olsen A, Overvad K, Clavel-Chapelon F, et al. Body size and breast cancer risk: findings from the European Prospective Investigation into Cancer And Nutrition (EPIC). Int J Cancer 2004;111:762-71.
3. Friedenreich CM, Orenstein MR. Physical activity and cancer prevention: etiologic evidence and biological mechanisms. J Nutr 2002;132:3456S-3464S.
4. Henriksen EJ. Invited review: effects of acute exercise and exercise training on insulin resistance. J Appl Physiol 2002;93:788-96.
5. Kahn BB, Flier JS. Obesity and insulin resistance. J Clin Invest 2000;106:473-81.
6. Chlebowski RT, Pettinger M, Stefanick ML, Howard BV, Mossavar-Rahmani Y, McTieman A. Insulin, physical activity, and caloric intake in postmenopausal women: breast cancer implications. J Clin Oncol 2004;22:4507-13.
7. Laban C, Bustin SA, Jenkins PJ. The GH-IGF-I axis and breast cancer. Trends Endocrinol Metab 2003;14:28-34.
8. Sachdev D, Yee D. The IGF system and breast cancer. Endocr Relat Cancer 2001;8:197-209.
9. Shi R, Yu H, McLarty J, Glass J. IGF-I and breast cancer: a meta-analysis. Int J Cancer 2004;111:418-23.
10. Chappell J, Leitner JW, Solomon S, Golovchenko I, Goalstone ML, Draznin B. Effect of insulin on cell cycle progression in MCF-7 breast cancer cells. Direct and potentiating influence. J Biol Chem 2001;276:38023-8.
11. Ish-Shalom D, Christoffersen CT, Vorwerk P, Sacerdoti-Sierra N, Shymko RM, Naor D, De Meyts P. Mitogenic properties of insulin and insulin analogues mediated by the insulin receptor. Diabetologia 1997;40 (Suppl. 2):S25-S31.
12. Shafie SM, Grantham FH. Role of hormones in the growth and regression of human breast cancer cells (MCF-7) transplanted into athymic nude mice. J Natl Cancer Inst 1981;67:51-6.
13. Shafie SM, Hilf R. Insulin receptor levels and magnitude of insulin-induced responses in 7,12-dimethylbenz(a)anthracene-induced mammary tumors in rats. Cancer Res 1981;41:826-9.
14. Heuson JC, Legros N. Influence of insulin deprivation on growth of the 7,12-dimethylbenz(a)anthracene-induced mammary carcinoma in rats subjected to alloxan diabetes and food restriction. Cancer Res 1972;32:226-32.
15. Heuson JC, Legros N. Effect of insulin and of alloxan diabetes on growth of the rat mammary carcinoma in vivo. Eur J Cancer 1970;6:349-51.
16. Cocca C, Gutierrez A, Nunez M, Croci M, Martin G, Cricco G, Rivera E, Bergoc R. Suppression of mammary gland tumorigenesis in diabetic rats. Cancer Detect Prev 2003;27:37-46.
17. Cocca C, Martin G, Rivera E, Davio C, Cricco G, Lemos B, Fitzsimons C, Gutierrez A, Levin E, Levin R, Croci M, Bergoc RM. An experimental model of diabetes and cancer in rats. Eur J Cancer 1998;34:889-94.
18. Byrne C, Colditz GA, Willett WC, Speizer FE, Pollak M, Hankinson SE. Plasma insulin-like growth factor (IGF) I, IGF-binding protein 3, and mammographic density. Cancer Res 2000;60:3744-8.
19. Nestler JE. Insulin regulation of human ovarian androgens. Hum Reprod 1997;12 (Suppl. 1):53-62.
20. Awartani KA, Cheung AP. Metformin and polycystic ovary syndrome: a literature review. J Obstet Gynaecol Can 2002;24:393-401.
21. Kaaks R, Rinaldi S, Key TJ, Berrino F, Peeters PH, Biessy C, et al. Postmenopausal serum androgens, oestrogens and breast cancer risk: the European Prospective Investigation into Cancer and Nutrition (EPIC). Endocr Relat Cancer 2005;12(4):1071-82.
22. Key T, Appleby P, Barnes I, Reeves G. Endogenous sex hormones and breast cancer in postmenopausal women: reanalysis of nine prospective studies. J Natl Cancer Inst 2002;94:606-16.
23. Kaaks R. Nutrition, hormones, and breast cancer: is insulin the missing link? Cancer Causes Control 1996;7:605-25.
24. Kaaks R, Berrino F, Key T, Rinaldi S, Dossus L, Biessy C, Secreto G, Amiano P, Bingham S, Boeing H, Bueno de Mesquita HB, Chang-Claude J, et al. Serum sex steroids in premenopausal women and breast cancer risk within the European Prospective Investigation into Cancer and Nutrition (EPIC). J Natl Cancer Inst 2005;97:755-65.
25. Travis RC, Key TJ. Oestrogen exposure and breast cancer risk. Breast Cancer Res 2003;5:239-47.
26. Toniolo P, Bruning PF, Akhmedkhanov A, Bonfrer JM, Koenig KL, Lukanova A, Shore RE, Zeleniuch-Jacquotte A. Serum insulin-like growth factor-I and breast cancer. Int J Cancer 2000;88:828-32.
27. Kaaks R, Lundin E, Rinaldi S, Manjer J, Biessy C, Soderberg S, Lenner P, Janzon L, Riboli E, Berglund G, Hallmans G. Prospective study of IGF-I, IGF-binding proteins, and breast cancer risk, in northern and southern Sweden. Cancer Causes Control 2002;13:307-16.
28. Keinan-Boker L, Bueno de Mesquita HB, Kaaks R, Van Gils CH, Van Noord PA, Rinaldi S, Riboli E, Seidell JC, Grobbee DE, Peeters PH. Circulating levels of insulin-like growth factor I, its binding proteins-1, -2, -3, C-peptide and risk of postmenopausal breast cancer. Int J Cancer 2003;106:90-5.
29. Mink PJ, Shahar E, Rosamond WD, Alberg AJ, Folsom AR. Serum insulin and glucose levels and breast cancer incidence: the atherosclerosis risk in communities study. Am J Epidemiol 2002;156:349-52.
30. Muti P, Quattrin T, Grant BJ, Krogh V, Micheli A, Schunemann HJ, Ram M, Freudenheim JL, Sieri S, Trevisan M, Berrino F. Fasting glucose is a risk factor for breast cancer: a prospective study. Cancer Epidemiol Biomarkers Prev 2002;11:1361-8.
31. Riboli E, Hunt KJ, Slimani N, Ferrari P, Norat T, Fahey M, Charrondiere UR, Hemon B, Casagrande C, Vignat J, Overvad K, Tjonneland A, et al. European Prospective Investigation into Cancer and Nutrition (EPIC): study populations and data collection. Public Health Nutr 2002;5:1113-24.
32. Bingham S, Riboli E. Diet and cancer-the European Prospective Investigation into Cancer and Nutrition. Nat Rev Cancer 2004;4:206-15.
33. Ainsworth BE, Haskell WL, Whitt MC, Irwin ML, Swartz AM, Strath SJ, O'Brien WL, Bassett DR, Jr., Schmitz KH, Emplaincourt PO, Jacobs DR, Jr, Leon AS. Compendium of physical activities: an update of activity codes and MET intensities. Med Sci Sports Exerc 2000;32: S498-S504.
34. Rinaldi S, Dechaud H, Biessy C, Morin-Raverot V, Toniolo P, Zeleniuch-Jacquotte A, Akhmedkhanov A, Shore RE, Secreto G, Ciampi A, Riboli E, Kaaks R. Reliability and validity of commercially available, direct radioimmunoassays for measurement of blood androgens and estrogens in postmenopausal women. Cancer Epidemiol Biomarkers Prev 2001;10:757-65.
35. Rinaldi S, Geay A, Dechaud H, Biessy C, Zeleniuch-Jacquotte A, Akhmedkhanov A, Shore RE, Riboli E, Toniolo P, Kaaks R. Validity of free testosterone and free estradiol determinations in serum samples from postmenopausal women by theoretical calculations. Cancer Epidemiol Biomarkers Prev 2002;11:1065-71.
36. Bruning PF, Bonfrer JM, Van Noord PA, Hart AA, Jong-Bakker M, Nooijen WJ. Insulin resistance and breast-cancer risk. Int J Cancer 1992;52:511-6.
37. Schairer C, Hill D, Sturgeon SR, Fears T, Pollak M, Mies C, Ziegler RG, Hoover RN, Sherman ME. Serum concentrations of IGF-I, IGFBP-3 and c-peptide and risk of hyperplasia and cancer of the breast in postmenopausal women. Int J Cancer 2004;108:773-9.
38. Yang G, Lu G, Jin F, Dai Q, Best R, Shu XO, Chen JR, Pan XY, Shrubsole M, Zheng W. Population-based, case-control study of blood C-peptide level and breast cancer risk. Cancer Epidemiol Biomarkers Prev 2001;10:1207-11.
39. Hirose K, Toyama T, Iwata H, Takezaki T, Hamajima N, Tajima K. Insulin, insulin-like growth factor-I and breast cancer risk in Japanese women. Asian Pac J Cancer Prev 2003;4:239-46.
40. Del Giudice ME, Fantus IG, Ezzat S, McKeown-Eyssen G, Page D, Goodwin PJ. Insulin and related factors in premenopausal breast cancer risk. Breast Cancer Res Treat 1998;47:111-20.
41. de Waard F, de Laive J, Baanders-van Halewijn EA. On the bimodal age distribution of mammary carcinoma. Br J Cancer 1960;14:437-48.
42. Barcelo A. Monograph series on aging-related diseases. VIII. Non-insulin-dependent diabetes mellitus (NIDDM). Chronic Dis Can 1996;17:1-20.
43. Wolf I, Sadetzki S, Catane R, Karasik A, Kaufman B. Diabetes mellitus and breast cancer. Lancet Oncol 2005;6:103-11.
44. Waldhausl W, Bratusch-Marrain P, Gasic S, Korn A, Nowotny P. Insulin production rate following glucose ingestion estimated by splanchnic C-peptide output in normal man. Diabetologia 1979;17:221-7.
45. Polonsky K, Jaspan J, Pugh W, Cohen D, Schneider M, Schwartz T, Moossa AR, Tager H, Rubenstein AH. Metabolism of C-peptide in the dog. In vivo demonstration of the absence of hepatic extraction. J Clin Invest 1983;72:1114-23.
46. Polonsky KS, Rubenstein AH. C-peptide as a measure of the secretion and hepatic extraction of insulin. Pitfalls and limitations. Diabetes 1984;33:486-94.
47. Hovorka R, Jones RH. How to measure insulin secretion. Diabetes Metab Rev 1994;10:91-117.
48. Tura A, Ludvik B, Nolan JJ, Pacini G, Thomaseth K. Insulin and C-peptide secretion and kinetics in humans: direct and model-based measurements during OGTT. Am J Physiol Endocrinol Metab 2001;281:E966-E974.
49. Palmqvist R, Stattin P, Rinaldi S, Biessy C, Stenling R, Riboli E, Hallmans G, Kaaks R. Plasma insulin, IGF-binding proteins-1 and -2 and risk of colorectal cancer: a prospective study in northern Sweden. Int J Cancer 2003;107:89-93.
50. Giovannucci E. Insulin and colon cancer. Cancer Causes Control 1995;6:164-79.
51. Ruige JB, Dekker JM, Nijpels G, Popp-Snijders C, Stehouwer CD, Kostense PJ, Bouter LM, Heine RJ. Hyperproinsulinaemia in impaired glucose tolerance is associated with a delayed insulin response to glucose. Diabetologia 1999;42:177-80.
52. Key TJ, Allen NE, Verkasalo PK, Banks E. Energy balance and cancer: the role of sex hormones. Proc Nutr Soc 2001;60:81-9.
53. De Leo V, la Marca A, Petraglia F. Insulin-lowering agents in the management of polycystic ovary syndrome. Endocr Rev 2003;24:633-67.
54. Potischman N, Swanson CA, Siiteri P, Hoover RN. Reversal of relation between body mass and endogenous estrogen concentrations with menopausal status. J Natl Cancer Inst 1996;88:756-8.