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Published in: European Journal of Epidemiology 2/2014

01-02-2014 | CANCER

Prospective associations between serum biomarkers of lipid metabolism and overall, breast and prostate cancer risk

Authors: Mathilde His, Laurent Zelek, Mélanie Deschasaux, Camille Pouchieu, Emmanuelle Kesse-Guyot, Serge Hercberg, Pilar Galan, Paule Latino-Martel, Jacques Blacher, Mathilde Touvier

Published in: European Journal of Epidemiology | Issue 2/2014

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Abstract

Experimental studies provided evidence about mechanisms by which cholesterol, especially high density lipoprotein cholesterol (HDL-C), could influence carcinogenesis, notably through antioxidant and anti-inflammatory properties. However, prospective studies that investigated the associations between specific lipid metabolism biomarkers and cancer risk provided inconsistent results. The objective was to investigate the prospective associations between total cholesterol (T-C), HDL-C, low density lipoprotein cholesterol, apolipoproteins A1 (apoA1) and B, and triglycerides and overall, breast and prostate cancer risk. Analyses were performed on 7,557 subjects of the Supplémentation en Vitamines et Minéraux Antioxydants Study, a nationwide French cohort study. Biomarkers of lipid metabolism were measured at baseline and analyzed regarding the risk of first primary incident cancer (N = 514 cases diagnosed during follow-up, 1994–2007), using Cox proportional hazards models. T-C was inversely associated with overall (HR1mmol/L increment = 0.91, 95 % CI 0.82–1.00; P = 0.04) and breast (HR1mmol/L increment = 0.83, 95 % CI 0.69–0.99; P = 0.04) cancer risk. HDL-C was also inversely associated with overall (HR1mmol/L increment = 0.61, 95 % CI 0.46–0.82; P = 0.0008) and breast (HR1mmol/L increment = 0.48, 95 % CI 0.28–0.83; P = 0.009) cancer risk. Consistently, apoA1 was inversely associated with overall (HR1g/L increment = 0.56, 95 % CI 0.39–0.82; P = 0.003) and breast (HR1g/L increment = 0.36, 95 % CI 0.18–0.73; P = 0.004) cancer risk. This prospective study suggests that pre-diagnostic serum levels of T-C, HDL-C and ApoA1 are associated with decreased overall and breast cancer risk. The confirmation of a role of cholesterol components in cancer development, by further large prospective and experimental studies, may have important implications in terms of public health, since cholesterol is already crucial in cardiovascular prevention.
Literature
1.
go back to reference Huxley R, Lewington S, Clarke R. Cholesterol, coronary heart disease and stroke: a review of published evidence from observational studies and randomized controlled trials. Semin Vasc Med. 2002;2:315–23.PubMedCrossRef Huxley R, Lewington S, Clarke R. Cholesterol, coronary heart disease and stroke: a review of published evidence from observational studies and randomized controlled trials. Semin Vasc Med. 2002;2:315–23.PubMedCrossRef
2.
go back to reference Law MR, Thompson SG. Low serum cholesterol and the risk of cancer: an analysis of the published prospective studies. Cancer Causes Control. 1991;2:253–61.PubMedCrossRef Law MR, Thompson SG. Low serum cholesterol and the risk of cancer: an analysis of the published prospective studies. Cancer Causes Control. 1991;2:253–61.PubMedCrossRef
3.
go back to reference Melvin JC, Holmberg L, Rohrmann S, et al. Serum lipid profiles and cancer risk in the context of obesity: four meta-analyses. J Cancer Epidemiol. 2013;2013:823849.PubMedCentralPubMedCrossRef Melvin JC, Holmberg L, Rohrmann S, et al. Serum lipid profiles and cancer risk in the context of obesity: four meta-analyses. J Cancer Epidemiol. 2013;2013:823849.PubMedCentralPubMedCrossRef
4.
go back to reference Bjorge T, Lukanova A, Tretli S, et al. Metabolic risk factors and ovarian cancer in the metabolic syndrome and cancer project. Int J Epidemiol. 2011;40:1667–77.PubMedCrossRef Bjorge T, Lukanova A, Tretli S, et al. Metabolic risk factors and ovarian cancer in the metabolic syndrome and cancer project. Int J Epidemiol. 2011;40:1667–77.PubMedCrossRef
5.
go back to reference Eichholzer M, Stahelin HB, Gutzwiller F, et al. Association of low plasma cholesterol with mortality for cancer at various sites in men: 17-y follow-up of the prospective Basel study. Am J Clin Nutr. 2000;71:569–74.PubMed Eichholzer M, Stahelin HB, Gutzwiller F, et al. Association of low plasma cholesterol with mortality for cancer at various sites in men: 17-y follow-up of the prospective Basel study. Am J Clin Nutr. 2000;71:569–74.PubMed
6.
go back to reference Nago N, Ishikawa S, Goto T, et al. Low cholesterol is associated with mortality from stroke, heart disease, and cancer: the Jichi Medical School Cohort Study. J Epidemiol. 2011;21:67–74.PubMedCentralPubMedCrossRef Nago N, Ishikawa S, Goto T, et al. Low cholesterol is associated with mortality from stroke, heart disease, and cancer: the Jichi Medical School Cohort Study. J Epidemiol. 2011;21:67–74.PubMedCentralPubMedCrossRef
7.
go back to reference Strohmaier S, Edlinger M, Manjer J, et al. Total serum cholesterol and cancer incidence in the metabolic syndrome and cancer project (Me-Can). PLoS One. 2013;8:e54242.PubMedCentralPubMedCrossRef Strohmaier S, Edlinger M, Manjer J, et al. Total serum cholesterol and cancer incidence in the metabolic syndrome and cancer project (Me-Can). PLoS One. 2013;8:e54242.PubMedCentralPubMedCrossRef
8.
go back to reference Kitahara CM, de Berrington GA, Freedman ND, et al. Total cholesterol and cancer risk in a large prospective study in Korea. J Clin Oncol. 2011;29:1592–8.PubMedCentralPubMedCrossRef Kitahara CM, de Berrington GA, Freedman ND, et al. Total cholesterol and cancer risk in a large prospective study in Korea. J Clin Oncol. 2011;29:1592–8.PubMedCentralPubMedCrossRef
9.
go back to reference Iso H, Ikeda A, Inoue M, et al. Serum cholesterol levels in relation to the incidence of cancer: the JPHC study cohorts. Int J Cancer. 2009;125:2679–86.PubMedCrossRef Iso H, Ikeda A, Inoue M, et al. Serum cholesterol levels in relation to the incidence of cancer: the JPHC study cohorts. Int J Cancer. 2009;125:2679–86.PubMedCrossRef
10.
go back to reference Jacobs EJ, Gapstur SM. Cholesterol and cancer: answers and new questions. Cancer Epidemiol Biomarkers Prev. 2009;18:2805–6.PubMedCrossRef Jacobs EJ, Gapstur SM. Cholesterol and cancer: answers and new questions. Cancer Epidemiol Biomarkers Prev. 2009;18:2805–6.PubMedCrossRef
11.
go back to reference Henriksson P, Eriksson M, Ericsson S, et al. Hypocholesterolaemia and increased elimination of low-density lipoproteins in metastatic cancer of the prostate. Lancet. 1989;2:1178–80.PubMedCrossRef Henriksson P, Eriksson M, Ericsson S, et al. Hypocholesterolaemia and increased elimination of low-density lipoproteins in metastatic cancer of the prostate. Lancet. 1989;2:1178–80.PubMedCrossRef
12.
go back to reference Vitols S, Gahrton G, Bjorkholm M, et al. Hypocholesterolaemia in malignancy due to elevated low-density-lipoprotein-receptor activity in tumour cells: evidence from studies in patients with leukaemia. Lancet. 1985;2:1150–4.PubMedCrossRef Vitols S, Gahrton G, Bjorkholm M, et al. Hypocholesterolaemia in malignancy due to elevated low-density-lipoprotein-receptor activity in tumour cells: evidence from studies in patients with leukaemia. Lancet. 1985;2:1150–4.PubMedCrossRef
13.
go back to reference Dessi S, Batetta B, Pulisci D, et al. Altered pattern of lipid metabolism in patients with lung cancer. Oncology. 1992;49:436–41.PubMedCrossRef Dessi S, Batetta B, Pulisci D, et al. Altered pattern of lipid metabolism in patients with lung cancer. Oncology. 1992;49:436–41.PubMedCrossRef
14.
go back to reference Ahn J, Lim U, Weinstein SJ, et al. Prediagnostic total and high-density lipoprotein cholesterol and risk of cancer. Cancer Epidemiol Biomarkers Prev. 2009;18:2814–21.PubMedCentralPubMedCrossRef Ahn J, Lim U, Weinstein SJ, et al. Prediagnostic total and high-density lipoprotein cholesterol and risk of cancer. Cancer Epidemiol Biomarkers Prev. 2009;18:2814–21.PubMedCentralPubMedCrossRef
15.
16.
go back to reference von Eckardstein A, Hersberger M, Rohrer L. Current understanding of the metabolism and biological actions of HDL. Curr Opin Clin Nutr Metab Care. 2005;8:147–52.CrossRef von Eckardstein A, Hersberger M, Rohrer L. Current understanding of the metabolism and biological actions of HDL. Curr Opin Clin Nutr Metab Care. 2005;8:147–52.CrossRef
17.
go back to reference Agnoli C, Berrino F, Abagnato CA, et al. Metabolic syndrome and postmenopausal breast cancer in the ORDET cohort: a nested case–control study. Nutr Metab Cardiovasc Dis. 2010;20:41–8.PubMedCentralPubMedCrossRef Agnoli C, Berrino F, Abagnato CA, et al. Metabolic syndrome and postmenopausal breast cancer in the ORDET cohort: a nested case–control study. Nutr Metab Cardiovasc Dis. 2010;20:41–8.PubMedCentralPubMedCrossRef
18.
go back to reference Furberg AS, Veierod MB, Wilsgaard T, et al. Serum high-density lipoprotein cholesterol, metabolic profile, and breast cancer risk. J Natl Cancer Inst. 2004;96:1152–60.PubMedCrossRef Furberg AS, Veierod MB, Wilsgaard T, et al. Serum high-density lipoprotein cholesterol, metabolic profile, and breast cancer risk. J Natl Cancer Inst. 2004;96:1152–60.PubMedCrossRef
19.
go back to reference Gaard M, Tretli S, Urdal P. Risk of breast cancer in relation to blood lipids: a prospective study of 31,209 Norwegian women. Cancer Causes Control. 1994;5:501–9.PubMedCrossRef Gaard M, Tretli S, Urdal P. Risk of breast cancer in relation to blood lipids: a prospective study of 31,209 Norwegian women. Cancer Causes Control. 1994;5:501–9.PubMedCrossRef
20.
go back to reference Hoyer AP, Engholm G. Serum lipids and breast cancer risk: a cohort study of 5,207 Danish women. Cancer Causes Control. 1992;3:403–8.PubMedCrossRef Hoyer AP, Engholm G. Serum lipids and breast cancer risk: a cohort study of 5,207 Danish women. Cancer Causes Control. 1992;3:403–8.PubMedCrossRef
21.
go back to reference Inoue M, Noda M, Kurahashi N, et al. Impact of metabolic factors on subsequent cancer risk: results from a large-scale population-based cohort study in Japan. Eur J Cancer Prev. 2009;18:240–7.PubMedCrossRef Inoue M, Noda M, Kurahashi N, et al. Impact of metabolic factors on subsequent cancer risk: results from a large-scale population-based cohort study in Japan. Eur J Cancer Prev. 2009;18:240–7.PubMedCrossRef
22.
go back to reference Kucharska-Newton AM, Rosamond WD, Mink PJ, et al. HDL-cholesterol and incidence of breast cancer in the ARIC cohort study. Ann Epidemiol. 2008;18:671–7.PubMedCentralPubMedCrossRef Kucharska-Newton AM, Rosamond WD, Mink PJ, et al. HDL-cholesterol and incidence of breast cancer in the ARIC cohort study. Ann Epidemiol. 2008;18:671–7.PubMedCentralPubMedCrossRef
23.
go back to reference Melvin JC, Seth D, Holmberg L, et al. Lipid profiles and risk of breast and ovarian cancer in the Swedish AMORIS study. Cancer Epidemiol Biomarkers Prev. 2012;21:1381–4.PubMedCrossRef Melvin JC, Seth D, Holmberg L, et al. Lipid profiles and risk of breast and ovarian cancer in the Swedish AMORIS study. Cancer Epidemiol Biomarkers Prev. 2012;21:1381–4.PubMedCrossRef
24.
go back to reference Moorman PG, Hulka BS, Hiatt RA, et al. Association between high-density lipoprotein cholesterol and breast cancer varies by menopausal status. Cancer Epidemiol Biomarkers Prev. 1998;7:483–8.PubMed Moorman PG, Hulka BS, Hiatt RA, et al. Association between high-density lipoprotein cholesterol and breast cancer varies by menopausal status. Cancer Epidemiol Biomarkers Prev. 1998;7:483–8.PubMed
25.
go back to reference Esposito K, Chiodini P, Capuano A, et al. Metabolic syndrome and postmenopausal breast cancer: systematic review and meta-analysis. Menopause. 2013;20:1301–9.PubMedCrossRef Esposito K, Chiodini P, Capuano A, et al. Metabolic syndrome and postmenopausal breast cancer: systematic review and meta-analysis. Menopause. 2013;20:1301–9.PubMedCrossRef
26.
27.
go back to reference Van Hemelrijck M, Walldius G, Jungner I, et al. Low levels of apolipoprotein A-I and HDL are associated with risk of prostate cancer in the Swedish AMORIS study. Cancer Causes Control. 2011;22:1011–9.PubMedCrossRef Van Hemelrijck M, Walldius G, Jungner I, et al. Low levels of apolipoprotein A-I and HDL are associated with risk of prostate cancer in the Swedish AMORIS study. Cancer Causes Control. 2011;22:1011–9.PubMedCrossRef
28.
go back to reference Esposito K, Chiodini P, Capuano A, et al. Effect of metabolic syndrome and its components on prostate cancer risk: meta-analysis. J Endocrinol Invest. 2013;36:132–9.PubMed Esposito K, Chiodini P, Capuano A, et al. Effect of metabolic syndrome and its components on prostate cancer risk: meta-analysis. J Endocrinol Invest. 2013;36:132–9.PubMed
29.
go back to reference Hercberg S, Galan P, Preziosi P, et al. The SU.VI.MAX Study: a randomized, placebo-controlled trial of the health effects of antioxidant vitamins and minerals. Arch Intern Med. 2004;164:2335–42.PubMedCrossRef Hercberg S, Galan P, Preziosi P, et al. The SU.VI.MAX Study: a randomized, placebo-controlled trial of the health effects of antioxidant vitamins and minerals. Arch Intern Med. 2004;164:2335–42.PubMedCrossRef
30.
go back to reference Stamey TA. Second Stanford conference on international standardization of prostate-specific antigen immunoassays: September 1 and 2, 1994. Urology. 1995;45:173–84.PubMedCrossRef Stamey TA. Second Stanford conference on international standardization of prostate-specific antigen immunoassays: September 1 and 2, 1994. Urology. 1995;45:173–84.PubMedCrossRef
31.
go back to reference Le Moullec N, Deheeger M, Preziosi P, et al. Validation du manuel photos utilisé pour l’enquête alimentaire de l’étude SU.VI.MAX. Cah Nutr Diet. 1996;31:158–64. Le Moullec N, Deheeger M, Preziosi P, et al. Validation du manuel photos utilisé pour l’enquête alimentaire de l’étude SU.VI.MAX. Cah Nutr Diet. 1996;31:158–64.
32.
go back to reference Hercberg S. Table de composition SU.VI.MAX des aliments. Paris: Les éditions INSERM/Economica; 2005. Hercberg S. Table de composition SU.VI.MAX des aliments. Paris: Les éditions INSERM/Economica; 2005.
33.
go back to reference Kritchevsky SB, Wilcosky TC, Morris DL, et al. Changes in plasma lipid and lipoprotein cholesterol and weight prior to the diagnosis of cancer. Cancer Res. 1991;51:3198–203.PubMed Kritchevsky SB, Wilcosky TC, Morris DL, et al. Changes in plasma lipid and lipoprotein cholesterol and weight prior to the diagnosis of cancer. Cancer Res. 1991;51:3198–203.PubMed
34.
go back to reference Planella T, Cortes M, Martinez-Bru C, et al. Calculation of LDL-cholesterol by using apolipoprotein B for classification of nonchylomicronemic dyslipemia. Clin Chem. 1997;43:808–15.PubMed Planella T, Cortes M, Martinez-Bru C, et al. Calculation of LDL-cholesterol by using apolipoprotein B for classification of nonchylomicronemic dyslipemia. Clin Chem. 1997;43:808–15.PubMed
35.
go back to reference Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem. 1972;18:499–502.PubMed Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem. 1972;18:499–502.PubMed
36.
go back to reference Huang R, Silva RA, Jerome WG, et al. Apolipoprotein A–I structural organization in high-density lipoproteins isolated from human plasma. Nat Struct Mol Biol. 2011;18:416–22.PubMedCentralPubMedCrossRef Huang R, Silva RA, Jerome WG, et al. Apolipoprotein A–I structural organization in high-density lipoproteins isolated from human plasma. Nat Struct Mol Biol. 2011;18:416–22.PubMedCentralPubMedCrossRef
37.
go back to reference Aleksandrova K, Boeing H, Jenab M, et al. Metabolic syndrome and risks of colon and rectal cancer: the European prospective investigation into cancer and nutrition study. Cancer Prev Res (Phila). 2011;4:1873–83.CrossRef Aleksandrova K, Boeing H, Jenab M, et al. Metabolic syndrome and risks of colon and rectal cancer: the European prospective investigation into cancer and nutrition study. Cancer Prev Res (Phila). 2011;4:1873–83.CrossRef
39.
go back to reference Mihaylova B, Emberson J, Blackwell L, et al. The effects of lowering LDL cholesterol with statin therapy in people at low risk of vascular disease: meta-analysis of individual data from 27 randomised trials. Lancet. 2012;380:581–90.PubMedCrossRef Mihaylova B, Emberson J, Blackwell L, et al. The effects of lowering LDL cholesterol with statin therapy in people at low risk of vascular disease: meta-analysis of individual data from 27 randomised trials. Lancet. 2012;380:581–90.PubMedCrossRef
40.
go back to reference Schatzkin A, Hoover RN, Taylor PR, et al. Serum cholesterol and cancer in the NHANES I epidemiologic followup study. National Health and Nutrition Examination Survey. Lancet. 1987;2:298–301.PubMedCrossRef Schatzkin A, Hoover RN, Taylor PR, et al. Serum cholesterol and cancer in the NHANES I epidemiologic followup study. National Health and Nutrition Examination Survey. Lancet. 1987;2:298–301.PubMedCrossRef
41.
go back to reference Cleeman JI, Grundy SM, Becker D, Clark LT. Expert panel on detection, evaluation, and treatment of high blood cholesterol in adults. Executive summary of the third report of the National Cholesterol Education Program (NCEP) Adult Treatment Panel (ATP III). Jama. 2001;285:2486–97. Cleeman JI, Grundy SM, Becker D, Clark LT. Expert panel on detection, evaluation, and treatment of high blood cholesterol in adults. Executive summary of the third report of the National Cholesterol Education Program (NCEP) Adult Treatment Panel (ATP III). Jama. 2001;285:2486–97.
42.
go back to reference Leon AS, Sanchez OA. Response of blood lipids to exercise training alone or combined with dietary intervention. Med Sci Sports Exerc. 2001;33:S502–15.PubMedCrossRef Leon AS, Sanchez OA. Response of blood lipids to exercise training alone or combined with dietary intervention. Med Sci Sports Exerc. 2001;33:S502–15.PubMedCrossRef
43.
go back to reference World Cancer Research Fund/American Institute for Cancer Research. Food, nutrition, physical activity, and the prevention of cancer: a global perspective. Washington, DC: AICR; 2007. World Cancer Research Fund/American Institute for Cancer Research. Food, nutrition, physical activity, and the prevention of cancer: a global perspective. Washington, DC: AICR; 2007.
44.
go back to reference Kraus WE, Houmard JA, Duscha BD, et al. Effects of the amount and intensity of exercise on plasma lipoproteins. N Engl J Med. 2002;347:1483–92.PubMedCrossRef Kraus WE, Houmard JA, Duscha BD, et al. Effects of the amount and intensity of exercise on plasma lipoproteins. N Engl J Med. 2002;347:1483–92.PubMedCrossRef
45.
go back to reference Esteve E, Ricart W, Fernandez-Real JM. Dyslipidemia and inflammation: an evolutionary conserved mechanism. Clin Nutr. 2005;24:16–31.PubMedCrossRef Esteve E, Ricart W, Fernandez-Real JM. Dyslipidemia and inflammation: an evolutionary conserved mechanism. Clin Nutr. 2005;24:16–31.PubMedCrossRef
46.
go back to reference Beynen AC, Katan MB, Van Zutphen LF. Hypo- and hyperresponders: individual differences in the response of serum cholesterol concentration to changes in diet. Adv Lipid Res. 1987;22:115–71.PubMed Beynen AC, Katan MB, Van Zutphen LF. Hypo- and hyperresponders: individual differences in the response of serum cholesterol concentration to changes in diet. Adv Lipid Res. 1987;22:115–71.PubMed
47.
go back to reference Ordovas JM, Lopez-Miranda J, Mata P, et al. Gene-diet interaction in determining plasma lipid response to dietary intervention. Atherosclerosis. 1995;118(Suppl.):S11–27.PubMedCrossRef Ordovas JM, Lopez-Miranda J, Mata P, et al. Gene-diet interaction in determining plasma lipid response to dietary intervention. Atherosclerosis. 1995;118(Suppl.):S11–27.PubMedCrossRef
48.
go back to reference Al-Delaimy WK, Jansen EH, Peeters PH, et al. Reliability of biomarkers of iron status, blood lipids, oxidative stress, vitamin D, C-reactive protein and fructosamine in two Dutch cohorts. Biomarkers. 2006;11:370–82.PubMedCrossRef Al-Delaimy WK, Jansen EH, Peeters PH, et al. Reliability of biomarkers of iron status, blood lipids, oxidative stress, vitamin D, C-reactive protein and fructosamine in two Dutch cohorts. Biomarkers. 2006;11:370–82.PubMedCrossRef
49.
go back to reference Bairaktari E, Hatzidimou K, Tzallas C, et al. Estimation of LDL cholesterol based on the Friedewald formula and on apo B levels. Clin Biochem. 2000;33:549–55.PubMedCrossRef Bairaktari E, Hatzidimou K, Tzallas C, et al. Estimation of LDL cholesterol based on the Friedewald formula and on apo B levels. Clin Biochem. 2000;33:549–55.PubMedCrossRef
50.
go back to reference Binder-Foucard F, Belot A, Delafosse P, et al. National estimate of the incidence and mortality from cancer in France between 1980 and 2012. Part 1—solid tumors. Saint-Maurice: Institut de veille sanitaire; 2013. Binder-Foucard F, Belot A, Delafosse P, et al. National estimate of the incidence and mortality from cancer in France between 1980 and 2012. Part 1—solid tumors. Saint-Maurice: Institut de veille sanitaire; 2013.
51.
go back to reference Anderson KM, Odell PM, Wilson PW, et al. Cardiovascular disease risk profiles. Am Heart J. 1991;121:293–8.PubMedCrossRef Anderson KM, Odell PM, Wilson PW, et al. Cardiovascular disease risk profiles. Am Heart J. 1991;121:293–8.PubMedCrossRef
Metadata
Title
Prospective associations between serum biomarkers of lipid metabolism and overall, breast and prostate cancer risk
Authors
Mathilde His
Laurent Zelek
Mélanie Deschasaux
Camille Pouchieu
Emmanuelle Kesse-Guyot
Serge Hercberg
Pilar Galan
Paule Latino-Martel
Jacques Blacher
Mathilde Touvier
Publication date
01-02-2014
Publisher
Springer Netherlands
Published in
European Journal of Epidemiology / Issue 2/2014
Print ISSN: 0393-2990
Electronic ISSN: 1573-7284
DOI
https://doi.org/10.1007/s10654-014-9884-5

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