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Published in: Cancer Causes & Control 4/2010

01-04-2010 | Original paper

Longitudinal associations of blood markers of insulin and glucose metabolism and cancer mortality in the third National Health and Nutrition Examination Survey

Authors: Niyati Parekh, Yong Lin, Richard B. Hayes, Jeanine B. Albu, Grace L. Lu-Yao

Published in: Cancer Causes & Control | Issue 4/2010

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Abstract

Insulin and glucose may influence cancer mortality via their proliferative and anti-apoptotic properties. Using longitudinal data from the nationally representative Third National Health and Nutrition Examination Survey (NHANES III; 1988–1994), with an average follow-up of 8.5 years to death, we evaluated markers of glucose and insulin metabolism, with cancer mortality, ascertained using death certificates or the National Death Index. Plasma glucose, insulin, C-peptide, and lipid concentrations were measured. Anthropometrics, lifestyle, medical, and demographic information was obtained during in-person interviews. After adjusting for age, race, sex, smoking status, physical activity, and body mass index, for every 50 mg/dl increase in plasma glucose, there was a 22% increased risk of overall cancer mortality. Insulin resistance was associated with a 41% (95% confidence interval (CI) (1.07–1.87; p = 0.01) increased risk of overall cancer mortality. These associations were stronger after excluding lung cancer deaths for insulin-resistant individuals (HR: 1.67; 95% CI: 1.15–2.42; p = 0.01), specifically among those with lower levels of physical activity (HR: 2.06; 95% CI: 1.4–3.0; p = 0.0001). Similar associations were observed for other blood markers of glucose and insulin, albeit not statistically significant. In conclusion, hyperglycemia and insulin resistance may be ‘high-risk’ conditions for cancer mortality. Managing these conditions may be effective cancer control tools.
Literature
1.
2.
go back to reference US Mortality Data (2006) 1960–2004, National Center for Health Statistics, Centers for Disease Control and Prevention, Atlanta, GA and National Center for Health Statistics, Hyattsville, MD pp 1–754 US Mortality Data (2006) 1960–2004, National Center for Health Statistics, Centers for Disease Control and Prevention, Atlanta, GA and National Center for Health Statistics, Hyattsville, MD pp 1–754
3.
5.
go back to reference Reaven GM (1991) Insulin resistance, hyperinsulinemia, hypertriglyceridemia, and hypertension. Parallels between human disease and rodent models. Diabetes Care 14(3):195–202CrossRefPubMed Reaven GM (1991) Insulin resistance, hyperinsulinemia, hypertriglyceridemia, and hypertension. Parallels between human disease and rodent models. Diabetes Care 14(3):195–202CrossRefPubMed
7.
go back to reference Hedley AA, Ogden CL, Johnson CL, Carroll MD, Curtin LR, Flegal KM (2004) Prevalence of overweight and obesity among US children, adolescents, and adults, 1999–2002. JAMA 291(23):2847–2850CrossRefPubMed Hedley AA, Ogden CL, Johnson CL, Carroll MD, Curtin LR, Flegal KM (2004) Prevalence of overweight and obesity among US children, adolescents, and adults, 1999–2002. JAMA 291(23):2847–2850CrossRefPubMed
8.
go back to reference Ogden CL, Carroll MD, Curtin LR, McDowell MA, Tabak CJ, Flegal KM (2006) Prevalence of overweight and obesity in the United States, 1999–2004. JAMA 295(13):1549–1555CrossRefPubMed Ogden CL, Carroll MD, Curtin LR, McDowell MA, Tabak CJ, Flegal KM (2006) Prevalence of overweight and obesity in the United States, 1999–2004. JAMA 295(13):1549–1555CrossRefPubMed
9.
go back to reference Vainio H, Kaaks R, Bianchini F (2002) Weight control and physical activity in cancer prevention: international evaluation of the evidence. Eur J Cancer Prev 11(Suppl 2):S94–S100PubMed Vainio H, Kaaks R, Bianchini F (2002) Weight control and physical activity in cancer prevention: international evaluation of the evidence. Eur J Cancer Prev 11(Suppl 2):S94–S100PubMed
10.
go back to reference Calle EE, Rodriguez C, Walker-Thurmond K, Thun MJ (2003) Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N Engl J Med 348(17):1625–1638CrossRefPubMed Calle EE, Rodriguez C, Walker-Thurmond K, Thun MJ (2003) Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N Engl J Med 348(17):1625–1638CrossRefPubMed
11.
go back to reference Komninou D, Ayonote A, Richie JP Jr, Rigas B (2003) Insulin resistance and its contribution to colon carcinogenesis. Exp Biol Med (Maywood) 228(4):396–405 Komninou D, Ayonote A, Richie JP Jr, Rigas B (2003) Insulin resistance and its contribution to colon carcinogenesis. Exp Biol Med (Maywood) 228(4):396–405
12.
go back to reference LeRoith D, Novosyadlyy R, Gallagher EJ, Lann D, Vijayakumar A, Yakar S (2008) Obesity and type 2 diabetes are associated with an increased risk of developing cancer and a worse prognosis; epidemiological and mechanistic evidence. Exp Clin Endocrinol Diabetes 116(Suppl 1):S4–S6CrossRefPubMed LeRoith D, Novosyadlyy R, Gallagher EJ, Lann D, Vijayakumar A, Yakar S (2008) Obesity and type 2 diabetes are associated with an increased risk of developing cancer and a worse prognosis; epidemiological and mechanistic evidence. Exp Clin Endocrinol Diabetes 116(Suppl 1):S4–S6CrossRefPubMed
13.
go back to reference Saydah SH, Platz EA, Rifai N, Pollak MN, Brancati FL, Helzlsouer KJ (2003) Association of markers of insulin and glucose control with subsequent colorectal cancer risk. Cancer Epidemiol Biomark Prev 12(5):412–418 Saydah SH, Platz EA, Rifai N, Pollak MN, Brancati FL, Helzlsouer KJ (2003) Association of markers of insulin and glucose control with subsequent colorectal cancer risk. Cancer Epidemiol Biomark Prev 12(5):412–418
14.
go back to reference Rinaldi S, Rohrmann S, Jenab M et al (2008) Glycosylated hemoglobin and risk of colorectal cancer in men and women, the European prospective investigation into cancer and nutrition. Cancer Epidemiol Biomark Prev 17(11):3108–3115CrossRef Rinaldi S, Rohrmann S, Jenab M et al (2008) Glycosylated hemoglobin and risk of colorectal cancer in men and women, the European prospective investigation into cancer and nutrition. Cancer Epidemiol Biomark Prev 17(11):3108–3115CrossRef
15.
go back to reference Jee SH, Ohrr H, Sull JW, Yun JE, Ji M, Samet JM (2005) Fasting serum glucose level and cancer risk in Korean men and women. JAMA 293(2):194–202CrossRefPubMed Jee SH, Ohrr H, Sull JW, Yun JE, Ji M, Samet JM (2005) Fasting serum glucose level and cancer risk in Korean men and women. JAMA 293(2):194–202CrossRefPubMed
16.
go back to reference Siddiqui AA, Spechler SJ, Huerta S, Dredar S, Little BB, Cryer B (2008) Elevated HbA1c is an independent predictor of aggressive clinical behavior in patients with colorectal cancer: a case-control study. Dig Dis Sci 53(9):2486–2494CrossRefPubMed Siddiqui AA, Spechler SJ, Huerta S, Dredar S, Little BB, Cryer B (2008) Elevated HbA1c is an independent predictor of aggressive clinical behavior in patients with colorectal cancer: a case-control study. Dig Dis Sci 53(9):2486–2494CrossRefPubMed
17.
go back to reference Jullumstro E, Kollind M, Lydersen S, Edna TH (2009) Diabetes mellitus and outcomes of colorectal cancer. Acta Oncol 48(3):361–367CrossRefPubMed Jullumstro E, Kollind M, Lydersen S, Edna TH (2009) Diabetes mellitus and outcomes of colorectal cancer. Acta Oncol 48(3):361–367CrossRefPubMed
18.
go back to reference Coughlin SS, Calle EE, Teras LR, Petrelli J, Thun MJ (2004) Diabetes mellitus as a predictor of cancer mortality in a large cohort of US adults. Am J Epidemiol 159(12):1160–1167CrossRefPubMed Coughlin SS, Calle EE, Teras LR, Petrelli J, Thun MJ (2004) Diabetes mellitus as a predictor of cancer mortality in a large cohort of US adults. Am J Epidemiol 159(12):1160–1167CrossRefPubMed
19.
go back to reference Oba S, Nagata C, Nakamura K, Takatsuka N, Shimizu H (2008) Self-reported diabetes mellitus and risk of mortality from all causes, cardiovascular disease, and cancer in Takayama: a population-based prospective cohort study in Japan. J Epidemiol 18(5):197–203CrossRefPubMed Oba S, Nagata C, Nakamura K, Takatsuka N, Shimizu H (2008) Self-reported diabetes mellitus and risk of mortality from all causes, cardiovascular disease, and cancer in Takayama: a population-based prospective cohort study in Japan. J Epidemiol 18(5):197–203CrossRefPubMed
20.
go back to reference Trevisan M, Liu J, Muti P, Misciagna G, Menotti A, Fucci F (2001) Markers of insulin resistance and colorectal cancer mortality. Cancer Epidemiol Biomark Prev 10(9):937–941 Trevisan M, Liu J, Muti P, Misciagna G, Menotti A, Fucci F (2001) Markers of insulin resistance and colorectal cancer mortality. Cancer Epidemiol Biomark Prev 10(9):937–941
21.
go back to reference Goodwin PJ, Ennis M, Pritchard KI et al (2002) Fasting insulin and outcome in early-stage breast cancer: results of a prospective cohort study. J Clin Oncol 20(1):42–51CrossRefPubMed Goodwin PJ, Ennis M, Pritchard KI et al (2002) Fasting insulin and outcome in early-stage breast cancer: results of a prospective cohort study. J Clin Oncol 20(1):42–51CrossRefPubMed
22.
go back to reference Colangelo LA, Gapstur SM, Gann PH, Dyer AR, Liu K (2002) Colorectal cancer mortality and factors related to the insulin resistance syndrome. Cancer Epidemiol Biomark Prev 11(4):385–391 Colangelo LA, Gapstur SM, Gann PH, Dyer AR, Liu K (2002) Colorectal cancer mortality and factors related to the insulin resistance syndrome. Cancer Epidemiol Biomark Prev 11(4):385–391
23.
go back to reference Jaggers JR, Sui X, Hooker SP et al. (2009) Metabolic syndrome and risk of cancer mortality in men. Eur J Cancer 45(10):1831–1838 Jaggers JR, Sui X, Hooker SP et al. (2009) Metabolic syndrome and risk of cancer mortality in men. Eur J Cancer 45(10):1831–1838
24.
go back to reference National Center of Health Statistics (1995) Plan and operation of the third National Health and Nutrition Examination Survey, 1988-1994. National Center of Health Statistics, Hyattsville, MD, pp 1–754 National Center of Health Statistics (1995) Plan and operation of the third National Health and Nutrition Examination Survey, 1988-1994. National Center of Health Statistics, Hyattsville, MD, pp 1–754
25.
go back to reference Executive summary of the third report of the National Cholesterol Education Program (NCEP) (2001) Expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (Adult Treatment Panel III). JAMA 285(19):2486–2497 Executive summary of the third report of the National Cholesterol Education Program (NCEP) (2001) Expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (Adult Treatment Panel III). JAMA 285(19):2486–2497
26.
go back to reference Gunter EW, Lewis BG, Koncikowski SM (1996) Laboratory procedures used for the third National Health and Nutrition Examination Survey (NHANES III), 1988–1994. U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, Hyattsville Gunter EW, Lewis BG, Koncikowski SM (1996) Laboratory procedures used for the third National Health and Nutrition Examination Survey (NHANES III), 1988–1994. U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, Hyattsville
27.
go back to reference Standards of medical care in diabetes (2008) Diabetes Care. Suppl 1:S12–S54 Standards of medical care in diabetes (2008) Diabetes Care. Suppl 1:S12–S54
28.
go back to reference Nguyen NT, Magno CP, Lane KT, Hinojosa MW, Lane JS (2008) Association of hypertension, diabetes, dyslipidemia, and metabolic syndrome with obesity: findings from the National Health and Nutrition Examination Survey, 1999 to 2004. J Am Coll Surg 207(6):928–934CrossRefPubMed Nguyen NT, Magno CP, Lane KT, Hinojosa MW, Lane JS (2008) Association of hypertension, diabetes, dyslipidemia, and metabolic syndrome with obesity: findings from the National Health and Nutrition Examination Survey, 1999 to 2004. J Am Coll Surg 207(6):928–934CrossRefPubMed
29.
go back to reference Wallace TM, Levy JC, Matthews DR (2004) Use and abuse of HOMA modeling. Diabetes Care 27(6):1487–1495CrossRefPubMed Wallace TM, Levy JC, Matthews DR (2004) Use and abuse of HOMA modeling. Diabetes Care 27(6):1487–1495CrossRefPubMed
30.
go back to reference Yokoyama H, Emoto M, Fujiwara S et al (2004) Quantitative insulin sensitivity check index and the reciprocal index of homeostasis model assessment are useful indexes of insulin resistance in type 2 diabetic patients with wide range of fasting plasma glucose. J Clin Endocrinol Metab 89(3):1481–1484CrossRefPubMed Yokoyama H, Emoto M, Fujiwara S et al (2004) Quantitative insulin sensitivity check index and the reciprocal index of homeostasis model assessment are useful indexes of insulin resistance in type 2 diabetic patients with wide range of fasting plasma glucose. J Clin Endocrinol Metab 89(3):1481–1484CrossRefPubMed
31.
go back to reference Simental-Mendia LE, Rodriguez-Moran M, Guerrero-Romero F (2008) The product of fasting glucose and triglycerides as surrogate for identifying insulin resistance in apparently healthy subjects. Metab Syndr Relat Disord 6(4):299–304CrossRefPubMed Simental-Mendia LE, Rodriguez-Moran M, Guerrero-Romero F (2008) The product of fasting glucose and triglycerides as surrogate for identifying insulin resistance in apparently healthy subjects. Metab Syndr Relat Disord 6(4):299–304CrossRefPubMed
32.
go back to reference Mack R, Skurnick B, Sterling-Jean Y, Pedra-Nobre M, Bigg D (2003) Fasting insulin levels as a measure of insulin resistance in American Blacks. J Med 34(1–6):31–38PubMed Mack R, Skurnick B, Sterling-Jean Y, Pedra-Nobre M, Bigg D (2003) Fasting insulin levels as a measure of insulin resistance in American Blacks. J Med 34(1–6):31–38PubMed
33.
go back to reference Bonser AM, Garcia-Webb P (1984) C-peptide measurement: methods and clinical utility. Crit Rev Clin Lab Sci 19(4):297–352CrossRefPubMed Bonser AM, Garcia-Webb P (1984) C-peptide measurement: methods and clinical utility. Crit Rev Clin Lab Sci 19(4):297–352CrossRefPubMed
34.
go back to reference World Health Organization (1995) World Health Organization physical status: the use and interpretation of anthropometry. World Health Organization, Geneva World Health Organization (1995) World Health Organization physical status: the use and interpretation of anthropometry. World Health Organization, Geneva
36.
go back to reference Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ (2009) Cancer statistics, 2009. CA Cancer J Clin 59(4):225–249CrossRefPubMed Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ (2009) Cancer statistics, 2009. CA Cancer J Clin 59(4):225–249CrossRefPubMed
37.
go back to reference Papanas N, Giatromanolaki A, Galazios G, Maltezos E, Sivridis E (2006) Endometrial carcinoma and diabetes revisited. Eur J Gynaecol Oncol 27(5):505–508PubMed Papanas N, Giatromanolaki A, Galazios G, Maltezos E, Sivridis E (2006) Endometrial carcinoma and diabetes revisited. Eur J Gynaecol Oncol 27(5):505–508PubMed
38.
go back to reference Hammarsten J, Hogstedt B (2005) Hyperinsulinaemia: a prospective risk factor for lethal clinical prostate cancer. Eur J Cancer 41(18):2887–2895CrossRefPubMed Hammarsten J, Hogstedt B (2005) Hyperinsulinaemia: a prospective risk factor for lethal clinical prostate cancer. Eur J Cancer 41(18):2887–2895CrossRefPubMed
39.
go back to reference Barone BB, Yeh HC, Snyder CF et al (2008) Long-term all-cause mortality in cancer patients with preexisting diabetes mellitus: a systematic review and meta-analysis. JAMA 300(23):2754–2764CrossRefPubMed Barone BB, Yeh HC, Snyder CF et al (2008) Long-term all-cause mortality in cancer patients with preexisting diabetes mellitus: a systematic review and meta-analysis. JAMA 300(23):2754–2764CrossRefPubMed
40.
go back to reference Ganapathy V, Thangaraju M, Prasad PD (2009) Nutrient transporters in cancer: relevance to Warburg hypothesis and beyond. Pharmacol Ther 121(1):29–40CrossRefPubMed Ganapathy V, Thangaraju M, Prasad PD (2009) Nutrient transporters in cancer: relevance to Warburg hypothesis and beyond. Pharmacol Ther 121(1):29–40CrossRefPubMed
41.
go back to reference Okumura M, Yamamoto M, Sakuma H et al (2002) Leptin and high glucose stimulate cell proliferation in MCF-7 human breast cancer cells: reciprocal involvement of PKC-alpha and PPAR expression. Biochim Biophys Acta 1592(2):107–116PubMed Okumura M, Yamamoto M, Sakuma H et al (2002) Leptin and high glucose stimulate cell proliferation in MCF-7 human breast cancer cells: reciprocal involvement of PKC-alpha and PPAR expression. Biochim Biophys Acta 1592(2):107–116PubMed
42.
go back to reference Vander Heiden MG, Plas DR, Rathmell JC, Fox CJ, Harris MH, Thompson CB (2001) Growth factors can influence cell growth and survival through effects on glucose metabolism. Mol Cell Biol 21(17):5899–5912CrossRef Vander Heiden MG, Plas DR, Rathmell JC, Fox CJ, Harris MH, Thompson CB (2001) Growth factors can influence cell growth and survival through effects on glucose metabolism. Mol Cell Biol 21(17):5899–5912CrossRef
43.
go back to reference Giovannucci E (2001) Insulin, insulin-like growth factors and colon cancer: a review of the evidence. J Nutr 131(11 Suppl):3109S–3120SPubMed Giovannucci E (2001) Insulin, insulin-like growth factors and colon cancer: a review of the evidence. J Nutr 131(11 Suppl):3109S–3120SPubMed
44.
go back to reference Becker S, Dossus L, Kaaks R (2009) Obesity related hyperinsulinaemia and hyperglycemia and cancer development. Arch Physiol Biochem 115(2):86–96 Becker S, Dossus L, Kaaks R (2009) Obesity related hyperinsulinaemia and hyperglycemia and cancer development. Arch Physiol Biochem 115(2):86–96
45.
go back to reference Semple RK, Sleigh A, Murgatroyd PR et al (2009) Postreceptor insulin resistance contributes to human dyslipidemia and hepatic steatosis. J Clin Invest 119(2):315–322PubMed Semple RK, Sleigh A, Murgatroyd PR et al (2009) Postreceptor insulin resistance contributes to human dyslipidemia and hepatic steatosis. J Clin Invest 119(2):315–322PubMed
46.
go back to reference Yudkin JS, Stehouwer CD, Emeis JJ, Coppack SW (1999) C-reactive protein in healthy subjects: associations with obesity, insulin resistance, and endothelial dysfunction: a potential role for cytokines originating from adipose tissue? Arterioscler Thromb Vasc Biol 19(4):972–978PubMed Yudkin JS, Stehouwer CD, Emeis JJ, Coppack SW (1999) C-reactive protein in healthy subjects: associations with obesity, insulin resistance, and endothelial dysfunction: a potential role for cytokines originating from adipose tissue? Arterioscler Thromb Vasc Biol 19(4):972–978PubMed
47.
go back to reference Choi KM, Ryu OH, Lee KW et al (2006) Serum adiponectin, interleukin-10 levels and inflammatory markers in the metabolic syndrome. Diabetes Res Clin Pract Choi KM, Ryu OH, Lee KW et al (2006) Serum adiponectin, interleukin-10 levels and inflammatory markers in the metabolic syndrome. Diabetes Res Clin Pract
48.
go back to reference Erlinger TP, Platz EA, Rifai N, Helzlsouer KJ (2004) C-reactive protein and the risk of incident colorectal cancer. JAMA 291(5):585–590CrossRefPubMed Erlinger TP, Platz EA, Rifai N, Helzlsouer KJ (2004) C-reactive protein and the risk of incident colorectal cancer. JAMA 291(5):585–590CrossRefPubMed
49.
go back to reference Il’yasova D, Colbert LH, Harris TB et al (2005) Circulating levels of inflammatory markers and cancer risk in the health aging and body composition cohort. Cancer Epidemiol Biomark Prev 14(10):2413–2418CrossRef Il’yasova D, Colbert LH, Harris TB et al (2005) Circulating levels of inflammatory markers and cancer risk in the health aging and body composition cohort. Cancer Epidemiol Biomark Prev 14(10):2413–2418CrossRef
50.
go back to reference Bahia L, Aguiar LG, Villela N et al (2006) Relationship between adipokines, inflammation, and vascular reactivity in lean controls and obese subjects with metabolic syndrome. Clinics 61(5):433–440CrossRefPubMed Bahia L, Aguiar LG, Villela N et al (2006) Relationship between adipokines, inflammation, and vascular reactivity in lean controls and obese subjects with metabolic syndrome. Clinics 61(5):433–440CrossRefPubMed
51.
go back to reference Grivennikov SI and Karin M (2009) Inflammation and oncogenesis: a vicious connection. Curr Opin Genet Dev 20:1–7 Grivennikov SI and Karin M (2009) Inflammation and oncogenesis: a vicious connection. Curr Opin Genet Dev 20:1–7
52.
go back to reference Michaud DS, Wolpin B, Giovannucci E et al (2007) Prediagnostic plasma C-peptide and pancreatic cancer risk in men and women. Cancer Epidemiol Biomark Prev 16(10):2101–2109CrossRef Michaud DS, Wolpin B, Giovannucci E et al (2007) Prediagnostic plasma C-peptide and pancreatic cancer risk in men and women. Cancer Epidemiol Biomark Prev 16(10):2101–2109CrossRef
53.
go back to reference Wei EK, Ma J, Pollak MN et al (2005) A prospective study of C-peptide, insulin-like growth factor-I, insulin-like growth factor binding protein-1, and the risk of colorectal cancer in women. Cancer Epidemiol Biomark Prev 14(4):850–855CrossRef Wei EK, Ma J, Pollak MN et al (2005) A prospective study of C-peptide, insulin-like growth factor-I, insulin-like growth factor binding protein-1, and the risk of colorectal cancer in women. Cancer Epidemiol Biomark Prev 14(4):850–855CrossRef
54.
go back to reference Ma J, Giovannucci E, Pollack M et al. (2004) Prospective study of plasma C-peptide and colorectal cancer risk in men J Nat Cancer Inst 96:546–553 Ma J, Giovannucci E, Pollack M et al. (2004) Prospective study of plasma C-peptide and colorectal cancer risk in men J Nat Cancer Inst 96:546–553
55.
go back to reference Batty GD, Shipley MJ, Jarrett RJ, Breeze E, Marmot MG, Smith GD (2005) Obesity and overweight in relation to organ-specific cancer mortality in London (UK): findings from the original Whitehall study. Int J Obes (Lond) 29(10):1267–1274 Batty GD, Shipley MJ, Jarrett RJ, Breeze E, Marmot MG, Smith GD (2005) Obesity and overweight in relation to organ-specific cancer mortality in London (UK): findings from the original Whitehall study. Int J Obes (Lond) 29(10):1267–1274
56.
go back to reference Percy C, Stanek E III, Gloeckler L (1981) Accuracy of cancer death certificates and its effect on cancer mortality statistics. Am J Public Health 71(3):242–250CrossRefPubMed Percy C, Stanek E III, Gloeckler L (1981) Accuracy of cancer death certificates and its effect on cancer mortality statistics. Am J Public Health 71(3):242–250CrossRefPubMed
57.
go back to reference Melamed ML, Michos ED, Post W, Astor B (2008) 25-Hydroxyvitamin D levels and the risk of mortality in the general population. Arch Intern Med 168(15):1629–1637CrossRefPubMed Melamed ML, Michos ED, Post W, Astor B (2008) 25-Hydroxyvitamin D levels and the risk of mortality in the general population. Arch Intern Med 168(15):1629–1637CrossRefPubMed
58.
go back to reference Saydah S, Graubard B, Ballard-Barbash R, Berrigan D (2007) Insulin-like growth factors and subsequent risk of mortality in the United States. Am J Epidemiol 166(5):518–526CrossRefPubMed Saydah S, Graubard B, Ballard-Barbash R, Berrigan D (2007) Insulin-like growth factors and subsequent risk of mortality in the United States. Am J Epidemiol 166(5):518–526CrossRefPubMed
59.
go back to reference Zhang Q, Wang Y, Huang ES (2009) Changes in racial/ethnic disparities in the prevalence of Type 2 diabetes by obesity level among US adults. Ethn Health 9:1–19 Zhang Q, Wang Y, Huang ES (2009) Changes in racial/ethnic disparities in the prevalence of Type 2 diabetes by obesity level among US adults. Ethn Health 9:1–19
60.
go back to reference Gregg EW, Cheng YJ, Narayan KM, Thompson TJ, Williamson DF (2007) The relative contributions of different levels of overweight and obesity to the increased prevalence of diabetes in the United States: 1976–2004. Prev Med 45(5):348–352CrossRefPubMed Gregg EW, Cheng YJ, Narayan KM, Thompson TJ, Williamson DF (2007) The relative contributions of different levels of overweight and obesity to the increased prevalence of diabetes in the United States: 1976–2004. Prev Med 45(5):348–352CrossRefPubMed
Metadata
Title
Longitudinal associations of blood markers of insulin and glucose metabolism and cancer mortality in the third National Health and Nutrition Examination Survey
Authors
Niyati Parekh
Yong Lin
Richard B. Hayes
Jeanine B. Albu
Grace L. Lu-Yao
Publication date
01-04-2010
Publisher
Springer Netherlands
Published in
Cancer Causes & Control / Issue 4/2010
Print ISSN: 0957-5243
Electronic ISSN: 1573-7225
DOI
https://doi.org/10.1007/s10552-009-9492-y

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