Advertisement

Cancer Causes & Control

, Volume 18, Issue 1, pp 7–27 | Cite as

Trace elements and cancer risk: a review of the epidemiologic evidence

  • Stephanie A. Navarro Silvera
  • Thomas E. Rohan
Review

Abstract

Worldwide, there are more than 10 million new cancer cases each year, and cancer is the cause of approximately 12% of all deaths. Given this, a large number of epidemiologic studies have been undertaken to identify potential risk factors for cancer, amongst which the association with trace elements has received considerable attention. Trace elements, such as selenium, zinc, arsenic, cadmium, and nickel, are found naturally in the environment, and human exposure derives from a variety of sources, including air, drinking water, and food. Trace elements are of particular interest given that the levels of exposure to them are potentially modifiable. In this review, we focus largely on the association between each of the trace elements noted above and risk of cancers of the lung, breast, colorectum, prostate, urinary bladder, and stomach. Overall, the evidence currently available appears to support an inverse association between selenium exposure and prostate cancer risk, and possibly also a reduction in risk with respect to lung cancer, although additional prospective studies are needed. There is also limited evidence for an inverse association between zinc and breast cancer, and again, prospective studies are needed to confirm this. Most studies have reported no association between selenium and risk of breast, colorectal, and stomach cancer, and between zinc and prostate cancer risk. There is compelling evidence in support of positive associations between arsenic and risk of both lung and bladder cancers, and between cadmium and lung cancer risk.

Keywords

Trace elements Selenium Zinc Arsenic Cadmium Nickel Neoplasms 

Abbreviations

ATBC

Alpha-Tocopherol Beta-Carotene Cancer Prevention Cohort

As

arsenic

AAS

atomic absorption spectrophotometry

AES

atomic emission spectrophotometry

AR

attributable risk

Cd

cadmium

EMR

excessive mortality rate

FAA

flame atomic absorption

GC

gastric cardia adenocarcinoma

ICP-MS

inductively coupled plasma mass spectometry

IARC

International Agency for Research on Cancer

NAA

neutron activation analysis

Ni

nickel

OG

non-cardia gastric adenocarcinoma

ppb

part per billion

Se

selenium

SIR

standardized incidence ratio

SMR

standardized mortality ratio

SELECT

The Selenium and Vitamin E Cancer Prevention Trial

ATSDR

United States Department of Health and Human Services Agency for Toxic Substances & Disease Registry

Zn

zinc

References

  1. 1.
    Parkin DM, Bray F, Ferlay J, Pisani P (2005) Global cancer statistics, 2002. CA Cancer J Clin 55: 74–108PubMedGoogle Scholar
  2. 2.
    World Health Organization (1996) Trace elements in human nutrition and health. World Health Organization, GenevaGoogle Scholar
  3. 3.
    Whanger PD (2004) Selenium and its relationship to cancer: an update dagger. Br J Nutr 91:11–28PubMedCrossRefGoogle Scholar
  4. 4.
    Prasad AS, Kucuk O (2002) Zinc in cancer prevention. Cancer Metastasis Rev 21:291–295PubMedCrossRefGoogle Scholar
  5. 5.
    Sattar N, Scott HR, McMillan DC, Talwar D, O’Reilly DSJ, Fell GS (1997) Acute-phase reactants and plasma trace element concentrations in non-small cell lung cancer patients and controls. Nutr Cancer 28:308–312PubMedCrossRefGoogle Scholar
  6. 6.
    Blot WJ, Brown LM, Pottern LM, Stone BJ, Fraumeni Jr JF (1983) Lung cancer among long-term steel workers. Am J Epidemiol 117:706–716PubMedGoogle Scholar
  7. 7.
    Hayes RB (1997) The carcinogenicity of metals in humans. Cancer Causes Control 8:371–385PubMedCrossRefGoogle Scholar
  8. 8.
    International Agency for Research on Cancer (IARC) (1993) IARC monographs on the evaluation of the carcinogenic risk to man: beryllium, cadmium, mercury, and exposures in the glass manufacturing industry. Working Group views and expert opinions. IARC Press, LyonGoogle Scholar
  9. 9.
    International Agency for Research on Cancer (IARC) (1999) Arsenic and arsenic compounds. Overall evaluations of carcinogenicity: an updating of IARC Monographs Volumes 1 to 42. IARC, Lyon (France). Report No.: Supplement 7Google Scholar
  10. 10.
    International Agency for Research on Cancer (IARC) (1990) Chromium, nickel and welding. IARC Monogr Eval Carcinog Risk Chem Man 49:1–648Google Scholar
  11. 11.
    Agency for Toxic Substances and Disease Registry (ATSDR) (2003) Toxicological profile for arsenic. United States Department of Health and Human Services Agency for Toxic Substances and Disease Registry, Atlanta, GA, Report No.: 7440-38-2Google Scholar
  12. 12.
    Rasmussen L, Andersen KJ (2003) Environmental health and human exposure assessment. In: World Health Organization, UNICEF, editors. Arsenic in drinking water. IWA, London, pp 67–168Google Scholar
  13. 13.
    Agency for Toxic Substances and Disease Registry (ATSDR) (1999) Toxicological profile for cadmium. United States Department of Health and Human Services Agency for Toxic Substances and Disease Registry, Atlanta, GA, Report No.: 7440-43-9Google Scholar
  14. 14.
    WHO Regional Office for Europe (2000) Air quality guidelines, 2nd edn. World Health Organization, Copenhagen, DenmarkGoogle Scholar
  15. 15.
    Agency for Toxic Substances and Disease Registry (ATSDR) (2003) Toxicological profile for nickel. United States Department of Health and Human Services Agency for Toxic Substances and Disease Registry, Atlanta, GA, Report No.: 7440-02-0Google Scholar
  16. 16.
    Lamm SH, Engel A, Kruse MB, et al (2004) Arsenic in drinking water and bladder cancer mortality in the United States: an analysis based on 133 U.S. counties and 30 years of observation. J Occup Environ Med 46:298–306PubMedCrossRefGoogle Scholar
  17. 17.
    Agency for Toxic Substances, Disease Registry (ATSDR) (2003) Toxicological profile for zinc. United States Department of Health and Human Services Agency for Toxic Substances and Disease Registry, Atlanta, GA, Report No.: 7440-66-6Google Scholar
  18. 18.
    Agency for Toxic Substances and Disease Registry (ATSDR) (2003) Toxicological profile for selenium. United States Department of Health and Human Services Agency for Toxic Substances and Disease Registry, Atlanta, GA, Report No.: 7782-49-2Google Scholar
  19. 19.
    Abdulla M, Parr RM, Iyengar GV (1993) Trace element requirements, intake and recommendations. In: Prasad AS (eds) Essential and toxic trace elements in human health and disease: an update. Wiley-Liss, New York, pp 311–328Google Scholar
  20. 20.
    Hunter, D, Morris, JS, Chute, CG,  et al. 1990Predictors of selenium concentration in human toenailsAm J Epidemiol132114122PubMedGoogle Scholar
  21. 21.
    Burguera JL, Burguera M, Gallignani M, Alarcon OM, Burguera JA (1990) Blood serum selenium in the province of Merida, Venezuela, related to sex, cancer incidence, and soil selenium contnet. J Trace Elem Electrolytes Health Dis 4:73–77PubMedGoogle Scholar
  22. 22.
    Agency for Toxic Substances and Disease Registry (ATSDR) (2001) ToxFAQs. U.S. Department of Health and Human Services, Public Health Service, Atlanta, GAGoogle Scholar
  23. 23.
    Meyer F, Verreault R (1987) Erythrocyte selemium and breast cancer risk. Am J Epidemiol 125:917–919PubMedGoogle Scholar
  24. 24.
    Garland M, Morris JS, Rosner B, et al (1993) Toenail trace element levels as biomarkers: reproducibility over a 6-year period. Cancer Epidemiol Biomarkers Prev 2:493–497Google Scholar
  25. 25.
    Swanson CA, Longnecker MP, Veillon C, et al (1990) Selenium intake, age, gender, and smoking in relation to indices of selenium status of adults residing in seleniferous area. Am J Clin Nutr 52:858–862PubMedGoogle Scholar
  26. 26.
    Longnecker MP, Stram DO, Taylor PA, et al (1996) Use of selenium concentration in whole blood, serum, toenails, or urine as a surrogate measure of selenium intake. Epidemiol 7:384–390Google Scholar
  27. 27.
    Agahian B, Lee JS, Nelson JH, John RE (1990) Arsenic levels in fingernails as a biological indicator of exposure to arsenic. Am Ind Hyg Assoc J 51:646–651PubMedGoogle Scholar
  28. 28.
    King JC (1990) Assessment of zinc status. J Nutr 120:1474–1479PubMedGoogle Scholar
  29. 29.
    Wood RJ (2000) Assessment of marginal zinc status in humans. J Nutr 130:1350S–1354SPubMedGoogle Scholar
  30. 30.
    Nielsen FH (1993) Ultratrace elements of possible importance for human health: an update. In: Prasad AS (eds) Essential and toxic trace elements in human health and disease: an update. Wiley-Liss, New York, pp 355–376Google Scholar
  31. 31.
    Uthus EO, Seaborn CD (1996) Deliberations and evaluations of the approaches, endpoints and paradigms for dietary recommendations of the other trace elements. J Nutr 126:2452S–2459SPubMedGoogle Scholar
  32. 32.
    Leonard A, Gerber GB (1994) Mutagenicity, carcinogenicity and teratogenicity of vanadium compounds. Mutat Res 317:81–88PubMedGoogle Scholar
  33. 33.
    Hossain K, Akhand AA, Kato M, et al (2000) Arsenite induces apoptosis of murine T lymphocytes through membrane raft-linked signaling for activation of c-Jun amino-terminal kinase. J Immunol 165:4290–4297PubMedGoogle Scholar
  34. 34.
    Chen W, Martindale JL, Holbrook NJ, Liu Y (1998) Tumor promoter arsenite activates extracellular signal-regulated kinase through a signaling pathway mediated by epidermal growth factor receptor and Shc. Mol Cell Biol 18:5178–5188PubMedGoogle Scholar
  35. 35.
    Office of Environmental Health Hazard Assessment (2004) Public health goal for arsenic in drinking water. California Environmental Protection AgencyGoogle Scholar
  36. 36.
    Bates MN, Smith AH, Hopenhayn-Rich C (1992) Arsenic ingestion and internal cancers: a review. Am J Epidemiol 135:462–476PubMedGoogle Scholar
  37. 37.
    Chen CJ, Chuang YC, You SL, Lin HY (1986) A retrospective study on malignant neoplasms of bladder, lung and liver in blackfoot disease endemic area in Taiwan. Br J Cancer 53:399–405PubMedGoogle Scholar
  38. 38.
    Ferreccio C, Gonzalez PC, Milosavjlevic SV, Marshall GG, Sancha AM, Smith AH (2000) Lung cancer and arsenic concentrations in drinking water in Chile. Epidemiology 11:673–679PubMedCrossRefGoogle Scholar
  39. 39.
    Chiou HY, Hsueh YM, Liaw KF, et al (1995) Incidence of internal cancers and ingested inorganic arsenic: a seven-year follow-up study in Taiwan. Cancer Res 55:1296–1300PubMedGoogle Scholar
  40. 40.
    Chen Y, Ahsan H (2004) Cancer burden from arsenic in drinking water in Bangladesh. Am J Public Health 94:741–744PubMedGoogle Scholar
  41. 41.
    Lewis DR, Southwick JW, Ouellet-Hellstrom R, Rench J, Calderon RJ (1999) Drinking water arsenic in Utah: A cohort mortality study. Environ Health Perspect 107:359–365PubMedGoogle Scholar
  42. 42.
    Bates MN, Rey OA, Biggs ML, et al (2004) Case–control study of bladder cancer and exposure to arsenic in Argentina. Am J Epidemiology 159:381–389CrossRefGoogle Scholar
  43. 43.
    Chiou HY, Chiou ST, Hsu YH, et al (2001) Incidence of transitional cell carcinoma and arsenic in drinking water: a follow-up study of 8,102 residents in an arseniasis-endemic area in northeastern Taiwan. Am J Epidemiol 153:411–418PubMedCrossRefGoogle Scholar
  44. 44.
    Kurttio P, Pukkala E, Kahelin A, Auvinen A, Pekkanen J (1999) Arsenic concentrations in well water and risk of bladder and kidney cancer in Finland. Environ Health Perspect 107:705–710PubMedGoogle Scholar
  45. 45.
    Garland M, Morris JS, Colditz GA, et al (1996) Toenail trace element levels and breast cancer: a prospective study. Am J Epidemiol 144:653–660PubMedGoogle Scholar
  46. 46.
    Pershagen G (1985) Lung cancer mortality among men living near an arsenic-emitting smelter. Am J Epidemiology 122:684–694Google Scholar
  47. 47.
    Hazelton WD, Leubeck EG, Heidenreich WF, Moolgavkar SH (2001) Analysis of a historical cohort of Chinese tin miners with arsenic, radon, cigarette smoke, and pipe smoke exposures using the biologically based two-stage clonal expansion model. Radiation Research 156:78–94PubMedCrossRefGoogle Scholar
  48. 48.
    Mabuchi K, Lilienfeld AM, Snell LM (1980) Cancer and occupational exposure to arsenic: a study of pesticide workers. Prev Med 9:51–77PubMedCrossRefGoogle Scholar
  49. 49.
    Coggon D, Pannett B, Acheson ED (1984) Use of job-exposure matrix in an occupational analysis of lung and bladder cancers on the basis of death certificates. JNCI 72:61–65PubMedGoogle Scholar
  50. 50.
    Bates MN, Smith AH, Cantor KP (1995) Case–control study of bladder cancer and arsenic in drinking water. Am J Epidemiology 141:523–530Google Scholar
  51. 51.
    Steinmaus C, Yuan Y, Bates MN, Smith AH (2003) Case–control study of bladder cancer and drinking water arsenic in the western United States. Am J Epidemiol 158:1193–1201PubMedCrossRefGoogle Scholar
  52. 52.
    Michaud DS, Wright ME, Cantor KP, Taylor PR, Virtamo J, Albanes D (2004) Arsenic concentrations in prediagnostic toenails and the risk of bladder cancer in a cohort of male smokers. Am J Epidemiol 160:835–859CrossRefGoogle Scholar
  53. 53.
    U.S. Department of Health and Human Services, Public Health Service, National Toxicology Program (2002) Report on Carcinogens, 10th edn. 2002 DecemberGoogle Scholar
  54. 54.
    McMurray CT, Tainer JA (2003) Cancer, cadmium and genome integrity. Nature Genetics 34:239–241PubMedCrossRefGoogle Scholar
  55. 55.
    Waalkes MP (2000) Cadmium carcinogenesis in review. J Inorg Chem 79:241–244Google Scholar
  56. 56.
    Zheng H, Liu J, Choo KH, Michalska AE, Klaassen CD (1996) Metallothionein-I and -II knock-out mice are sensitive to cadmium-induced liver mRNA expression of c-jun and p53. Toxicol Appl Pharmacol 136:229–235PubMedCrossRefGoogle Scholar
  57. 57.
    Abshire MK, Buzard GS, Shiraishi N, Waalkes MP (1996) Induction of c-myc and c-jun proto-oncogene expression in rat L6 myoblasts by cadmium is inhibited by zinc preinduction of the metallothionein gene. J Toxicol Environ Health 48:359–377PubMedCrossRefGoogle Scholar
  58. 58.
    Shimada H, Shiao YH, Shibata M, Waalkes MP (1998) Cadmium suppresses apoptosis induced by chromium. J Toxicol Environ Health 54:159–168CrossRefGoogle Scholar
  59. 59.
    Lemen RA, Lee JS, Wagoner JK, Blejer HP (1976) Cancer mortality among cadmium production workers. Ann NY Acad Sci 271:273–279PubMedCrossRefGoogle Scholar
  60. 60.
    Sorahan T, Watherhouse JAH (1983) Mortality study of nickel–cadmium battery workers by the method of regression models in life tables. Br J Ind Med 40:293–300PubMedGoogle Scholar
  61. 61.
    Elinder CG, Kjellstrom T, Hogstedt C, Andersson K, Spang G (1985) Cancer mortality of cadmium workers. Br J Ind Med 42:651–655PubMedGoogle Scholar
  62. 62.
    Sorahan T (1987) Mortality from lung cancer among a cohort of nickel cadmium battery workers: 1946–84. Br J Ind Med 44:803–809PubMedGoogle Scholar
  63. 63.
    Kazantzis G, Lam TH, Sullivan KR (1988) Mortality of cadmium-exposed workers. Scand J Work Environ Health 14:220–223PubMedGoogle Scholar
  64. 64.
    Stayner L, Smith R, Thun M, Schnorr T, Lemen R (1992) A dose-response analysis and quantitative assessment of lung cancer risk and occupational cadmium exposure. Ann Epidemiol 2:177–194PubMedCrossRefGoogle Scholar
  65. 65.
    Sorahan T, Lister A, Gilthorpe MS, Harrington JM (1995) Mortality of copper cadmium alloy workers with special reference to lung cancer and non-malignant diseases of the respiratory system, 1946–92. Occup Environ Med 52:804–812PubMedGoogle Scholar
  66. 66.
    West DW, Slattery ML, Robison LM, French TK, Mahoney AW (1991) Adult dietary intake and prostate cancer risk in Utah: a case–control study with special emphasis on aggressive tumors. Cancer Causes Control 2:85–94PubMedCrossRefGoogle Scholar
  67. 67.
    Platz EA, Helzlsouer KJ, Hoffman SC, Morris JS, Baskett CK, Comstock GW (2002) Prediagnostic toenail cadmium and zinc and subsequent prostate cancer risk. Prostate 52:288–296PubMedCrossRefGoogle Scholar
  68. 68.
    Armstrong BG, Kazantzis G (1985) Prostatic cancer and chronic respiratory and renal disease in British cadmium workers: a case–control study. Br J Ind Med 42:540–545PubMedGoogle Scholar
  69. 69.
    Miki H, Kasprzak KS, Kenney S, Heine UI (1987) Inhibition of intercellular communication by nickel (II): antagonistic effect of magnesium. Carcinogensis 8:1757–1760Google Scholar
  70. 70.
    DiPaolo JA, Casto BC (1979) Quantitative studies of in vitro morphological transformation of Syrian hamster cells by inorganic metal salts. Cancer Res 39:1008–1013PubMedGoogle Scholar
  71. 71.
    Biedermann KA, Landolph JT (1987) Induction of anchorage independence in human diploid foreskin fibroblasts by carcinogenic metal salts. Cancer Res 47:3815–3823PubMedGoogle Scholar
  72. 72.
    Patierno SR, Dirscherl L, Xu J (1993) Transformation of rat tracheal epithelial cells to immortal growth variants by particulate and soluble nickel compounds. Mutat Res 300:179–193PubMedCrossRefGoogle Scholar
  73. 73.
    Costa M (1996) Mehcanisms of nickel genotoxicity and carcinogenicity. In: Chang LW (eds) Toxicology of metals. CRC Press, Boca Raton, FL, pp 245–251Google Scholar
  74. 74.
    Sen P, Conway K, Costa M (1987) Comparison of the localization of chromosome damage induced by calcium chromate and nickel compounds. Cancer Res 47:2142–2147PubMedGoogle Scholar
  75. 75.
    Kasprzak KS (1991) The role of oxidative damage in metal carcinogenicity. Chem Res Toxicol 4:604–615PubMedCrossRefGoogle Scholar
  76. 76.
    Hartwig A, Mullenders LHF, Schlepegrell R, Kasten U, Beyersmann D (1994) Nickel (II) interferes with the incision step in nucleotide excision repair in mammalian cells. Cancer Res 54:4045–4051PubMedGoogle Scholar
  77. 77.
    Lee YW, Klein CB, Kargacin B, et al (1995) Carcinogenic nickel silences gene expression by chromatin condensation and DNA methylation: a new model for epigenetic carcinogens. Mol Cell Biol 15:2547–2557PubMedGoogle Scholar
  78. 78.
    Grimsrud TK, Berge SR, Haldorsen T, Andersen A (2002) Exposure to different forms of nickel and risk of lung cancer. Am J Epidemiol 156:1123–1132PubMedCrossRefGoogle Scholar
  79. 79.
    Grimsrud TK, Berge SR, Martinsen JI, Andersen A (2003) Lung cancer incidence among Norwegian nickel-refinery workers 1953–2000. J Environ Monit 5:190–197PubMedCrossRefGoogle Scholar
  80. 80.
    Karjalainen S, Kerttula R, Pukkala E (1992) Cancer risk among workers at a copper/nickel smelter and nickel refinery in Finland. Int Arch Occup Environ Health 63:547–551PubMedCrossRefGoogle Scholar
  81. 81.
    Pang, D, Burges, DCL, Sorahan, T 1996Mortality study of nickel platers with special reference to cancers of the stomach and lung, 1945–93Occup Environ Med53714717PubMedGoogle Scholar
  82. 82.
    Jarup L, Bellander T, Hogstedt C, Spang G (1998) Mortality and cancer incidence in Swedish battery workers exposed to cadmium and nickel. Occup Environ Med 55:755–759PubMedGoogle Scholar
  83. 83.
    Andersen A, Berge SR, Engeland A, Norseth T (1996) Exposure to nickel compounds and smoking in relation to incidence of lung and nasal cancer among nickel refinery workers. Occup Environ Med 53:708–713PubMedGoogle Scholar
  84. 84.
    Goldhaber SB (2003) Trace element risk assessment: essentiality vs. toxicity. Regul Toxicol Pharmacol 38:232–242PubMedCrossRefGoogle Scholar
  85. 85.
    van’t Veer P, van der Wielen RP, Kok F, Hermus RJ, Sturmans F (1990) Selenium in diet, blood and toenails in relation to breast cancer: a case–control study. Am J Epidemiol 131:987–994Google Scholar
  86. 86.
    van’t Veer P, Strain JJ, Fernandez-Crehuet J, et al (1996) Tissue antioxidants and postmenopausal breast cancer: the European Community Multicentre Study on Antioxidants, Myocardial Infarction, and Cancer of the Breast (EURAMIC). Cancer Epidemiol Biomark Prev 5:441–447Google Scholar
  87. 87.
    Ghadirian P, Maisonneuve P, Perret C, et al (2000) A case-control study of toenail selenium and cancer of the breast, colon, and prostate. Cancer Detection Prev 24: 305–313Google Scholar
  88. 88.
    van Noord PA, de Waard F, Collette C, Mass MJ (1987) Selenium levels in nails of premenopausal breast cancer patients assessed prediagnostically in a cohort-nested case-referent study among women screened in the DOM project. Int J Epidemiol 16: 318–322PubMedGoogle Scholar
  89. 89.
    Hunter DJ, Morris JS, Stampfer MJ, Colditz GA, Speizer FE, Willett WC (1990) A prospective study of selenium status and breast cancer risk. JAMA 264:1128–1131PubMedCrossRefGoogle Scholar
  90. 90.
    van den Brandt PA, Goldbohm RA, van’t Veer P, et al (1994) Toenail selenium and risk of breast cancer. Am J Epidemiol 140:20–26PubMedGoogle Scholar
  91. 91.
    Strain JJ, Bokje E, van’t Veer P, et al (1997) Thyroid hormones and selenium status in breast cancer. Nutr Cancer 27:48–52PubMedGoogle Scholar
  92. 92.
    Coates RJ, Weiss NS, Daling JR, Morris JS, Labbe RF (1988) Serum levels of selenium and retinol and the subsequent risk of cancer. Am J Epidemiol 128:515–523PubMedGoogle Scholar
  93. 93.
    Schrauzer GN, Molenaar T, Mead S, Kuehn K, Yamamoto H, Araki E (1985) Selenium in the blood of Japanese and American women with and without breast cancer and fibrocystic disease. Jpn J Cancer Res 76:374–377PubMedGoogle Scholar
  94. 94.
    Willett WC, Polk BF, Morris JS, et al (1983) Prediagnostic serum selenium and risk of cancer. Lancet 2:130–134PubMedCrossRefGoogle Scholar
  95. 95.
    Longnecker MP, Stampfer MJ, Morris JS, et al (1993) A 1-y trial of the effect of high-selenium bread on selenium concentrations in blood and toenails. Am J Clin Nutr 57:408–413PubMedGoogle Scholar
  96. 96.
    Morris JS, Stampfer MJ, Willett WC (1983) Dietary selenium in humans. Toenails as an indicator. Biol Trace Elem Res 5:529–537Google Scholar
  97. 97.
    Clark LC, Hixson LJ, Combs GF Jr, Reid ME, Turnbull BW, Sampliner RE (1993) Plasma selenium concentration predicts the prevalence of colorectal adenomatous polyps. Cancer Epidemiol Biomark Prev 2:41–46Google Scholar
  98. 98.
    Fernandez-Banares F, Cabre E, Esteve M, et al (2002) Serum selenium and risk of large size colorectal adenomas in a geographical area with a low selenium status. Am J Gastroenterol 97:2103–2108PubMedGoogle Scholar
  99. 99.
    Nomura A, Heilbrun LK, Morris JS, Stemmermann GN (1987) Serum selenium and the risk of cancer, by specific sites: case–control analysis of prospective data. JNCI 79:103–108PubMedGoogle Scholar
  100. 100.
    Wallace K, Byers T, Morris JS, et al (2003) Prediagnostic serum selenium concentration and the risk of recurrent colorectal adenoma: a nested case–controls study. Cancer Epidemiol Biomark Prev 12:464–467Google Scholar
  101. 101.
    Garland M, Morris JS, Stampfer MJ, et al (1995) Prospective study of toenail selenium levels and cancer among women. J Natl Cancer Inst 87:497–505PubMedGoogle Scholar
  102. 102.
    Mannisto S, Alfthan G, Virtanen M, Kataja V, Uusitupa M, Pietinen P (2000) Toenail selenium and breast cancer – a case–control study in Finland. Eur J Clin Nutr 54:98–103PubMedCrossRefGoogle Scholar
  103. 103.
    van den Brandt PA, Goldbohm RA, van’t Veer P, et al (1993) A prospective cohort study on toenail selenium levels and risk of gastrointestinal cancer. JNCI 85:224–229PubMedGoogle Scholar
  104. 104.
    Kabuto M, Imai H, Yonezawa C, et al (1994) Prediagnostic serum selenium and zinc levels and subsequent risk of lung and stomach cancer in Japan. Cancer Epidemiol Biomark Prev 3:465–469Google Scholar
  105. 105.
    Ratnasinghe D, Tangrea JA, Forman MR, et al (2000) Serum tocopherols, selenium and lung cancer risk among tin miners in China. Cancer Causes Control 11:129–135PubMedCrossRefGoogle Scholar
  106. 106.
    Reid ME, Duffield-Lillico AJ, Garland L, Turnbull BW, Clark LC, Marshall JR (2002) Selenium supplementation and lung cancer incidence: an update of the nutritional prevention of cancer trial. Cancer Epidemiol Biomark Prev 11:1285–1291Google Scholar
  107. 107.
    Hartman TJ, Taylor PR, Alfthan G, et al (2002) Toenail selenium concentration and lung cancer in male smokers. Cancer Causes Control 13:923–928PubMedCrossRefGoogle Scholar
  108. 108.
    van den Brandt PA, Goldbohm RA, van’t Veer P, et al (1993) A prospective study on selenium status and the risk of lung cancer. Cancer Res 53:4860–4865PubMedGoogle Scholar
  109. 109.
    Nakaji S, Fukuda S, Sakamoto J, et al (2001) Relationship between mineral and trace element concentrations in drinking water and gastric cancer mortality in Japan. Nutr Cancer 40:99–102PubMedCrossRefGoogle Scholar
  110. 110.
    Kneller RW, Guo WD, Hsing AW, et al (1992) Risk factors for stomach cancer in sixty-five Chinese counties. Cancer Epidemiol Biomark Prev 1:113–118Google Scholar
  111. 111.
    Chen SY, Liu TY, Shun CT, et al (2004) Modification effects of GSTM1, GSTT1 and CYP2E1 polymorphisms on associates between raw salted food and incomplete intestinal metaplasia in a high-risk area of stomach cancer. Int J Cancer 108:606–612PubMedCrossRefGoogle Scholar
  112. 112.
    Zhang L, Blot WJ, You WC, et al (1994) Serum micronutrients in relation to pre-cancerous gastric lesions. Int J Cancer 56:650–654PubMedGoogle Scholar
  113. 113.
    Knekt P, Aromaa A, Maatela J, et al (1990) Serum selenium and subsequent risk of cancer among Finnish men and women. JNCI 82:864–868PubMedGoogle Scholar
  114. 114.
    Wei WQ, Abnet CC, Qiao YL, et al (2004) Prospective study of serum selenium concentrations and esophageal and gastric cardia cancer, heart disease, stroke, and total death. Am J Clin Nutr 79:80–85PubMedGoogle Scholar
  115. 115.
    Mark SD, Qiao YL, Dawsey SM, et al (2000) Prospective study of serum selenium levels and incident esophageal and gastric cancers. J Natl Cancer Inst 92:1753–1763PubMedCrossRefGoogle Scholar
  116. 116.
    Dawsey SM, Wang GQ, Taylor PR, et al (1994) Effects of vitamin/mineral supplementation on the prevalence of histological dysplasia and early cancer of the esophagus and stomach: results from the Dysplasia Trial in Linxian, China. Cancer Epidemiol Biomark Prev 3:167–172Google Scholar
  117. 117.
    Wang GQ, Dawsey SM, Li JY, et al (1994) Effects of vitamin/mineral supplementation on the prevalence of histological dysplasia and early cancer of the esophagus and stomach: results from the General Population Trial in Linxian, China. Cancer Epidemiol Biomark Prev 3:161–166Google Scholar
  118. 118.
    Helzlsouer KJ, Comstock GW, Morris JS (1989) Selenium, lycopene, alpha-tocopherol, beta-carotene, retinol, and subsequent bladder cancer. Cancer Res 49:6144–6148PubMedGoogle Scholar
  119. 119.
    Zeegers MP, Goldbohm A, Bode P, van den Brandt PA (2002) Prediagnostic toenail selenium and risk of bladder cancer. Cancer Epidemiol Biomark Prev 11:1292–1297Google Scholar
  120. 120.
    Michaud DS, Hartman TJ, Taylor PR, et al (2002) No association between toenail selenium levels and bladder cancer risk. Cancer Epidemiol Biomark Prev 11:1505–1506Google Scholar
  121. 121.
    Vogt TM, Ziegler RG, Graubard BI, et al (2003) Serum selenium and risk of prostate cancer in US blacks and whites. Int J Cancer 103:664–670PubMedCrossRefGoogle Scholar
  122. 122.
    Allen NE, Morris JS, Ngwenyama RA, Key TJ (2004) A case–control study of selenium in nails and prostate cancer risk in British men. Br J Cancer 90:1392–1396PubMedCrossRefGoogle Scholar
  123. 123.
    Brooks JD, Metter EJ, Chan DW, et al (2001) Plasma selenium level before diagnosis and the risk of prostate cancer development. J Urol 166: 2034–2038PubMedCrossRefGoogle Scholar
  124. 124.
    Helzlsouer KJ, Huang HY, Alberg AJ, et al (2000) Association between alpha-tocopherol, gamma-tocopherol, selenium, and subsequent prostate cancer. J Natl Cancer Inst 92:2018–2023PubMedCrossRefGoogle Scholar
  125. 125.
    Nomura AMY, Lee J, Stemmermann GN, Combs GF Jr (2000) Serum selenium and subsequent risk of prostate cancer. Cancer Epidemiol Biomark Prev 9:883–887Google Scholar
  126. 126.
    Yoshizawa K, Willett WC, Morris SJ, et al (1998) Study of prediagnostic selenium level in toenails and the risk of advanced prostate cancer. JNCI 90:1219–1224PubMedCrossRefGoogle Scholar
  127. 127.
    Li H, Stampfer MJ, Giovannucci EL, et al (2004) A prospective study of plasma selenium levels and prostate cancer risk. J Natl Cancer Inst 96:696–703PubMedCrossRefGoogle Scholar
  128. 128.
    van den Brandt PA, Zeegers MPA, Bode P, Goldbohm RA (2003) Toenail selenium levels and the subsequent risk of prostate cancer: a prospective cohort study. Cancer Epidemiol Biomark Prev 12:866–871Google Scholar
  129. 129.
    Hartman TJ, Albanes D, Pietinen P, et al (1998) The association between baseline vitamin E, selenium, and prostate cancer in the Alpha-Tocopherol, Beta-Carotene Cancer Prevention Study. Cancer Epidemiol Biomark Prev 7:335–340Google Scholar
  130. 130.
    Clark LC, Dalkin B, Krongrad A, et al (1998) Decreased incidence of prostate cancer with selenium supplementation: results of a double-blind cancer prevention trial. Br J Urol 81:730–734PubMedGoogle Scholar
  131. 131.
    Prasad AS, Halsted JA, Nadimi M (1961) Syndrome of iron deficiency anemia, hepatospenomegaly, hyopgonadism, dwarfism,and geophagia. Am J Med 31:532–546PubMedCrossRefGoogle Scholar
  132. 132.
    Prasad AS, Miale A, Farid Z, Sandstead HH, Schulert AR (1963) Zinc metabolism in patients with the syndrome of iron deficiency anemia, hypogonadism and dwarfism. J Lab Clin Med 61:537–549PubMedGoogle Scholar
  133. 133.
    Prasad AS (1998) Zinc in human health: an update. J Trace Elem Exp Med 11:63–78CrossRefGoogle Scholar
  134. 134.
    O’Connor JM (2001) Trace elements and DNA damage. Biochem Soc Trans 29:354–357PubMedCrossRefGoogle Scholar
  135. 135.
    Leccia MT, Richard MJ, Favier A, Beani JC (1999) Zinc protects against ultraviolet A1-induced DNA damage and apoptosis in cultured human fibroblasts. Biol Trace Elem Res 69:177–190PubMedGoogle Scholar
  136. 136.
    Gupta SK, Shukla VK, Vaidya MP, Roy SK, Gupta S (1991) Serum trace elements and Cu/Zn ratio in breast cancer patients. J Surg Oncol 46:178–181PubMedGoogle Scholar
  137. 137.
    Adzersen KH, Jess P, Freivogel KW, Gerhard I, Bastert G (2003) Raw and cooked vegetables, fruits, selected micronutrients, and breast cancer risk: a case–control study in Germany. Nutr Cancer 46:131–137PubMedCrossRefGoogle Scholar
  138. 138.
    Harris RWC, Key TJA, Silcocks PB, Bull D, Wald NJ (1991) A case–control study of dietary carotene in men with lung cancer and in men with other epithelial cancers. Nutr Cancer 15:63–68PubMedGoogle Scholar
  139. 139.
    Cocco PL, Carta P, Belli S, Picchiri GF, Flore MV (1994) Mortality of Sardinian lead and zinc miners: 1960–88. Occup Environ Med 51:674–682PubMedCrossRefGoogle Scholar
  140. 140.
    Zhang ZF, Kurtz RC, Yu GP, et al (1997) Adenocarcinomas of the esophagus and gastric cardia: the role of diet. Nutr Cancer 27:298–309PubMedGoogle Scholar
  141. 141.
    Costello LC, Franklin RB, Tan M, Bagasra O (2005) Zinc and prostate cancer: a critical scientific, medical, and public interest issue (United States). Cancer Causes Control 16:901–915PubMedCrossRefGoogle Scholar
  142. 142.
    Kolonel LN, Yoshizawa CN, Hankin JH (1988) Diet and prostatic cancer: a case–control study in Hawaii. Am J Epidemiol 127:999–1012PubMedGoogle Scholar
  143. 143.
    Leitzmann MF, Stampfer MJ, Wu K, Colditz GA, Willett WC, Giovannucci EL (2003) Zinc supplement use and risk of prostate cancer. J Natl Cancer Inst 95:1004–1007PubMedGoogle Scholar
  144. 144.
    Kristal AR, Stanford JL, Cohen JH, Wicklund K, Patterson RE (1999) Vitamin and mineral supplement use is associated with reduced risk of prostate cancer. Cancer Epidemiol Biomarkers Prev 8:887–892PubMedGoogle Scholar
  145. 145.
    Vlajinac HD, Marinkovic JM, Ilic MD, Kocev NI (1997) Diet and prostate cancer: a case–control study. Eur J Nutr 33:101–107Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  • Stephanie A. Navarro Silvera
    • 1
  • Thomas E. Rohan
    • 1
  1. 1.Department of Epidemiology and Population HealthAlbert Einstein College of MedicineNew YorkUSA

Personalised recommendations