European Journal of Cancer
Volume 45, Issue 18 , Pages 3156-3165 , December 2009

Oesophageal cancer in Golestan Province, a high-incidence area in northern Iran – A review

  • Farhad Islami

      Affiliations

    • Digestive Disease Research Center, Shariati Hospital, Tehran University of Medical Sciences, Kargar Shomali Avenue, 14117 Tehran, Iran
    • International Agency for Research on Cancer, 69008 Lyon, France
    • King’s College London, Thames Cancer Registry, London SE1 3QD, UK
  • ,
  • Farin Kamangar

      Affiliations

    • Digestive Disease Research Center, Shariati Hospital, Tehran University of Medical Sciences, Kargar Shomali Avenue, 14117 Tehran, Iran
    • Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD 20892-7232, USA
    • Department of Public Health Analysis, School of Community Health and Policy, Morgan State University, Baltimore, MD 21251, USA
  • ,
  • Dariush Nasrollahzadeh

      Affiliations

    • Digestive Disease Research Center, Shariati Hospital, Tehran University of Medical Sciences, Kargar Shomali Avenue, 14117 Tehran, Iran
    • Department of Medical Epidemiology and Biostatistics, Karolinska Institute, SE-171 77 Stockholm, Sweden
  • ,
  • Henrik Møller

      Affiliations

    • King’s College London, Thames Cancer Registry, London SE1 3QD, UK
  • ,
  • Paolo Boffetta

      Affiliations

    • International Agency for Research on Cancer, 69008 Lyon, France
  • ,
  • Reza Malekzadeh

      Affiliations

    • Digestive Disease Research Center, Shariati Hospital, Tehran University of Medical Sciences, Kargar Shomali Avenue, 14117 Tehran, Iran
    • Corresponding Author InformationCorresponding author: Tel.: +98 21 82415300; fax: +98 21 82415400.

Received 26 July 2009 ,Revised 11 September 2009 ,Accepted 15 September 2009.

References 

  1. Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin. 2005;55:74–108
  2. Mahboubi E, Kmet J, Cook PJ, et al. Oesophageal cancer studies in the Caspian Littoral of Iran: the Caspian cancer registry. Br J Cancer. 1973;28:197–214
  3. Kmet J, Mahboubi E. Esophageal cancer in the Caspian littoral of Iran: initial studies. Science. 1972;175:846–853
  4. Blot WJ, McLaughlin JK, Fraumeni JF. Esophageal Cancer. In:  Schottenfeld D,  Fraumeni JF editor. Cancer epidemiology and prevention. New York: Oxford University Press; 2006;p. 697–706
  5. Semnani S, Sadjadi A, Fahimi S, et al. Declining incidence of esophageal cancer in the Turkmen Plain, eastern part of the Caspian Littoral of Iran: a retrospective cancer surveillance. Cancer Detect Prev. 2006;30:14–19
  6. Islami F, Kamangar F, Aghcheli K, et al. Epidemiologic features of upper gastrointestinal tract cancers in Northeastern Iran. Br J Cancer. 2004;90:1402–1406
  7. Trivers KF, Sabatino SA, Stewart SL. Trends in esophageal cancer incidence by histology, United States, 1998–2003. Int J Cancer. 2008;123:1422–1428
  8. Karim-Kos HE, de Vries E, Soerjomataram I, et al. Recent trends of cancer in Europe: a combined approach of incidence, survival and mortality for 17 cancer sites since the 1990s. Eur J Cancer. 2008;44:1345–1389
  9. Steevens J, Botterweck AA, Dirx MJ, van den Brandt PA, Schouten LJ. Trends in incidence of oesophageal and stomach cancer subtypes in Europe. Eur J Gastroenterol Hepatol. 2009;
  10. Robins G, Crabtree JE, Bailey A, Forman D. International variation in Helicobacter pylori infection and rates of oesophageal cancer. Eur J Cancer. 2008;44:726–732
  11. Kamangar F, Chow WH, Abnet CC, Dawsey SM. Environmental causes of esophageal cancer. Gastroenterol Clin North Am. 2009;38:27–57vii
  12. IARC Working Group . Tobacco smoke and involuntary smoking. IARC Monographs on the evaluation of carcinogenic risks to humans. vol. 83. Lyon: IARC Press; 2004;
  13. Boffetta P, Hecht S, Gray N, Gupta P, Straif K. Smokeless tobacco and cancer. Lancet Oncol. 2008;9:667–675
  14. Pourshams A, Saadatian-Elahi M, Nouraie M, et al. Golestan cohort study of oesophageal cancer: feasibility and first results. Br J Cancer. 2005;92:176–181
  15. Nasrollahzadeh D, Kamangar F, Aghcheli K, et al. Opium, tobacco, and alcohol use in relation to oesophageal squamous cell carcinoma in a high-risk area of Iran. Br J Cancer. 2008;98:1857–1863
  16. Tran GD, Sun XD, Abnet CC, et al. Prospective study of risk factors for esophageal and gastric cancers in the Linxian general population trial cohort in China. Int J Cancer. 2005;113:456–463
  17. Baan R, Straif K, Grosse Y, et al. Carcinogenicity of alcoholic beverages. Lancet Oncol. 2007;8:292–293
  18. Cook-Mozaffari PJ, Azordegan F, Day NE, et al. Oesophageal cancer studies in the Caspian Littoral of Iran: results of a case–control study. Br J Cancer. 1979;39:293–309
  19. Ghadirian P, Stein GF, Gorodetzky C, et al. Oesophageal cancer studies in the Caspian littoral of Iran: some residual results, including opium use as a risk factor. Int J Cancer. 1985;35:593–597
  20. Malaveille C, Friesen M, Camus AM, et al. Mutagens produced by the pyrolysis of opium and its alkaloids as possible risk factors in cancer of the bladder and oesophagus. Carcinogenesis. 1982;3:577–585
  21. Abnet CC, Saadatian-Elahi M, Pourshams A, et al. Reliability and validity of opiate use self-report in a population at high risk for esophageal cancer in Golestan, Iran. Cancer Epidemiol Biomarkers Prev. 2004;13:1068–1070
  22. Islami F, Boffetta P, Ren JS, et al. High-temperature beverages and foods and esophageal cancer risk – a systematic review. Int J Cancer. 2009;125:491–524
  23. Yang CS, Wang X, Lu G, Picinich SC. Cancer prevention by tea: animal studies, molecular mechanisms and human relevance. Nat Rev Cancer. 2009;9:429–439
  24. Ghadirian P. Thermal irritation and esophageal cancer in northern Iran. Cancer. 1987;60:1909–1914
  25. Islami F, Pourshams A, Nasrollahzadeh D, et al. Tea drinking habits, oesophageal cancer in a high risk area in northern Iran: population based case–control study. BMJ. 2009;338:b929
  26. 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;
  27. Greenwald P, Anderson D, Nelson SA, Taylor PR. Clinical trials of vitamin and mineral supplements for cancer prevention. Am J Clin Nutr. 2007;85:314S–317S
  28. Islami F, Malekshah AF, Kimiagar M, et al. Patterns of food and nutrient consumption in northern Iran, a high-risk area for esophageal cancer. Nutr Cancer. 2009;61:475–483
  29. Nouarie M, Pourshams A, Kamangar F, et al. Ecologic study of serum selenium and upper gastrointestinal cancers in Iran. World J Gastroenterol. 2004;10:2544–2546
  30. Tao X, Zhu H, Matanoski GM. Mutagenic drinking water and risk of male esophageal cancer: a population-based case–control study. Am J Epidemiol. 1999;150:443–452
  31. Xibib S, Meilan H, Moller H, et al. Risk factors for oesophageal cancer in Linzhou, China: a case–control study. Asian Pac J Cancer Prev. 2003;4:119–124
  32. Yang CX, Wang HY, Wang ZM, et al. Risk factors for esophageal cancer: a case–control study in South-western China. Asian Pac J Cancer Prev. 2005;6:48–53
  33. Yu Y, Taylor PR, Li JY, et al. Retrospective cohort study of risk-factors for esophageal cancer in Linxian, People’s Republic of China. Cancer Causes Control. 1993;4:195–202
  34. Yokokawa Y, Ohta S, Hou J, et al. Ecological study on the risks of esophageal cancer in Ci-Xian, China: the importance of nutritional status and the use of well water. Int J Cancer. 1999;83:620–624
  35. Yang CY, Chiu HF, Tsai SS, Wu TN, Chang CC. Magnesium and calcium in drinking water and the risk of death from esophageal cancer. Magnes Res. 2002;15:215–222
  36. Joint Iran-IARC Study Group . Esophageal cancer studies in the Caspian littoral of Iran: results of population studies – a prodrome. Joint Iran-International Agency for Research on Cancer Study Group. J Natl Cancer Inst. 1977;59:1127–1138
  37. Perello G, Marti-Cid R, Castell V, Llobet JM, Domingo JL. Concentrations of polybrominated diphenyl ethers, hexachlorobenzene and polycyclic aromatic hydrocarbons in various foodstuffs before and after cooking. Food Chem Toxicol. 2008;47:709–715
  38. Evanoff BA, Gustavsson P, Hogstedt C. Mortality and incidence of cancer in a cohort of Swedish chimney sweeps: an extended follow up study. Br J Ind Med. 1993;50:450–459
  39. Kamangar F, Strickland PT, Pourshams A, et al. High exposure to polycyclic aromatic hydrocarbons may contribute to high risk of esophageal cancer in northeastern Iran. Anticancer Res. 2005;25:425–428
  40. Hakami R, Mohtadinia J, Etemadi A, et al. Dietary intake of benzo(a)pyrene and risk of esophageal cancer in North of Iran. Nutr Cancer. 2008;60:216–221
  41. McColl KE. When saliva meets acid: chemical warfare at the oesophagogastric junction. Gut. 2005;54:1–3
  42. Kurooka M, Hongyo T, Nakajima H, et al. High incidence of esophageal cancer in esophageal achalasia by the oral administration of N-amyl-N-methylnitrosamine and its prevention by nicardipine hydrochloride in mice. Cancer Lett. 1998;127:55–61
  43. Jakszyn P, Gonzalez CA. Nitrosamine and related food intake and gastric and oesophageal cancer risk: a systematic review of the epidemiological evidence. World J Gastroenterol. 2006;12:4296–4303
  44. Lu SH, Yang WX, Guo LP, et al. Determination of N-nitrosamines in gastric juice and urine and a comparison of endogenous formation of N-nitrosoproline and its inhibition in subjects from high- and low-risk areas for oesophageal cancer. IARC Sci Publ. 1987;84:538–543
  45. Eisenbrand G, Spiegelhalder B, Preussmann R. Nitrate and nitrite in saliva. Oncology. 1980;37:227–231
  46. O’Neill CH, Hodges GM, Riddle PN, et al. A fine fibrous silica contaminant of flour in the high oesophageal cancer area of north-east Iran. Int J Cancer. 1980;26:617–628
  47. O’Neill C, Pan Q, Clarke G, et al. Silica fragments from millet bran in mucosa surrounding oesophageal tumours in patients in northern China. Lancet. 1982;1:1202–1206
  48. Jabbari A, Besharat S, Semnani S. Role of silis in esophageal cancer. World J Gastroenterol. 2008;14:3106–3107
  49. Luo Y, Yoshizawa T, Katayama T. Comparative study on the natural occurrence of Fusarium mycotoxins (trichothecenes and zearalenone) in corn and wheat from high- and low-risk areas for human esophageal cancer in China. Appl Environ Microbiol. 1990;56:3723–3726
  50. Martins ML, Martins HM, Bernardo F. Fumonisins B1 and B2 in black tea and medicinal plants. J Food Prot. 2001;64:1268–1270
  51. Lacey J. The microbiology of cereal-grains from areas of Iran with a high-incidence of esophageal cancer. J Stored Prod Res. 1988;24:39–50
  52. Yazdanpanah Y, Chene G, Losina E, et al. Incidence of primary opportunistic infections in two human immunodeficiency virus-infected French clinical cohorts. Int J Epidemiol. 2001;30:864–871
  53. Bouvard V, Baan R, Straif K, et al. A review of human carcinogens – Part B: biological agents. Lancet Oncol. 2009;10:321–322
  54. Islami F, Kamangar F. Helicobacter pylori and esophageal cancer risk: a meta-analysis. Cancer Prev Res (Phila Pa). 2008;1:329–338
  55. Moradi A, de Villiers EM, Mokhtari-Azad T, et al. Detection of human papillomavirus DNA by PCR in esophageal squamous cell carcinoma from Turkmen Sahra, north-east of Iran. Iran Biomed J. 2002;6:19–23
  56. Farhadi M, Tahmasebi Z, Merat S, et al. Human papillomavirus in squamous cell carcinoma of esophagus in a high-risk population. World J Gastroenterol. 2005;11:1200–1203
  57. Mirsadraee M, Kalantari MR, Saffari A, Mahmoudi M. Association of HTLV1 Infection and Esophageal Squamous Cell Carcinoma. Int J Gastrointest Cancer. 2007;38:15–18
  58. Smith M, Zhou M, Whitlock G, et al. Esophageal cancer and body mass index: results from a prospective study of 220,000 men in China and a meta-analysis of published studies. Int J Cancer. 2008;122:1604–1610
  59. Bahrami H, Sadatsafavi M, Pourshams A, et al. Obesity, hypertension in an Iranian cohort study; Iranian women experience higher rates of obesity, hypertension than American women. BMC Public Health. 2006;6:158
  60. Khoshnia M, Pourshams A, Mohammadkhani A, et al. Celiac disease in Gonbad-Kavoos. Govaresh. 2005;10:131–133
  61. Abnet CC, Qiao YL, Mark SD, et al. Prospective study of tooth loss and incident esophageal and gastric cancers in China. Cancer Causes Control. 2001;12:847–854
  62. Sepehr A, Kamangar F, Fahimi S, et al. Poor oral health as a risk factor for esophageal squamous dysplasia in northeastern Iran. Anticancer Res. 2005;25:543–546
  63. Abnet CC, Kamangar F, Islami F, et al. Tooth loss and lack of regular oral hygiene are associated with higher risk of esophageal squamous cell carcinoma. Cancer Epidemiol Biomarkers Prev. 2008;17:3062–3068
  64. Corley DA, Kerlikowske K, Verma R, Buffler P. Protective association of aspirin/NSAIDs and esophageal cancer: a systematic review and meta-analysis. Gastroenterology. 2003;124:47–56
  65. Islami F, Kamangar F, Nasrollahzadeh D, et al. Socio-economic status and oesophageal cancer: results from a population-based case–control study in a high-risk area. Int J Epidemiol. 2009;38:978–988
  66. Ghadirian P. Familial history of esophageal cancer. Cancer. 1985;56:2112–2116
  67. Akbari MR, Malekzadeh R, Nasrollahzadeh D, et al. Familial risks of esophageal cancer among the Turkmen population of the Caspian littoral of Iran. Int J Cancer. 2006;119:1047–1051
  68. Hiyama T, Yoshihara M, Tanaka S, Chayama K. Genetic polymorphisms and esophageal cancer risk. Int J Cancer. 2007;121:1643–1658
  69. Akbari MR, Malekzadeh R, Nasrollahzadeh D, et al. Germline BRCA2 mutations and the risk of esophageal squamous cell carcinoma. Oncogene. 2008;27:1290–1296
  70. Sepehr A, Kamangar F, Abnet CC, et al. Genetic polymorphisms in three Iranian populations with different risks of esophageal cancer, an ecologic comparison. Cancer Lett. 2004;213:195–202
  71. Hainaut P, Hollstein M. P53 and human cancer: the first ten thousand mutations. Adv Cancer Res. 2000;77:81–137
  72. Biramijamal F, Allameh A, Mirbod P, et al. Unusual profile and high prevalence of p53 mutations in esophageal squamous cell carcinomas from northern Iran. Cancer Res. 2001;61:3119–3123
  73. Sepehr A, Taniere P, Martel-Planche G, et al. Distinct pattern of TP53 mutations in squamous cell carcinoma of the esophagus in Iran. Oncogene. 2001;20:7368–7374
  74. Breton J, Sichel F, Abbas A, et al. Simultaneous use of DGGE and DHPLC to screen TP53 mutations in cancers of the esophagus and cardia from a European high incidence area (Lower Normandy, France). Mutagenesis. 2003;18:299–306
  75. Pourshams A, Khademi H, Malekshah AF, et al. Cohort profile: The Golestan Cohort Study – a prospective study of oesophageal cancer in northern Iran. Int J Epidemiol. 2009;
  76. Malekshah AF, Kimiagar M, Saadatian-Elahi M, et al. Validity and reliability of a new food frequency questionnaire compared to 24 h recalls and biochemical measurements: pilot phase of Golestan cohort study of esophageal cancer. Eur J Clin Nutr. 2006;60:971–977
  77. Saidi F, Sepehr A, Fahimi S, et al. Oesophageal cancer among the Turkomans of northeast Iran. Br J Cancer. 2000;83:1249–1254
  78. Sadjadi A, Malekzadeh R, Derakhshan MH, et al. Cancer occurrence in Ardabil: results of a population-based cancer registry from Iran. Int J Cancer. 2003;107:113–118
  79. Derakhshan MH, Yazdanbod A, Sadjadi AR, et al. High incidence of adenocarcinoma arising from the right side of the gastric cardia in NW Iran. Gut. 2004;53:1262–1266
  80. Babaei M, Mousavi S, Malek M, et al. Cancer occurrence in Semnan Province, Iran: results of a population-based cancer registry. Asian Pac J Cancer Prev. 2005;6:159–164
  81. The Coordinating Group for Research on Etiology of Esophageal Cancer in North China . The epidemiology and etiology of esophageal cancer in north China. A preliminary report. Chin Med J (Engl). 1975;1:167–183
  82. Kamangar F, Qiao YL, Blaser MJ, et al. Helicobacter pylori and oesophageal and gastric cancers in a prospective study in China. Br J Cancer. 2007;96:172–176
  83. Tsuchiya Y, Kiyohara C, Sato T, et al. Polymorphisms of cytochrome P450 1A1, glutathione S-transferase class mu, and tumour protein p53 genes and the risk of developing gallbladder cancer in Japanese. Clin Biochem. 2007;40:881–886
  84. Garte S, Gaspari L, Alexandrie AK, et al. Metabolic gene polymorphism frequencies in control populations. Cancer Epidemiol Biomarkers Prev. 2001;10:1239–1248
  85. Nakajima M, Fukami T, Yamanaka H, et al. Comprehensive evaluation of variability in nicotine metabolism and CYP2A6 polymorphic alleles in four ethnic populations. Clin Pharmacol Ther. 2006;80:282–297
  86. Yokoyama T, Yokoyama A, Kato H, et al. Alcohol flushing, alcohol and aldehyde dehydrogenase genotypes, and risk for esophageal squamous cell carcinoma in Japanese men. Cancer Epidemiol Biomarkers Prev. 2003;12:1227–1233

PII: S0959-8049(09)00704-7

doi: 10.1016/j.ejca.2009.09.018

European Journal of Cancer
Volume 45, Issue 18 , Pages 3156-3165 , December 2009