Epidemiology and Risk Factors of Esophageal Cancer
Keywords:
Epidemiology, Esophageal Cancer, Risk FactorAbstract
Esophageal cancer is the eighth most common malignancy in the world. In general, squamous cell
carcinoma is more common than adenocarcinoma, except in the USA. The etiology of the cancer is multifactorial,
involving such things as smoking, alcohol, dietary habits, viral infections, GERD, environmental
carcinogens, and socioeconomic status. This review also shows factors that may protect against the development
of esophageal cancer such as a diet rich in fruits and vegetables or consumption of NSAIDs or helicobactor
pylori infection in adenocarcinoma.
References
1. Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics,
2002. CA Cancer J Clin 2005;55:74-108.
2. Kamanger F, Dores GM, Anderson WF. Patterns of cancer
incidence, mortality and prevalence across five continents:
defining priorities to reduce cancer disparities in different
geographic regions of the world. J Clin Oncol 2006;24:2137-
50.
3. Ke L. Mortality and incidence trends from esophagus cancer
in selected geographic areas of China circa 1970-90. Int J
Cancer 2002;102:271-4.
4. Wang Z, Tang L, Sun G, et al. Etiological study of esophageal
squamous cell carcinoma in an endemic region: a
population-based case control study in Huaian, China.
BMC Cancer 2006;6:287.
5. 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;
113:456-63.
6. Sriplung H, Wiangnon S, Sontipong S, et al. Cancer incidence
trends in Thailand, 1989-2000. Asian Pac J Cancer Prev 2006;
7:239-44.
7. Holmes RS, Vaughan TL. Epidemiology and pathogenesis of
esophageal cancer. Semin Radiat Oncol 200717:2-9.
8. Hashibe M, Boffetta P, Janout V, et al. Esophageal cancer
in Central and Eastern Europe: tobacco and alcohol. Int J
Cancer 2007;120:1518-22.
9. Jiang JM, Zeng XJ, Chen JS, et al. Smoking and mortality
from esophageal cancer in China: a large case-control
study of 19,734 male esophageal cancer deaths and 104,846
living spouse controls. Int J Cancer 2006;119:1427-32.
10. Wu IC, Lu CY, Kuo FC, et al. Interaction between cigarette,
alcohol and betel nut use on esophageal cancer risk in
Taiwan. Eur J Clin Invest 2006;36:236-41.
11. Wu M, Zhao JK, Hu XS, et al. Association of smoking, alcohol
drinking and dietary factors with esophageal cancer in
high- and low-risk areas of Jiangsu Province, China. World
J Gastroenterol 2006;12:1686-93.
12. Lee CH, Lee JM, Wu DC, et al. Independent and combined
effects of alcohol intake, tobacco smoking and betel quid
chewing on the risk of esophageal cancer in Taiwan. Int J
Cancer 2005;113:475-82.
13. de Jonge PJ, Steyerberg EW, Kuipers EJ, et al. Risk factors for
the development of esophageal adenocarcinoma in
Barrett’s esophagus. Am J Gastroenterol 2006;101:1421-9.
14. Ranka S, Gee JM, Johnson IT, et al. Non-steroidal antiinflammatory
drugs, lower oesophageal sphincter-relaxing
drugs and oesophageal cancer. A case-control study.
Digestion 2006;74:109-15.
15. Whiteman DC, Sadeghi S, Pandeya N, et al. Combined
effects of obesity, acid reflux and smoking on the risk of
adenocarcinomas of the oesophagus. Gut 2008;57:173-80.
16. Crew KD, Neugut AI. Epidemiology of upper gastrointestinal
malignancies. Semin Oncol 2004;31:450-64.
17. Lagergren J. Adenocarcinoma of oesophagus: what exactly
is the size of the problem and who is at risk? Gut 2005;54
(Suppl 1):i1-5.
18. Pera M, Manterola C, Vidal O, Grande L. Epidemiology of
esophageal adenocarcinoma. J Surg Oncol 2005;92:151-9.
19. Freedman ND, Abnet CC, Leitzmann MF, et al. A prospective
study of tobacco, alcohol, and the risk of esophageal and
gastric cancer subtypes. Am J Epidemiol 2007;165:1424-33.
20. Brown LM, Hoover R, Silverman D, et al. Excess incidence of
squamous cell esophageal cancer among US Black men:
role of social class and other risk factors. Am J Epidemiol
2001;153:114-22.
21. Hung HC, Huang MC, Lee JM, et al. Association between
diet and esophageal cancer in Taiwan. J Gastroenterol
Hepatol 2004;9:632-7.
22. De Stefani E, Deneo-Pellegrini H, Ronco AL, et al. Food
groups and risk of squamous cell carcinoma of the
oesophagus: a case-control study in Uruguay. Br J Cancer
2003;89:1209-14.
23. Wang JM, Xu B, Rao JY, et al. Diet habits, alcohol drinking,
tobacco smoking, green tea drinking, and the risk of
esophageal squamous cell carcinoma in the Chinese
population. Eur J Gastroenterol Hepatol 2007;19:171-6.
24. De Stefani E, Ronco AL, Boffetta P, et al. Nutrient intake and
risk of squamous cell carcinoma of the esophagus: a casecontrol
study in Uruguay. Nutr Cancer 2006;56:149-57.
25. Bollschweiler E, Wolfgarten E, Nowroth T, et al. Vitamin
intake and risk of subtypes of esophageal cancer in
Germany. J Cancer Res Clin Oncol 2002;128:575-80.
26. Franceschi S, Bidoli E, Negri E, et al. Role of macronutrients,
vitamins and minerals in the aetiology of squamous-cell
carcinoma of the oesophagus. Int J Cancer 2000;86:626-31.
27. Blot WJ, Li JY, Taylor PR, et al. Nutrition intervention trials in
Linxian, China: supplementation with specific vitamin/
mineral combinations, cancer incidence, and diseasespecific
mortality in the general population. J Natl Cancer
Inst 1993;85:1483-92.
28. Mark SD, Qiao YL, Dawsey SM, et al. Prospective study of
serum selenium levels and incident esophageal and gastric
cancers. J Natl Cancer Inst 2000;92:1753-63.
29. Wei WQ, Abnet CC, Qiao YL, et al. Prospective study of
serum selenium concentrations and esophageal and gastric
cardia cancer, heart disease, stroke, and total death. Am
J Clin Nutr 2004;79:80-5.
30. Abnet CC, Lai B, Qiao Y-L, et al. Zinc concentration in
esophageal biopsies measured by X-ray fluorescence and
cancer risk. J Natl Cancer Inst 2005;97:301-6.
31. Terry P, Lagergren J, Ye W, Nyrén O, Wolk A. Antioxidants
and cancers of the esophagus and gastric cardia. Int J
Cancer 2000;87:750-4.
32. Kubo A, Corley DA. Meta-analysis of antioxidant intake and
the risk of esophageal and gastric cardia adenocarcinoma.
Am J Gastroenterol 2007;102:2323-30.
33. González CA, Pera G, Agudo A, et al. Fruit and vegetable
intake and the risk of stomach and oesophagus
adenocarcinoma in the European Prospective Investigation
into Cancer and Nutrition (EPIC-EURGAST). Int J Cancer
2006;118:2559-66.
34. González CA, Jakszyn P, Pera G, et al. Meat intake and risk
of stomach and esophageal adenocarcinoma within the
European Prospective Investigation Into Cancer and
Nutrition (EPIC). J Natl Cancer Inst 2006;98:345-54.
35. 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.
36. Lindblad M, Lagergren J, García Rodríguez LA. Nonsteroidal
anti-inflammatory drugs and risk of esophageal and gastric
cancer. Cancer Epidemiol Biomarkers Prev 2005;14:444-50.
37. Anderson LA, Johnston BT, Watson RG, et al. Nonsteroidal
anti-inflammatory drugs and the esophageal inflammationmetaplasia-
adenocarcinoma sequence. Cancer Res 2006;
66:4975-82.
38. Fortuny J, Johnson CC, Bohlke K, et al. Use of antiinflammatory
drugs and lower esophageal sphincter-relaxing
drugs and risk of esophageal and gastric cancers. Clin
Gastroenterol Hepatol 2007;5:1154-9.
39. Duan L, Wu AH, Sullivan-Halley J, Bernstein L. Nonsteroidal
anti-inflammatory drugs and risk of esophageal and gastric
adenocarcinomas in Los Angeles County. Cancer Epidemiol
Biomarkers Prev 2008;17:126-34.
40. Limburg PJ, Wei W, Ahnen DJ, et al. Randomized, placebocontrolled,
esophageal squamous cell cancer chemoprevention
trial of selenomethionine and celecoxib.
Gastroenterology 2005;129:863-73.
41. IARC Working Group on the Evaluation of Carcinogenic
Risks to Humans. Human papillomaviruses. IARC Monogr
Eval Carcinog Risks Hum 2007;90:1-636.
42. Gillison ML, Shah KV. Chapter 9: Role of mucosal human
papillomavirus in nongenital cancers. J Natl Cancer Inst
Monogr 2003;31:57-65.
43. Yao PF, Li GC, Li J, et al. Evidence of human papilloma virus
infection and its epidemiology in esophageal squamous
cell carcinoma. World J Gastroenterol 2006;12:1352-5.
44. Koh JS, Lee SS, Baek HJ, Kim YI. No association of high-risk
human papillomavirus with esophageal squamous cell
carcinomas among Koreans, as determined by polymerase
chain reaction. Dis Esophagus 2008;21:114-7.
45. Talamini G, Capelli P, Zamboni G, et al. Alcohol, smoking
and papillomavirus infection as risk factors for esophageal
squamous-cell papilloma and esophageal squamous-cell
carcinoma in Italy. Int J Cancer 2000;86:874-8.
46. White RE, Mungatana C, Mutuma G, et al. Absence of
human papillomavirus in esophageal carcinomas from
southwestern Kenya. Dis Esophagus 2005;18:28-30.
47. Gao GF, Roth MJ, Wei WQ, et al. No association between
HPV infection and the neoplastic progression of esophageal
squamous cell carcinoma: result from a cross-sectional
study in a high-risk region of China. Int J Cancer 2006;119:
1354-9.
48. International Agency for Research on Cancer. Human
papillomaviruses. IARC Monogr Eval Carcinog Risks Hum.
2007;90:1-636.
49. Nideobitek G. Epstein-Barr virus infection in the pathogenesis
of nasopharyngeal carcinoma. J Clin Pathol: Mol Pathol, 53:
248-54.
50. Wang LS, Chow KC, Wu YC, Li WY, Huang MH. Detection of
Epstein-Barr virus in esophageal squamous cell carcinoma
in Taiwan. Am J Gastroenterol 1999;94:2834-9.
51. Awerkiew S, Bollschweiler E, Metzger R, Schneider PM,
Hölscher AH, Pfister H. Esophageal cancer in Germany is
associated with Epstein-Barr-virus but not with
papillomaviruses. Med Microbiol Immunol 2003;192:137-40.
52. Sunpaweravong S, Mitarnun W, Puttawibul P. Absence of
Epstein-Barr virus in esophageal squamous cell carcinoma
Dis Esophagus 2005;18:319-35.
53. Yanai H, Hirano A, Matsusaki K, et al. Epstein-Barr virus
association is rare in esophageal squamous cell carcinoma.
Int J Gastrointest Cancer 2003;33:165-70.
54. Mizobuchi S, Sakamoto H, Tachimori Y, Kato H, Watanabe H,
Terada M. Absence of human papillomavirus-16 and -18
DNA and Epstein-Barr virus DNA in esophageal squamous
cell carcinoma. Jpn J Clin Oncol 1997;27:1-5.
55. Hong T, Shimada Y, Kano M, et al. The Epstein-Barr virus is
rarely associated with esophageal cancer. Int J Mol Med
2000;5:363-8.
56. Chang F, Syrjänen S, Shen Q, et al. Evaluation of HPV, CMV,
HSV and EBV in esophageal squamous cell carcinomas
from a high-incidence area of China. Anticancer Res. 2000;
20: 3935-40.
57. Wang J, Noffsinger A, Stemmermann G, Fenoglio-Preiser C.
Esophageal squamous cell carcinomas arising in patients
from a high-risk area of North China lack an association with
Epstein-Barr virus. Cancer Epidemiol Biomarkers Prev 1999;
8:1111-4.
58. Cho YJ, Chang MS, Park SH, Kim HS, Kim WH. In situ
hybridization of Epstein-Barr virus in tumor cells and tumorinfiltrating
lymphocytes of the gastrointestinal tract. Hum
Pathol 2001;32:297-301.
59. Peek, RM, Crabtree JE. Helicobacter infection and gastric
neoplasia. J Pathol 2006;208:233-48.
60. Suerbaum S. and Michetti P. Helicobacter pylori infection.
N Engl. J Med 2002;347:1175-86.
61. Islami F, Kamangar F. Helicobacter pylori and esophageal
cancer risk: a meta-analysis. Cancer Prev Res (Phila Pa)
2008;1:329-38.
62. Rokkas T, Pistiolas D, Sechopoulos P, Robotis I, Margantinis G.
Relationship between Helicobacter pylori infection and
esophageal neoplasia: a meta-analysis. Clin Gastroenterol
Hepatol 2007;5:1413-7.
63. Zhuo X, Zhang Y, Wang Y, Zhuo W, Zhu Y, Zhang X.
Helicobacter pylori infection and oesophageal cancer risk:
association studies via evidence-based meta-analyses. Clin
Oncol (R Coll Radiol) 2008;20:757-62.
64. Chow WH, Blaser MJ, Blot WJ, et al. An inverse relation
between cagA+ strains of Helicobacter pylori infection and
risk of esophageal and gastric cardia adenocarcinoma.
Cancer Res 1998;58:588-90.
65. Fong LY, Lau KM, Huebner K, Magee PN. Induction of
esophageal tumors in zinc-deficient rats by single low doses
of N-nitrosomethylbenzylamine (NMBA): analysis of cell
proliferation, and mutations in H-ras and p53 genes.
Carcinogenesis 1997;18:1477-84.
66. Lijinsky W, Singer GM, Kovatch RM. Similar carcinogenic
effects in rats of 1-ethyl-1-nitroso-3-hydroxyethylurea and 1-
hydroxyethyl-1-nitroso-3-ethylurea. Carcinogenesis 1985;6:
641-3.
67. Ivankovic S, Seibel J, Komitowski D, Spiegelhalder B,
Preussmann R, Siddiqi M. Caffeine-derived N-nitroso
compounds. V. Carcinogenicity of mononitrosocaffeidine
and dinitrosocaffeidine in bd-ix rats. Carcinogenesis 1998
19:933-7.
68. Preussmann R, Habs M, Habs H, Stummeyer D. Fluorosubstituted
N-nitrosamines. 6. carcinogenicity of N-nitroso-
(2,2,2-trifluoroethyl)-ethylamine in rats. Carcinogenesis 1983;
4:755-7.
69. Bartsch H, Frank N, Frei E, Marks F, Schroeder CH, Lin JK.
Taiwanese-German workshop on tumour prevention. Eur J
Cancer Prev 1996;5:83-8.
70. Tricker AR. N-nitroso compounds and man: sources of
exposure, endogenous formation and occurrence in body
fluids. Eur J Cancer Prev 1997;6:226-68.
71. Abnet CC, Qiao YL, Mark SD, Dong ZW, Taylor PR, Dawsey
SM. Prospective study of tooth loss and incident esophageal
and gastric cancers in China. Cancer Causes Control 2001;
12:847-54.
72. Abnet CC, Kamangar F, Dawsey SM, et al. Tooth loss is
associated with increased risk of gastric non-cardia
adenocarcinoma in a cohort of Finnish smokers. Scand J
Gastroenterol 2005;40:681-7.
73. 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;12:4296-303.
74. Danaei G, Vander Hoorn S, Lopez AD, Murray CJ, Ezzati M.
Comparative Risk Assessment collaborating group
(Cancers). Causes of cancer in the world: comparative risk
assessment of nine behavioural and environmental risk
factors. Lancet 2005;366:1784-93.
75. Kazerouni N, Sinha R, Hsu CH, Greenberg A, Rothman N.
Analysis of 200 food items for benzo[a]pyrene and estimation
of its intake in an epidemiologic study. Food Chem Toxicol
2001;39:423-36.
76. Chang KF, Fang GC, Chen JC, Wu YS. Atmospheric
polycyclic aromatic hydrocarbons (PAHs) in Asia: a review
from 1999 to 2004. Environ Pollut 2006;142:388-96.
77. Boffetta P, Jourenkova N, Gustavsson P. Cancer risk from
occupational and environmental exposure to polycyclic
aromatic hydrocarbons. Cancer Causes Control 1997;8:
444-72.
78. Roth MJ, Guo-Qing W, Lewin KJ, et al. Histopathologic
changes seen in esophagectomy specimens from the highrisk
region of Linxian, China: potential clues to an etiologic
exposure? Hum Pathol 1998;29:1294-8.
79. Roth MJ, Strickland KL, Wang GQ, Rothman N, Greenberg A,
Dawsey SM. High levels of carcinogenic polycyclic aromatic
hydrocarbons present within food from Linxian, China may
contribute to that region’s high incidence of oesophageal
cancer. Eur J Cancer 1998;34:757-8.
80. Roth MJ, Qiao YL, Rothman N, et al. High urine 1-
hydroxypyrene glucuronide concentrations in Linxian, China,
an area of high risk for squamous oesophageal cancer.
Biomarkers 2001;6:381-6.
81. Strickland P, Kang D, Sithisarankul P. Polycyclic aromatic
hydrocarbon metabolites in urine as biomarkers of exposure
and effect. Environ Health Perspect 1996;104 (Suppl 5): 927-
32.
82. Yokoyama A, Omori T. Genetic polymorphisms of alcohol
and aldehyde dehydrogenases and risk for esophageal
and head and neck cancers. Alcohol 2005;35:175-85.
83. International Agency for Research on Cancer.
Acetaldehyde. IARC Monogr Eval Carcinog Risks Hum
1999;71Pt2:319-35.
84. Lagergren J, Bergström R, Lindgren A, Nyrén O. Symptomatic
gastroesophageal reflux as a risk factor for esophageal
adenocarcinoma. N Engl J Med 1999;340:825-31.
85. Wu AH, Tseng CC, Bernstein L. Hiatal hernia, reflux symptoms,
body size, and risk of esophageal and gastric
adenocarcinoma. Cancer 2003;98:940-8.
86. Farrow DC, Vaughan TL, Sweeney C, et al. Gastroesophageal
reflux disease, use of H2 receptor antagonists,
and risk of esophageal and gastric cancer. Cancer Causes
Control 2000;11:231-8.
87. Shaheen NJ, Crosby MA, Bozymski EM, Sandler RS. Is there
publication bias in the reporting of cancer risk in Barrett’s
esophagus? Gastroenterology 2000;119:333-8.
88. Jankowski JA, Provenzale D, Moayyedi P. Esophageal
adenocarcinoma arising from Barrett’s metaplasia has
regional variations in the west. Gastroenterology 2002;122:
588-90.
89. Lieberman DA, Oehlke M, Helfand M. Risk factors for Barrett’s
esophagus in community-based practice. GORGE
consortium. Gastroenterology Outcomes Research Group
in Endoscopy. Am J Gastroenterol 1997;92:1293-7.
90. Ryan AM, Rowley SP, Fitzgerald AP, Ravi N, Reynolds JV.
Adenocarcinoma of the oesophagus and gastric cardia
male preponderance in association with obesity. Eur J
Cancer 2006;42:1151-8.
91. Merry AH, Schouten LJ, Goldbohm RA, van den Brandt PA.
Body mass index, height and risk of adenocarcinoma of the
oesophagus and gastric cardia: a prospective cohort study.
Gut 2007;56:1503-11.
92. Kubo A, Corley DA. Body mass index and adenocarcinomas
of the esophagus or gastric cardia: a systematic review and
meta-analysis. Cancer Epidemiol Biomarkers Prev 2006;15:
872-8.
93. Hampel H, Abraham NS, El-Serag HB. Meta-analysis: obesity
and the risk for gastroesophageal reflux disease and its
complications. Ann Intern Med 2005;143:199-211.
94. Corley DA, Levin TR, Habel LA, Buffler PA. Barrett’s esophagus
and medications that relax the lower esophageal sphincter.
Am J Gastroenterol 2006;101:937-44.
95. Lindblad M, Rodríguez LA, Lagergren J. Body mass, tobacco
and alcohol and risk of esophageal, gastric cardia, and
gastric non-cardia adenocarcinoma among men and
women in a nested case-control study. Cancer Causes
Control 2005;16:285-94.
96. Jansson C, Johansson AL, Nyrén O, Lagergren J. Socioeconomic
factors and risk of esophageal adenocarcinoma:
a nationwide Swedish case-control study. Cancer Epidemiol
Biomarkers Prev 2005;14:1754-61.
97. Brown LM, Devesa SS. Epidemiologic trends in esophageal
and gastric cancer in the United States. Surg Oncol Clin N
Am 2002;11:235-56.
2002. CA Cancer J Clin 2005;55:74-108.
2. Kamanger F, Dores GM, Anderson WF. Patterns of cancer
incidence, mortality and prevalence across five continents:
defining priorities to reduce cancer disparities in different
geographic regions of the world. J Clin Oncol 2006;24:2137-
50.
3. Ke L. Mortality and incidence trends from esophagus cancer
in selected geographic areas of China circa 1970-90. Int J
Cancer 2002;102:271-4.
4. Wang Z, Tang L, Sun G, et al. Etiological study of esophageal
squamous cell carcinoma in an endemic region: a
population-based case control study in Huaian, China.
BMC Cancer 2006;6:287.
5. 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;
113:456-63.
6. Sriplung H, Wiangnon S, Sontipong S, et al. Cancer incidence
trends in Thailand, 1989-2000. Asian Pac J Cancer Prev 2006;
7:239-44.
7. Holmes RS, Vaughan TL. Epidemiology and pathogenesis of
esophageal cancer. Semin Radiat Oncol 200717:2-9.
8. Hashibe M, Boffetta P, Janout V, et al. Esophageal cancer
in Central and Eastern Europe: tobacco and alcohol. Int J
Cancer 2007;120:1518-22.
9. Jiang JM, Zeng XJ, Chen JS, et al. Smoking and mortality
from esophageal cancer in China: a large case-control
study of 19,734 male esophageal cancer deaths and 104,846
living spouse controls. Int J Cancer 2006;119:1427-32.
10. Wu IC, Lu CY, Kuo FC, et al. Interaction between cigarette,
alcohol and betel nut use on esophageal cancer risk in
Taiwan. Eur J Clin Invest 2006;36:236-41.
11. Wu M, Zhao JK, Hu XS, et al. Association of smoking, alcohol
drinking and dietary factors with esophageal cancer in
high- and low-risk areas of Jiangsu Province, China. World
J Gastroenterol 2006;12:1686-93.
12. Lee CH, Lee JM, Wu DC, et al. Independent and combined
effects of alcohol intake, tobacco smoking and betel quid
chewing on the risk of esophageal cancer in Taiwan. Int J
Cancer 2005;113:475-82.
13. de Jonge PJ, Steyerberg EW, Kuipers EJ, et al. Risk factors for
the development of esophageal adenocarcinoma in
Barrett’s esophagus. Am J Gastroenterol 2006;101:1421-9.
14. Ranka S, Gee JM, Johnson IT, et al. Non-steroidal antiinflammatory
drugs, lower oesophageal sphincter-relaxing
drugs and oesophageal cancer. A case-control study.
Digestion 2006;74:109-15.
15. Whiteman DC, Sadeghi S, Pandeya N, et al. Combined
effects of obesity, acid reflux and smoking on the risk of
adenocarcinomas of the oesophagus. Gut 2008;57:173-80.
16. Crew KD, Neugut AI. Epidemiology of upper gastrointestinal
malignancies. Semin Oncol 2004;31:450-64.
17. Lagergren J. Adenocarcinoma of oesophagus: what exactly
is the size of the problem and who is at risk? Gut 2005;54
(Suppl 1):i1-5.
18. Pera M, Manterola C, Vidal O, Grande L. Epidemiology of
esophageal adenocarcinoma. J Surg Oncol 2005;92:151-9.
19. Freedman ND, Abnet CC, Leitzmann MF, et al. A prospective
study of tobacco, alcohol, and the risk of esophageal and
gastric cancer subtypes. Am J Epidemiol 2007;165:1424-33.
20. Brown LM, Hoover R, Silverman D, et al. Excess incidence of
squamous cell esophageal cancer among US Black men:
role of social class and other risk factors. Am J Epidemiol
2001;153:114-22.
21. Hung HC, Huang MC, Lee JM, et al. Association between
diet and esophageal cancer in Taiwan. J Gastroenterol
Hepatol 2004;9:632-7.
22. De Stefani E, Deneo-Pellegrini H, Ronco AL, et al. Food
groups and risk of squamous cell carcinoma of the
oesophagus: a case-control study in Uruguay. Br J Cancer
2003;89:1209-14.
23. Wang JM, Xu B, Rao JY, et al. Diet habits, alcohol drinking,
tobacco smoking, green tea drinking, and the risk of
esophageal squamous cell carcinoma in the Chinese
population. Eur J Gastroenterol Hepatol 2007;19:171-6.
24. De Stefani E, Ronco AL, Boffetta P, et al. Nutrient intake and
risk of squamous cell carcinoma of the esophagus: a casecontrol
study in Uruguay. Nutr Cancer 2006;56:149-57.
25. Bollschweiler E, Wolfgarten E, Nowroth T, et al. Vitamin
intake and risk of subtypes of esophageal cancer in
Germany. J Cancer Res Clin Oncol 2002;128:575-80.
26. Franceschi S, Bidoli E, Negri E, et al. Role of macronutrients,
vitamins and minerals in the aetiology of squamous-cell
carcinoma of the oesophagus. Int J Cancer 2000;86:626-31.
27. Blot WJ, Li JY, Taylor PR, et al. Nutrition intervention trials in
Linxian, China: supplementation with specific vitamin/
mineral combinations, cancer incidence, and diseasespecific
mortality in the general population. J Natl Cancer
Inst 1993;85:1483-92.
28. Mark SD, Qiao YL, Dawsey SM, et al. Prospective study of
serum selenium levels and incident esophageal and gastric
cancers. J Natl Cancer Inst 2000;92:1753-63.
29. Wei WQ, Abnet CC, Qiao YL, et al. Prospective study of
serum selenium concentrations and esophageal and gastric
cardia cancer, heart disease, stroke, and total death. Am
J Clin Nutr 2004;79:80-5.
30. Abnet CC, Lai B, Qiao Y-L, et al. Zinc concentration in
esophageal biopsies measured by X-ray fluorescence and
cancer risk. J Natl Cancer Inst 2005;97:301-6.
31. Terry P, Lagergren J, Ye W, Nyrén O, Wolk A. Antioxidants
and cancers of the esophagus and gastric cardia. Int J
Cancer 2000;87:750-4.
32. Kubo A, Corley DA. Meta-analysis of antioxidant intake and
the risk of esophageal and gastric cardia adenocarcinoma.
Am J Gastroenterol 2007;102:2323-30.
33. González CA, Pera G, Agudo A, et al. Fruit and vegetable
intake and the risk of stomach and oesophagus
adenocarcinoma in the European Prospective Investigation
into Cancer and Nutrition (EPIC-EURGAST). Int J Cancer
2006;118:2559-66.
34. González CA, Jakszyn P, Pera G, et al. Meat intake and risk
of stomach and esophageal adenocarcinoma within the
European Prospective Investigation Into Cancer and
Nutrition (EPIC). J Natl Cancer Inst 2006;98:345-54.
35. 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.
36. Lindblad M, Lagergren J, García Rodríguez LA. Nonsteroidal
anti-inflammatory drugs and risk of esophageal and gastric
cancer. Cancer Epidemiol Biomarkers Prev 2005;14:444-50.
37. Anderson LA, Johnston BT, Watson RG, et al. Nonsteroidal
anti-inflammatory drugs and the esophageal inflammationmetaplasia-
adenocarcinoma sequence. Cancer Res 2006;
66:4975-82.
38. Fortuny J, Johnson CC, Bohlke K, et al. Use of antiinflammatory
drugs and lower esophageal sphincter-relaxing
drugs and risk of esophageal and gastric cancers. Clin
Gastroenterol Hepatol 2007;5:1154-9.
39. Duan L, Wu AH, Sullivan-Halley J, Bernstein L. Nonsteroidal
anti-inflammatory drugs and risk of esophageal and gastric
adenocarcinomas in Los Angeles County. Cancer Epidemiol
Biomarkers Prev 2008;17:126-34.
40. Limburg PJ, Wei W, Ahnen DJ, et al. Randomized, placebocontrolled,
esophageal squamous cell cancer chemoprevention
trial of selenomethionine and celecoxib.
Gastroenterology 2005;129:863-73.
41. IARC Working Group on the Evaluation of Carcinogenic
Risks to Humans. Human papillomaviruses. IARC Monogr
Eval Carcinog Risks Hum 2007;90:1-636.
42. Gillison ML, Shah KV. Chapter 9: Role of mucosal human
papillomavirus in nongenital cancers. J Natl Cancer Inst
Monogr 2003;31:57-65.
43. Yao PF, Li GC, Li J, et al. Evidence of human papilloma virus
infection and its epidemiology in esophageal squamous
cell carcinoma. World J Gastroenterol 2006;12:1352-5.
44. Koh JS, Lee SS, Baek HJ, Kim YI. No association of high-risk
human papillomavirus with esophageal squamous cell
carcinomas among Koreans, as determined by polymerase
chain reaction. Dis Esophagus 2008;21:114-7.
45. Talamini G, Capelli P, Zamboni G, et al. Alcohol, smoking
and papillomavirus infection as risk factors for esophageal
squamous-cell papilloma and esophageal squamous-cell
carcinoma in Italy. Int J Cancer 2000;86:874-8.
46. White RE, Mungatana C, Mutuma G, et al. Absence of
human papillomavirus in esophageal carcinomas from
southwestern Kenya. Dis Esophagus 2005;18:28-30.
47. Gao GF, Roth MJ, Wei WQ, et al. No association between
HPV infection and the neoplastic progression of esophageal
squamous cell carcinoma: result from a cross-sectional
study in a high-risk region of China. Int J Cancer 2006;119:
1354-9.
48. International Agency for Research on Cancer. Human
papillomaviruses. IARC Monogr Eval Carcinog Risks Hum.
2007;90:1-636.
49. Nideobitek G. Epstein-Barr virus infection in the pathogenesis
of nasopharyngeal carcinoma. J Clin Pathol: Mol Pathol, 53:
248-54.
50. Wang LS, Chow KC, Wu YC, Li WY, Huang MH. Detection of
Epstein-Barr virus in esophageal squamous cell carcinoma
in Taiwan. Am J Gastroenterol 1999;94:2834-9.
51. Awerkiew S, Bollschweiler E, Metzger R, Schneider PM,
Hölscher AH, Pfister H. Esophageal cancer in Germany is
associated with Epstein-Barr-virus but not with
papillomaviruses. Med Microbiol Immunol 2003;192:137-40.
52. Sunpaweravong S, Mitarnun W, Puttawibul P. Absence of
Epstein-Barr virus in esophageal squamous cell carcinoma
Dis Esophagus 2005;18:319-35.
53. Yanai H, Hirano A, Matsusaki K, et al. Epstein-Barr virus
association is rare in esophageal squamous cell carcinoma.
Int J Gastrointest Cancer 2003;33:165-70.
54. Mizobuchi S, Sakamoto H, Tachimori Y, Kato H, Watanabe H,
Terada M. Absence of human papillomavirus-16 and -18
DNA and Epstein-Barr virus DNA in esophageal squamous
cell carcinoma. Jpn J Clin Oncol 1997;27:1-5.
55. Hong T, Shimada Y, Kano M, et al. The Epstein-Barr virus is
rarely associated with esophageal cancer. Int J Mol Med
2000;5:363-8.
56. Chang F, Syrjänen S, Shen Q, et al. Evaluation of HPV, CMV,
HSV and EBV in esophageal squamous cell carcinomas
from a high-incidence area of China. Anticancer Res. 2000;
20: 3935-40.
57. Wang J, Noffsinger A, Stemmermann G, Fenoglio-Preiser C.
Esophageal squamous cell carcinomas arising in patients
from a high-risk area of North China lack an association with
Epstein-Barr virus. Cancer Epidemiol Biomarkers Prev 1999;
8:1111-4.
58. Cho YJ, Chang MS, Park SH, Kim HS, Kim WH. In situ
hybridization of Epstein-Barr virus in tumor cells and tumorinfiltrating
lymphocytes of the gastrointestinal tract. Hum
Pathol 2001;32:297-301.
59. Peek, RM, Crabtree JE. Helicobacter infection and gastric
neoplasia. J Pathol 2006;208:233-48.
60. Suerbaum S. and Michetti P. Helicobacter pylori infection.
N Engl. J Med 2002;347:1175-86.
61. Islami F, Kamangar F. Helicobacter pylori and esophageal
cancer risk: a meta-analysis. Cancer Prev Res (Phila Pa)
2008;1:329-38.
62. Rokkas T, Pistiolas D, Sechopoulos P, Robotis I, Margantinis G.
Relationship between Helicobacter pylori infection and
esophageal neoplasia: a meta-analysis. Clin Gastroenterol
Hepatol 2007;5:1413-7.
63. Zhuo X, Zhang Y, Wang Y, Zhuo W, Zhu Y, Zhang X.
Helicobacter pylori infection and oesophageal cancer risk:
association studies via evidence-based meta-analyses. Clin
Oncol (R Coll Radiol) 2008;20:757-62.
64. Chow WH, Blaser MJ, Blot WJ, et al. An inverse relation
between cagA+ strains of Helicobacter pylori infection and
risk of esophageal and gastric cardia adenocarcinoma.
Cancer Res 1998;58:588-90.
65. Fong LY, Lau KM, Huebner K, Magee PN. Induction of
esophageal tumors in zinc-deficient rats by single low doses
of N-nitrosomethylbenzylamine (NMBA): analysis of cell
proliferation, and mutations in H-ras and p53 genes.
Carcinogenesis 1997;18:1477-84.
66. Lijinsky W, Singer GM, Kovatch RM. Similar carcinogenic
effects in rats of 1-ethyl-1-nitroso-3-hydroxyethylurea and 1-
hydroxyethyl-1-nitroso-3-ethylurea. Carcinogenesis 1985;6:
641-3.
67. Ivankovic S, Seibel J, Komitowski D, Spiegelhalder B,
Preussmann R, Siddiqi M. Caffeine-derived N-nitroso
compounds. V. Carcinogenicity of mononitrosocaffeidine
and dinitrosocaffeidine in bd-ix rats. Carcinogenesis 1998
19:933-7.
68. Preussmann R, Habs M, Habs H, Stummeyer D. Fluorosubstituted
N-nitrosamines. 6. carcinogenicity of N-nitroso-
(2,2,2-trifluoroethyl)-ethylamine in rats. Carcinogenesis 1983;
4:755-7.
69. Bartsch H, Frank N, Frei E, Marks F, Schroeder CH, Lin JK.
Taiwanese-German workshop on tumour prevention. Eur J
Cancer Prev 1996;5:83-8.
70. Tricker AR. N-nitroso compounds and man: sources of
exposure, endogenous formation and occurrence in body
fluids. Eur J Cancer Prev 1997;6:226-68.
71. Abnet CC, Qiao YL, Mark SD, Dong ZW, Taylor PR, Dawsey
SM. Prospective study of tooth loss and incident esophageal
and gastric cancers in China. Cancer Causes Control 2001;
12:847-54.
72. Abnet CC, Kamangar F, Dawsey SM, et al. Tooth loss is
associated with increased risk of gastric non-cardia
adenocarcinoma in a cohort of Finnish smokers. Scand J
Gastroenterol 2005;40:681-7.
73. 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;12:4296-303.
74. Danaei G, Vander Hoorn S, Lopez AD, Murray CJ, Ezzati M.
Comparative Risk Assessment collaborating group
(Cancers). Causes of cancer in the world: comparative risk
assessment of nine behavioural and environmental risk
factors. Lancet 2005;366:1784-93.
75. Kazerouni N, Sinha R, Hsu CH, Greenberg A, Rothman N.
Analysis of 200 food items for benzo[a]pyrene and estimation
of its intake in an epidemiologic study. Food Chem Toxicol
2001;39:423-36.
76. Chang KF, Fang GC, Chen JC, Wu YS. Atmospheric
polycyclic aromatic hydrocarbons (PAHs) in Asia: a review
from 1999 to 2004. Environ Pollut 2006;142:388-96.
77. Boffetta P, Jourenkova N, Gustavsson P. Cancer risk from
occupational and environmental exposure to polycyclic
aromatic hydrocarbons. Cancer Causes Control 1997;8:
444-72.
78. Roth MJ, Guo-Qing W, Lewin KJ, et al. Histopathologic
changes seen in esophagectomy specimens from the highrisk
region of Linxian, China: potential clues to an etiologic
exposure? Hum Pathol 1998;29:1294-8.
79. Roth MJ, Strickland KL, Wang GQ, Rothman N, Greenberg A,
Dawsey SM. High levels of carcinogenic polycyclic aromatic
hydrocarbons present within food from Linxian, China may
contribute to that region’s high incidence of oesophageal
cancer. Eur J Cancer 1998;34:757-8.
80. Roth MJ, Qiao YL, Rothman N, et al. High urine 1-
hydroxypyrene glucuronide concentrations in Linxian, China,
an area of high risk for squamous oesophageal cancer.
Biomarkers 2001;6:381-6.
81. Strickland P, Kang D, Sithisarankul P. Polycyclic aromatic
hydrocarbon metabolites in urine as biomarkers of exposure
and effect. Environ Health Perspect 1996;104 (Suppl 5): 927-
32.
82. Yokoyama A, Omori T. Genetic polymorphisms of alcohol
and aldehyde dehydrogenases and risk for esophageal
and head and neck cancers. Alcohol 2005;35:175-85.
83. International Agency for Research on Cancer.
Acetaldehyde. IARC Monogr Eval Carcinog Risks Hum
1999;71Pt2:319-35.
84. Lagergren J, Bergström R, Lindgren A, Nyrén O. Symptomatic
gastroesophageal reflux as a risk factor for esophageal
adenocarcinoma. N Engl J Med 1999;340:825-31.
85. Wu AH, Tseng CC, Bernstein L. Hiatal hernia, reflux symptoms,
body size, and risk of esophageal and gastric
adenocarcinoma. Cancer 2003;98:940-8.
86. Farrow DC, Vaughan TL, Sweeney C, et al. Gastroesophageal
reflux disease, use of H2 receptor antagonists,
and risk of esophageal and gastric cancer. Cancer Causes
Control 2000;11:231-8.
87. Shaheen NJ, Crosby MA, Bozymski EM, Sandler RS. Is there
publication bias in the reporting of cancer risk in Barrett’s
esophagus? Gastroenterology 2000;119:333-8.
88. Jankowski JA, Provenzale D, Moayyedi P. Esophageal
adenocarcinoma arising from Barrett’s metaplasia has
regional variations in the west. Gastroenterology 2002;122:
588-90.
89. Lieberman DA, Oehlke M, Helfand M. Risk factors for Barrett’s
esophagus in community-based practice. GORGE
consortium. Gastroenterology Outcomes Research Group
in Endoscopy. Am J Gastroenterol 1997;92:1293-7.
90. Ryan AM, Rowley SP, Fitzgerald AP, Ravi N, Reynolds JV.
Adenocarcinoma of the oesophagus and gastric cardia
male preponderance in association with obesity. Eur J
Cancer 2006;42:1151-8.
91. Merry AH, Schouten LJ, Goldbohm RA, van den Brandt PA.
Body mass index, height and risk of adenocarcinoma of the
oesophagus and gastric cardia: a prospective cohort study.
Gut 2007;56:1503-11.
92. Kubo A, Corley DA. Body mass index and adenocarcinomas
of the esophagus or gastric cardia: a systematic review and
meta-analysis. Cancer Epidemiol Biomarkers Prev 2006;15:
872-8.
93. Hampel H, Abraham NS, El-Serag HB. Meta-analysis: obesity
and the risk for gastroesophageal reflux disease and its
complications. Ann Intern Med 2005;143:199-211.
94. Corley DA, Levin TR, Habel LA, Buffler PA. Barrett’s esophagus
and medications that relax the lower esophageal sphincter.
Am J Gastroenterol 2006;101:937-44.
95. Lindblad M, Rodríguez LA, Lagergren J. Body mass, tobacco
and alcohol and risk of esophageal, gastric cardia, and
gastric non-cardia adenocarcinoma among men and
women in a nested case-control study. Cancer Causes
Control 2005;16:285-94.
96. Jansson C, Johansson AL, Nyrén O, Lagergren J. Socioeconomic
factors and risk of esophageal adenocarcinoma:
a nationwide Swedish case-control study. Cancer Epidemiol
Biomarkers Prev 2005;14:1754-61.
97. Brown LM, Devesa SS. Epidemiologic trends in esophageal
and gastric cancer in the United States. Surg Oncol Clin N
Am 2002;11:235-56.
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Sunpaweravong S. Epidemiology and Risk Factors of Esophageal Cancer. Thai J Surg [Internet]. 2010 Dec. 31 [cited 2024 Nov. 23];31(4). Available from: https://he02.tci-thaijo.org/index.php/ThaiJSurg/article/view/227597
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