Skip to main content

High-Risk and Low-Risk Human Papillomavirus in Esophageal Squamous Cell Carcinoma at Mazandaran, Northern Iran

Pathology & Oncology Research volume 19, pages 385–391 (2013)Cite this article

Abstract

Cancers are the second most common cause of non-accidental deaths in Iran, following cardiovascular deaths. Mazandaran, near the Caspian Littoral at north of Iran have identified as a several-high incidence area for Esophageal Squamous Cell Carcinoma (ESCC) in the world. Several associated risk factors, such as dietary and cultural habits, infectious agents, nutritional deficiencies, too much use of tobacco and alcohol and infection to certain DNA tumor viruses (HPVs), including environmental and genetic factors are attributed to this disease. To explore this issue, we analyzed HPV DNA prevalence and HPV types together in relation to tumor sites a high-incidence population. Archived tissue blocks from 46, 69 and 62 upper, middle and lower third of esophagus, respectively from ESCC patients were evaluated for the presence of HPV DNA by PCR using the degenerate HPV L1 consensus primer pairs MY09/MY11. The positive specimens were evaluated by Real-time PCR to determine HPV genotypes. From the 49 HPV positive cases, of ESCC patients, 5 (23.1 %), 11 (55 %) and 9 (56.3 %) of upper, middle and lower third of ESCC specimens, respectively were positive by at least one high and one low-risk HPV genotypes. In general, HPV45 and HPV11 were the most common high- risk and low-risk HPV genotypes in HPV L1 positive cases, respectively, followed by HPV6, HPV52 and HPV39. Therefore, the high prevalence of HPV DNA in different anatomical sites of ESCC patients from the Mazandaran region in North of Iran provides more evidence for a role of HPV in this cancer.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2

References

  1. Parkin DM, Bray F, Ferlay J, Pisani P (2005) Global cancer statistics, 2002. CA Cancer J Clin 55(2):74–108

    PubMed  Article  Google Scholar 

  2. Naghavi M (2000) Death report from 10 provinces in Iran. Ministry of Health, Tehran

    Google Scholar 

  3. Kamangar F, Dores GM, Anderson WF (2006) 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 24(14):2137–2150

    PubMed  Article  Google Scholar 

  4. Li MH, Li P, Li PJ (1980) Recent progress in research on esophageal cancer in China. Adv Cancer Res 33:173–249

    PubMed  Article  CAS  Google Scholar 

  5. Li JY (1982) Epidemiology of esophageal cancer in China. Natl Cancer Inst Monogr 62:113–120

    PubMed  CAS  Google Scholar 

  6. Siddiqi M, Preussmann R (1989) Esophageal cancer in Kashmir—an assessment. J Cancer Res Clin Oncol 115:111–117

    PubMed  Article  CAS  Google Scholar 

  7. Kodsi BE, Wickremesinghe C, Kozinn PJ, Iswara K, Goldberg PK (1976) Candida esophagitis: a prospective study of 27 cases. Gastroenterology 71:715–719

    PubMed  CAS  Google Scholar 

  8. Jarrett WF (1987) The leeuwenhoek lecture, 1986. Environmental carcinogens and papillomaviruses in the pathogenesis of cancer. Proc R Soc Lond B Biol Sci 231:11

    Article  Google Scholar 

  9. Goff JS (1988) Infectious causes of esophagitis. Annu Rev Med 39:163–169

    PubMed  Article  CAS  Google Scholar 

  10. Syrjanen KJ (2002) HPV infections oesophageal cancer. J Clin Pathol 55:721–728

    PubMed  Article  CAS  Google Scholar 

  11. Engel LS, Chow WH, Vaughan TL, Gammon M, Risch H, Stanford J et al (2003) Population attributable risks of esophageal and gastric cancers. J Natl Cancer Inst 95(18):1404–1413

    PubMed  Article  Google Scholar 

  12. Brown LM, Hoover R, Silverman D, Baris D, Hayes R, Swansonet GM et al (2001) Excess incidence of squamous cell esophageal cancer among US black men: role of social class and other risk factors. Am J Epidemiol 153(2):114–122

    PubMed  Article  CAS  Google Scholar 

  13. Kamangar F, Qiao YL, Schiller JT et al (2006) Human papillomavirus serology and the risk of esophageal and gastric cancers: results from a cohort in a high-risk region in China. Int J Cancer 119:579–584

    PubMed  Article  CAS  Google Scholar 

  14. Lu XM, Monnier-Benoit S, Mo LZ et al (2008) Human papillomavirus in esophageal squamous cell carcinoma of the high-risk Kazakh ethnic group in Xinjiang, China. Eur J Surg Oncol 34:765–770

    PubMed  Article  CAS  Google Scholar 

  15. Nasrollahzadeh D, Kamangar F, Aghcheli K, Sotoudeh M, Islami F, Abnet C et al (2008) Opium, tobacco, and alcohol use in relation to oesophageal squamous cell carcinoma in a high-risk area of Iran. Br J Cancer 98(11):1857–1863

    PubMed  Article  CAS  Google Scholar 

  16. Akbari MR, Malekzadeh R, Nasrollahzadeh D, Amanian D, Sun P, Islami F et al (2006) Familial risks of esophageal cancer among the Turkmen population of the Caspian Littoral of Iran. Int J Cancer 119(5):1047–1051

    PubMed  Article  CAS  Google Scholar 

  17. Kamangar F, Strickland PT, Pourshams A, Malekzadeh R, Boffetta P, Roth M et al (2005) High exposure to polycyclic aromatic hydrocarbons may contribute to high risk of esophageal cancer in northeastern Iran. Anticancer Res 25(1B):425–428

    PubMed  CAS  Google Scholar 

  18. Taghavi N, Nasrollahzadeh D, Merat S, Yazdanbod A, Hormazdi M, Sotoudeh M et al (2007) Epidemiology of upper gastrointestinal cancers in Iran: a sub site analysis of 761 cases. World J Gastroenterol 13(40):5367–5370

    PubMed  Google Scholar 

  19. Akbari MR, Malekzadeh R, Nasrollahzadeh D, Amanian D, Islami F, Li S et al (2008) Germline BRCA2 mutations and the risk of esophageal squamous cell carcinoma. Oncogene 27(9):1290–1296

    PubMed  Article  CAS  Google Scholar 

  20. Islami F, Nasrollahzadeh D, Kamangar F (2008) Socioeconomic status in relation to esophageal cancer in a high-risk area of Iran. Gastroenterology 134(4):301–301

    Article  Google Scholar 

  21. Munoz N, Bosch FX, de Sanjose S et al (2003) Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med 348(6):518–527

    PubMed  Article  Google Scholar 

  22. de Villiers EM, Fauquet C, Broker TR, Bernard HU, zur Hausen H (2004) Classification of papillomaviruses. Virology 324(1):17–27

    PubMed  Article  Google Scholar 

  23. Bahnassy AA, Zekri AR, Abdallah S, El-Shehaby AM, Sherif GM (2005) Human papillomavirus infection in Egyptian esophageal carcinoma: correlation with p53, p21, mdm2, C-erbB2 and impact on survival. Pathol Int 55:53–62

    PubMed  Article  CAS  Google Scholar 

  24. Castillo A, Aguayo F, Koriyama C et al (2006) Human papillomavirus in esophageal squamous cell carcinoma in Colombia and Chile. World J Gastroenterol 12:6188–6192

    PubMed  Google Scholar 

  25. Souto Damin AP, Guedes Frazzon AP, de Carvalho Damin D et al (2006) Detection of human papillomavirus DNA in squamous cell carcinoma of the esophagus by auto-nested PCR. Dis Esophagus 19:64–68

    PubMed  Article  CAS  Google Scholar 

  26. Pantelis A, Pantelis D, Ruemmele P et al (2007) p53 Codon 72 polymorphism, loss of heterozygosity and high-risk human papillomavirus infection in a low-incidence German esophageal squamous cell carcinoma patient cohort. Oncol Rep 17:1243–1248

    PubMed  CAS  Google Scholar 

  27. Koh JS, Lee SS, Baek HJ, Kim YI (2008) No association of high-risk human papilloma virus with esophageal squamous cell carcinomas among Koreans, as determined by polymerase chain reaction. Dis Esophagus 21:114–117

    PubMed  Article  CAS  Google Scholar 

  28. Eslami Far A, Aghakhani A, Hamkar R, Ramezani A, Froutan Pishbigar H et al (2007) Frequency of human papillomavirus infection in esophageal squamous cell carcinoma in Iranian patients. Scand J Infect Dis 39:58–62

    Article  Google Scholar 

  29. Shuyama K, Castillo A, Aguayo F et al (2007) Human papillomavirus in high- and low-risk areas of oesophageal squamous cell carcinoma in China. Br J Cancer 96:1554–1559

    PubMed  Article  CAS  Google Scholar 

  30. Lambert R, Hainaut P (2007) Esophageal cancer: cases and causes (part I). Endoscopy 39:550–555

    PubMed  Article  CAS  Google Scholar 

  31. Kamangar F, Malekzadeh R, Dawsey SM, Saidi F (2007) Esophageal cancer in Northeastern Iran: a review. Arch Iran Med 10:70–82

    PubMed  CAS  Google Scholar 

  32. Islami F, Kamangar F, Aghcheli K, Fahimi S, Semnani S, Taghavi N et al (2004) Epidemiologic features of upper gastrointestinal tract cancers in Northeastern Iran. Br J Cancer 90:1402–1406

    PubMed  Article  CAS  Google Scholar 

  33. Moradi AV, de Villers EM, Mokhtari-Azad T, Mahmoudi M, Hazrati B et al (2002) Detection of human papillomavirus DNA by PR in esophageal squamous cell carcinoma from Turkmen Sahra, North-East of Iran. Iranian Biomed J 6(1):19–23

    CAS  Google Scholar 

  34. Wang X, Tian X, Liu F, Zhao Y, Sun M, Chen D et al (2010) Detection of HPV DNA in esophageal cancer specimens from different regions and ethnic groups: a descriptive study. BMC Cancer 10:19

    PubMed  Article  Google Scholar 

  35. Zhang D, Zhang Q, Zhou L, Huo L, Zhang Y, Shen Z et al (2010) Comparison of prevalence, viral load, physical status and expression of human papillomavirus- 16, −18 and −58 in esophageal and cervical cancer: a case–control study. BMC Cancer 10:650–658

    PubMed  Article  CAS  Google Scholar 

  36. Zhang QY, Zhang DH, Shen ZY, Xu LY, Li EM, Au WW (2011) Infection and integration of human papillomavirus in esophageal carcinoma. Int J Hyg Environ Health 214:156–161

    PubMed  Article  CAS  Google Scholar 

  37. Matsha T, Erasmus R, Kafuko AB, Mugwanya D, Stepien A, Parker MI (2002) Human papillomavirus associated with esophageal cancer. J Clin Pathol 55:587–590

    PubMed  Article  CAS  Google Scholar 

  38. Matsha T, Donninger H, Erasmus RT et al (2007) Expression of p53 and its homolog, p73, in HPV DNA positive oesophageal squamous cell carcinomas. Virology 369:182–190

    PubMed  Article  CAS  Google Scholar 

  39. Farhadi M, Tahmasebi Z, Merat S, Kamangar F, Nasrollahzadeh D, Malekzadeh R (2005) Human papillomavirus in squamous cell carcinoma of esophagus in a high-risk population. World J Gastroenterol 11(8):1200–1203

    PubMed  Google Scholar 

  40. Dreilich M, Bergqvist M, Moberg M, Daniel Brattström D, Gustavsson I, Bergström S (2006) High-risk human papilloma virus (HPV) and survival in patients with esophageal carcinoma: a pilot study. BMC Cancer 6:94

    PubMed  Article  Google Scholar 

  41. Herrera-Goepfert R, Lizano M, Akiba S, Carrillo-García A, Becker-D’Acosta M (2009) Human papilloma virus and esophageal carcinoma in a Latin-American region. World J Gastroenterol 15(25):3142–3147

    PubMed  Article  Google Scholar 

  42. de Villiers EM, Gunst K, Stein H, Scherübl H (2004) Esophageal squamous cell cancer in patients with head and neck cancer: prevalence of human papillomavirus DNA sequences. Int J Cancer 109:253–258

    PubMed  Article  Google Scholar 

  43. D’Souza G, Kreimer AR, Viscidi R, Pawlita M, Fakhry C, Koch WM, Westra WH, Gillison ML (2007) Case–control study of human papillomavirus and oropharyngeal cancer. N Engl J Med 356:1944–1956

    PubMed  Article  Google Scholar 

  44. Rintala MA, Grénman SE, Puranen MH, Isolauri E, Ekblad U, Kero PO, Syrjänen SM (2005) Transmission of high-risk human papillomavirus (HPV) between parents and infant: a prospective study of HPV in families in Finland. J Clin Microbiol 43:376–381

    PubMed  Article  Google Scholar 

Download references

Acknowledgments

This work was supported by a grant from Tehran University of Medical Sciences, Government of Iran. Also, we would like to thank Dr. Joghataei, Dr. Irajian, Mis. Bakhshayesh, Mis Solgi for operation of project. Also, we would thanks’ to personals of Shahid Beheshti Hospital and Amol Central Laboratory.

Author information

Affiliations

  1. Infectious Diseases & Tropical Medicine Research Center, Babol University of Medical Sciences, Babol, Iran

    Y. Yahyapour, S. Siadati, S. Shefaii & J. Shokri Shirvani

  2. Department of Virology, Faculty of Medicine, Tehran University of Medical Sciences, Tehran, Iran

    M. Shamsi-Shahrabadi, H. R. Mollaie & Hossein Keyvani

  3. Department of Epidemiology and Biostatistics, School of Health, Tehran University of Medical Sciences, Tehran, Iran

    M. Mahmoudi & A. Motevallian

  4. Department of Virology and Antimicrobial Resistance Research Center, Faculty of Medicine, Tehran University of Medical Sciences, Tehran, Iran

    Seyed Hamid Reza Monavari

Authors
  1. Y. Yahyapour
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Shamsi-Shahrabadi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Mahmoudi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. Motevallian
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. S. Siadati
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. S. Shefaii
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. J. Shokri Shirvani
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. H. R. Mollaie
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Seyed Hamid Reza Monavari
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Hossein Keyvani
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Seyed Hamid Reza Monavari.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Yahyapour, Y., Shamsi-Shahrabadi, M., Mahmoudi, M. et al. High-Risk and Low-Risk Human Papillomavirus in Esophageal Squamous Cell Carcinoma at Mazandaran, Northern Iran. Pathol. Oncol. Res. 19, 385–391 (2013). https://doi.org/10.1007/s12253-012-9590-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12253-012-9590-0

Keywords

  • High-risk and Low-risk HPV
  • Genotyping
  • ESCC
  • Mazandaran
  • North of Iran