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Is There Any Role of Arsenic Toxicity in HPV Related Oral Squamous Cell Carcinoma?

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Abstract

Arsenic is a potent human carcinogen affecting the rate of cancer deaths worldwide. In India, West Bengal is the worst affected state by arsenic. To our best knowledge, this is the first study relating arsenic toxicity with oral carcinoma, along with HPV infection, the latter being well established in western countries. To find out a possible correlation between arsenic toxicity and oral carcinoma in the population of West Bengal, in or without any association with human papilloma virus infection. Ethical clearance of this study was obtained from the institutional committee. One hundred and four malignant and 103 premalignant cases were selected for this study along with 200 healthy age and sex-matched individuals selected as control (100 each for malignant and premalignant) (2013–2017). On proper consent, their buccal swab and hair samples were assessed for the presence of HPV DNA by DNA extraction, followed by PCR and arsenic estimation by flow injection hydride generation atomic absorption spectrometry respectively. A very highly significant correlation has been observed between arsenic toxicity, HPV infection and the occurrence of oral carcinoma (p value = 2.18e−06; p value = 0.00100 respectively). A correlation has also been observed between these two factors simultaneously, contributing to this malignancy (phi coefficient = 0.2194839). A statistically significant correlation observed between this metal toxicity and viral infection in the occurrence of oral carcinoma in this population indicates a possible symbiotic role between these two factors in this malignancy.

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References

  1. Mondal D, Banerjee M, Kundu M, Banerjee N, Bhattacharya U, Giri AK, Ganguli B, Sen Roy S, Polya DA (2010) Comparison of drinking water, raw rice and cooking of rice as arsenic exposure routes in three contrasting areas of West Bengal, India. Environ Geochem Health 32:463–477

    Article  CAS  PubMed  Google Scholar 

  2. Ratnaike RN (2003) Acute and chronic arsenic toxicity. Postgrad Med J 79:391–396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Banerjee N, Giri A (2014) Arsenic induced health effects, genetic damage and genetic variants in the population exposed to arsenic through drinking water in West Bengal. Proc Indian Natl Sci Acad 80(3):565–581. https://doi.org/10.16943/ptinsa/2014/v80i3/55130

    Article  Google Scholar 

  4. Arain SS, Kazi TG, Afridi HI, Talpur FN, Kazi AG, Brahman KD et al (2015) Correlation of arsenic levels in smokeless tobacco products and biological samples of oral cancer patients and control consumers. Biol Trace Elem Res 168(2):287–295. https://doi.org/10.1007/s12011-015-0355-y

    Article  CAS  PubMed  Google Scholar 

  5. Su CC, Lin YY, Chang TK, Chiang CT, Chung JA, Hsu YY, Lian IB (2010) Incidence of oral cancer in relation to nickel and arsenic concentrations in farm soils of patients’ residential areas in Taiwan. BMC Public Health 10:67. https://doi.org/10.1186/1471-2458-10-67

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Pal P, Raychowdhury R, Dolai TK, Roy S, Dastidar R, Halder A (2017) Study of arsenic exposure in oral/oropharyngeal carcinoma in West Bengal. Int J Occup Med Environ Health 30(2):271–279. https://doi.org/10.13075/ijomeh.1896.00806.

    Article  PubMed  Google Scholar 

  7. Rakesh S, Janardhanan M, Vinodkumar RB et al (2010) Association of human papilloma virus with oral squamous cell carcinoma—a brief review. Oral Maxillofac Pathol J 1(2):1–9

  8. Koo K, Barrowman R, McCullough M, Iseli T, Wiesenfeld D (2013) Nonsmoking non drinking elderly females: a clinically distinct subgroup of oral squamous cell carcinoma patients. Int J Oral Maxillofac Surg 42:92933

    Article  Google Scholar 

  9. Marur S, D’Souza G, Westra WH et al (2010) HPV associated head and neck cancer: a virus-related cancer epidemic. Lancet Oncol 11:781–789

    Article  PubMed  PubMed Central  Google Scholar 

  10. Ramqvist T, Dalianis T (2010) Oropharyngeal cancer epidemic and human papilloma virus. Emerg Infect Dis 16:1671–1677

    Article  PubMed  PubMed Central  Google Scholar 

  11. Chaturvedi AK (2012) Epidemiology and clinical aspects of HPV in head and neck cancers. Head Neck Pathol 6(suppl 1):S16–S24

    Article  PubMed  Google Scholar 

  12. Gillison ML, Alemany L, Snijders PJ et al (2012) Human papilloma virus and diseases of the upper airway: head and neck cancer and respiratory papillomatosis. Vaccine 30(suppl 5):F34–F54

    Article  PubMed  Google Scholar 

  13. Hong AM, Grulich AE, Jones D, Lee CS, Garland SM, Dobbins TA, Clark JR, Harnett GB, Milross CG, O’Brien CJ, Rose BR (2010) Squamous cell carcinoma of the oropharynx in Australian males induced by human papilloma virus vaccine targets. Vaccine 28:3269–3272

    Article  CAS  PubMed  Google Scholar 

  14. Auluck A, Hislop G, Bajdik C, Poh C, Zhang L, Rosin M (2010) Trends in oropharyngeal and oral cavity cancer incidence of human papilloma virus (HPV)-related and HPV unrelated sites in a multicultural population: the British Columbia experience. Cancer 116:2635–2644

    PubMed  Google Scholar 

  15. Blomberg M, Nielsen A, Munk C et al (2010) Trends in head and neck cancer incidence in Denmark, 1978-2007: focus on human papilloma virus associated sites. Int J Cancer 129:733–741

    Article  CAS  PubMed  Google Scholar 

  16. Braakhuis BJ, Visser O, Leemans CR (2009) Oral and oropharyngeal cancer in the Netherlands between 1989 and 2006: increasing incidence, but not in young adults. Oral Oncol 45:e85–e89

    Article  PubMed  Google Scholar 

  17. Mork J, Møller B, Dahl T, Bray F (2010) Time trends in pharyngeal cancer incidence in Norway 1981-2005: a subsite analysis based on a reabstraction and recoding of registered cases. Cancer Causes Control 21:1397–1405

    Article  PubMed  Google Scholar 

  18. Hammarstedt L, Lindquist D, Dahlstrand H, Romanitan M, (Dahlgren) LO, Joneberg J, Creson N, Lindholm J, Ye W, Dalianis T, Munck-Wikland E (2006) Human papilloma virus as a risk factor for the increase in incidence of tonsillar cancer. Int J Cancer 119:2620–2623

    Article  CAS  PubMed  Google Scholar 

  19. Chaturvedi AK, Engels EA, Anderson WF et al (2008) Incidence trends for human papilloma virus related and -unrelated oral squamous cell carcinomas in the United States. J Clin Oncol 26:612–619

    Article  PubMed  Google Scholar 

  20. Reddy VM, Cundall-Curry D, Bridger MW (2010) Trends in the incidence rates of tonsil and base of tongue cancer in England, 1985-2006. Ann R Coll Surg Engl l92:655–659

    Article  Google Scholar 

  21. Laprise C, Madathil SA, Allison P, Abraham P, Raghavendran A, Shahul HP, ThekkePurakkal AS, Castonguay G, Coutlée F, Schlecht NF, Rousseau MC, Franco EL, Nicolau B (2016) No role for human papilloma virus infection in oral cancers in a region in southern India. Int J Cancer 138(4):912–917. https://doi.org/10.1002/ijc.29827

    Article  CAS  PubMed  Google Scholar 

  22. Elango KJ, Suresh A, Erode EM, Subhadradevi L, Ravindran HK, Iyer SK, Iyer SK, Kuriakose MA (2011) Role of human papilloma virus in oral tongue squamous cell carcinoma. Asian Pac J Cancer Prev 12(4):889–896

    PubMed  Google Scholar 

  23. Kulkarni SS, Kulkarni SS, Vastrad PP et al (2011) Prevalence and distribution of high risk human papilloma virus (HPV) types 16 and 18 in carcinoma of cervix, saliva of patients with oral squamous cell carcinoma and in the general population in Karnataka, India. Asian Pac J Cancer Prev 12(3):645–648

    PubMed  Google Scholar 

  24. Mitra S, Banerjee S, Misra C, Singh RK, Roy A, Sengupta A, Panda CK, Roychoudhury S (2007) Interplay between human papilloma virus infection and p53 gene alterations in head and neck squamous cell carcinoma of an Indian patient population. J Clin Pathol 60(9):1040–1047

    Article  CAS  PubMed  Google Scholar 

  25. Kadashetti V, Chaudhary M, Patil S, Gawande M, Shivakumar KM, Patil S, Pramod RC (2015) Analysis of various risk factors affecting potentially malignant disorders and oral cancer patients of Central India. J Cancer Res Ther 11(2):280–286. https://doi.org/10.4103/0973-1482.151417

    Article  CAS  PubMed  Google Scholar 

  26. Coelho KR (2012) Challenges of the oral cancer burden in India. J Cancer Epidemiol 2012:Article ID 701932, 17 pages. https://doi.org/10.1155/2012/701932

  27. Fazeli Z, Pourhoseingholi MA, Pourhoseingholi A, Vahedi M, Zali MR (2011) Mortality of oral cavity cancer in Iran. Asian Pac J Cancer Prev 12:2763–2766

    PubMed  Google Scholar 

  28. Atkinson L, Chester IC, Smyth FG, Ten S (1964) Oral cancer in New Guinea. A study in demography and etiology. Cancer 17:1289–1298

    Article  CAS  PubMed  Google Scholar 

  29. Gupta S, Singh R, Gupta OP, Tripathi A (2014) Prevalence of oral cancer and pre-cancerous lesions and the association with numerous risk factors in North India: a hospital based study. Natl J Maxillofac Surg 5(2):142–148. https://doi.org/10.4103/0975-5950.154816

    Article  PubMed  PubMed Central  Google Scholar 

  30. Bhattacharjee B (2016) Global experts meet to boost cancer screening. Times of India

  31. Chakraborti D, Das B, Rahman MM, Chowdhury UK, Biswas B, Goswami AB, Nayak B, Pal A, Sengupta MK, Ahamed S, Hossain A, Basu G, Roychowdhury T, Das D (2009) Status of groundwater arsenic contamination in the state of West Bengal, India: a 20-year study report. Mol Nutr Food Res 53:542–551. https://doi.org/10.1002/mnfr.200700517

    Article  CAS  PubMed  Google Scholar 

  32. Arnold HL, Odam RB, James WD (1990) Disease of the skin. In: Saunders WB (ed) Clinical dermatology, Philadelphia, pp 121–122

  33. Singh AP, Goel RK, Kaur T (2011) Mechanisms pertaining to arsenic toxicity. Toxicol Int 18(2):87–93. https://doi.org/10.4103/0971-6580.84258

    Article  PubMed  PubMed Central  Google Scholar 

  34. Matschullat J (2000) Arsenic in the geosphere—a review. Sci Total Environ 249:297–312

    Article  CAS  PubMed  Google Scholar 

  35. Steinmaus C, Carrigan K, KalmanD AR, Yuan Y, Smith AH (2005) Dietary intake and arsenic methylation in a U.S. population. Environ Health Perspect 113:1153–1159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Washington DC (2001) Arsenic in drinking water. National Academy Press; National Research Council

  37. Kinniburgh DG, Smedley PL (2001) Arsenic contamination of ground water in Bangladesh: volume 2: final report. Keyworth, Nottinghamshire: British Geological Survey

  38. Chowdhury UK, Biswas BK, Chowdhury TR, Samanta G, Mandal BK, Basu GC, Chanda CR, Lodh D, Saha KC, Mukherjee SK, Roy S, Kabir S, Quamruzzaman Q, Chakraborti D (2000) Groundwater arsenic contamination in Bangladesh and West Bengal, India. Environ Health Perspect 108:393–397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Guha Mazumder DN, Haque R, Ghosh N, de BK, Santra A, Chakraborty D, Smith AH (1998) Arsenic levels in drinking water and the prevalence of skin lesions in West Bengal, India. Int J Epidemiol 27:871–877

    Article  CAS  PubMed  Google Scholar 

  40. Mukherjee AB, Bhattacharya P (2001) Arsenic in ground water in the Bengal Delta Plain: slow poisoning in Bangladesh. Environ Rev 9:189–220

    Article  CAS  Google Scholar 

  41. Buchet JP, Lison D, Ruggeri M et al (1996) Assessment of exposure to inorganic arsenic, a human carcinogen, due to the consumption of seafood. Arch Toxicol 70:773–778

    Article  CAS  PubMed  Google Scholar 

  42. Yuan TH, Lian IB, Tsai KY, Chang TK, Chiang CT, Su CC, Hwang YH (2011) Possible association between nickel and chromium and oral cancer: a case–control study in central Taiwan. Sci Total Environ 409:1046–1052. https://doi.org/10.1016/j.scitotenv.2010.11.038

    Article  CAS  PubMed  Google Scholar 

  43. zurHausen H, Meinhof W, Scheiber W, Bornkamm GW (1974) Attempts to detect virus specific DNA in human tumors. I. Nucleic acid hybridizations with complementary RNA of human wart virus. Int J Cancer 13:6506

    Google Scholar 

  44. zurHausen H (1976) Condylomata acuminata and human genital cancer. Cancer Res 36(2 pt 2):794

    CAS  Google Scholar 

  45. zurHausen H (1977) Human papilloma viruses and their possible role in squamous cell carcinomas. Curr Top Microbiol Immunol 78:130

    Google Scholar 

  46. Smith EM, Rubenstein LM, Haugen TH, Hamsikova E, Turek LP (2010) Tobacco and alcohol use increases the risk of both HPV associated and HPV independent head and neck cancers. Cancer Causes Control 21:1369–1378

    Article  PubMed  Google Scholar 

  47. Campisi G, Panzarella V, Giuliani M, Lajolo C, Di Fede O, Falaschini S et al (2007) Human papilloma virus: its identity and controversial role in oral oncogenesis, premalignant and malignant lesions (review). Int J Oncol 30:813–823

    CAS  PubMed  Google Scholar 

  48. Lima LA, Silva CG, Rabenhorst SH (2014) Association between human papilloma virus and oral squamous cell carcinoma: a systematic review. J Bras Patol Med Lab 50:75–84

    Article  Google Scholar 

  49. Friedman JM, Stavas MJ, Cmelak AJ (2014) Clinical and scientific impact of human papilloma virus on head and neck cancer. World J Clin Oncol 5:781–791

    Article  PubMed  PubMed Central  Google Scholar 

  50. Benson E, Li R, Eisele D, Fakhry C (2014) The clinical impact of HPV tumor status upon head and neck squamous cell carcinomas. Oral Oncol 50:565–574

    Article  PubMed  Google Scholar 

  51. Blot WJ, McLaughlin JK, Winn DM, Austin DF, Greenberg RS, Preston Martin S et al (1988) Smoking and drinking in relation to oral and pharyngeal cancer. Cancer Res 48:3282–3287

    CAS  PubMed  Google Scholar 

  52. Chaturvedi AK, Anderson WF, Lortet-Tieulent J, Curado MP, Ferlay J, Franceschi S, Rosenberg PS, Bray F, Gillison ML (2013) Worldwide trends in incidence rates for oral cavity and oropharyngeal cancers. J Clin Oncol 31(36):4550–4559. https://doi.org/10.1200/JCO.2013.50.3870

    Article  PubMed  PubMed Central  Google Scholar 

  53. Singh V, Husain N, Akhtar N, Kumar V, Tewari S, Mishra S, Misra S, Khan MY (2015) Do human papilloma viruses play any role in oral squamous cell carcinoma in North Indians? Asian Pac J Cancer Prev 16(16):7077–7084

    Article  PubMed  Google Scholar 

  54. Bijina BR, Ahmed J, Shenoy N, Ongole R, Shenoy S, Baliga S (2016) Detection of human papilloma virus in potentially malignant and malignant lesions of the oral cavity and a study of associated risk factors. South Asian J Cancer 5(4):179–181. https://doi.org/10.4103/2278-330X.195337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Gupta S, Gupta S (2015) Role of human papilloma virus in oral squamous cell carcinoma and oral potentially malignant disorders: a review of the literature. Indian J Dent 6(2):91–98. https://doi.org/10.4103/0975-962X.155877

    Article  PubMed  PubMed Central  Google Scholar 

  56. Balaram P, Nalinakumari KR, Abraham E et al (1995) Human papilloma virus in 91 oral cancers from Indian betel quid chewers—high prevalence and multiplicity of infections. Int J Cancer 61:450–454

    Article  CAS  PubMed  Google Scholar 

  57. Schwartz SM, Daling JR, Doody DR et al (1998) Oral cancer risk in relation to sexual history and evidence of human papilloma virus infection. J Natl Cancer Inst 90:1626–1636

    Article  CAS  PubMed  Google Scholar 

  58. Smith EM, Ritchie JM, Summersgill KF, Hoffman HT, Wang DH, Haugen TH, Turek LP (2004) Human papilloma virus in oral exfoliated cells and risk of head and neck cancer. J Natl Cancer Inst 96:449–455

    Article  PubMed  Google Scholar 

  59. Azhar N, Sohail M, Ahmad F, Fareeha S, Jamil S, Mughal N, Salam H (2018) Risk factors of oral cancer—a hospital based case control study. J Clin Exp Dent 10(4):e396–e401. https://doi.org/10.4317/jced.54618

    Article  PubMed  PubMed Central  Google Scholar 

  60. Jacob L, Freyn M, Kalder M, Dinas K, Kostev K (2018) Impact of tobacco smoking on the risk of developing 25 different cancers in the UK: a retrospective study of 422,010 patients followed for up to 30 years. Oncotarget 9(25):17420–17429. https://doi.org/10.18632/oncotarget.24724

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We are grateful to Swami Nityakamananda, Secretary of Ramakrishna Mission Seva Pratishthan, for kindly allowing us to conduct the study in this institution.

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We are indebted to DST Inspire Fellowship, New Delhi for giving the financial assistance required for this study.

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Correspondence to Ajanta Halder.

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All procedures performed in this study involving human participants were in accordance with the ethical standards of the institutional committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

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Informed consent was obtained from all individual participants included in the study.

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Pal, P., Halder, A. Is There Any Role of Arsenic Toxicity in HPV Related Oral Squamous Cell Carcinoma?. Biol Trace Elem Res 188, 274–283 (2019). https://doi.org/10.1007/s12011-018-1419-6

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