Role of bacteria in oral carcinogenesis

R Rajeev; Kanaram Choudhary; Swagatika Panda; Neha Gandhi

doi:10.4103/2278-330X.103719

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Review Article

01 (

); 78-83

doi:

10.4103/2278-330X.103719

Role of bacteria in oral carcinogenesis

R Rajeev¹, Kanaram Choudhary^1,, Swagatika Panda², Neha Gandhi³

1 Department of Oral Pathology and Microbiology, Government Dental College, Trivandrum, Kerala

2 Institute of Dental Sciences – Bhubaneshwar, Odisha

3 Oral Pathology and Microbiology, Government Dental College, Ahmedabad, Gujarat, India

*Corresponding author: Dr. Kanaram Choudhary. drk84choyal@gmail.com

Published: 2020-12-30

MedIntel Services Pvt Ltd. This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial-License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commercial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/licenses/by-nc-nd/4.0/.)

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Abstract

Oral cancer is the most common cancer diagnosed in Indian men and is the leading cause of cancer deaths. It is considered as a multistep and multifactorial disease. Besides accumulation of genetic mutations, numerous other carcinogens are involved. In this category, viral and chemical carcinogens are well studied and documented. However, in the oral cavity, the role of microbiota in carcinogenesis is not known. Microbial populations on mouth mucosa differ between healthy and malignant sites, and certain oral bacterial species have been linked with malignancies, but the evidence is still weak in this respect. Nevertheless, oral microorganisms inevitably up-regulate cytokines and other inflammatory mediators that affect the complex metabolic pathways, and may thus be involved in carcinogenesis. Poor oral health associates statistically with prevalence of many types of cancer such as pancreatic and gastrointestinal cancer. This review presents possible carcinogenesis pathway involved in bacterial carcinogenesis, commonly implicated bacteria in oral carcinogenesis, and their role in cancer therapeutics as well.

Keywords

References

Chocolatewala N, Chaturvedi P, Desale R. The role of bacteria in oral cancer. Indian J Med Paediatr Oncol 2010;31:126-31.
Chocolatewala NM, Chaturvedi P. Role of human papilloma virus in the oral carcinogenesis: An Indian perspective. J Cancer Res Ther 2009;5:71-7.
Vinay K, Nelso F, Abul A, Philadelphia. Pathological basis of disease. 7th ed. W.B Sunders Company; 2010. p. 269-342.
Vaishnavi C, Kochhar R, Singh G, Kumar S, Singh S, Singh K. Epidemiology of typhoid carriers among blood donors and patients with biliary, gastrointestinal and other related diseases. Microbiol Immunol 2005;49:107-12.
Lax AJ, Thomas W. How bacteria could cause cancer: One step at a time. Trends Microbiol 2002;10:293-9.
Dutta U, Garg PK, Kumar R, Tandon RK. Typhoid carriers among patients with gallstones are at increased risk for carcinoma of the gallbladder. Am J Gastroenterol 2000;95:784-7.
Shukla VK, Singh H, Pandey M, Upadhyay SK, Nath G. Carcinoma of the gallbladder - is it a sequel of typhoid? Dig Dis Sci 2000;45:900-3.
Littman AJ, White E, Jackson LA, Thornquist MD, Gaydos CA, Goodman GE, et al. Chlamydia pneumoniae infection and risk of lung cancer. Cancer Epidemiol Biomarkers Prev 2004;13:1624-30.
Koyi H, Branden E, Gnarpe J, Gnarpe H, Steen B. An association between chronic infection with Chlamydia pneumoniae and lung cancer. A prospective 2-year study. APMIS 2001;109:572-80.
Anttila T, Koskela P, Leinonen M, Laukkanen P, Hakulinen T, Lehtinen M, et al. Chlamydia pneumoniae infection and the risk of female early-onset lung cancer. Int J Cancer 2003;107:681-2.
Biarc J, Nguyen IS, Pini A, Gosse F, Richert S, Thierse D, et al. Carcinogenic properties of proteins with pro-inflammatory activity from Streptococcus infantarius (formerly S. bovis). Carcinogenesis 2004;25:1477-84.
Gold JS, Bayar S, Salem RR. Association of Streptococcus bovis bacteremia with colonic neoplasia and extracolonic malignancy. Neoplasia and extracolonic malignancy. Arch Surg 2004;139:760-5.
Ellmerich S, Scholler M, Duranton B, Gosse F, Galluser M, Klein JP, et al. Promotion of intestinal carcinogenesis by Streptococcus bovis. Carcinogenesis 2000;21:753-6.
Zarkin BA, Lillemoe KD, Cameron JL, Effron PN, Magnuson TH, Pitt HA. The triad of Streptococcus bovis bacteremia, colonic pathology, and liver disease. Ann Surg 1990;211:786-91.
Kocazeybek B. Chronic Chlamydophila pneumoniae infection in lung cancer, a risk factor: A case-control study. J Med Microbiol 2003;52:721-6.
Coussens LM, Werb Z. Inflammation and cancer. Nature 2002;420:860-7.
Parsonnet J. Bacterial infection as a cause of cancer. Environ Health Perspect 1995;103:263-8.
Nougayrede JP, Taieb F, De Rycke J, Oswald E. Cyclomodulins: Bacterial effectors that modulate the eukaryotic cell cycle. Trends Microbiol 2005;13:103-10.
Lara-Tejero M, Galán JE. A bacterial toxin that controls cell cycle progression as a deoxyribonuclease I-like protein. Science 2000;290:354-7.
Lax AJ. Bacterial toxins and cancer-case to answer? Nat Rev Microbiol 2005;3:343-9.
Pöschl G, Seitz HK. Alcohol and cancer. Alcohol Alcohol 2004;39:155-65.
Salaspuro MP. Acetaldehyde, microbes, and cancer of the digestive tract. Crit Rev Clin Lab Sci 2003;40:183-208.
Meurman JH. Oral microbiota and cancer. J Oral Microbiol 2010;2:5195.
Calmels S, Ohshima H, Vincent P, Gounot AM, Bartsch H. Screening of microorganisms for nitrosation catalysis at pH 7 and kinetic studies on nitrosamine formation from-secondary amines by E.coli strains. Carcinogenesis 1985;6:911-5.
Lijinsky W, Saavedra JE, Reuber MD, Singer SS. Esophageal carcinogenesis in F344 rats by nitrosomethylethylamines substituted in the ethyl group. J Natl Cancer Inst 1982;68:681-4.
Miyazaki Y, Kikuchi K, González-Alva P, Inoue H, Noguchi Y, Hozumi T, et al. Association of butyric acid produced by periodontopathic bacteria with progression of oral cancer. J Cancer Sci Ther 2010;2:26-32.
Tateda M, Shiga K, Saijo S, Sone M, Hori T, Yokoyama J, et al. Streptococcus anginosus in head and neck squamous cell carcinoma: Implication in carcinogenesis. Int J Mol Med 2000;6:699-703.
Anand D, Vineeta S, Mridula S, Royana S, Manoj P. Helicobacter pylori and oral cancer: possible association in a preliminary case control study. Asian Pac J Cancer Prev 2011;12:1333-6.
Fernando N, Jayakumar G, Perera N, Amarasingha I, Meedin F, Holton J. Presence of Helicobacter pylori in betel chewers and non betel chewers with and without oral cancers. BMC Oral Health 2009;9:23.
Rajendran R, Rajeev R, Anil S, Alasqah M, Rabi AG. Helicobacter pylori coinfection is a confounder, modulating mucosal inflammation in oral submucous fibrosis. Indian J Dent Res 2009;20:206-11.
Rajendra R, Sivapathasundharam B. Shafer′s text book of oral pathology. 5 th ed. Elsevier, a Division of Reed Elsevier Private Limited; Gurgaon, India 2007. p. 37.
Mager DL, Haffajee AD, Devlin PM, Norris CM, Posner MR, Goodson JM. The salivary microbiota as a diagnostic indicator of oral cancer: A descriptive, non-randomized study of cancer-free and oral squamous cell carcinoma subjects. J Transl Med 2005;3:27.
Hooper SJ, Crean SJ, Lewis MA, Spratt DA, Wade WG, Wilson MJ. Viable bacteria present within oral squamous cell carcinoma tissue. J Clin Microbiol 2006;44:1719-25.
Hooper SJ, Crean SJ, Lewis MA, Spratt DA, Wade WG, Wilson MJ. A molecular analysis of the bacteria present within oral squamous cell carcinoma. J Med Microbiol 2007;56:1651-9.
Sasaki M, Yamaura C, Ohara-Nemoto Y, Tajika S, Kodama Y, Ohya T, et al. Streptococcus anginosus infection in oral cancer and its infection route. Oral Diseases 2005;11:151-6.
Yoshihiro A, Masto S, Michiko N, Mami Y, Daisuke S, Tohru K. Role of b-defensins in oral epithelial health and disease. Med Mol Morphol 2007;40:179-84.
Jeong-Hae C, Moo-Hyung L, Yun-Jung C, Bong-Soo P, Shin K, Gyoo-Cheon K. The bacterial protein azurin enhances sensitivity of oral squamous carcinoma cells to anticancer drugs. Yonsei Med J 2011;52:773-8.
Yamada T, Fialho AM, Punj V, Bratescu L, Gupta TK, Chakrabarty AM. Internalization of bacterial redox protein azurin in mammalian cells: Entry domain and specificity. Cell Microbiol 2005;7:1418-31.
Yamada T, Goto M, Punj V, Zaborina O, Chen ML, Kimbara K, et al. Bacterial redox protein azurin, tumor suppressor protein p53, and regression of cancer. Proc Natl Acad Sci U S A 2002;99:14098-103.
Punj V, Bhattacharyya S, Saint-Dic D, Vasu C, Cunningham EA, Graves J, et al. Bacterial cupredoxin azurin as an inducer of apoptosis and regression in human breast cancer. Oncogene 2004;23:2367-78.
Yamada T, Goto M, Punj V, Zaborina O, Kimbara K, Das Gupta TK, et al. The bacterial redox protein azurin induces apoptosis in J774 macrophages through complex formation and stabilization of the tumor suppressor protein p53. Infect Immun 2002;70:7054-62.
Thomas W, Alyson MB, Lisa LS, Susan GR, Walle UK. Flavonoid glucosides; are hydrolyzed and thus activated in the oral cavity in humans. Hum Nutr Metabol 2005;49-52.
Farrell JJ, Zhang L, Zhou H, Chia D, Elashoff D, Akin D, et al. Variations of oral microbiota are associated with pancreatic diseases including pancreatic cancer. Gut 2012;61:582-8.

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[1] Chocolatewala N, Chaturvedi P, Desale R. The role of bacteria in oral cancer. Indian J Med Paediatr Oncol 2010;31:126-31.

[2] Chocolatewala NM, Chaturvedi P. Role of human papilloma virus in the oral carcinogenesis: An Indian perspective. J Cancer Res Ther 2009;5:71-7.

[3] Vinay K, Nelso F, Abul A, Philadelphia. Pathological basis of disease. 7th ed. W.B Sunders Company; 2010. p. 269-342.

[4] Vaishnavi C, Kochhar R, Singh G, Kumar S, Singh S, Singh K. Epidemiology of typhoid carriers among blood donors and patients with biliary, gastrointestinal and other related diseases. Microbiol Immunol 2005;49:107-12.

[5] Lax AJ, Thomas W. How bacteria could cause cancer: One step at a time. Trends Microbiol 2002;10:293-9.

[6] Dutta U, Garg PK, Kumar R, Tandon RK. Typhoid carriers among patients with gallstones are at increased risk for carcinoma of the gallbladder. Am J Gastroenterol 2000;95:784-7.

[7] Shukla VK, Singh H, Pandey M, Upadhyay SK, Nath G. Carcinoma of the gallbladder - is it a sequel of typhoid? Dig Dis Sci 2000;45:900-3.

[8] Littman AJ, White E, Jackson LA, Thornquist MD, Gaydos CA, Goodman GE, et al. Chlamydia pneumoniae infection and risk of lung cancer. Cancer Epidemiol Biomarkers Prev 2004;13:1624-30.

[9] Koyi H, Branden E, Gnarpe J, Gnarpe H, Steen B. An association between chronic infection with Chlamydia pneumoniae and lung cancer. A prospective 2-year study. APMIS 2001;109:572-80.

[10] Anttila T, Koskela P, Leinonen M, Laukkanen P, Hakulinen T, Lehtinen M, et al. Chlamydia pneumoniae infection and the risk of female early-onset lung cancer. Int J Cancer 2003;107:681-2.

[11] Biarc J, Nguyen IS, Pini A, Gosse F, Richert S, Thierse D, et al. Carcinogenic properties of proteins with pro-inflammatory activity from Streptococcus infantarius (formerly S. bovis). Carcinogenesis 2004;25:1477-84.

[12] Gold JS, Bayar S, Salem RR. Association of Streptococcus bovis bacteremia with colonic neoplasia and extracolonic malignancy. Neoplasia and extracolonic malignancy. Arch Surg 2004;139:760-5.

[13] Ellmerich S, Scholler M, Duranton B, Gosse F, Galluser M, Klein JP, et al. Promotion of intestinal carcinogenesis by Streptococcus bovis. Carcinogenesis 2000;21:753-6.

[14] Zarkin BA, Lillemoe KD, Cameron JL, Effron PN, Magnuson TH, Pitt HA. The triad of Streptococcus bovis bacteremia, colonic pathology, and liver disease. Ann Surg 1990;211:786-91.

[15] Kocazeybek B. Chronic Chlamydophila pneumoniae infection in lung cancer, a risk factor: A case-control study. J Med Microbiol 2003;52:721-6.

[16] Coussens LM, Werb Z. Inflammation and cancer. Nature 2002;420:860-7.

[17] Parsonnet J. Bacterial infection as a cause of cancer. Environ Health Perspect 1995;103:263-8.

[18] Nougayrede JP, Taieb F, De Rycke J, Oswald E. Cyclomodulins: Bacterial effectors that modulate the eukaryotic cell cycle. Trends Microbiol 2005;13:103-10.

[19] Lara-Tejero M, Galán JE. A bacterial toxin that controls cell cycle progression as a deoxyribonuclease I-like protein. Science 2000;290:354-7.

[20] Lax AJ. Bacterial toxins and cancer-case to answer? Nat Rev Microbiol 2005;3:343-9.

[21] Pöschl G, Seitz HK. Alcohol and cancer. Alcohol Alcohol 2004;39:155-65.

[22] Salaspuro MP. Acetaldehyde, microbes, and cancer of the digestive tract. Crit Rev Clin Lab Sci 2003;40:183-208.

[23] Meurman JH. Oral microbiota and cancer. J Oral Microbiol 2010;2:5195.

[24] Calmels S, Ohshima H, Vincent P, Gounot AM, Bartsch H. Screening of microorganisms for nitrosation catalysis at pH 7 and kinetic studies on nitrosamine formation from-secondary amines by E.coli strains. Carcinogenesis 1985;6:911-5.

[25] Lijinsky W, Saavedra JE, Reuber MD, Singer SS. Esophageal carcinogenesis in F344 rats by nitrosomethylethylamines substituted in the ethyl group. J Natl Cancer Inst 1982;68:681-4.

[26] Miyazaki Y, Kikuchi K, González-Alva P, Inoue H, Noguchi Y, Hozumi T, et al. Association of butyric acid produced by periodontopathic bacteria with progression of oral cancer. J Cancer Sci Ther 2010;2:26-32.

[27] Tateda M, Shiga K, Saijo S, Sone M, Hori T, Yokoyama J, et al. Streptococcus anginosus in head and neck squamous cell carcinoma: Implication in carcinogenesis. Int J Mol Med 2000;6:699-703.

[28] Anand D, Vineeta S, Mridula S, Royana S, Manoj P. Helicobacter pylori and oral cancer: possible association in a preliminary case control study. Asian Pac J Cancer Prev 2011;12:1333-6.

[29] Fernando N, Jayakumar G, Perera N, Amarasingha I, Meedin F, Holton J. Presence of Helicobacter pylori in betel chewers and non betel chewers with and without oral cancers. BMC Oral Health 2009;9:23.

[30] Rajendran R, Rajeev R, Anil S, Alasqah M, Rabi AG. Helicobacter pylori coinfection is a confounder, modulating mucosal inflammation in oral submucous fibrosis. Indian J Dent Res 2009;20:206-11.

[31] Rajendra R, Sivapathasundharam B. Shafer′s text book of oral pathology. 5 th ed. Elsevier, a Division of Reed Elsevier Private Limited; Gurgaon, India 2007. p. 37.

[32] Mager DL, Haffajee AD, Devlin PM, Norris CM, Posner MR, Goodson JM. The salivary microbiota as a diagnostic indicator of oral cancer: A descriptive, non-randomized study of cancer-free and oral squamous cell carcinoma subjects. J Transl Med 2005;3:27.

[33] Hooper SJ, Crean SJ, Lewis MA, Spratt DA, Wade WG, Wilson MJ. Viable bacteria present within oral squamous cell carcinoma tissue. J Clin Microbiol 2006;44:1719-25.

[34] Hooper SJ, Crean SJ, Lewis MA, Spratt DA, Wade WG, Wilson MJ. A molecular analysis of the bacteria present within oral squamous cell carcinoma. J Med Microbiol 2007;56:1651-9.

[35] Sasaki M, Yamaura C, Ohara-Nemoto Y, Tajika S, Kodama Y, Ohya T, et al. Streptococcus anginosus infection in oral cancer and its infection route. Oral Diseases 2005;11:151-6.

[36] Yoshihiro A, Masto S, Michiko N, Mami Y, Daisuke S, Tohru K. Role of b-defensins in oral epithelial health and disease. Med Mol Morphol 2007;40:179-84.

[37] Jeong-Hae C, Moo-Hyung L, Yun-Jung C, Bong-Soo P, Shin K, Gyoo-Cheon K. The bacterial protein azurin enhances sensitivity of oral squamous carcinoma cells to anticancer drugs. Yonsei Med J 2011;52:773-8.

[38] Yamada T, Fialho AM, Punj V, Bratescu L, Gupta TK, Chakrabarty AM. Internalization of bacterial redox protein azurin in mammalian cells: Entry domain and specificity. Cell Microbiol 2005;7:1418-31.

[39] Yamada T, Goto M, Punj V, Zaborina O, Chen ML, Kimbara K, et al. Bacterial redox protein azurin, tumor suppressor protein p53, and regression of cancer. Proc Natl Acad Sci U S A 2002;99:14098-103.

[40] Punj V, Bhattacharyya S, Saint-Dic D, Vasu C, Cunningham EA, Graves J, et al. Bacterial cupredoxin azurin as an inducer of apoptosis and regression in human breast cancer. Oncogene 2004;23:2367-78.

[41] Yamada T, Goto M, Punj V, Zaborina O, Kimbara K, Das Gupta TK, et al. The bacterial redox protein azurin induces apoptosis in J774 macrophages through complex formation and stabilization of the tumor suppressor protein p53. Infect Immun 2002;70:7054-62.

[42] Thomas W, Alyson MB, Lisa LS, Susan GR, Walle UK. Flavonoid glucosides; are hydrolyzed and thus activated in the oral cavity in humans. Hum Nutr Metabol 2005;49-52.

[43] Farrell JJ, Zhang L, Zhou H, Chia D, Elashoff D, Akin D, et al. Variations of oral microbiota are associated with pancreatic diseases including pancreatic cancer. Gut 2012;61:582-8.

Role of bacteria in oral carcinogenesis

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