Abstract
Purpose
Dysbiosis has been identified in oral squamous cell carcinoma (OSCC). The aim of this study was to carry out a systematic review of an electronic research that was carried out on articles published between January 2008 and September 2018.
Methods
Eight studies were selected after applying the inclusion and exclusion criteria.
Results
All articles targeted the hypervariable regions of the 16S rRNA gene. At the phylum level, it was found reduction of Bacteroidetes (2/8 studies) and increase of Firmicutes (2/8 studies). At the genus level, Rothia increased (1/8 studies) and decreased (2/8 studies) in tumor samples, and Streptococcus also was found increased (3/8 studies) and reduced (3/8 studies). Fusobacterium only increased in OSCC samples (3/8 studies). At species level, an increase in F. nucleatum subsp. polymorphum was more associated to OSCC (2/8 studies) than with controls, as was P. aeruginosa (3/8 studies).
Conclusion
In summary, the results corroborated dysbiosis in OSCC patients, with enrichment of microbial taxa that are associated with inflammation and production of acetaldehyde. However, variations of study design and sample size were observed among the studies, as well as a shortage of more detailed analyses of possible correlations between risk habits and OSCC. This lack of more detailed analysis may be the cause of the inconsistencies in regard of the alterations reported for certain genera and species. In conclusion, there is an association between OSCC and oral microbiota dysbiosis, but its role in oral carcinogenesis needs to be clarified in more detail.
Similar content being viewed by others
References
Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68(6):394–424. https://doi.org/10.3322/caac.21492
Omran AR (1971) The epidemiologic transition: a theory of the epidemiology of population change. The Milbank quarterly 2005 83(4):731–757. https://doi.org/10.1111/j.1468-0009.2005.00398.x
Gersten O, Wilmoth JR (1951) The cancer transition in Japan since. Demogr Res 2002(7):271–306. https://doi.org/10.4054/DemRes.2002.7.5
Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136(5):359–386. https://doi.org/10.1002/ijc.29210
Instituto Nacional de Câncer José Alencar Gomes da Silva (2017) Estimativa 2018: incidência de câncer no Brasil. Rio de Janeiro: INCA:128
Markopoulos AK (2012) Current aspects on oral squamous cell carcinoma. The Open Dent J 6:126–130. https://doi.org/10.2174/1874210601206010126
Rodini CO, Lopes NM, Lara VS, Mackenzie IC (2017) Oral cancer stem cells - properties and consequences. J Appl Oral Sci 25(6):708–715. https://doi.org/10.1590/1678-7757-2016-0665
Rivera C, Venega B (2014) Histological and molecular aspects of oral squamous cell carcinoma (review). Oncol Left 8(1):7–11. https://doi.org/10.3892/ol.2014.2103
Elmurati AA, Pilborough AE, Khurram SA, Lambert DW (2017) Cancer-associated fibroblasts promote bone invasion in oral squamous cell carcinoma. Br J Cancer 117(6):867–875. https://doi.org/10.1038/bjc.2017.239
Bagordakis E, Sawazaki-Calone I, Macedo CCS, Carnielli CM, de Oliveira CE, Rodrigues PC, Rangel AL, Dos Santos JN, Risteli J, Graner E, Salo T, Paes Leme AF, Coletta RD (2016) Secretome profiling of oral squamous cell carcinoma-associated fibroblasts reveals organization and disassembly of extracellular matrix and collagen metabolic process signatures. Tumour Biol 37(7):9045–9057. https://doi.org/10.1007/s13277-015-4629-y
De Assis S, Warri A, Cruz MI, Laja O, Tian Y, Zhang B, Wang Y, Huang TH, Hilakivi-Clarke L (2012) High-fat or ethinyl-oestradiol intake during pregnancy increases mammary cancer risk in several generations of offspring. Nat Commun 3:1053. https://doi.org/10.1038/ncomms2058
Perera M, Al-hebshi NN, Speicher DJ, Perera I, Johnson NW (2016) Emerging role of bacteria in oral carcinogenesis: a review with special reference to perio-pathogenic bacteria. J Oral Microbiol 8:3276. https://doi.org/10.3402/jom.v8.32762
Syrjänen S, Lodi G, von Bültzingslöwen I, Aliko A, Arduino P, Campisi G, Challacombe S, Ficarra G, Flaitz C, Zhou HM, Maeda H, Miller C, Jontell M (2011) Human papilloma viruses in oral carcinoma and oral potentially malignant disorders: a systematic review. Oral Dis 17(1):58–72. https://doi.org/10.1111/j.1601-0825.2011.01792.x
Petti S (2009) Lifestyle risk factors for oral cancer. Oral Oncol 45(4–5):340–350. https://doi.org/10.1016/j.oraloncology.2008.05.018
Handa Y, Fujita H, Watanabe Y, Honma S, Kaneuchi M, Minakami KR (2010) Does dietary estrogen intake from meat relate to the incidence of hormone-dependent cancers? J Clin Oncol 28(15):1553–1553
Li TH, Qin Y, Sham PC, Lau KS, Chu KM, Leung WK (2017) Alterations in gastric microbiota After H. pylori eradication and in different histological stages of gastric carcinogenesis. Sci Rep 21:44935. https://doi.org/10.1038/srep44935
Meurman JH (2010) Oral microbiota and cancer. J Oral Microbiol 2. https://doi.org/10.3402/jom.v2i0.5195
Sasaki H, Ishzuka T, Muto M, Nezu M, Nakanishi Y, Inagaki Y, Watanabe H, Watanabe H, Terada M (1998) Presence of Streptococcus anginosus DNA in esophageal cancer, dysplasia of esophagus, and gastric cancer. Cancer Res 58(14):2991–2995
Hooper SJ, Crean SJ, Lewis MAO, Spratt DA, Wade G, Wilson MJ (2006) Viable bacteria present within oral squamous cell carcinoma tissue. J Clin Microbiol 44(5):1719–1725. https://doi.org/10.1099/jmm.0.46918-0
Meyer MS, Joshipura K, Giovannucci E, Michaud DS (2008) A review of the relationship between tooth loss, periodontal disease, and cancer. Cancer Causes Control 19(9):895–907. https://doi.org/10.1007/s10552-008-9163-4
Noto JM, Peek RM Jr (2017) The gastric microbiome, its interaction with Helicobacter pylori, and its potential role in the progression to stomach cancer. PLoS Pathog 13(10):e1006573. https://doi.org/10.1371/journal.ppat.1006573
Chen J, Domingue JC, Sears CL (2017) Microbiota dysbiosis in select human cancers: evidence of association and causality. Semin Immunol 32:25–34. https://doi.org/10.1016/j.smim.2017.08.001
Sheflin AM, Whitney AK, Weir TL (2014) Cancer-promoting effects of microbial dysbiosis. Curr Oncol Rep 16(10):406
Mao S, Park Y, Hasegawa Y, Tribble GD, James CE, Handfield M, Stavropoulos MF, Yilmaz O, Lamont RJ (2007) Intrinsic apoptotic pathways of gingival epithelial cells modulated by Porphyromonas gingivalis. Cell Microbiol 9(8):1997–2007
Inaba H, Sugita H, Kuboniwa M, Iwai S, Hamada M, Noda T, Morisaki I, Lamont RJ, Amano A (2014) Porphyromonasgingivalis promotes invasion of oral squamous cell carcinoma through induction of proMMP9 and its activation. Cell Microbiol 16(1):131–145
Moritani K, Takeshita T, Shibata Y, Ninomiya T, Kiyohara Y, Yamashita Y (2015) Acetaldehyde production by major oral microbes. Oral Dis 21(6):748–754. https://doi.org/10.1111/odi.12341
Sathiyasekar AC, Chandrasekar P, Pakash A, Kumar KU, Jaishlal MS (2016) Overview of immunology of oral squamous cell carcinoma. J Pharm Bioallied Sci 8(Suppl 1):S8–S12. https://doi.org/10.4103/0975-7406.191974
Di Bella JM, Bao Y, Gloor GB, Burton JP, Reid G (2013) High throughput sequencing methods and analysis for microbiome research. J Microbiol Methods 95(3):401–414
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Meg Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336
Al-Hebshi NN, Borgnakke WS, Johnson NW, Borgnakke WS (2019) The microbiome of oral squamous cell carcinomas: a functional perspective. Current Oral Health Reports 6:145–160. https://doi.org/10.1007/s40496-019-0215-5
Umam LS (2011) Systematic reviews and meta-analyses. J Can Acad Child Adolesc Psychiatry 20(1):57–59
Lee WH, Chen HM, Yang SF, Liang C, Peng CY, Lin FM, Tsai LL, Wu BC, Hsin CH, Chuang CY, Yang T, Yang TL, Ho SY, Chen WL, Ueng KC, Huang HD, Huang CN, Jong YJ (2017) Bacterial alterations in salivary microbiota and their association in oral cancer. Sci Rep 7(1):16540
Mukherjee PK, Wang H, Retuerto M, Zhang H, Burkey B, Ghannoum MA, Eng C (2017) Bacteriome and mycobiome associations in oral tongue cancer. Oncotarget 8(57):97273–97289
Zhao H, Chu M, Huang Z, Yang X, Ran S, Hu B, Zhang C, Liang J (2017) Variations in oral microbiota associated with oral cancer. Sci Rep 7:11773
Perera M, Al-hebshi NN, Perera I, Ipe D, Ulett GC, Speicher DJ, Chen T, Johnson N (2018) Inflammatory bacteriome and oral squamous cell carcinoma. J Dent Res 97(6):725–732
Al-hebshi NN, Nasher AT, Maryoud MY, Homeida HE, Chen T, Idris AM, Johnson NW (2017) Inflammatory bacteriome featuring Fusobacterium nucleatum and Pseudomonas aeruginosa identified in association with oral squamous cell carcinoma. Sci Rep 7(1):1834. https://doi.org/10.1038/s41598-017-02079-3
Yang HY, Yeh YM, Yu HY, Chin CY, Hsu CW, Liu H, Huang PJ, Hu SN, Liao CT, Chang KP, Chang YL (2018) Oral microbiota community dynamics associated with oral squamous cell carcinoma staging. Front Microbiol 9:862. https://doi.org/10.3389/fmicb.2018.00862
Wolf A, Moissl-Eichinger C, Perras A, Koskinen KTomazic PV, Dietmar TD (2017) The salivary microbiome as an indicator of carcinogenesis in patients with oropharyngeal squamous cell carcinoma: a pilot study. Sci Rep 7:5867. https://doi.org/10.1038/s41598-017-06361-2
Guerrero-Preston R, Godoy-Vitorino F, Jedlicka A, Rodríguez-Hilario A, González H, Bondy J, Lawson F, Folawiyo O, Michailidi C, Dziedzic A, Thangavel R, Hadar T, Noordhuis MG, Westra W, Koch W, Sidransky D (2016) 16S rRNA Amplicon sequencing identifies microbiota associated with oral cancer, human papilloma virus infection and surgical treatment. Oncotarget. 7(32):51320–51334. https://doi.org/10.18632/oncotarget.9710
Yuhan Hao, Zhiheng Pei, Stuart M. Brown (2017) Chapter 1 - bioinformatics in microbiome analysis. Colin Harwood. Methods in microbiology. Academic Press. New York
Langille MG, Zaneveld J, Caporaso JG, Mc Donald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Thurber RLV, Knight R, Beiko RG, Huttenhower C (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31(9):814–821. https://doi.org/10.1038/nbt.2676
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garret WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60. https://doi.org/10.1186/gb-2011-12-6-r60
Reuter JA, Spacek D, Snyder M (2015) High-throughput sequencing technologies. Mol Cell 58(4):586–597
Abdul-Hamid G, Saeed NM, Al-Kahiry W, Shukry S (2010) Pattern of head and neck cancer in Yemen. Gulf J Oncolog 7:21–24
Nasher AT, Al-Hebshi NN, Al-Moayad EE, Suleiman AM (2014) Viral infection and oral habits as risk factors for oral squamous cell carcinoma in Yemen: a case-control study. Oral Surg Med Oral Pathol Oral Radiol 118(5):566–572.e1. https://doi.org/10.1016/j.oooo.2014.08.005
McIsaac SM, Stadnyk AW, Lin TJ (2012) Toll-like receptors in the host defense against Pseudomonas aeruginosa respiratory infection and cystic fibrosis. J Leukoc Biol 92(5):977–985. https://doi.org/10.1189/jlb.0811410
Adamo R, Sokol S, Soong G, Gomez MI, Prince A (2004) Pseudomonas aeruginosa flagella activate airway epithelial cells through asialoGM1 and toll-like receptor as well as toll-like receptor 5. Am J Respir Cell Mol Biol 30(5):627–634. https://doi.org/10.1165/rcmb.2003-0260OC
Krisanaprakornkit S, Kimball JR, Weinberg A, Darveau RP, Bainbridge BW, Dale BA (2000) Inducible expression of human β-defensin 2 by Fusobacteriumnucleatum in oral epithelial cells: multiple signaling pathways and role of commensal cacteria in innate immunity and the epithelial barrier. Infect Immun 68(5):2907–2915
Gallimidi AB, Fischman S, Revach B, Bulvik R, Maliutina A, Rubinstein AM, Nussbaum G, Elkin M (2015) Periodontal pathogens Porphyromonasgingivalis and Fusobacteriumnucleatum promote tumor progression in an oral-specific chemical carcinogenesis model. Oncotarget 6(26):22613–22623. https://doi.org/10.18632/oncotarget.4209
Nagy KN, Sonkodi Szöke I, Nagy E, Newman HN (1998) The microflora associated with human oral carcinomas. Oral Oncol 34(4):304–308
Seitz HK, Becker P (2007) Alcohol metabolism and cancer risk. Alcohol Research and Health 30(1):38–41 44–7
Ye L, Jiang Y, Liu W, Tao H Correlation between periodontal disease and oral cancer risk: a meta-analysis. J Can Res Ther 12(Supplement):C237–C240. https://doi.org/10.4103/0973-1482.200746
Fan X, Peters BA, Jacobs EJ, Gapstur SM, Purdue MP, Freedman ND, Alekseyenko AV, Wu J, Yang L, Pei Z, Hayes RB, Ahn J (2018) Drinking alcohol is associated with variation in the human oral microbiome ina large study of American adults. Microbiome 6(1):59. https://doi.org/10.1186/s40168-018-0448-x
Yost S, Stashenko P, Choi Y, Kukuruzinska M, Genco CA, Salama A, Weinberg EO, Kramer CD, Frias-Lopez J (2018) Increased virulence of the oral microbiome in oral squamous cell carcinoma revealed by metatranscriptome analyses. Int J Oral Sci 10(4):32. https://doi.org/10.1038/s41368-018-0037-7
Tian L, Wu A-K, Friedman J, et al (2017) Deciphering functional redundancy in the human microbiome. bioRxiv. (n/a):176313. https://doi.org/10.1101/176313
Kurkivuori J, Salaspuro V, Kaihovaara P, Kari K, Rautemaa R, Grönroos L, Meurman JH, Salaspuro M (2007) Acetaldehyde production from ethanol by oral streptococci. Oral oncol 43(2):181. https://doi.org/10.1016/j.oraloncology.2006.02.005
Hsiao JR, Chang CC, Lee WT, Huang CC, Ou CY, Tsai ST, Chen KC, Huang JS, Wong TY, Lai YH, Wu YH, Hsueh WT, Wu SY, Yen CJ, Chang JY, Lin CL, Weng YL, Yang HC, Chen YS, Chang JS The interplay between oral microbiome, lifestyle factors and genetic polymorphisms in the risk of oral squamous cell carcinoma. Carcinogenesis 39(6):778–787. https://doi.org/10.1093/carcin/bgy053
Funding
This work was supported by the National Council for Scientific and Technological Development (CNPq) (Project: 211309/2013-3) and the Foundation for Research Financial Support in the State of Rio de Janeiro (FAPERJ), Rio de Janeiro, Brazil (Project: E26/103.001/2012).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Ramos, R.T., Sodré, C.S., de Sousa Rodrigues, P.M.G.R. et al. High-throughput nucleotide sequencing for bacteriome studies in oral squamous cell carcinoma: a systematic review. Oral Maxillofac Surg 24, 387–401 (2020). https://doi.org/10.1007/s10006-020-00873-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10006-020-00873-4