Fungal Gut Microbiota Dysbiosis and Its Role in Colorectal, Oral, and Pancreatic Carcinogenesis

. 2020 May 22 ; 12 (5) : . [epub] 20200522

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid32455985

The association between bacterial as well as viral gut microbiota imbalance and carcinogenesis has been intensively analysed in many studies; nevertheless, the role of fungal gut microbiota (mycobiota) in colorectal, oral, and pancreatic cancer development is relatively new and undiscovered field due to low abundance of intestinal fungi as well as lack of well-characterized reference genomes. Several specific fungi amounts are increased in colorectal cancer patients; moreover, it was observed that the disease stage is strongly related to the fungal microbiota profile; thus, it may be used as a potential diagnostic biomarker for adenomas. Candida albicans, which is the major microbe contributing to oral cancer development, may promote carcinogenesis via several mechanisms, mainly triggering inflammation. Early detection of pancreatic cancer provides the opportunity to improve survival rate, therefore, there is a need to conduct further studies regarding the role of fungal microbiota as a potential prognostic tool to diagnose this cancer at early stage. Additionally, growing attention towards the characterization of mycobiota may contribute to improve the efficiency of therapeutic methods used to alter the composition and activity of gut microbiota. The administration of Saccharomyces boulardii in oncology, mainly in immunocompromised and/or critically ill patients, is still controversial.

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Mahnic A., Rupnik M. Different host factors are associated with patterns in bacterial and fungal gut microbiota in Slovenian healthy cohort. PLoS ONE. 2018;12:e0209209. doi: 10.1371/journal.pone.0209209. PubMed DOI PMC

Bhatt A.P., Redinbo M.R., Bultman S.J. The role of the microbiome in cancer development and therapy. Cancer J. Clin. 2017;4:326–344. doi: 10.3322/caac.21398. PubMed DOI PMC

Vivarelli S., Salemi R., Candido S., Falzone L., Santagati M., Stefani S., Torino F., Banna G.L., Tonini G., Libra M. Gut Microbiota and Cancer: From Pathogenesis to Therapy. Cancers. 2019;1:38. doi: 10.3390/cancers11010038. PubMed DOI PMC

Kaźmierczak-Siedlecka K., Ruszkowski J., Skonieczna-Żydecka K., Jędrzejczak J., Folwarski M., Makarewicz W. Gastrointestinal cancers: The role of microbiota in carcinogenesis and the role of probiotics and microbiota in the anti-cancer therapy efficiency. Cent. Eur. J. Immunol. (accepted) PubMed PMC

Kaźmierczak-Siedlecka K., Fic M., Folwarski M., Makarewicz W. Diet & Microbes: Gut health for the brain and body; Proceedings of the 6th Nutrition Winter School 2020; Levi, Finland. 27–31 January 2020.

Vyshenska D., Lam K.C., Shulzhenko N., Morgun A. Interplay between viruses and bacterial microbiota in cancer development. Semin. Immunol. 2017;32:14–24. doi: 10.1016/j.smim.2017.05.003. PubMed DOI PMC

Schottenfeld D., Beebe-Dimmer J. The cancer burden attributable to biologic agents. Ann. Epidemiol. 2015;3:183–187. doi: 10.1016/j.annepidem.2014.11.016. PubMed DOI

Coker O.O., Nakatsu G., Dai R.Z., Wu W.K.K., Wong S.H., Ng S.C., Leung chan F.K., Jao Yiu Sung J., Yu J. Enteric fungal microbiota dysbiosis and ecological alterations in colorectal cancer. Gut. 2019;4:654–662. doi: 10.1136/gutjnl-2018-317178. PubMed DOI PMC

Klimesova K., Jiraskova Zakostelska Z., Tlaskalova-Hogenova H. Oral Bacterial and Fungal Microbiome Impacts Colorectal Carcinogenesis. Front. Microbiol. 2018;9:774. doi: 10.3389/fmicb.2018.00774. PubMed DOI PMC

Limon J.J., Skalski J.H., Underhill D.M. Commensal Fungi in Health and Disease. Cell Host Microbe. 2017;2:156–165. doi: 10.1016/j.chom.2017.07.002. PubMed DOI PMC

[(accessed on 15 May 2020)]; Available online: https://www.cancer.org/content/dam/cancer-org/research/cancer-facts-and-statistics/annual-cancer-facts-and-figures/2019/cancer-facts-and-figures-2019.pdf?fbclid=IwAR24wyni_jp6BAwwQ0Xj7-1E2aSFSjHPq4BrG-KSMcF2Vuee5o-wJMuaalc.

Mukherjee P.K., Sendid B., Hoarau G., Colombel J.F., Poulain D., Ghannoum M.A. Mycobiota in gastrointestinal diseases. Nat. Rev. Gastroenterol. Hepatol. 2015;2:77–87. doi: 10.1038/nrgastro.2014.188. PubMed DOI

Hoffmann C., Dollive S., Grunberg S., Chen J., Li H., Wu G.D., Lewis J.D., Bushman F.D. Archaea and Fungi of the Human Gut Microbiome: Correlations with Diet and Bacterial Residents. PLoS ONE. 2013;6:e66019. doi: 10.1371/journal.pone.0066019. PubMed DOI PMC

Iliev I.D., Leonardi I. Fungal Dysbiosis: Immunity and Interactions at Mucosal Barriers. Nat. Rev. Immunol. 2017;10:635–646. doi: 10.1038/nri.2017.55. PubMed DOI PMC

Ghannoum M.A., Jurevic R.J., Mukherjee P.K., Cui F., Sikaroodi M., Naqvi A., Gillevet P.M. Characterization of the oral fungal microbiome (mycobiome) in healthy individuals. PLoS Pathog. 2010;1:e1000713. doi: 10.1371/journal.ppat.1000713. PubMed DOI PMC

Murzyn A., Krasowska A., Stefanowicz P., Dziadkowiec D., Łukaszewicz M. Capric acid secreted by S. boulardii inhibits C. albicans filamentous growth, adhesion and biofilm formation. PLoS ONE. 2010;8:e12050. doi: 10.1371/journal.pone.0012050. PubMed DOI PMC

Koliada A., Syzenko G., Moseiko V., Budovska L., Puchkov K., Perederiy V., Gavalko Y., Dorofeyev A., Romanenko M., Tkach S., et al. Association between body mass index and Firmicutes/Bacteroidetes ratio in an adult Ukrainian population. BMC Microbiol. 2017;1:120. doi: 10.1186/s12866-017-1027-1. PubMed DOI PMC

Strati F., Di Paola M., Stefanini I., Albanese D., Rizzetto L., Lionetti P., Calabrò A., Jousson O., Donati C., Cavalieri D., et al. Age and Gender Affect the Composition of Fungal Population of the Human Gastrointestinal Tract. Front. Microbiol. 2016;7:1227. doi: 10.3389/fmicb.2016.01227. PubMed DOI PMC

Kapitan M., Niemiec M.J., Steimle A., Frick J.S., Jacobsen I.D. Fungi as Part of the Microbiota and Interactions with Intestinal Bacteria. Curr. Top. Microbiol. Immunol. 2019;422:265–301. PubMed

Paterson M.J., Oh S., Underhill D.M. Host-microbe Interactions: Commensal Fungi in the Gut. Curr. Opin. Microbiol. 2017;40:131–137. doi: 10.1016/j.mib.2017.11.012. PubMed DOI PMC

Richard M.L., Sokol H. The Gut Mycobiota: Insights Into Analysis, Environmental Interactions and Role in Gastrointestinal Diseases. Nat. Rev. Gastroenterol. Hepatol. 2019;6:331–345. doi: 10.1038/s41575-019-0121-2. PubMed DOI

Li S., Yu X., Wu W., Chen D.Z., Xiao M., Huang X. The opportunistic human fungal pathogen Candida albicans promotes the growth and proliferation of commensal Escherichia coli through an iron-responsive pathway. Microbiol. Res. 2018;207:232–239. doi: 10.1016/j.micres.2017.12.008. PubMed DOI

Peleg A.Y., Hogan D.A., Mylonakis E. Medically important bacterial-fungal interactions. Nat. Rev. Microbiol. 2010;8:340–349. doi: 10.1038/nrmicro2313. PubMed DOI

Chiaro T.R., Soto R., Stephens W.Z., Kubinak J.L., Petersen C., Gogokhia L. A member of the gut mycobiota modulates host purine metabolism exacerbating colitis in mice. Sci. Transl. Med. 2017;380:eaaf9044. doi: 10.1126/scitranslmed.aaf9044. PubMed DOI PMC

Martinon F., Pétrilli V., Mayor A., Tardivel A., Tschopp J. Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature. 2006;440:237–241. doi: 10.1038/nature04516. PubMed DOI

Wu M., Li J., An Y., Li P., Xiong W., Li J., Yan D., Wang M.Y., Zhong G.S. Chitooligosaccharides Prevents the Development of Colitis-Associated Colorectal Cancer by Modulating the Intestinal Microbiota and Mycobiota. Front. Microbiol. 2019;10:2101. doi: 10.3389/fmicb.2019.02101. PubMed DOI PMC

Jahani-Sherafat S., Alebouyeh M., Moghim S., Ahmadi Amoli H., Ghasemian-Safaei H. Role of gut microbiota in the pathogenesis of colorectal cancer; a review article. Gastroenterol. Hepatol. Bed Bench. 2018;2:101–109. PubMed PMC

Lin C., Cai X., Zhang J., Wang W., Sheng Q., Hua H., Zhou X. Role of Gut Microbiota in the Development and Treatment of Colorectal Cancer. Digestion. 2019;1:72–78. doi: 10.1159/000494052. PubMed DOI

Dai Z., Zhang J., Wu Q., Chen J., Liu J., Wang L., Chen C.W., Xu J.M., Zhang H.P., Shi C.F., et al. The role of microbiota in the development of colorectal cancer. Int. J. Cancer. 2019;8:2032–2041. doi: 10.1002/ijc.32017. PubMed DOI PMC

Gagnière J., Raisch J., Veziant J., Barnich N., Bonnet R., Buc E., Bringer M.-A., Pezet D., Bonnet M. Gut microbiota imbalance and colorectal cancer. World J. Gastroenterol. 2016;2:501–518. PubMed PMC

Kaźmierczak-Siedlecka K., Daca A., Fic M., van de Wetering T., Folwarski M., Makareiwcz W. Therapeutic methods of gut microbiota modification in colorectal cancer management–fecal microbiota transplantation, prebiotics, probiotics, and synbiotics. Gut Microbes. 2020 doi: 10.1080/19490976.2020.1764309. (accepted) PubMed DOI PMC

Kim S., Rajapakse N. Enzymatic production and biological activities of chitosan oligosaccharides (COS): A review. Carbohydr. Polym. 2005;4:357–368. doi: 10.1016/j.carbpol.2005.08.012. DOI

Caiqin Q., Wei W., Huie P., Rong H., Wei L. Preparation and properties of reduced chitooligomers. Carbohydr. Polym. 2008;4:701–706. doi: 10.1016/j.carbpol.2007.10.014. DOI

Zhang T., Li Q., Cheng L., Buch H., Zhang F. Akkermansia muciniphila is a promising probiotic. Microb. Biotechnol. 2019;6:1109–1125. doi: 10.1111/1751-7915.13410. PubMed DOI PMC

Nurhayati Y., Abdul Manaf A., Osman H., Che Abdullah A.B., Huat Tang J.Y. Effect of Chitosan Oligosaccharides on the Growth of Bifidobacterium Species. Mal. J. Appl. Sci. 2016;1:13–23.

Pan X., Chen F., Wu T., Tang H., Zhao Z. Prebiotic oligosaccharides change the concentrations of short-chain fatty acids and the microbial population of mouse bowel. J. Zhejiang Univ. Sci. B. 2009;4:258–263. doi: 10.1631/jzus.B0820261. PubMed DOI PMC

Jawhara S., Habib K., Maggiotto F., Pignede G., Vandekerckove P., Maes E., Dubuquoy L., Fontaine T., Guerardel Y., Poulain D. Modulation of Intestinal Inflammation by Yeasts and Cell Wall Extracts: Strain Dependence and Unexpected Anti-Inflammatory Role of Glucan Fractions. PLoS ONE. 2012;7:e40648. doi: 10.1371/journal.pone.0040648. PubMed DOI PMC

Gao R., Kong C., Li H., Huang L., Qu X., Qin N., Qin H. Dysbiosis signature of mycobiota in colon polyp and colorectal cancer. Eur. J. Clin. Microbiol. Infect. Dis. 2017;12:2457–2468. doi: 10.1007/s10096-017-3085-6. PubMed DOI

Luan C., Xie L., Yang X., Miao H., Lv N., Zhang R., Xiao X., Hu Y.F., Liu Y.L., Wu N., et al. Dysbiosis of Fungal Microbiota in the Intestinal Mucosa of Patients with Colorectal Adenomas. Sci. Rep. 2015;5:7980. doi: 10.1038/srep07980. PubMed DOI PMC

Arzmi M.H., Dashper S., McCullough M. Polymicrobial interactions of Candida albicans and its role in oral carcinogenesis. J. Oral Pathol. Med. 2019;7:546–551. doi: 10.1111/jop.12905. PubMed DOI

Pushalkar S., Mane S.P., Ji X., Li Y., Evans C., Crasta O.R., Morse D., Meagher R., Singh A., Saxena D. Microbial diversity in saliva of oral squamous cell carcinoma. Immunol. Med. Microbiol. 2011;3:269–277. doi: 10.1111/j.1574-695X.2010.00773.x. PubMed DOI PMC

Alnuaimi A.D., Ramdzan A.N., Wiesenfeld D., O’Brien-Simpson N.M., Kolev S.D., Reynolds E.C., McCullough M.J. Candida virulence and ethanol-derived acetaldehyde production in oral cancer and non-cancer subjects. Oral Dis. 2016;8:805–814. doi: 10.1111/odi.12565. PubMed DOI

Stornetta A., Guidolin V., Balbo S. Alcohol-Derived Acetaldehyde Exposure in the Oral Cavity. Cancers. 2018;1:20. doi: 10.3390/cancers10010020. PubMed DOI PMC

Mäkinen A., Nawaz A., Mäkitie A., Meurman J.H. Role of Non-Albicans Candida and Candida Albicans in Oral Squamous Cell Cancer Patients. J. Oral Maxillofac. Surg. 2018;12:2564–2571. doi: 10.1016/j.joms.2018.06.012. PubMed DOI

Mukherjee P.K., Wang H., Retuerto M., Zhang H., Burkey B., Ghannoum M.A., Eng C. Bacteriome and mycobiome associations in oral tongue cancer. Oncotarget. 2017;57:97273–97289. doi: 10.18632/oncotarget.21921. PubMed DOI PMC

Ramirez-Garcia A., Rementeria A., Aguirre-Urizar J.M., Moragues M.D., Antoran A., Pellon A., Abad-Diaz-de-Cerio A., Hernando F.L. Candida albicans and cancer: Can this yeast induce cancer development or progression? Crit. Rev. Microbiol. 2016;2:181–193. PubMed

Dongari-Bagtzoglou A., Kashleva H. Candida albicans triggers interleukin-8 secretion by oral epithelial cells. Microb. Pathog. 2003;4:169–177. doi: 10.1016/S0882-4010(03)00004-4. PubMed DOI

Simoes P.K., Olson S.H., Saldia A., Kurtz R.C. Epidemiology of pancreatic adenocarcinoma. Chin. Clin. Oncol. 2017;3:24. doi: 10.21037/cco.2017.06.32. PubMed DOI

Meng C., Bai C., Brown T.D., Hood L.E., Tian Q. Human Gut Microbiota and Gastrointestinal Cancer. Genom. Proteom. Bioinform. 2018;1:33–49. doi: 10.1016/j.gpb.2017.06.002. PubMed DOI PMC

Wei M.Y., Shi S., Liang C., Meng Q.C., Hua J., Zhang Y.Y., Liu J., Zhang B., Xu J., Yu X.-J. The microbiota and microbiome in pancreatic cancer: More influential than expected. Mol. Cancer. 2019;18:97. doi: 10.1186/s12943-019-1008-0. PubMed DOI PMC

Aykut B., Pushalkar S., Chen R., Li Q., Abengozar R., Kim J.I., Shadaloey S.A., Wu D.L., Preiss P., Verma N., et al. The fungal mycobiome promotes pancreatic oncogenesis via activation of MBL. Nature. 2019;7777:264–267. doi: 10.1038/s41586-019-1608-2. PubMed DOI PMC

Turner M.W. The role of mannose-binding lectin in health and disease. Mol. Immunol. 2003;7:423–429. doi: 10.1016/S0161-5890(03)00155-X. PubMed DOI

Eissa M.A.L., Lerner L., Abdelfatah E., Shankar N., Canner J.K., Hasan N.M., Yaghoobi V., Huang B., Kerner Z., Takaesu F., et al. Promoter methylation of ADAMTS1 and BNC1 as potential biomarkers for early detection of pancreatic cancer in blood. Clin. Epigenetics. 2019;1:59. doi: 10.1186/s13148-019-0650-0. PubMed DOI PMC

Orth M., Metzger P., Gerum S., Mayerle J., Schneider G., Belka C., Schnurr M., Lauber K. Pancreatic ductal adenocarcinoma: Biological hallmarks, current status, and future perspectives of combined modality treatment approaches. Radiat. Oncol. 2019;1:141. doi: 10.1186/s13014-019-1345-6. PubMed DOI PMC

Mendez R., Kesh K., Arora N., Di Martino L., McAllister F., Merchant N., Banerjee S. Microbial dysbiosis and polyamine metabolism as predictive markers for early detection of pancreatic cancer. Carcinogenesis. 2019:bgz116. doi: 10.1093/carcin/bgz116. PubMed DOI PMC

Zhou B., Xu J.W., Cheng Y.G., Gao J.Y., Hu S.Y., Wang L., Zhan H.-X. Early detection of pancreatic cancer: Where are we now and where are we going? Int. J. Cancer. 2017;2:231–241. doi: 10.1002/ijc.30670. PubMed DOI

Selander C., Engblom C., Nilsson G., Scheynius A., Andersson C.L. TLR2/MyD88-dependent and -independent activation of mast cell IgE responses by the skin commensal yeast Malassezia sympodialis. J. Immunol. 2009;7:4208–4216. doi: 10.4049/jimmunol.0800885. PubMed DOI

Zhang D., Wang Y., Shen S., Hou Y., Chen Y., Wang T. The Mycobiota of the Human Body: A Spark Can Start a Prairie Fire. Gut Microbes. 2020;9:1–25. doi: 10.1080/19490976.2020.1731287. PubMed DOI PMC

Conche C., Greten F.R. Fungi Enter the Stage of Colon Carcinogenesis. Immunity. 2018;3:384–386. doi: 10.1016/j.immuni.2018.09.002. PubMed DOI

Montoya A.M., González G.M., Martinez-Castilla A.M., Aguilar S.A., Franco-Molina M.A., Coronado-Cerda E. Cytokines Profile in Immunocompetent Mice During Trichosporon Asahii Infection. Med. Mycol. 2018;1:103–109. doi: 10.1093/mmy/myx018. PubMed DOI

Edwards-Ingram L., Gitsham P., Burton N., Warhurst G., Clarke I., Hoyle D., Oliver S.G., Stateva L. Genotypic and physiological characterization of Saccharomyces boulardii, the probiotic strain of Saccharomyces cerevisiae. Appl. Environ. Microbiol. 2007;8:2458–2467. doi: 10.1128/AEM.02201-06. PubMed DOI PMC

Czerucka D., Rampal P. Diversity of Saccharomyces boulardii CNCM I-745 mechanisms of action against intestinal infections. World J. Gastroenterol. 2019;18:2188–2203. doi: 10.3748/wjg.v25.i18.2188. PubMed DOI PMC

Neut C., Mahieux S., Dubreuil L.J. Antibiotic Susceptibility of Probiotic Strains: Is It Reasonable to Combine Probiotics with Antibiotics? Med. Mal. Infect. 2017;7:477–483. doi: 10.1016/j.medmal.2017.07.001. PubMed DOI

Moré M.I., Swidsinski A. Saccharomyces boulardii CNCM I-745 supports regeneration of the intestinal microbiota after diarrheic dysbiosis–a review. Clin. Exp. Gastroenterol. 2015;8:237–255. doi: 10.2147/CEG.S85574. PubMed DOI PMC

Dong J.P., Zheng Y., Wu T., He Q., Teng G.G., Wang H.H. Protective effect of Saccharomyces boulardii on intestinal mucosal barrier of dextran sodium sulfate-induced colitis in mice. Chin. Med. J. 2019;16:1951–1958. doi: 10.1097/CM9.0000000000000364. PubMed DOI PMC

Kaźmierczak-Siedlecka K., Fic M., Ruszkowski J., Folwarski M., Makarewicz W. Saccharomyces boulardii (CNCM I-745): A non-bacterial microorganism used as probiotic agent in supporting treatment of selected diseases. Curr. Microbiol. (under review) PubMed PMC

Sulik-Tyszka B., Snarski E., Niedźwiedzka M., Augustyniak M., Myhre T.N., Kacprzyk A., Swoboda-Kopeć E., Roszkowska M., Dwilewicz-Trojaczek J., Jędrzejczak W.W., et al. Experience with Saccharomyces boulardii Probiotic in Oncohaematological Patients. Probiotics Antimicro. Proteins. 2018;2:350–355. doi: 10.1007/s12602-017-9332-4. PubMed DOI PMC

Burkhardt O., Köhnlein T., Pletz M., Welte T. Saccharomyces boulardii induced sepsis: Successful therapy with voriconazole after treatment failure with fluconazole. Scand. J. Infect. Dis. 2005;1:69–72. doi: 10.1080/00365540510026454. PubMed DOI

Lolis N., Veldekis D., Moraitou H., Kanavaki S., Velegraki A., Triandafyllidis C., Tasioudis C., Pefanis A., Pneumatikos I. Saccharomyces boulardii fungaemia in an intensive care unit patient treated with caspofungin. Crit. Care Lond. Engl. 2008;2:414. PubMed PMC

Cesaro S., Chinello P., Rossi L., Zanesco L. Saccharomyces cerevisiae fungemia in a neutropenic patient treated with Saccharomyces boulardii. Support Care Cancer. 2000;6:504–505. doi: 10.1007/s005200000123. PubMed DOI

Tomblyn M., Chiller T., Einsele H., Gress R., Sepkowitz K., Storek J., Wingard J.R., Young J.-A.H., Boeckh M.J. Guidelines for preventing infectious complications among hematopoietic cell transplantation recipients: A global perspective. Biol. Blood Marrow Transplant. 2009;10:1143–1238. doi: 10.1016/j.bbmt.2009.06.019. PubMed DOI PMC

Kaźmierczak-Siedlecka K., Piekarska A., Lubieniecka-Archutowska E., Bicz M., Folwarski M., Makarewicz W. Nutritional status in patients after hematopoietic cell transplantation. Acta Haematol. Pol. 2019;1:1–9.

Muñoz P., Bouza E., Cuenca-Estrella M., Eiros J.M., Pérez M.J., Sánchez-Somolinos M., Rincón C., Hortal J., Peláez T. Saccharomyces cerevisiae Fungemia: An Emerging Infectious Disease. Clin. Infect. Dis. 2005;11:1625–1634. doi: 10.1086/429916. PubMed DOI

Anaissie E., Bodey G.P., Kantarjian H., Ro J., Vartivarian S.E., Hopfer R., Hoy J., Rolston K. New spectrum of fungal infections in patients with cancer. Rev. Infect. Dis. 1989;3:369–378. doi: 10.1093/clinids/11.3.369. PubMed DOI

Aucott J.N., Fayen J., Grossnicklas H., Morrissey A., Lederman M.M., Salata R.A. Invasive infection with Saccharomyces cerevisiae: Report of three cases and review. Rev. Infect. Dis. 1990;3:406–411. doi: 10.1093/clinids/12.3.406. PubMed DOI

Appel-da-Silva M.C., Narvaez G.A., Perez L.R.R., Drehmer L., Lewgoy J. Saccharomyces cerevisiae var. boulardii fungemia following probiotic treatment. Med. Mycol. Case Rep. 2017;18:15–17. doi: 10.1016/j.mmcr.2017.07.007. PubMed DOI PMC

Wang C., Li W., Wang H., Ma Y., Zhao X., Zhang X., Yang H., Qian J., Li J. Saccharomyces boulardii alleviates ulcerative colitis carcinogenesis in mice by reducing TNF-α and IL-6 levels and functions and by rebalancing intestinal microbiota. BMC Microbiol. 2019;1:246. doi: 10.1186/s12866-019-1610-8. PubMed DOI PMC

Fortin O., Aguilar-Uscanga B.R., Vu K.D., Salmieri S., Lacroix M. Effect of Saccharomyces Boulardii Cell Wall Extracts on Colon Cancer Prevention in Male F344 Rats Treated with 1,2-Dimethylhydrazine. Nutr. Cancer. 2018;4:632–642. doi: 10.1080/01635581.2018.1460672. PubMed DOI

Waszkiewicz N., Szajda S.D., Konarzewska-Duchnowska E., Zalewska-Szajda B., Gałązkowski R., Sawko A., Nammous H., Buko V., Szulc A., Zwierz K., et al. Serum β-glucuronidase as a potential colon cancer marker: A preliminary study. Postepy Hig. Med. Dosw. 2015;69:436–439. doi: 10.5604/17322693.1148704. PubMed DOI

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