Bacteroides fragilis in saliva: investigating links with ulcerative colitis.
Bacteroides fragilis
Bacteroides fragilis toxin
Colitis
Ulcerative
Journal
Brazilian journal of microbiology : [publication of the Brazilian Society for Microbiology]
ISSN: 1678-4405
Titre abrégé: Braz J Microbiol
Pays: Brazil
ID NLM: 101095924
Informations de publication
Date de publication:
19 Aug 2024
19 Aug 2024
Historique:
received:
17
03
2024
accepted:
05
08
2024
medline:
19
8
2024
pubmed:
19
8
2024
entrez:
18
8
2024
Statut:
aheadofprint
Résumé
Ulcerative colitis (UC) is a long-term bowel inflammation of unknown cause. Recent research points to gut microbiota, especially Enterotoxigenic Bacteroides fragilis (ETBF), in UC's development. This study examined the presence of Bacteroides fragilis (B. fragilis) and ETBF in the saliva of UC patients and Healthy Controls (HCs) in Iran. A total of 40 UC patients and 40 healthy controls were included in the study. Saliva samples were collected and analyzed for the presence of B. fragilis and ETBF using real-time polymerase chain reaction (PCR). B. fragilis was more prevalent in HCs (70%) than UC patients (67.5%), but not significantly (p = 0.809). ETBF was significantly more prevalent in UC patients (50%) than HCs (10%) (p < 0.0001). The mean count of B. fragilis was higher in UC patients, but not significantly (p = 0.47). However, the mean count of ETBF was significantly higher in UC patients (p = 0.000089). In terms of gender, the number of B. fragilis in women was not significant (p = 0.16), but the number of ETBF was significantly higher in women with UC (p = 0.000458). For men, no significant differences were observed. The present study suggest a higher prevalence of B. fragilis observed in UC patients compared to HCs. Further research is needed to confirm these findings and explore potential mechanisms underlying this association.
Sections du résumé
BACKGROUND
BACKGROUND
Ulcerative colitis (UC) is a long-term bowel inflammation of unknown cause. Recent research points to gut microbiota, especially Enterotoxigenic Bacteroides fragilis (ETBF), in UC's development. This study examined the presence of Bacteroides fragilis (B. fragilis) and ETBF in the saliva of UC patients and Healthy Controls (HCs) in Iran.
METHODS
METHODS
A total of 40 UC patients and 40 healthy controls were included in the study. Saliva samples were collected and analyzed for the presence of B. fragilis and ETBF using real-time polymerase chain reaction (PCR).
RESULTS
RESULTS
B. fragilis was more prevalent in HCs (70%) than UC patients (67.5%), but not significantly (p = 0.809). ETBF was significantly more prevalent in UC patients (50%) than HCs (10%) (p < 0.0001). The mean count of B. fragilis was higher in UC patients, but not significantly (p = 0.47). However, the mean count of ETBF was significantly higher in UC patients (p = 0.000089). In terms of gender, the number of B. fragilis in women was not significant (p = 0.16), but the number of ETBF was significantly higher in women with UC (p = 0.000458). For men, no significant differences were observed.
CONCLUSIONS
CONCLUSIONS
The present study suggest a higher prevalence of B. fragilis observed in UC patients compared to HCs. Further research is needed to confirm these findings and explore potential mechanisms underlying this association.
Identifiants
pubmed: 39155343
doi: 10.1007/s42770-024-01484-x
pii: 10.1007/s42770-024-01484-x
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s) under exclusive licence to Sociedade Brasileira de Microbiologia.
Références
Gomaa EZ (2020) Human gut microbiota/microbiome in health and diseases: a review. Antonie Van Leeuwenhoek 113(12):2019–2040. https://doi.org/10.1007/s10482-020-01474-7 Epub 2020 Nov 2. PMID: 33136284
doi: 10.1007/s10482-020-01474-7
pubmed: 33136284
Ghouri YA, Tahan V, Shen B (2020) Secondary causes of inflammatory bowel diseases. World J Gastroenterol 26(28):3998–4017. https://doi.org/10.3748/wjg.v26.i28.3998 PMID: 32821067; PMCID: PMC7403802
doi: 10.3748/wjg.v26.i28.3998
pubmed: 32821067
pmcid: 7403802
Seyedian SS, Nokhostin F, Malamir MD (2019 Apr-Jun) A review of the diagnosis, prevention, and treatment methods of inflammatory bowel disease. J Med Life 12(2):113–122. https://doi.org/10.25122/jml-2018-0075 PMID: 31406511; PMCID: PMC6685307
Dharni K, Singh A, Sharma S, Midha V, Kaur K, Mahajan R, Dulai PS, Sood A (2024) Trends of inflammatory bowel disease from the Global Burden of Disease Study (1990–2019). Indian J Gastroenterol.;43(1):188–198. https://doi.org/10.1007/s12664-023-01430-z . Epub 2023 Oct 3. PMID: 37783933
Preda CM, Istrătescu D (2022) Etiology of Ulcerative Colitis [Internet]. Ulcerative Colitis - Etiology, Diagnosis, Diet, Special Populations, and the Role of Interventional Endoscopy. IntechOpen; https://doi.org/10.5772/intechopen.106842
Kaur A, Goggolidou P (2020) Ulcerative colitis: understanding its cellular pathology could provide insights into novel therapies. J Inflamm (Lond) 17:15. https://doi.org/10.1186/s12950-020-00246-4 PMID: 32336953; PMCID: PMC7175540
doi: 10.1186/s12950-020-00246-4
pubmed: 32336953
Sartor RB (2010) Genetics and environmental interactions shape the intestinal microbiome to promote inflammatory bowel disease versus mucosal homeostasis. Gastroenterology 139(6):1816–1819. https://doi.org/10.1053/j.gastro.2010.10.036 Epub 2010 Oct 26. PMID: 21029802
doi: 10.1053/j.gastro.2010.10.036
pubmed: 21029802
Basha OM, Hafez RA, Salem SM, Anis RH, Hanafy AS (2023) Impact of gut microbiome alteration in Ulcerative Colitis patients on disease severity and outcome. Clin Exp Med 23(5):1763–1772. https://doi.org/10.1007/s10238-022-00917-x Epub 2022 Nov 7. PMID: 36344781; PMCID: PMC10460709
doi: 10.1007/s10238-022-00917-x
pubmed: 36344781
Feng T, Elson CO (2011) Adaptive immunity in the host-microbiota dialog. Mucosal Immunol 4(1):15–21. https://doi.org/10.1038/mi.2010.60 Epub 2010 Oct 13. PMID: 20944557; PMCID: PMC4557730
doi: 10.1038/mi.2010.60
pubmed: 20944557
Cui J, Cui H, Yang M, Du S, Li J, Li Y, Liu L, Zhang X, Li S (2019) Tongue coating microbiome as a potential biomarker for gastritis including precancerous cascade. Protein Cell 10(7):496–509. https://doi.org/10.1007/s13238-018-0596-6 Epub 2018 Nov 26. PMID: 30478535; PMCID: PMC6588651
doi: 10.1007/s13238-018-0596-6
pubmed: 30478535
Flemer B, Warren RD, Barrett MP, Cisek K, Das A, Jeffery IB, Hurley E, O’Riordain M, Shanahan F, O’Toole PW (2018) The oral microbiota in colorectal cancer is distinctive and predictive. Gut 67(8):1454–1463. https://doi.org/10.1136/gutjnl-2017-314814 Epub 2017 Oct 7. PMID: 28988196; PMCID: PMC6204958
doi: 10.1136/gutjnl-2017-314814
pubmed: 28988196
Liu Y, Baba Y, Ishimoto T, Iwatsuki M, Hiyoshi Y, Miyamoto Y, Yoshida N, Wu R, Baba H (2019) Progress in characterizing the linkage between Fusobacterium nucleatum and gastrointestinal cancer. J Gastroenterol 54(1):33–41. https://doi.org/10.1007/s00535-018-1512-9 Epub 2018 Sep 22. PMID: 30244399
doi: 10.1007/s00535-018-1512-9
pubmed: 30244399
Becker C, Neurath MF, Wirtz S (2015) The Intestinal Microbiota in Inflammatory Bowel Disease. ILAR J.;56(2):192–204. https://doi.org/10.1093/ilar/ilv030 . PMID: 26323629
Zamani S, Hesam Shariati S, Zali MR, Asadzadeh Aghdaei H, Sarabi Asiabar A, Bokaie S, Nomanpour B, Sechi LA, Feizabadi MM (2017) Detection of enterotoxigenic Bacteroides fragilis in patients with ulcerative colitis. Gut Pathog 9:53. https://doi.org/10.1186/s13099-017-0202-0 PMID: 28924454; PMCID: PMC5599888
doi: 10.1186/s13099-017-0202-0
pubmed: 28924454
pmcid: 5599888
Elsaghir H, Reddivari AKR, Bacteroides F (2023) May 23. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2024 Jan–. PMID: 31971708
Zafar H, Saier MH Jr (2021 Jan-Dec) Gut Bacteroides species in health and disease. Gut Microbes 13(1):1–20 PMID: 33535896; PMCID: PMC7872030
Jamal W, Khodakhast FB, AlAzmi A, Sόki J, AlHashem G, Rotimi VO (2020) Prevalence and antimicrobial susceptibility of enterotoxigenic extra-intestinal Bacteroides fragilis among 13-year collection of isolates in Kuwait. BMC Microbiol 20(1):14. https://doi.org/10.1186/s12866-020-1703-4 PMID: 31941446; PMCID: PMC6964027
doi: 10.1186/s12866-020-1703-4
pubmed: 31941446
pmcid: 6964027
Purcell RV, Pearson J, Aitchison A, Dixon L, Frizelle FA, Keenan JI (2017) Colonization with enterotoxigenic Bacteroides fragilis is associated with early-stage colorectal neoplasia. PLoS ONE 12(2):e0171602. https://doi.org/10.1371/journal.pone.0171602 PMID: 28151975; PMCID: PMC5289627
doi: 10.1371/journal.pone.0171602
pubmed: 28151975
pmcid: 5289627
Purcell RV, Permain J, Keenan JI (2022) Enterotoxigenic Bacteroides fragilis activates IL-8 expression through Stat3 in colorectal cancer cells. Gut Pathog 14(1):16. https://doi.org/10.1186/s13099-022-00489-x PMID: 35468857; PMCID: PMC9036718
doi: 10.1186/s13099-022-00489-x
pubmed: 35468857
pmcid: 9036718
Abdulla MH, Agarwal D, Singh JK, Traiki TB, Pandey MK, Ahmad R, Srivastava SK (2021) Association of the microbiome with colorectal cancer development (review). Int J Oncol 58(5):17. https://doi.org/10.3892/ijo.2021.5197 Epub 2021 Mar 24. PMID: 33760154
doi: 10.3892/ijo.2021.5197
pubmed: 33760154
Wexler AG, Goodman AL (2017) An insider’s perspective: Bacteroides as a window into the microbiome. Nat Microbiol.;2:17026. https://doi.org/10.1038/nmicrobiol.2017.26 . PMID: 28440278; PMCID: PMC5679392
Moncrief JS, Duncan AJ, Wright RL, Barroso LA, Wilkins TD (1998) Molecular characterization of the fragilysin pathogenicity islet of enterotoxigenic Bacteroides fragilis. Infect Immun 66(4):1735–1739. https://doi.org/10.1128/IAI.66.4.1735-1739.1998 PMID: 9529104; PMCID: PMC108111
doi: 10.1128/IAI.66.4.1735-1739.1998
pubmed: 9529104
pmcid: 108111
Molodecky NA, Soon IS, Rabi DM, Ghali WA, Ferris M, Chernoff G, Benchimol EI, Panaccione R, Ghosh S, Barkema HW, Kaplan GG (2012) Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology 142(1):46–54.e42; quiz e30. https://doi.org/10.1053/j.gastro.2011.10.001
doi: 10.1053/j.gastro.2011.10.001
pubmed: 22001864
Nishida A, Inoue R, Inatomi O, Bamba S, Naito Y, Andoh A (2018) Gut microbiota in the pathogenesis of inflammatory bowel disease. Clin J Gastroenterol 11(1):1–10. https://doi.org/10.1007/s12328-017-0813-5 Epub 2017 Dec 29. PMID: 29285689
doi: 10.1007/s12328-017-0813-5
pubmed: 29285689
Hegazy AN, West NR, Stubbington MJT, Wendt E, Suijker KIM, Datsi A, This S, Danne C, Campion S, Duncan SH, Owens BMJ, Uhlig HH, McMichael A, Oxford IBD, Cohort A, Teichmann SA, Keshav S, Powrie F (2017) Circulating and Tissue-Resident CD4 + T Cells With Reactivity to Intestinal Microbiota Are Abundant in Healthy Individuals and Function Is Altered During Inflammation. Gastroenterology.;153(5):1320–1337.e16. https://doi.org/10.1053/j.gastro.2017.07.047 . Epub 2017 Aug 4. PMID: 28782508; PMCID: PMC5687320
Wang C, Li S, Hong K, Yu L, Tian F, Zhao J et al (2021) The roles of different Bacteroides fragilis strains in protecting against DSS-induced ulcerative colitis and related functional genes. Food Funct. https://doi.org/10.1039/D1FO00875G
doi: 10.1039/D1FO00875G
pubmed: 34860220
Hammer T, Langholz EJDMR. The epidemiology of inflammatory bowel disease: balance between East and West? A narrative review. 2020. 2020;3. doi: https://doi.org/10.21037/dmr-20-149 .
Ahmed I, Roy BC, Khan SA, Septer S, Umar S. Microbiome, Metabolome and Inflammatory Bowel Disease. Microorganisms. 2016 Jun 15;4(2):20. doi: https://doi.org/10.3390/microorganisms4020020 . PMID: 27,681,914; PMCID: PMC5029486.
Zamani S, Taslimi R, Sarabi A, Jasemi S, Sechi LA, Feizabadi MM. Enterotoxigenic Bacteroides fragilis: A Possible Etiological Candidate for Bacterially-Induced Colorectal Precancerous and Cancerous Lesions. Front Cell Infect Microbiol. 2020 Jan 17;9:449. doi: https://doi.org/10.3389/fcimb.2019.00449 . PMID: 32,010,637; PMCID: PMC6978650.
Dewhirst FE, Chen T, Izard J, Paster BJ, Tanner AC, Yu WH, Lakshmanan A, Wade WG. The human oral microbiome. J Bacteriol. 2010 Oct;192(19):5002-17. doi: https://doi.org/10.1128/JB.00542-10 . Epub 2010 Jul 23. PMID: 20,656,903; PMCID: PMC2944498.
Berbisá MÁF, Nielsen KR, Ingham AC, Midjord J, Hammer T, Patursson P, Vest NMO, Gregersen NO, Burisch J, Vang A. Similar Gut Bacterial Composition Between Patients With Ulcerative Colitis and Healthy Controls in a High Incidence Population: A Cross-sectional Study of the Faroe Islands IBD Cohort. Inflamm Bowel Dis. 2022 Jul 1;28(7):1081–1089. doi: https://doi.org/10.1093/ibd/izab355 . PMID: 35,138,361; PMCID: PMC9247847.
Khodaverdi N, Zeighami H, Jalilvand A, Haghi F, Hesami N. High frequency of enterotoxigenic Bacteroides fragilis and Enterococcus faecalis in the paraffin-embedded tissues of Iranian colorectal cancer patients. BMC Cancer. 2021 Dec 22;21(1):1353. doi: https://doi.org/10.1186/s12885-021-09110-x . PMID: 34,937,552; PMCID: PMC8693489.
Wang C, Li S, Hong K, Yu L, Tian F, Zhao J, et al. The roles of different Bacteroides fragilis strains in protecting against DSS-induced ulcerative colitis and related functional genes. Food & Function. 2021;12(18):8300-13. DOI https://doi.org/10.1039/D1FO00875G .
Chung L, Thiele Orberg E, Geis AL, Chan JL, Fu K, DeStefano Shields CE, Dejea CM, Fathi P, Chen J, Finard BB, Tam AJ, McAllister F, Fan H, Wu X, Ganguly S, Lebid A, Metz P, Van Meerbeke SW, Huso DL, Wick EC, Pardoll DM, Wan F, Wu S, Sears CL, Housseau F. Bacteroides fragilis Toxin Coordinates a Pro-carcinogenic Inflammatory Cascade via Targeting of Colonic Epithelial Cells. Cell Host Microbe. 2018 Feb 14;23(2):203–214.e5. doi: https://doi.org/10.1016/j.chom.2018.01.007 . Epub 2018 Feb 1. Erratum in: Cell Host Microbe. 2018 Mar 14;23 (3):421. PMID: 29,398,651; PMCID: PMC5954996.
Geis AL, Fan H, Wu X, Wu S, Huso DL, Wolfe JL, Sears CL, Pardoll DM, Housseau F. Regulatory T-cell Response to Enterotoxigenic Bacteroides fragilis Colonization Triggers IL17-Dependent Colon Carcinogenesis. Cancer Discov. 2015 Oct;5(10):1098 − 109. doi: https://doi.org/10.1158/2159-8290.CD-15-0447 . Epub 2015 Jul 22. PMID: 26,201,900; PMCID: PMC4592451.
Kawasaki M, Ikeda Y, Ikeda E, Takahashi M, Tanaka D, Nakajima Y, Arakawa S, Izumi Y, Miyake S. Oral infectious bacteria in dental plaque and saliva as risk factors in patients with esophageal cancer. Cancer. 2021 Feb 15;127(4):512–519. doi: https://doi.org/10.1002/cncr.33316 . Epub 2020 Nov 6. PMID: 33,156,979.
Slots J, Slots H. Bacterial and viral pathogens in saliva: disease relationship and infectious risk. Periodontol 2000. 2011 Feb;55(1):48–69. doi: https://doi.org/10.1111/j.1600-0757.2010.00361.x . PMID: 21,134,228; PMCID: PMC7159101.
Kitamoto S, Nagao-Kitamoto H, Hein R, Schmidt TM, Kamada N. The Bacterial Connection between the Oral Cavity and the Gut Diseases. J Dent Res. 2020 Aug;99(9):1021–1029. doi: https://doi.org/10.1177/0022034520924633 . Epub 2020 May 28. PMID: 32,464,078; PMCID: PMC7375741.
Basilicata M, Pieri M, Marrone G, Nicolai E, Di Lauro M, Paolino V, Tomassetti F, Vivarini I, Bollero P, Bernardini S, Noce A. Saliva as Biomarker for Oral and Chronic Degenerative Non-Communicable Diseases. Metabolites. 2023 Jul 27;13(8):889. doi: https://doi.org/10.3390/metabo13080889 . PMID: 37,623,833; PMCID: PMC10456419.
Paqué PN, Herz C, Jenzer JS, Wiedemeier DB, Attin T, Bostanci N, Belibasakis GN, Bao K, Körner P, Fritz T, Prinz J, Schmidlin PR, Thurnheer T, Wegehaupt FJ, Mitsakakis K, Peham JR. Microbial Analysis of Saliva to Identify Oral Diseases Using a Point-of-Care Compatible qPCR Assay. J Clin Med. 2020 Sep 11;9(9):2945. doi: https://doi.org/10.3390/jcm9092945 . PMID: 32,933,084; PMCID: PMC7565348.