Meta-analysis is a statistical process summarizing comparable data from a number of scientific papers. The use of meta-analysis in microbiology allows decision-making that has an impact on public health policy. It can happen that the primary researches come to different conclusions, although these are targeted with the same research question. It is, therefore, inevitable to have the means to systematically evaluate information and compare research results. Ulcerative colitis together with Crohn's disease are among the two main inflammatory bowel diseases. This chronic disease of the gastrointestinal tract, with an as yet unclear etiology, is presented by an uncontrolled inflammatory immune response in genetically predisposed individuals to as yet undefined environmental factors in interaction with the intestinal microbiota itself. In patients with ulcerative colitis (UC), changes in the composition and relative abundance of microorganisms could be observed. Sulfate-reducing bacteria (SRB), which commonly occur in the large intestine as part of the commensal microbiota of animals and humans involved in the pathogenesis of the disease, have been shown to occur. SRB are anaerobic organisms affecting short-chain fatty acid metabolism. This work outlines the perspectives of the use of meta-analysis for UC and changes in the representation of intestinal organisms in these patients.

Archaea Physiology and Biotechnology Group Department of Functional and Evolutionary Ecology Universität Wien 1090 Vienna Austria

Department of Experimental Biology Faculty of Science Masaryk University 62500 Brno Czech Republic

See more in PubMed

Ahmed I., Niaz Z. Ulcerative Colitis. Epidemiology, Pathogenesis and Complications. IntechOpen; London, UK: 2011. Ulcerative Colitis; pp. 1–12. DOI

Ho G.-T., Boyapati R., Satsangi J. Ulcerative colitis. Medicine. 2015;43:276–281. doi: 10.1016/j.mpmed.2015.02.004. DOI

Kushkevych I., Dordević D., Vítězová M. Toxicity of hydrogen sulfide toward sulfate-reducing bacteria Desulfovibrio piger Vib-7. Arch. Microbiol. 2019;201:389–397. doi: 10.1007/s00203-019-01625-z. PubMed DOI

Kushkevych I., Kotrsová V., Dordević D., Buňková L., Vítězová M., Amedei A. Hydrogen Sulfide Effects on the Survival of Lactobacilli with Emphasis on the Development of Inflammatory Bowel Diseases. Biomolecules. 2019;9:752. doi: 10.3390/biom9120752. PubMed DOI PMC

Vilela E.G. Evaluation of inflammatory activity in Crohn’s disease and ulcerative colitis. WJG. 2012;18:872. doi: 10.3748/wjg.v18.i9.872. PubMed DOI PMC

Gibson G.R., Macfarlane S., Macfarlane G.T. Metabolic interactions involving sulphate-reducing and methanogenic bacteria in the human large intestine. FEMS Microbiol. Ecol. 1993;12:117–125. doi: 10.1111/j.1574-6941.1993.tb00023.x. DOI

Cummings J.H., Macfarlane G.T. Colonic microflora: Nutrition and health. Nutrition. 1997;13:476–478. doi: 10.1016/S0899-9007(97)00114-7. PubMed DOI

Cummings J.H., Macfarlane G.T., Macfarlane S. Intestinal bacteria and ulcerative colitis. Curr. Issues Intestig. Microbiol. 2003;4:9–20. PubMed

Malik T.A. Inflammatory Bowel Disease. Surg. Clin. N. Am. 2015;95:1105–1122. doi: 10.1016/j.suc.2015.07.006. PubMed DOI

Gibson G.R., Cummings J.H., Macfarlane G.T. Growth and activities of sulphate-reducing bacteria in gut contents of healthy subjects and patients with ulcerative colitis. FEMS Microbiol. Lett. 1991;86:103–112. doi: 10.1111/j.1574-6968.1991.tb04799.x. DOI

Kushkevych I.V. Kinetic Properties of Pyruvate Ferredoxin Oxidoreductase of Intestinal Sulfate-Reducing Bacteria Desulfovibrio piger Vib-7 and Desulfomicrobium sp. Rod-9. Pol. J. Microbiol. 2015;64:107–114. doi: 10.33073/pjm-2015-016. PubMed DOI

Kushkevych I.V. Activity and kinetic properties of phosphotransacetylase from intestinal sulfate-reducing bacteria. Acta Biochim. Pol. 2015;62:103–108. doi: 10.18388/abp.2014_845. PubMed DOI

Kushkevych I. Isolation and Purification of Sulfate-Reducing Bacteria. In: Blumenberg M., Shaaban M., Elgaml A., editors. Microorganisms. IntechOpen; London, UK: 2020.

Kushkevych I., Kollar P., Suchy P., Parak T., Pauk K., Imramovsky A. Activity of selected salicylamides against intestinal sulfate-reducing bacteria. Neuro Endocrinol. Lett. 2015;36(Suppl. 1):106–113. PubMed

Kushkevych I., Fafula R., Parák T., Bartoš M. Activity of Na+/K+-activated Mg2+-dependent ATP-hydrolase in the cell-free extracts of the sulfate-reducing bacteria Desulfovibrio piger Vib-7 and Desulfomicrobium sp. Rod-9. Acta Vet. Brno. 2015;84:3–12. doi: 10.2754/avb201585010003. DOI

Kushkevych I., Kováč J., Vítězová M., Vítěz T., Bartoš M. The diversity of sulfate-reducing bacteria in the seven bioreactors. Arch. Microbiol. 2018;200:945–950. doi: 10.1007/s00203-018-1510-6. PubMed DOI

Pitcher M.C., Cummings J.H. Hydrogen sulphide: A bacterial toxin in ulcerative colitis? Gut. 1996;39:1–4. doi: 10.1136/gut.39.1.1. PubMed DOI PMC

Yuan Y., Hunt R.H. Systematic Reviews: The Good, the Bad and the Ugly. Am. J. Gastroenterol. 2009;104:1086–1092. doi: 10.1038/ajg.2009.118. PubMed DOI

Ergal İ., Fuchs W., Hasibar B., Thallinger B., Bochmann G., Rittmann S.K.-M.R. The physiology and biotechnology of dark fermentative biohydrogen production. Biotechnol. Adv. 2018;36:2165–2186. doi: 10.1016/j.biotechadv.2018.10.005. PubMed DOI

Rittmann S.K.-M.R., Seifert A.H., Bernacchi S. Kinetics, multivariate statistical modelling, and physiology of CO2-based biological methane production. Appl. Energy. 2018;216:751–760. doi: 10.1016/j.apenergy.2018.01.075. DOI

Dordević D., Jančíková S., Vítězová M., Kushkevych I. Hydrogen sulfide toxicity in the gut environment: Meta-analysis of sulfate-reducing and lactic acid bacteria in inflammatory processes. J. Adv. Res. 2020;27:55–69. doi: 10.1016/j.jare.2020.03.003. PubMed DOI PMC

Kushkevych I., Dordević D., Kollár P. Analysis of physiological parameters of Desulfovibrio strains from individuals with colitis. Open Life Sci. 2019;13:481–488. doi: 10.1515/biol-2018-0057. PubMed DOI PMC

Kováč J., Vítězová M., Kushkevych I. Metabolic activity of sulfate-reducing bacteria from rodents with colitis. Open Med. 2018;13:344–349. doi: 10.1515/med-2018-0052. PubMed DOI PMC

Kushkevych I., Vítězová M., Kos J., Kollár P., Jampílek J. Effect of selected 8-hydroxyquinoline-2-carboxanilides on viability and sulfate metabolism of Desulfovibrio piger. J. Appl. Biomed. 2018;16:241–246. doi: 10.1016/j.jab.2018.01.004. DOI

Kushkevych I., Dordević D., Vítězová M. Analysis of pH dose-dependent growth of sulfate-reducing bacteria. Open Med. 2019;14:66–74. doi: 10.1515/med-2019-0010. PubMed DOI PMC

Kushkevych I., Castro Sangrador J., Dordević D., Rozehnalová M., Černý M., Fafula R., Vítězová M., Rittmann S.K.-M.R. Evaluation of Physiological Parameters of Intestinal Sulfate-Reducing Bacteria Isolated from Patients Suffering from IBD and Healthy People. JCM. 2020;9:1920. doi: 10.3390/jcm9061920. PubMed DOI PMC

Kushkevych I., Dordević D., Vítězová M. Possible synergy effect of hydrogen sulfide and acetate produced by sulfate-reducing bacteria on inflammatory bowel disease development. J. Adv. Res. 2020;27:71–78. doi: 10.1016/j.jare.2020.03.007. PubMed DOI PMC

Stange E.F. Inflammatory bowel diseases. Preface. Dig. Dis. 2013;31:269. doi: 10.1159/000354674. PubMed DOI

Boyapati R.K., Rossi A.G., Satsangi J., Ho G.-T. Gut mucosal DAMPs in IBD: From mechanisms to therapeutic implications. Mucosal. Immunol. 2016;9:567–582. doi: 10.1038/mi.2016.14. PubMed DOI

Head K., Jurenka J.S. Inflammatory bowel disease. Part II: Crohn’s disease--pathophysiology and conventional and alternative treatment options. Altern. Med. Rev. 2004;9:360–401. PubMed

Ek W.E., D’Amato M., Halfvarson J. The history of genetics in inflammatory bowel disease. Ann. Gastroenterol. 2014;27:294–303. PubMed PMC

Boirivant M., Cossu A. Inflammatory bowel disease: Inflammatory bowel disease. Oral Dis. 2012;18:1–15. doi: 10.1111/j.1601-0825.2011.01811.x. PubMed DOI

Juyal G., Sood A., Midha V., Thelma B.K. Genetics of ulcerative colitis: Putting into perspective the incremental gains from Indian studies. J. Genet. 2018;97:1493–1507. doi: 10.1007/s12041-018-1015-8. PubMed DOI

Molodecky N.A., Kaplan G.G. Environmental risk factors for inflammatory bowel disease. Gastroenterol. Hepatol. (N. Y.) 2010;6:339–346. PubMed PMC

Koloski N.-A., Bret L., Radford-Smith G. Hygiene hypothesis in inflammatory bowel disease: A critical review of the literature. World J. Gastroenterol. 2008;14:165–173. doi: 10.3748/wjg.14.165. PubMed DOI PMC

Sonnenberg A. Occupational distribution of inflammatory bowel disease among German employees. Gut. 1990;31:1037–1040. doi: 10.1136/gut.31.9.1037. PubMed DOI PMC

Macfarlane M.J., Hopkins G.T., Ma S. Bacterial Growth and Metabolism on Surfaces in the Large Intestine. Microb. Ecol. Health Dis. 2000;12:64–72. doi: 10.3402/mehd.v12i2.8103. DOI

Macfarlane S., Steed H., Macfarlane G.T. Intestinal bacteria and inflammatory bowel disease. Crit. Rev. Clin. Lab. Sci. 2009;46:25–54. doi: 10.1080/10408360802485792. PubMed DOI

Savage D.C. Microbial Ecology of the Gastrointestinal Tract. Annu. Rev. Microbiol. 1977;31:107–133. doi: 10.1146/annurev.mi.31.100177.000543. PubMed DOI

Carbonnel F., Jantchou P., Monnet E., Cosnes J. Environmental risk factors in Crohn’s disease and ulcerative colitis: An update. Gastroenterol. Clin. ET Biol. 2009;33:S145–S157. doi: 10.1016/S0399-8320(09)73150-1. PubMed DOI

Campieri M. Bacteria as the cause of ulcerative colitis. Gut. 2001;48:132–135. doi: 10.1136/gut.48.1.132. PubMed DOI PMC

Sands B.E. Inflammatory bowel disease: Past, present, and future. J. Gastroenterol. 2007;42:16–25. doi: 10.1007/s00535-006-1995-7. PubMed DOI PMC

Clavel T., Haller D. Bacteria- and host-derived mechanisms to control intestinal epithelial cell homeostasis: Implications for chronic inflammation: Inflamm. Bowel Dis. 2007;13:1153–1164. doi: 10.1002/ibd.20174. PubMed DOI

Ng S.C., Shi H.Y., Hamidi N., Underwood F., Tang W., Benchimol E., Panaccione R., Ghosh S., Wu J., Chan F., et al. Evolving Trends in the Epidemiology of IBD in the 21st Century: A Systematic Review of Population-Based Studies: 594. Am. J. Gastroenterol. 2017;112:S319–S320. doi: 10.1038/ajg.2017.303. PubMed DOI

Sánchez de Medina F., Romero-Calvo I., Mascaraque C., Martínez-Augustin O. Intestinal Inflammation and Mucosal Barrier Function: Inflamm. Bowel Dis. 2014;20:2394–2404. doi: 10.1097/MIB.0000000000000204. PubMed DOI

Guarner F., Malagelada J.-R. Role of bacteria in experimental colitis. Best Pract. Res. Clin. Gastroenterol. 2003;17:793–804. doi: 10.1016/S1521-6918(03)00068-4. PubMed DOI

Li X., Bi Y. How Many Human and Bacteria Cells Are in the Human Body? Infect. Dis. Transl. Med. 2017:1–2. doi: 10.11979/idtm.201701001. DOI

Pushpanathan P., Mathew G., Selvarajan S., Seshadri K., Srikanth P. Gut microbiota and its mysteries. Indian J. Med. Microbiol. 2019;37:268. doi: 10.4103/ijmm.IJMM_19_373. PubMed DOI

Ziemer C.J. Newly Cultured Bacteria with Broad Diversity Isolated from Eight-Week Continuous Culture Enrichments of Cow Feces on Complex Polysaccharides. Appl. Environ. Microbiol. 2014;80:574–585. doi: 10.1128/AEM.03016-13. PubMed DOI PMC

Schroeder B.O. Fight them or feed them: How the intestinal mucus layer manages the gut microbiota. Gastroenterol. Rep. 2019;7:3–12. doi: 10.1093/gastro/goy052. PubMed DOI PMC

Johansson M.E.V., Gustafsson J.K., Holmén-Larsson J., Jabbar K.S., Xia L., Xu H., Ghishan F.K., Carvalho F.A., Gewirtz A.T., Sjövall H., et al. Bacteria penetrate the normally impenetrable inner colon mucus layer in both murine colitis models and patients with ulcerative colitis. Gut. 2014;63:281–291. doi: 10.1136/gutjnl-2012-303207. PubMed DOI PMC

Cummings J.H. Short chain fatty acids in the human colon. Gut. 1981;22:763–779. doi: 10.1136/gut.22.9.763. PubMed DOI PMC

Rowland I., Gibson G., Heinken A., Scott K., Swann J., Thiele I., Tuohy K. Gut microbiota functions: Metabolism of nutrients and other food components. Eur. J. Nutr. 2018;57:1–24. doi: 10.1007/s00394-017-1445-8. PubMed DOI PMC

Couto M.R., Gonçalves P., Magro F., Martel F. Microbiota-derived butyrate regulates intestinal inflammation: Focus on inflammatory bowel disease. Pharmacol. Res. 2020;159:104947. doi: 10.1016/j.phrs.2020.104947. PubMed DOI

Mauerhofer L.-M., Pappenreiter P., Paulik C., Seifert A.H., Bernacchi S., Rittmann S.K.-M.R. Methods for quantification of growth and productivity in anaerobic microbiology and biotechnology. Folia Microbiol. 2019;64:321–360. doi: 10.1007/s12223-018-0658-4. PubMed DOI PMC

Roy C.C., Kien C.L., Bouthillier L., Levy E. Short-Chain Fatty Acids: Ready for Prime Time? Nutr. Clin. Pract. 2006;21:351–366. doi: 10.1177/0115426506021004351. PubMed DOI

Treem W.R., Ahsan N., Shoup M., Hyams J.S. Fecal short-chain fatty acids in children with inflammatory bowel disease. J. Pediatr. Gastroenterol. Nutr. 1994;18:159–164. doi: 10.1097/00005176-199402000-00007. PubMed DOI

Hill M.J. Intestinal flora and endogenous vitamin synthesis. Eur. J. Cancer Prev. 1997;6:S43–S45. doi: 10.1097/00008469-199703001-00009. PubMed DOI

Martens H., Barg M., Warren D., Jah J.-H. Microbial production of vitamin B 12. Appl. Microbiol. Biotechnol. 2002;58:275–285. doi: 10.1007/s00253-001-0902-7. PubMed DOI

Tremaroli V., Bäckhed F. Functional interactions between the gut microbiota and host metabolism. Nature. 2012;489:242–249. doi: 10.1038/nature11552. PubMed DOI

Duncan S.H., Holtrop G., Lobley G.E., Calder A.G., Stewart C.S., Flint H.J. Contribution of acetate to butyrate formation by human faecal bacteria. Br. J. Nutr. 2004;91:915–923. doi: 10.1079/BJN20041150. PubMed DOI

Gonçalves P., Martel F. Butyrate and Colorectal Cancer: The Role of Butyrate Transport. CDM. 2013;14:994–1008. doi: 10.2174/1389200211314090006. PubMed DOI

LeBlanc J.G., Chain F., Martín R., Bermúdez-Humarán L.G., Courau S., Langella P. Beneficial effects on host energy metabolism of short-chain fatty acids and vitamins produced by commensal and probiotic bacteria. Microb. Cell Fact. 2017;16:79. doi: 10.1186/s12934-017-0691-z. PubMed DOI PMC

Oliphant K., Allen-Vercoe E. Macronutrient metabolism by the human gut microbiome: Major fermentation by-products and their impact on host health. Microbiome. 2019;7:91. doi: 10.1186/s40168-019-0704-8. PubMed DOI PMC

Clausen M.R., Mortensen P.B. Kinetic studies on colonocyte metabolism of short chain fatty acids and glucose in ulcerative colitis. Gut. 1995;37:684–689. doi: 10.1136/gut.37.5.684. PubMed DOI PMC

Moeinian M. Beneficial effect of butyrate, Lactobacillus casei and L-carnitine combination in preference to each in experimental colitis. WJG. 2014;20:10876. doi: 10.3748/wjg.v20.i31.10876. PubMed DOI PMC

den Besten G., Lange K., Havinga R., van Dijk T.H., Gerding A., van Eunen K., Müller M., Groen A.K., Hooiveld G.J., Bakker B.M., et al. Gut-derived short-chain fatty acids are vividly assimilated into host carbohydrates and lipids. Am. J. Physiol. Gastrointest. Liver Physiol. 2013;305:G900–G910. doi: 10.1152/ajpgi.00265.2013. PubMed DOI

Al-Asmakh M., Anuar F., Zadjali F., Rafter J., Pettersson S. Gut microbial communities modulating brain development and function. Gut Microbes. 2012;3:366–373. doi: 10.4161/gmic.21287. PubMed DOI PMC

De Vadder F., Kovatcheva-Datchary P., Goncalves D., Vinera J., Zitoun C., Duchampt A., Bäckhed F., Mithieux G. Microbiota-Generated Metabolites Promote Metabolic Benefits via Gut-Brain Neural Circuits. Cell. 2014;156:84–96. doi: 10.1016/j.cell.2013.12.016. PubMed DOI

Abdel Azim A., Rittmann S.K.-M.R., Fino D., Bochmann G. The physiological effect of heavy metals and volatile fatty acids on Methanococcus maripaludis S2. Biotechnol. Biofuels. 2018;11:301. doi: 10.1186/s13068-018-1302-x. PubMed DOI PMC

Frost G., Sleeth M.L., Sahuri-Arisoylu M., Lizarbe B., Cerdan S., Brody L., Anastasovska J., Ghourab S., Hankir M., Zhang S., et al. The short-chain fatty acid acetate reduces appetite via a central homeostatic mechanism. Nat. Commun. 2014;5:3611. doi: 10.1038/ncomms4611. PubMed DOI PMC

Louis P., Flint H.J. Formation of propionate and butyrate by the human colonic microbiota. Environ. Microbiol. 2017;19:29–41. doi: 10.1111/1462-2920.13589. PubMed DOI

Levitt M.D., Bond J.H. Volume, composition, and source of intestinal gas. Gastroenterology. 1970;59:921–929. doi: 10.1016/S0016-5085(19)33654-6. PubMed DOI

Figliuolo V.R., Coutinho-Silva R., Coutinho C.M.L.M. Contribution of sulfate-reducing bacteria to homeostasis disruption during intestinal inflammation. Life Sci. 2018;215:145–151. doi: 10.1016/j.lfs.2018.11.009. PubMed DOI

Christl S.U., Murgatroyd P.R., Gibson G.R., Cummings J.H. Production, metabolism, and excretion of hydrogen in the large intestine. Gastroenterology. 1992;102:1269–1277. doi: 10.1016/0016-5085(92)90765-Q. PubMed DOI

Wolf P.G., Biswas A., Morales S.E., Greening C., Gaskins H.R. H2 metabolism is widespread and diverse among human colonic microbes. Gut Microbes. 2016;7:235–245. doi: 10.1080/19490976.2016.1182288. PubMed DOI PMC

Florin T.H.J., Neale G., Goretski S., Cummings J.H. The Sulfate Content of Foods and Beverages. J. Food Compos. Anal. 1993;6:140–151. doi: 10.1006/jfca.1993.1016. DOI

Suarez F., Furne J., Springfield J., Levitt M. Insights into human colonic physiology obtained from the study of flatus composition. Am. J. Physiol. 1997;272:G1028–G1033. doi: 10.1152/ajpgi.1997.272.5.G1028. PubMed DOI

Postgate J. The Suphate-Reducing Bacteria. 2nd ed. Volume 1984 Cambridge University; Cambridge, UK: 1984.

Kushkevych I.V. Dissimilatory sulfate reduction in the intestinal sulfate-reducing bacteria. Biol. Stud. 2016;10:197–228. doi: 10.30970/sbi.1001.560. DOI

Kushkevych I., Vítězová M., Vítěz T., Kováč J., Kaucká P., Jesionek W., Bartoš M., Barton L. A new combination of substrates: Biogas production and diversity of the methanogenic microorganisms. Open Life Sci. 2018;13:119–128. doi: 10.1515/biol-2018-0017. PubMed DOI PMC

Kushkevych I., Leščanová O., Dordević D., Jančíková S., Hošek J., Vítězová M., Buňková L., Drago L. The Sulfate-Reducing Microbial Communities and Meta-Analysis of Their Occurrence during Diseases of Small–Large Intestine Axis. JCM. 2019;8:1656. doi: 10.3390/jcm8101656. PubMed DOI PMC

Černý M., Vítězová M., Vítěz T., Bartoš M., Kushkevych I. Variation in the Distribution of Hydrogen Producers from the Clostridiales Order in Biogas Reactors Depending on Different Input Substrates. Energies. 2018;11:3270. doi: 10.3390/en11123270. DOI

Kovac J., Kushkevych I. New modification of cultivation medium for isolation and growth of intestinal sulfate-reducing bacteria; Proceedings of the MendelNet 2017, Faculty of AgriSciences, Mendel University in Brno; Brno, Czech Republic. 8–9 November 2017; pp. 702–707.

Abdulina D., Kováč J., Iutynska G., Kushkevych I. ATP sulfurylase activity of sulfate-reducing bacteria from various ecotopes. 3 Biotech. 2020;10:55. doi: 10.1007/s13205-019-2041-9. PubMed DOI PMC

Kushkevych I., Dordević D., Kollar P., Vítězová M., Drago L. Hydrogen Sulfide as a Toxic Product in the Small–Large Intestine Axis and its Role in IBD Development. JCM. 2019;8:1054. doi: 10.3390/jcm8071054. PubMed DOI PMC

Loubinoux J., Valente F.M.A., Pereira I.A.C., Costa A., Grimont P.A.D., Le Faou A.E. Reclassification of the only species of the genus Desulfomonas, Desulfomonas pigra, as Desulfovibrio piger comb. nov. Int. J. Syst. Evol. Microbiol. 2002;52:1305–1308. doi: 10.1099/00207713-52-4-1305. PubMed DOI

Kushkevych I., Dordević D., Vítězová M., Kollár P. Cross-correlation analysis of the Desulfovibrio growth parameters of intestinal species isolated from people with colitis. Biologia. 2018;73:1137–1143. doi: 10.2478/s11756-018-0118-2. DOI

Kushkevych I., Coufalová M., Vítězová M., Rittmann S.K.-M.R. Sulfate-Reducing Bacteria of the Oral Cavity and Their Relation with Periodontitis—Recent Advances. JCM. 2020;9:2347. doi: 10.3390/jcm9082347. PubMed DOI PMC

Barton L.L., Fardeau M.-L., Fauque G.D. Hydrogen sulfide: A toxic gas produced by dissimilatory sulfate and sulfur reduction and consumed by microbial oxidation. Met. Ions Life Sci. 2014;14:237–277. doi: 10.1007/978-94-017-9269-1_10. PubMed DOI

Brenner D.J., Krieg N.R., Staley J.T., Garrity G.M. Bergey’s Manual of Systematic Bacteriology. Volume 2005. Springer; Boston, MA, USA: 2010. The Proteobacteria, Part C: The Alpha-, Beta-, Delta-, and Epsilonproteobacteria; p. 1388.

Glass G.V. Primary, Secondary, and Meta-Analysis of Research. Educ. Res. 1976;5:3–8. doi: 10.3102/0013189X005010003. DOI

Liberati A., Altman D.G., Tetzlaff J., Mulrow C., Gøtzsche P.C., Ioannidis J.P.A., Clarke M., Devereaux P.J., Kleijnen J., Moher D. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: Explanation and elaboration. BMJ. 2009;339:b2700. doi: 10.1136/bmj.b2700. PubMed DOI PMC

Pabalan N., Jarjanazi H., Steiner T.S. Meta-analysis in microbiology. Indian J. Med. Microbiol. 2014;32:229–235. doi: 10.4103/0255-0857.136547. PubMed DOI

Haidich A.B. Meta-analysis in medical research. Hippokratia. 2010;14:29–37. PubMed PMC

Goodman C.S. Introduction to Health Technology Assessment. National Library of Medicine; Rockville, MD, USA: 2014.

Kushkevych I., Vítězová M., Fedrová P., Vochyanová Z., Paráková L., Hošek J. Kinetic properties of growth of intestinal sulphate-reducing bacteria isolated from healthy mice and mice with ulcerative colitis. Acta Vet. Brno. 2017;86:405–411. doi: 10.2754/avb201786040405. DOI

Ishikawa H., Akedo I., Umesaki Y., Tanaka R., Imaoka A., Otani T. Randomized Controlled Trial of the Effect of Bifidobacteria-Fermented Milk on Ulcerative Colitis. J. Am. Coll. Nutr. 2003;22:56–63. doi: 10.1080/07315724.2003.10719276. PubMed DOI

Miele E., Pascarella F., Giannetti E., Quaglietta L., Baldassano R.N., Staiano A. Effect of a Probiotic Preparation (VSL#3) on Induction and Maintenance of Remission in Children with Ulcerative Colitis. Am. J. Gastroenterol. 2009;104:437–443. doi: 10.1038/ajg.2008.118. PubMed DOI

Sood A., Midha V., Makharia G.K., Ahuja V., Singal D., Goswami P., Tandon R.K. The Probiotic Preparation, VSL#3 Induces Remission in Patients with Mild-to-Moderately Active Ulcerative Colitis. Clin. Gastroenterol. Hepatol. 2009;7:1202–1209.e1. doi: 10.1016/j.cgh.2009.07.016. PubMed DOI

Rembacken B., Snelling A., Hawkey P., Chalmers D., Axon A. Non-pathogenic Escherichia coli versus mesalazine for the treatment of ulcerative colitis: A randomised trial. Lancet. 1999;354:635–639. doi: 10.1016/S0140-6736(98)06343-0. PubMed DOI

Fratila O.C., Craciun C. Ultrastructural evidence of mucosal healing after infliximab in patients with ulcerative colitis. J. Gastrointest. Liver Dis. 2010;19:147–153. PubMed

Ungar B., Mazor Y., Weisshof R., Yanai H., Ron Y., Goren I., Waizbard A., Yavzori M., Fudim E., Picard O., et al. Induction infliximab levels among patients with acute severe ulcerative colitis compared with patients with moderately severe ulcerative colitis. Aliment. Pharm. 2016;43:1293–1299. doi: 10.1111/apt.13631. PubMed DOI

Guo C., Wu K., Liang X., Liang Y., Li R. Infliximab clinically treating ulcerative colitis: A systematic review and meta-analysis. Pharmacol. Res. 2019;148:104455. doi: 10.1016/j.phrs.2019.104455. PubMed DOI

Dinesen L.C., Walsh A.J., Protic M.N., Heap G., Cummings F., Warren B.F., George B., Mortensen N.J.M., Travis S.P.L. The pattern and outcome of acute severe colitis. J. Crohns Colitis. 2010;4:431–437. doi: 10.1016/j.crohns.2010.02.001. PubMed DOI

Roberts S.E., Williams J.G., Yeates D., Goldacre M.J. Mortality in patients with and without colectomy admitted to hospital for ulcerative colitis and Crohn’s disease: Record linkage studies. BMJ. 2007;335:1033. doi: 10.1136/bmj.39345.714039.55. PubMed DOI PMC

Ananthakrishnan A.N., McGinley E.L., Saeian K., Binion D.G. Temporal trends in disease outcomes related to Clostridium difficile infection in patients with inflammatory bowel disease: Inflamm. Bowel Dis. 2011;17:976–983. doi: 10.1002/ibd.21457. PubMed DOI

Ran Z.-H., Shen J., Zhu Q., Peng J.-C. The impact of Clostridum difficile on surgical rate among ulcerative colitis patients: A systemic review and meta-analysis. Saudi J. Gastroenterol. 2015;21:208. doi: 10.4103/1319-3767.161644. PubMed DOI PMC