In Vitro and In Vivo Anti-Clostridioides difficile Effect of a Probiotic Bacillus amyloliquefaciens Strain |
Islam, Md Imtiazul
(Department of Microbiology and Immunology, School of Medicine, Soonchunhyang University)
Seo, Hoonhee (Department of Microbiology and Immunology, School of Medicine, Soonchunhyang University) Redwan, Asma (Department of Microbiology and Immunology, School of Medicine, Soonchunhyang University) Kim, Sukyung (Department of Microbiology and Immunology, School of Medicine, Soonchunhyang University) Lee, Saebim (Department of Microbiology and Immunology, School of Medicine, Soonchunhyang University) Siddiquee, Mashuk (Department of Microbiology and Immunology, School of Medicine, Soonchunhyang University) Song, Ho-Yeon (Department of Microbiology and Immunology, School of Medicine, Soonchunhyang University) |
1 | Johnson S. 2009. Recurrent Clostridium difficile infection: causality and therapeutic approaches. Int. J. Antimicrob. Agents 33 Suppl 1: S33-36. DOI |
2 | Kelly CP. 2012. Can we identify patients at high risk of recurrent Clostridium difficile infection? Clin. Microbiol. Infect. Off. Publ. Eur. Soc. Clin. Microbiol. Infect. Dis. 18 Suppl 6: 21-27. |
3 | Chai J, Lee CH. 2018. Management of primary and recurrent Clostridium difficile infection: an update. Antibiotics 7: 54. DOI |
4 | Abougergi MS, Kwon JH. 2011. Intravenous immunoglobulin for the treatment of Clostridium difficile infection: a review. Dig. Dis. Sci. 56: 19-26. DOI |
5 | Wilcox MH, Gerding DN, Poxton IR, Kelly C, Nathan R, Birch T, et al. 2017. Bezlotoxumab for prevention of recurrent Clostridium difficile infection. N. Engl. J. Med. 376: 305-317. DOI |
6 | Kociolek LK, Gerding DN. 2016. Breakthroughs in the treatment and prevention of Clostridium difficile infection. Nat. Rev. Gastroenterol. Hepatol. 13: 150-160. DOI |
7 | Bartlett JG, Moon N, Chang TW, Taylor N, Onderdonk AB. 1978. Role of Clostridium difficile in antibiotic-associated pseudomembranous colitis. Gastroenterology 75: 778-782. DOI |
8 | de Bruyn G, Saleh J, Workman D, Pollak R, Elinoff V, Fraser NJ, et al. 2016. Defining the optimal formulation and schedule of a candidate toxoid vaccine against Clostridium difficile infection: a randomized Phase 2 clinical trial. Vaccine 34: 2170-2178. DOI |
9 | Sougioultzis S, Kyne L, Drudy D, Keates S, Maroo S, Pothoulakis C, et al. 2005. Clostridium difficile toxoid vaccine in recurrent C. difficile-associated diarrhea. Gastroenterology 128: 764-770. DOI |
10 | Chen XH, Scholz R, Borriss M, Junge H, Mogel G, Kunz S, et al. 2009. Difficidin and bacilysin produced by plant-associated Bacillus amyloliquefaciens are efficient in controlling fire blight disease. J. Biotechnol. 140: 38-44. DOI |
11 | Kotowska M, Albrecht P, Szajewska H. 2005. Saccharomyces boulardii in the prevention of antibiotic-associated diarrhoea in children: a randomized double-blind placebo-controlled trial. Aliment. Pharmacol. Ther. 21: 583-590. DOI |
12 | Marahier MA, Nakano MM, Zuber P. 1993. Regulation of peptide antibiotic production in Bacillus. Mol. Microbiol. 7: 631-636. DOI |
13 | Cho Y-H, Hong S-M, Kim C-H. 2013. Isolation and characterization of lactic acid bacteria from Kimchi, Korean traditional fermented food to apply into fermented dairy products. Food Sci. Anim. Resour. 33: 75-82. DOI |
14 | Rolfe RD. 2000. The role of probiotic cultures in the control of gastrointestinal health. J. Nutr. 130: 396S-402S. DOI |
15 | Stein T. 2005. Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol. Microbiol. 56: 845-857. DOI |
16 | Tamariz-Angeles C, Olivera-Gonzales P, Villena GK, GutiA©rrez-Correa M. 2014. Isolation and identification of cellulolytic and xylanolytic bacteria from huancarhuaz hot spring, Peru. Annu. Res. Rev. Biol. 4: 2920-2930. DOI |
17 | Gao XW, Mubasher M, Fang CY, Reifer C, Miller LE. 2010. Dose-response efficacy of a proprietary probiotic formula of Lactobacillus acidophilus CL1285 and Lactobacillus casei LBC80R for antibiotic-associated diarrhea and Clostridium difficile-associated diarrhea prophylaxis in adult patients. Am. J. Gastroenterol. 105: 1636-1641. DOI |
18 | Shokryazdan P, Faseleh Jahromi M, Liang JB, Kalavathy R, Sieo CC, Ho YW. 2016. Safety assessment of two new Lactobacillus strains as probiotic for human using a rat model. PLoS One 11: e0159851. DOI |
19 | Colomb-Cotinat M, Assouvie L, Durand J, Daniau C, Leon L, Maugat S, et al. 2019. Epidemiology of Clostridioides difficile infections, France, 2010 to 2017. Eurosurveillance 24: 1800638. |
20 | Kotloff KL, Wasserman SS, Losonsky GA, Thomas W, Nichols R, Edelman R, et al. 2001. Safety and immunogenicity of increasing doses of a Clostridium difficile toxoid vaccine administered to healthy adults. Infect. Immun. 69: 988-995. DOI |
21 | Sambol SP, Merrigan MM, Tang JK, Johnson S, Gerding DN. 2002. Colonization for the prevention of Clostridium difficile disease in hamsters. J. Infect. Dis. 186: 1781-1789. DOI |
22 | Benitez L, Correa A, Daroit D, Brandelli A. 2011. Antimicrobial activity of Bacillus amyloliquefaciens LBM 5006 is enhanced in the presence of Escherichia coli. Curr. Microbiol. 62: 1017-1022. DOI |
23 | Benitez LB, Velho RV, Lisboa MP, da Costa Medina LF, Brandelli A. 2010. Isolation and characterization of antifungal peptides produced by Bacillus amyloliquefaciens LBM5006. J. Microbiol. 48: 791-797. DOI |
24 | Abutaleb NS, Seleem MN. 2021. In vivo efficacy of auranofin in a hamster model of Clostridioides difficile infection. Sci. Rep. 11: 7093. DOI |
25 | Hairul Islam VI, Prakash Babu N, Pandikumar P, Ignacimuthu S. 2011. Isolation and characterization of putative probiotic bacterial strain, Bacillus amyloliquefaciens, from north east Himalayan soil based on in vitro and in vivo functional properties. Probiotics Antimicrob. Proteins 3: 175-185. DOI |
26 | Wong JH, Hao J, Cao Z, Qiao M, Xu H, Bai Y, et al. 2008. An antifungal protein from Bacillus amyloliquefaciens. J. Appl. Microbiol. 105: 1888-1898. DOI |
27 | Herlemann DP, Labrenz M, Jurgens K, Bertilsson S, Waniek JJ, Andersson AF. 2011. Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J. 5: 1571-1579. DOI |
28 | Islam MI, Han CM, Seo H, Kim S, Mahmud HA, Nam KW, et al. 2019. In vitro activity of DNF-3 against drug-resistant Mycobacterium tuberculosis. Int. J. Antimicrob. Agents 54: 69-74. DOI |
29 | Ben Ayed H, Nasri R, Jemil N, Ben Amor I, Gargouri J, Hmidet N, et al. 2015. Acute and sub-chronic oral toxicity profiles of lipopeptides from Bacillus mojavensis A21 and evaluation of their in vitro anticoagulant activity. Chem. Biol. Interact. 236: 1-6. DOI |
30 | Ji J, Hu S, Li W. 2013. Probiotic Bacillus amyloliquefaciens SC06 prevents bacterial translocation in weaned mice. Indian J. Microbiol. 53: 323-328. DOI |
31 | Edwards AN, McBride SM. 2016. Isolating and purifying Clostridium difficile spores, pp. 117-128, In Roberts AP, Mullany P (eds.), Clostridium difficile: Methods and Protocols. Springer, New York, NY. USA. |
32 | Lee J-S, Chung M-J, Seo J-G. 2013. In Vitro Evaluation of Antimicrobial activity of lactic acid bacteria against Clostridium difficile. Toxicol. Res. 29: 99-106. DOI |
33 | Wu L, Wu H, Chen L, Yu X, Borriss R, Gao X. 2015. Difficidin and bacilysin from Bacillus amyloliquefaciens FZB42 have antibacterial activity against Xanthomonas oryzae rice pathogens. Sci. Rep. 5: 12975. DOI |
34 | Kim PI, Chung KC. 2006. Production of an antifungal protein for control of Colletotrichum lagenarium by Bacillus amyloliquefaciens MET0908. FEMS Microbiol. Lett. 234: 177-183. DOI |
35 | Borriello SP, Ketley JM, Mitchell TJ, Barclay FE, Welch AR, PRICE AB, et al. Clostridium difficile-a spectrum of virulence and analysis of putative virulence determinants in the hamster model of antibiotic-associated colitis. J. Med. Microbiol. 24: 53-64. DOI |
36 | Trzasko A, Leeds JA, Praestgaard J, LaMarche MJ, McKenney D. 2012. Efficacy of LFF571 in a hamster model of Clostridium difficile infection. Antimicrob. Agents Chemother. 56: 4459-4462. DOI |
37 | Borah T, Gogoi B, Khataniar A, Gogoi M, Das A, Borah D. 2019. Biocatalysis and agricultural biotechnology probiotic characterization of indigenous Bacillus velezensis strain DU14 isolated from Apong, a traditionally fermented rice beer of Assam. Biocatal. Agric. Biotechnol. 18: 101008. DOI |
38 | Monteiro CRAV, do Carmo MS, Melo BO, Alves MS, Dos Santos CI, Monteiro SG, et al. 2019. In Vitro antimicrobial activity and probiotic potential of Bifidobacterium and Lactobacillus against species of Clostridium. Nutrients 11: E448. |
39 | Levy DG, Stergachis A, McFarland LV, Van Vorst K, Graham DJ, Johnson ES, et al. 2000. Antibiotics and Clostridium difficile diarrhea in the ambulatory care setting. Clin. Ther. 22: 91-102. DOI |
40 | Blaabjerg S, Artzi DM, Aabenhus R. 2017. Probiotics for the prevention of antibiotic-associated diarrhea in outpatients-A systematic review and meta-analysis. Antibiotics 6: 21. DOI |
41 | Hu HQ, Li XS, He H. 2010. Characterization of an antimicrobial material from a newly isolated Bacillus amyloliquefaciens from mangrove for biocontrol of Capsicum bacterial wilt. Biol. Control 54: 359-365. DOI |
42 | Geeraerts S, Delezie E, Ducatelle R, Haesebrouck F, Devreese B, Immerseel FV. 2016. Vegetative Bacillus amyloliquefaciens cells do not confer protection against necrotic enteritis in broilers despite high antibacterial activity of its supernatant against Clostridium perfringens in vitro. Br. Poult. Sci. 57: 324-329. DOI |
43 | S Geeraerts, R Ducatelle, F Haesebrouck, F Van Immerseel. 2015. Bacillus amyloliquefaciens as prophylactic treatment for Clostridium difficile-associated disease in a mouse model. J. Gastroenterol. Hepatol. 30: 1275-1280. DOI |
44 | Lessa FC, Mu Y, Bamberg WM, Beldavs ZG, Dumyati GK, Dunn JR, et al. 2015. Burden of Clostridium difficile Infection in the United States. N. Engl. J. Med. 372: 825-834. DOI |
45 | Kato H, Senoh M, Honda H, Fukuda T, Tagashira Y, Horiuchi H, et al. 2019. Clostridioides (Clostridium) difficile infection burden in Japan: a multicenter prospective study. Anaerobe 60: 102011. DOI |
46 | Evans CT, Safdar N. 2015. Current trends in the epidemiology and outcomes of Clostridium difficile infection. Clin. Infect. Dis. 60: S66-S71. DOI |
47 | McDonald LC, Gerding DN, Johnson S, Bakken JS, Carroll KC, Coffin SE, et al. 2018. Clinical practice guidelines for Clostridium difficile infection in adults and children: 2017 update by the Infectious Diseases Society of America (IDSA) and Society for Healthcare Epidemiology of America (SHEA). Clin. Infect. Dis. 66: e1-e48. DOI |
48 | McFarland LV. 1998. Epidemiology, risk factors and treatments for antibiotic-associated diarrhea. Dig. Dis. 16: 292-307. DOI |
49 | Rao K, Young VB. 2015. Fecal microbiota transplantation for the management of Clostridium difficile infection. Infect. Dis. Clin. North Am. 29: 109-122. DOI |
50 | Vyas D, Aekka A, Vyas A. 2015. Fecal transplant policy and legislation. World J. Gastroenterol. WJG 21: 6-11. DOI |
51 | CDC. 2021. Antibiotic-resistant Germs: New Threats. Available from https://www.cdc.gov/drugresistance/biggest-threats.html. Accessed Jul. 25, 2021. |
52 | Curcio D, Cane A, Fernandez FA, Correa J. 2019. Clostridium difficile-associated diarrhea in developing countries: a systematic review and meta-analysis. Infect. Dis. Ther. 8: 87-103. DOI |
53 | Greenberg RN, Marbury TC, Foglia G, Warny M. 2012. Phase I dose finding studies of an adjuvanted Clostridium difficile toxoid vaccine. Vaccine 30: 2245-2249. DOI |
54 | Katz JA. 2006. Probiotics for the prevention of antibiotic-associated diarrhea and Clostridium difficile diarrhea. J. Clin. Gastroenterol. 40: 249-255. DOI |
55 | Basu S, Chatterjee M, Ganguly S, Chandra PK. 2007. Effect of Lactobacillus rhamnosus GG in persistent diarrhea in Indian children: a randomized controlled trial. J. Clin. Gastroenterol. 41: 756-760. DOI |
56 | Khattab RA, Ahmed NA, Ragab YM, Rasmy SA. 2020. Bacteria producing antimicrobials against Clostridium difficile isolated from human stool. Anaerobe 63: 102206. DOI |
57 | Jeon H-L, Lee N-K, Yang S-J, Kim W-S, Paik H-D. 2017. Probiotic characterization of Bacillus subtilis P223 isolated from kimchi. Food Sci. Biotechnol. 26: 1641-1648. DOI |
58 | Karska-Wysocki B, Bazo M, Smoragiewicz W. 2010. Antibacterial activity of Lactobacillus acidophilus and Lactobacillus casei against methicillin-resistant Staphylococcus aureus (MRSA). Microbiol. Res. 165: 674-686. DOI |
59 | DeFilipp Z, Bloom PP, Torres Soto M, Mansour MK, Sater MRA, Huntley MH, et al. 2019. Drug-resistant E. coli bacteremia transmitted by fecal microbiota transplant. N. Engl. J. Med. 381: 2043-2050. DOI |
60 | Cao H, He S, Wei R, Diong M, Lu L. 2011. Bacillus amyloliquefaciens G1: A Potential Antagonistic Bacterium against Eel-Pathogenic Aeromonas hydrophila. Evid.-Based Complement. Altern. Med. ECAM 2011: 824104. |
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