Evaluating the antibacterial, antibiofilm, and anti-toxigenic effects of postbiotics from lactic acid bacteria on Clostridium difficile
Abstract
Background and Objectives: The most common cause of healthcare-associated diarrhea is Clostridium difficile infection (CDI), which causes severe and recurring symptoms. The increase of antibiotic-resistant C. difficile requires alternate treatments. Postbiotics, metabolites produced by probiotics, fight CDI owing to their antibacterial capabilities. This study aims to evaluate the antibacterial, antibiofilm, and anti-toxigenic potential of postbiotics in combating CDI.
Materials and Methods: GC-MS evaluated postbiotics from Bifidobacterium bifidum and Lactobacillus plantarum. Disk diffusion and broth microdilution determined C. difficile antibacterial inhibition zones and MICs. Microtiter plates assessed antibiofilm activity. MTT assay evaluated postbiotics anti-viability on HEK293. ELISA testing postbiotic detoxification of toxins A and B. Postbiotics were examined for tcdA and tcdB genes expression using real-time PCR.
Results: The most identified B. bifidum and L. plantarum postbiotic compounds were glycolic acid (7.2%) and butyric acid (13.57%). B. bifidum and L. plantarum displayed 13 and 10 mm inhibition zones and 2.5 and 5 mg/ml MICs against C. difficile. B. bifidum reduced biofilm at 1.25 mg/ml by 49% and L. plantarum by 31%. MTT assay showed both postbiotics had little influence on cell viability, which was over 80%. The detoxification power of postbiotics revealed that B. bifidum decreased toxin A and B production more effectively than L. plantarum, and also their related tcdA and tcdB genes expression reduction were statistically significant (p < 0.05).
Conclusion: Postbiotics' ability to inhibit bacterial growth, biofilm disruption, and toxin reduction makes them a promising adjunctive for CDI treatment and a good solution to pathogens' antibiotic resistance.
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3. Ofosu A. Clostridium difficile infection: a review of current and emerging therapies. Ann Gastroenterol 2016; 29: 147-154.
4. Marra AR, Perencevich EN, Nelson RE, Samore M, Khader K, Chiang H-Y, et al. Incidence and outcomes associated with Clostridium difficile infections: a systematic review and meta-analysis. JAMA Netw Open 2020; 3(1): e1917597.
5. Skinner AM, Phillips ST, Merrigan MM, O’leary KJ, Sambol SP, Siddiqui F, et al. The relative role of toxins A and B in the virulence of Clotridioides difficile. J Clin Med 2020; 10: 96.
6. Kuehne SA, Cartman ST, Minton NP. Both, toxin A and toxin B, are important in Clostridium difficile infection. Gut Microbes 2011; 2: 252-255.
7. Kodori M, Ghalavand Z, Yadegar A, Eslami G, Azimirad M, Krutova M, et al. Molecular characterization of pathogenicity locus (PaLoc) and tcdC genetic diversity among tcdA+ B+ Clostridioides difficile clinical isolates in Tehran, Iran. Anaerobe 2020; 66: 102294.
8. Landenberger M, Nieland J, Roeder M, Nørgaard K, Papatheodorou P, Ernst K, et al. The cytotoxic effect of Clostridioides difficile pore-forming toxin CDTb. Biochim Biophys Acta Biomembr 2021; 1863: 183603.
9. Alhobayb T, Ciorba MA. Clostridium difficile in inflammatory bowel disease. Curr Opin Gastroenterol 2023; 39: 257-262.
10. Kunika, Frey N, Rangrez AY. Exploring the involvement of gut microbiota in cancer therapy-induced cardiotoxicity. Int J Mol Sci 2023; 24: 7261.
11. Bassotti G, Fruganti A, Stracci F, Marconi P, Fettucciari K. Cytotoxic synergism of Clostridioides difficile toxin B with proinflammatory cytokines in subjects with inflammatory bowel diseases. World J Gastroenterol 2023; 29: 582-596.
12. Chumbler NM, Rutherford SA, Zhang Z, Farrow MA, Lisher JP, Farquhar E, et al. Crystal structure of Clostridium difficile toxin A. Nat Microbiol 2016; 1: 15002.
13. Ozma MA, Khodadadi E, Pakdel F, Kamounah FS, Yousefi M, Yousefi B, et al. Baicalin, a natural antimicrobial and anti-biofilm agent. J Herb Med 2021; 27: 100432.
14. Spigaglia P. Recent advances in the understanding of antibiotic resistance in Clostridium difficile infection. Ther Adv Infect Dis 2016; 3: 23-42.
15. Dureja C, Olaitan AO, Hurdle JG. Mechanisms and impact of antimicrobial resistance in Clostridioides difficile. Curr Opin Microbiol 2022; 66: 63-72.
16. Ozma MA, Abbasi A, Asgharzadeh M, Pagliano P, Guarino A, Köse Ş, et al. Antibiotic therapy for pan-drug-resistant infections. Infez Med 2022; 30: 525-531.
17. Sabahi S, Homayouni Rad A, Aghebati-Maleki L, Sangtarash N, Ozma MA, Karimi A, et al. Postbiotics as the new frontier in food and pharmaceutical research. Crit Rev Food Sci Nutr 2023; 63: 8375-8402.
18. Mirzaei R, Kavyani B, Nabizadeh E, Kadkhoda H, Asghari Ozma M, Abdi M. Microbiota metabolites in the female reproductive system: Focused on the short-chain fatty acids. Heliyon 2023; 9(3): e14562.
19. Ozma MA, Abbasi A, Akrami S, Lahouty M, Shahbazi N, Ganbarov K, et al. Postbiotics as the key mediators of the gut microbiota-host interactions. Infez Med 2022; 30: 180-193.
20. Gopalan S, Ganapathy S, Mitra M, Neha, Kumar Joshi D, Veligandla KC, et al. Unique properties of yeast probiotic Saccharomyces boulardii CNCM I-745: A narrative review. Cureus 2023; 15(10): e46314.
21. Ghotaslou R, Nabizadeh E, Memar MY, Law WMH, Ozma MA, Abdi M, et al. The metabolic, protective, and immune functions of Akkermansia muciniphila. Microbiol Res 2023; 266: 127245.
22. Valdés-Varela L, Gueimonde M, Ruas-Madiedo P. Probiotics for prevention and treatment of Clostridium difficile infection. Adv Exp Med Biol 2018; 1050: 161-176.
23. Ozma MA, Moaddab SR, Hosseini H, Khodadadi E, Ghotaslou R, Asgharzadeh M, et al. A critical review of novel antibiotic resistance prevention approaches with a focus on postbiotics. Crit Rev Food Sci Nutr 2023; 1-19.
24. Vasilescu I-M, Chifiriuc M-C, Pircalabioru GG, Filip R, Bolocan A, Lazăr V, et al. Gut dysbiosis and Clostridioides difficile infection in neonates and adults. Front Microbiol 2022; 12: 651081.
25. Panpetch W, Phuengmaung P, Cheibchalard T, Somboonna N, Leelahavanichkul A, Tumwasorn S. Lacticaseibacillus casei strain T21 attenuates Clostridioides difficile infection in a murine model through reduction of inflammation and gut dysbiosis with decreased toxin lethality and enhanced mucin production. Front Microbiol 2021; 12: 745299.
26. Saadat YR, Gargari BP, Shahabi A, Nami Y, Khosroushahi AY. Prophylactic role of Lactobacillus Paracasei exopolysaccharides on colon cancer cells through apoptosis not ferroptosis. Pharm Sci 2021; 27: 251-261.
27. Ozma MA, Abbasi A, Sabahi S. Characterization of postbiotics derived from Lactobacillus paracasei ATCC 55544 and its application in Malva sylvestris seed mucilage edible coating to the improvement of the microbiological, and sensory properties of lamb meat during storage. Biointerface Res Appl Chem 2023; 13: 267.
28. Brockbals L, Habicht M, Hajdas I, Galassi FM, Rühli FJ, Kraemer T. Untargeted metabolomics-like screening approach for chemical characterization and differentiation of canopic jar and mummy samples from Ancient Egypt using GC-high resolution MS. Analyst 2018; 143: 4503-4512.
29. Nitisinprasert S, Nilphai V, Bunyun P, Sukyai P, Doi K, Sonomoto K. Screening and identification of effective thermotolerant lactic acid bacteria producing antimicrobial activity against Escherichia coli and Salmonella sp. resistant to antibiotics. Agric Nat Resour 2000; 34: 387-400.
30. Gerding DN, Hecht DW, Louie T, Nord CE, Talbot GH, Cornely OA, et al. Susceptibility of Clostridium difficile isolates from a Phase 2 clinical trial of cadazolid and vancomycin in C. difficile infection. J Antimicrob Chemother 2016; 71: 213-219.
31. Drudy D, Harnedy N, Fanning S, O'mahony R, Kyne L. Isolation and characterisation of toxin A-negative, toxin B-positive Clostridium difficile in Dublin, Ireland. Clin Microbiol Infect 2007; 13: 298-304.
32. Kapoor S, Nema S, Biswas D, Khadanga S, Saigal S, Maheshwari M. Antibiotic associated diarrhea due to Clostridium difficile in a tertiary care teaching hospital, central India. Iran J Microbiol 2023; 15: 55-61.
33. Hamo Z, Azrad M, Fichtman B, Peretz A. The cytopathic effect of different toxin concentrations from different Clostridium difficile sequence types strains in vero cells. Front Microbiol 2021; 12: 763129.
34. Jia XX, Wang YY, Zhang WZ, Li WG, Bai LL, Lu JX, et al. A rapid multiplex real-time PCR detection of toxigenic Clostridioides difficile directly from fecal samples. 3 Biotech 2023; 13: 54.
35. Shen Y, Lin S, You P, Chen Y, Luo Y, Song X, et al. Rapid discrimination between clinical Clostridioides difficile infection and colonization by quantitative detection of TcdB toxin using a real-time cell analysis system. Front Microbiol 2024; 15: 1348892.
36. Ozma MA, Khodadadi E, Rezaee MA, Kamounah FS, Asgharzadeh M, Ganbarov K, et al. Induction of proteome changes involved in biofilm formation of Enterococcus faecalis in response to gentamicin. Microb Pathog 2021; 157: 105003.
37. Paula-Ramos L, da Rocha Santos CE, Camargo Reis Mello D, Nishiama Theodoro L, De Oliveira FE, Back Brito GN, et al. Klebsiella pneumoniae planktonic and biofilm reduction by different plant extracts: In vitro study. ScientificWorldJournal 2016; 2016: 3521413.
38. Chung H-J, Lee H, Kim M, Lee JW, Saeed M, Lee H, et al. Development and metabolic profiling of a postbiotic complex exhibiting antibacterial activity against skin microorganisms and anti-inflammatory effect on human keratinocytes. Food Sci Biotechnol 2022; 31: 1325-1334.
39. Mohammadi R, Moradi M, Tajik H, Molaei R. Potential application of postbiotics metabolites from bioprotective culture to fabricate bacterial nanocellulose based antimicrobial packaging material. Int J Biol Macromol 2022; 220: 528-536.
40. Kiran F, Kibar Demirhan H, Haliscelik O, Zatari D. Metabolic profiles of Weissella spp. postbiotics with anti-microbial and anti-oxidant effects. J Infect Dev Ctries 2023; 17: 507-517.
41. Vajiha Banu HM, Sumithra P, Mohamed Mahroop Raja M, Swedha A. Postbiotic Food Packaging Based on Organic Acids. Postbiotics: Springer. 2023. p. 373-379.
42. Mangrolia U, Osborne WJ. Staphylococcus xylosus VITURAJ10: Pyrrolo [1, 2α] pyrazine-1, 4-dione, hexahydro-3-(2-methylpropyl)(PPDHMP) producing, potential probiotic strain with antibacterial and anticancer activity. Microb Pathog 2020; 147: 104259.
43. Britton RA, Young VB. Role of the intestinal microbiota in resistance to colonization by Clostridium difficile. Gastroenterology 2014; 146: 1547-1553.
44. Czepiel J, Dróżdż M, Pituch H, Kuijper EJ, Perucki W, Mielimonka A, et al. Clostridium difficile infection: review. Eur J Clin Microbiol Infect Dis 2019; 38: 1211-1221.
45. Ibrahim GA, Mabrouk AM, El-Ssayad MF, Mehaya FM, Sharaf OM, Ibrahim MI. Properties of postbiotics produced by probiotics: antimicrobial, antioxidant activities and production of vitamins, organic acids. 2024. https://doi.org/10.21203/rs.3.rs-4125934/v1
46. Wu Y, Pang X, Wu Y, Liu X, Zhang X. Enterocins: classification, synthesis, antibacterial mechanisms and food applications. Molecules 2022; 27: 2258.
47. Lee J-S, Chung M-J, Seo J-G. In vitro evaluation of antimicrobial activity of lactic acid bacteria against Clostridium difficile. Toxicol Res 2013; 29: 99-106.
48. Ozma MA, Khodadadi E, Rezaee MA, Asgharzadeh M, Aghazadeh M, Zeinalzadeh E, et al. Bacterial proteomics and its application in pathogenesis studies. Curr Pharm Biotechnol 2022; 23: 1245-1256.
49. Ozma MA, Abbasi A, Ahangarzadeh Rezaee M, Hosseini H, Hosseinzadeh N, Sabahi S, et al. A critical review on the nutritional and medicinal profiles of garlic’s (Allium sativum L.) bioactive compounds. Food Rev Int 2023; 39: 6324-6361.
50. Baines SD, Wilcox MH. Antimicrobial resistance and reduced susceptibility in Clostridium difficile: potential consequences for induction, treatment, and recurrence of C. difficile infection. Antibiotics (Basel) 2015; 4: 267-298.
51. Yang J, Li Y, Meng L. Combination of Bifidobacterium breve and antibiotics against Clostridioides difficile: effect of the time interval of combination on antagonistic activity. Int Microbiol 2023; 26: 833-840.
52. Aktories K. From signal transduction to protein toxins—a narrative review about milestones on the research route of C. difficile toxins. Naunyn Schmiedebergs Arch Pharmacol 2023; 396: 173-190.
53. Davies AH, Roberts AK, Shone CC, Acharya KR. Super toxins from a super bug: structure and function of Clostridium difficile toxins. Biochem J 2011; 436: 517-526.
54. Shen NT, Maw A, Tmanova LL, Pino A, Ancy K, Crawford CV, et al. Timely use of probiotics in hospitalized adults prevents Clostridium difficile infection: a systematic review with meta-regression analysis. Gastroenterology 2017; 152: 1889-1900. e9.
55. McFarland LV. Probiotics for the primary and secondary prevention of C. difficile infections: a meta-analysis and systematic review. Antibiotics (Basel) 2015; 4: 160-178.
56. Sapa D, Brosse A, Coullon H, Péan de Ponfilly G, Candela T, Le Monnier A. A streamlined method to obtain biologically active TcdA and TcdB toxins from Clostridioides difficile. Toxins (Basel) 2024; 16: 38.
57. Yang J, Yang H. Effect of Bifidobacterium breve in combination with different antibiotics on Clostridium difficile. Front Microbiol 2018; 9: 2953.
58. Gurung B, Stricklin M, Wang S. Gut microbiota–gut metabolites and Clostridioides difficile infection: approaching sustainable solutions for therapy. Metabolites 2024; 14: 74.
2. Ong GK, Reidy TJ, Huk MD, Lane FR. Clostridium difficile colitis: a clinical review. Am J Surg 2017; 213: 565-571.
3. Ofosu A. Clostridium difficile infection: a review of current and emerging therapies. Ann Gastroenterol 2016; 29: 147-154.
4. Marra AR, Perencevich EN, Nelson RE, Samore M, Khader K, Chiang H-Y, et al. Incidence and outcomes associated with Clostridium difficile infections: a systematic review and meta-analysis. JAMA Netw Open 2020; 3(1): e1917597.
5. Skinner AM, Phillips ST, Merrigan MM, O’leary KJ, Sambol SP, Siddiqui F, et al. The relative role of toxins A and B in the virulence of Clotridioides difficile. J Clin Med 2020; 10: 96.
6. Kuehne SA, Cartman ST, Minton NP. Both, toxin A and toxin B, are important in Clostridium difficile infection. Gut Microbes 2011; 2: 252-255.
7. Kodori M, Ghalavand Z, Yadegar A, Eslami G, Azimirad M, Krutova M, et al. Molecular characterization of pathogenicity locus (PaLoc) and tcdC genetic diversity among tcdA+ B+ Clostridioides difficile clinical isolates in Tehran, Iran. Anaerobe 2020; 66: 102294.
8. Landenberger M, Nieland J, Roeder M, Nørgaard K, Papatheodorou P, Ernst K, et al. The cytotoxic effect of Clostridioides difficile pore-forming toxin CDTb. Biochim Biophys Acta Biomembr 2021; 1863: 183603.
9. Alhobayb T, Ciorba MA. Clostridium difficile in inflammatory bowel disease. Curr Opin Gastroenterol 2023; 39: 257-262.
10. Kunika, Frey N, Rangrez AY. Exploring the involvement of gut microbiota in cancer therapy-induced cardiotoxicity. Int J Mol Sci 2023; 24: 7261.
11. Bassotti G, Fruganti A, Stracci F, Marconi P, Fettucciari K. Cytotoxic synergism of Clostridioides difficile toxin B with proinflammatory cytokines in subjects with inflammatory bowel diseases. World J Gastroenterol 2023; 29: 582-596.
12. Chumbler NM, Rutherford SA, Zhang Z, Farrow MA, Lisher JP, Farquhar E, et al. Crystal structure of Clostridium difficile toxin A. Nat Microbiol 2016; 1: 15002.
13. Ozma MA, Khodadadi E, Pakdel F, Kamounah FS, Yousefi M, Yousefi B, et al. Baicalin, a natural antimicrobial and anti-biofilm agent. J Herb Med 2021; 27: 100432.
14. Spigaglia P. Recent advances in the understanding of antibiotic resistance in Clostridium difficile infection. Ther Adv Infect Dis 2016; 3: 23-42.
15. Dureja C, Olaitan AO, Hurdle JG. Mechanisms and impact of antimicrobial resistance in Clostridioides difficile. Curr Opin Microbiol 2022; 66: 63-72.
16. Ozma MA, Abbasi A, Asgharzadeh M, Pagliano P, Guarino A, Köse Ş, et al. Antibiotic therapy for pan-drug-resistant infections. Infez Med 2022; 30: 525-531.
17. Sabahi S, Homayouni Rad A, Aghebati-Maleki L, Sangtarash N, Ozma MA, Karimi A, et al. Postbiotics as the new frontier in food and pharmaceutical research. Crit Rev Food Sci Nutr 2023; 63: 8375-8402.
18. Mirzaei R, Kavyani B, Nabizadeh E, Kadkhoda H, Asghari Ozma M, Abdi M. Microbiota metabolites in the female reproductive system: Focused on the short-chain fatty acids. Heliyon 2023; 9(3): e14562.
19. Ozma MA, Abbasi A, Akrami S, Lahouty M, Shahbazi N, Ganbarov K, et al. Postbiotics as the key mediators of the gut microbiota-host interactions. Infez Med 2022; 30: 180-193.
20. Gopalan S, Ganapathy S, Mitra M, Neha, Kumar Joshi D, Veligandla KC, et al. Unique properties of yeast probiotic Saccharomyces boulardii CNCM I-745: A narrative review. Cureus 2023; 15(10): e46314.
21. Ghotaslou R, Nabizadeh E, Memar MY, Law WMH, Ozma MA, Abdi M, et al. The metabolic, protective, and immune functions of Akkermansia muciniphila. Microbiol Res 2023; 266: 127245.
22. Valdés-Varela L, Gueimonde M, Ruas-Madiedo P. Probiotics for prevention and treatment of Clostridium difficile infection. Adv Exp Med Biol 2018; 1050: 161-176.
23. Ozma MA, Moaddab SR, Hosseini H, Khodadadi E, Ghotaslou R, Asgharzadeh M, et al. A critical review of novel antibiotic resistance prevention approaches with a focus on postbiotics. Crit Rev Food Sci Nutr 2023; 1-19.
24. Vasilescu I-M, Chifiriuc M-C, Pircalabioru GG, Filip R, Bolocan A, Lazăr V, et al. Gut dysbiosis and Clostridioides difficile infection in neonates and adults. Front Microbiol 2022; 12: 651081.
25. Panpetch W, Phuengmaung P, Cheibchalard T, Somboonna N, Leelahavanichkul A, Tumwasorn S. Lacticaseibacillus casei strain T21 attenuates Clostridioides difficile infection in a murine model through reduction of inflammation and gut dysbiosis with decreased toxin lethality and enhanced mucin production. Front Microbiol 2021; 12: 745299.
26. Saadat YR, Gargari BP, Shahabi A, Nami Y, Khosroushahi AY. Prophylactic role of Lactobacillus Paracasei exopolysaccharides on colon cancer cells through apoptosis not ferroptosis. Pharm Sci 2021; 27: 251-261.
27. Ozma MA, Abbasi A, Sabahi S. Characterization of postbiotics derived from Lactobacillus paracasei ATCC 55544 and its application in Malva sylvestris seed mucilage edible coating to the improvement of the microbiological, and sensory properties of lamb meat during storage. Biointerface Res Appl Chem 2023; 13: 267.
28. Brockbals L, Habicht M, Hajdas I, Galassi FM, Rühli FJ, Kraemer T. Untargeted metabolomics-like screening approach for chemical characterization and differentiation of canopic jar and mummy samples from Ancient Egypt using GC-high resolution MS. Analyst 2018; 143: 4503-4512.
29. Nitisinprasert S, Nilphai V, Bunyun P, Sukyai P, Doi K, Sonomoto K. Screening and identification of effective thermotolerant lactic acid bacteria producing antimicrobial activity against Escherichia coli and Salmonella sp. resistant to antibiotics. Agric Nat Resour 2000; 34: 387-400.
30. Gerding DN, Hecht DW, Louie T, Nord CE, Talbot GH, Cornely OA, et al. Susceptibility of Clostridium difficile isolates from a Phase 2 clinical trial of cadazolid and vancomycin in C. difficile infection. J Antimicrob Chemother 2016; 71: 213-219.
31. Drudy D, Harnedy N, Fanning S, O'mahony R, Kyne L. Isolation and characterisation of toxin A-negative, toxin B-positive Clostridium difficile in Dublin, Ireland. Clin Microbiol Infect 2007; 13: 298-304.
32. Kapoor S, Nema S, Biswas D, Khadanga S, Saigal S, Maheshwari M. Antibiotic associated diarrhea due to Clostridium difficile in a tertiary care teaching hospital, central India. Iran J Microbiol 2023; 15: 55-61.
33. Hamo Z, Azrad M, Fichtman B, Peretz A. The cytopathic effect of different toxin concentrations from different Clostridium difficile sequence types strains in vero cells. Front Microbiol 2021; 12: 763129.
34. Jia XX, Wang YY, Zhang WZ, Li WG, Bai LL, Lu JX, et al. A rapid multiplex real-time PCR detection of toxigenic Clostridioides difficile directly from fecal samples. 3 Biotech 2023; 13: 54.
35. Shen Y, Lin S, You P, Chen Y, Luo Y, Song X, et al. Rapid discrimination between clinical Clostridioides difficile infection and colonization by quantitative detection of TcdB toxin using a real-time cell analysis system. Front Microbiol 2024; 15: 1348892.
36. Ozma MA, Khodadadi E, Rezaee MA, Kamounah FS, Asgharzadeh M, Ganbarov K, et al. Induction of proteome changes involved in biofilm formation of Enterococcus faecalis in response to gentamicin. Microb Pathog 2021; 157: 105003.
37. Paula-Ramos L, da Rocha Santos CE, Camargo Reis Mello D, Nishiama Theodoro L, De Oliveira FE, Back Brito GN, et al. Klebsiella pneumoniae planktonic and biofilm reduction by different plant extracts: In vitro study. ScientificWorldJournal 2016; 2016: 3521413.
38. Chung H-J, Lee H, Kim M, Lee JW, Saeed M, Lee H, et al. Development and metabolic profiling of a postbiotic complex exhibiting antibacterial activity against skin microorganisms and anti-inflammatory effect on human keratinocytes. Food Sci Biotechnol 2022; 31: 1325-1334.
39. Mohammadi R, Moradi M, Tajik H, Molaei R. Potential application of postbiotics metabolites from bioprotective culture to fabricate bacterial nanocellulose based antimicrobial packaging material. Int J Biol Macromol 2022; 220: 528-536.
40. Kiran F, Kibar Demirhan H, Haliscelik O, Zatari D. Metabolic profiles of Weissella spp. postbiotics with anti-microbial and anti-oxidant effects. J Infect Dev Ctries 2023; 17: 507-517.
41. Vajiha Banu HM, Sumithra P, Mohamed Mahroop Raja M, Swedha A. Postbiotic Food Packaging Based on Organic Acids. Postbiotics: Springer. 2023. p. 373-379.
42. Mangrolia U, Osborne WJ. Staphylococcus xylosus VITURAJ10: Pyrrolo [1, 2α] pyrazine-1, 4-dione, hexahydro-3-(2-methylpropyl)(PPDHMP) producing, potential probiotic strain with antibacterial and anticancer activity. Microb Pathog 2020; 147: 104259.
43. Britton RA, Young VB. Role of the intestinal microbiota in resistance to colonization by Clostridium difficile. Gastroenterology 2014; 146: 1547-1553.
44. Czepiel J, Dróżdż M, Pituch H, Kuijper EJ, Perucki W, Mielimonka A, et al. Clostridium difficile infection: review. Eur J Clin Microbiol Infect Dis 2019; 38: 1211-1221.
45. Ibrahim GA, Mabrouk AM, El-Ssayad MF, Mehaya FM, Sharaf OM, Ibrahim MI. Properties of postbiotics produced by probiotics: antimicrobial, antioxidant activities and production of vitamins, organic acids. 2024. https://doi.org/10.21203/rs.3.rs-4125934/v1
46. Wu Y, Pang X, Wu Y, Liu X, Zhang X. Enterocins: classification, synthesis, antibacterial mechanisms and food applications. Molecules 2022; 27: 2258.
47. Lee J-S, Chung M-J, Seo J-G. In vitro evaluation of antimicrobial activity of lactic acid bacteria against Clostridium difficile. Toxicol Res 2013; 29: 99-106.
48. Ozma MA, Khodadadi E, Rezaee MA, Asgharzadeh M, Aghazadeh M, Zeinalzadeh E, et al. Bacterial proteomics and its application in pathogenesis studies. Curr Pharm Biotechnol 2022; 23: 1245-1256.
49. Ozma MA, Abbasi A, Ahangarzadeh Rezaee M, Hosseini H, Hosseinzadeh N, Sabahi S, et al. A critical review on the nutritional and medicinal profiles of garlic’s (Allium sativum L.) bioactive compounds. Food Rev Int 2023; 39: 6324-6361.
50. Baines SD, Wilcox MH. Antimicrobial resistance and reduced susceptibility in Clostridium difficile: potential consequences for induction, treatment, and recurrence of C. difficile infection. Antibiotics (Basel) 2015; 4: 267-298.
51. Yang J, Li Y, Meng L. Combination of Bifidobacterium breve and antibiotics against Clostridioides difficile: effect of the time interval of combination on antagonistic activity. Int Microbiol 2023; 26: 833-840.
52. Aktories K. From signal transduction to protein toxins—a narrative review about milestones on the research route of C. difficile toxins. Naunyn Schmiedebergs Arch Pharmacol 2023; 396: 173-190.
53. Davies AH, Roberts AK, Shone CC, Acharya KR. Super toxins from a super bug: structure and function of Clostridium difficile toxins. Biochem J 2011; 436: 517-526.
54. Shen NT, Maw A, Tmanova LL, Pino A, Ancy K, Crawford CV, et al. Timely use of probiotics in hospitalized adults prevents Clostridium difficile infection: a systematic review with meta-regression analysis. Gastroenterology 2017; 152: 1889-1900. e9.
55. McFarland LV. Probiotics for the primary and secondary prevention of C. difficile infections: a meta-analysis and systematic review. Antibiotics (Basel) 2015; 4: 160-178.
56. Sapa D, Brosse A, Coullon H, Péan de Ponfilly G, Candela T, Le Monnier A. A streamlined method to obtain biologically active TcdA and TcdB toxins from Clostridioides difficile. Toxins (Basel) 2024; 16: 38.
57. Yang J, Yang H. Effect of Bifidobacterium breve in combination with different antibiotics on Clostridium difficile. Front Microbiol 2018; 9: 2953.
58. Gurung B, Stricklin M, Wang S. Gut microbiota–gut metabolites and Clostridioides difficile infection: approaching sustainable solutions for therapy. Metabolites 2024; 14: 74.
| Files | ||
| Issue | Vol 16 No 4 (2024) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v16i4.16309 | |
| Keywords | ||
| Clostridium difficile; Biofilm; Postbiotics; Probiotics; Toxicity | ||
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How to Cite
1.
Asghari Ozma M, Mahmoodzadeh Hosseini H, Ataee MH, Mirhosseini SA. Evaluating the antibacterial, antibiofilm, and anti-toxigenic effects of postbiotics from lactic acid bacteria on Clostridium difficile. Iran J Microbiol. 2024;16(4):497-508.
