BACTEROIDES FRAGILIS IN THE DEVELOPMENT OF ABDOMINAL SURGICAL INFECTION
Abstract
The article presents the review of domestic and foreign literature and the authors’ own researches on the role of B. fragilis in the development of abdominal purulent-septic diseases and their postoperative complications (peritonitis, intra-abdominal abscesses, infected pancreatic necrosis, appendicitis, etc.). According to modern ideas, B. fragilis is one of the leading pathogens of human pathology.This review analyzes and summarizes information on the main factors of pathogenicity and virulence of toxigenic and nontoxigenic B. fragilis at the phenotypic, molecular-genetic level necessary for the survival of the bacteroid in pathophysiological conditions, the level of their antibiotic resistance. The role of aerotolerance of B. fragilis and complex of oxygen-detoxification enzymatic and non-enzymatic systems of antioxidant protection under oxidative stress (catalase, superoxide dismutase, fumarate reductase, thioredoxine-dependent peroxidase, alkylhydroperoxide reductase, gemm- ferritin, etc.) is discussed. New data on the known (capsular polysaccharides, proteases, neuraminidases, heparinase, hyaluronidase, fibrinolysin, enterotoxin frigilizin BFT-B. fragilis toxin, etc.) and less studied unique virulence factors (metalloproteinase BFT and IIMPII (BfPAI), bacterioprotein fragipainFpn protease, fibrinogen-binding protein BF-FBP, hemolysins (hlyA, hlyB, hlyC, hlyD, hlyE, hlyF, hlyG, hlyE, hlyF, hlyG and hlyIII, HlyBA), as well as the most probable way of secretion and extracellular delivery of toxins and B. fragilis vesicle. The authors draw attention to increasing resistance of B. fragilis to modern antimicrobial drugs, which must be taken into account when choosing adequate antimicrobial therapy.
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31. Lobo L.A., Jenkins A.L., Jeffrey S. C., Rocha E.R. Expression of Bacteroides fragilis hemolysins in vivo and role of HlyBA in an intra-abdominal infection model // Microbiologyopen. 2013. Vol. 2 №2. P.326–337. DOI: 10.1002/mbo3.76
32. Mazmanian S.K., Liu C.H., Tzianabos A.O., Kasper D.L. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system // Cell. 2005. Vol. 122. P.107–118.
33. Meehan B.M., Malamy M. H. Fumarate reductase is a major contributor to the generation of reactive oxygen species in the anaerobe Bacteroides fragilis // Microbiology. 2012. Vol. 158. P.539–546. DOI:10.1099/mic.0.054403-0.
34. Montravers P., Lepape A., Dubreuil L., et al. Clinical and microbiological profiles of community-acquired and nosocomial intra-abdominal infections: results of the French prospective, observational EBIIA study // The Journal of antimicrobial chemotherapy. 2009. Vol.63. №4. P.85-94. DOI: 10.1093/jac/dkp005.
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37. Patrick S., Blakely G.W., Houston S., et al. Twenty-eight divergent polysaccharide loci specifying within- and amongst-strain capsule diversity in three strains of Bacteroides fragilis // Microbiol. 2010. Vol. 156. P.3255–3269. DOI: 10.1099/mic.0.042978-0.
38. Patrick S., Duerden B.I. Gram-negative non-spore forming obligate anaerobes. In: Principles and Practice of Clinical Bacteriology. 2006. Chapter 45. P. 541–556.
39. Prindiville T.P., Sheikh R.A., Cohen S.H., et al. Bacteroides fragilis enterotoxin gene sequences in patients with inflammatory bowel disease // Emerg Infect Dis. 2000. Vol. 6 №2. P.171–174.
40. Pumbwe L., Skilbeck C.A., Nakano V., et al. Bile salts enhance bacterial co-aggregation, bacterial-intestinal epithelial cell adhesion, biofilm formation and antimicrobial resistance of Bacteroides fragilis // Microb Pathog. 2007. Vol. 43. №2–3. P.78–87.
41. Remacle A.G., Shiryaev S.A., Strongin A.Y. Distinct interactions with cellular E-cadherin of the two virulent metalloproteinases encoded by a Bacteroides fragilis pathogenicity island // PLoS One. 2014. Vol. 9. №11. P.e113896. DOI: 10.1371/journal.pone.0113896.
42. Ridlon J.M., Kang D.J., Hylemon P.B. Bile salt biotransformations by human intestinal bacteria // J Lipid Res. 2006. Vol. 47. № 2. P.241–259.
43. Robertson K.P., Smith S.J., Gough M.A., Rocha E.R. Characterization of bacteroides fragilis hemolysins and regulation and synergistic interactions of Hlya and HlyB // Infect. Immuno. 2006. №74. P.2304–2316.
44. Rocha E.R., Smith C.J. Ferritin-like family proteins in the anaerobe Bacteroides fragilis: when an oxygen storm is coming, take your iron to the shelter // BioMetals. 2013. Vol. 26. №4. P.577–591. DOI: 10.1007/s10534-013-9650-2.
45. Rudek W., Haque R.U. Extracellular enzymes of the genus Bacteroides // J Clin Microbiol. 1976. Vol. 4. № 5. P. 458–460.
46. Sampson T.R., Mazmanian S.K. Control of brain development, function, and behavior by the microbiome cell host microbe // Cell Host Microbe. 2016. №17. P. 565–576. DOI: 10.1016/j.chom.2015.04.011
47. Sartelli M., Catena F.L., Ansaloni L., et al. Complicated intra-abdominal infections in a worldwide context: an observational prospective study (CIAOW Study) // World Journal of Emergency Surgery. 2013. №8 P.1. doi.org/10.1186/1749–7922-8-1.
48. Sherwood J.E., Fraser S., Citron D.M., et al. Multi-drug resistant Bacteroides fragilis recovered from blood and severe leg wounds caused by an improvised explosive device (IED) in Afghanistan // Anaerobe. 2011. №17. P.152–155. DOI: 10.1016/j.anaerobe.2011.02.007.
49. Shiryaev S.A., Remacle A.G., Cieplak P., Strongin A.Y. Peptide Sequence Region That is Essential for the Interactions of the Enterotoxigenic Bacteroides fragilis Metalloproteinase II with E-cadherin // J Proteolysis. 2014. Vol. 1. № 1. P.3-14.
50. Simmon K.E., Mirrett S., Reller L.B., Petti C.A. Genotypic diversity of anaerobic isolates from bloodstream infections // J Clin Microbiol. 2008. Vol. 46. №5. P.1596–1601. doi:10.1128/JCM.02469-07.
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56. Zakharzhevskaya N.B., Tsvetkov V.B., Vanyushkina A.A., et al. Interaction of Bacteroides fragilis Toxin with Outer Membrane Vesicles Reveals New Mechanism of Its Secretion and Delivery // Front Cell Infect Microbiol. 2017. Vol. 7. P.2. DOI: 10.3389/fcimb.2017.00002.
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14. Claros M.C., Claros Z.C., Hecht D.W., et al. Characterization of the Bacteroides fragilis pathogenicity island in human blood culture isolates. // Anaerobe. 2006. №12. P.17–22.
15. Coyne M.J., Tzianabos A.O., Mallory B.C., et al. Polysaccharide Biosynthesis Locus Required for Virulence of Bacteroides fragilis Polysaccharide Biosynthesis Locus Required for Virulence of Bacteroides fragilis // Infect Immun. 2001. № 69. P. 4342–4350.
16. David J.M., Rajasekaran A.K. Dishonorable Discharge: The Oncogenic roles of cleaved E-cadherin fragments // Cancer Res. 2012. Vol.72 №12. P. 2917-2923. DOI: 10.1158/0008–5472.CAN–11–3498.
17. Elhenawy W., Debelyy M.O., Feldman M.F. Preferential packing of acidic glycosidases and proteases into Bacteroides outer membrane vesicles // MBio. 2014. Vol. 5. №2. – P.e00909-00914. DOI: 10.1128/mBio.00909–14.
18. Fathi P., Wu S. Isolation, detection, and characterization of enterotoxigenic Bacteroides fragilis in clinical samples // Open Microbiol. J. 2016. № 10. P. 57–63. doi: 10.2174/1874285801610010057
19. Fernández-Canigia L., Litterio M., Legaria M.C., et al. First national survey of antibiotic susceptibility of the Bacteroides fragilis group: emerging resistance to carbapenems in Argentina // Antimicrob Agents Chemother. 2012. Vol.56 №3. P.1309–1314. doi: 10.1128/AAC.05622–11.
20. Franco A.A. The Bacteroides Fragilis pathogenicity island is contained in a putative novel conjugative transposon // J Bacteriol. 2004. Vol.186. №18. P.6077–6092.
21. Gauzit R., Pean Y., Barth X., et al. Epidemiology, management and prognosis of secondary nonpostoperative peritonitis: a French prospective observational multicenter study // Surg Infect (Larchmt). Vol.10. № 2. P. 119–127. DOI: 10.1089/sur.2007.092.
22. Guzman C.A., Plate M., Pruzzo C. Role of neuraminidase-dependent adherence in Bacteroides fragilis attachment to human epithelial cells // FEMS Microbiol Lett. 1990. №59 (1–2). P. 187–192.
23. Houston S., Blakely G., McDowell A., et al. Binding anddegradation of fibrinogen by Bacteroides fragilis and characterization of a 54 kDa fibrinogen-binding protein // Microbiol. 2010. №156. P.2516–2526. DOI: 10.1099/mic.0.038588-0.
24. Hug L.A., Baker B.J., Anantharaman K., et al. A new view of the tree of life // Nat. Microbiol. 2016. №1. P. 16048. doi: 10.1038/nmicrobiol.2016.48.
25. Husain F., Veeranagouda Y., Hsi J., et al. Two multidrug-resistant clinical isolates of Bacteroides fragilis carry a novel metronidazole resistance nim gene (nimJ) // Antimicrob Agents Chemother. 2013. Vol. 57. P.3767–3774. DOI: 10.1128/AAC.00386-13.
26. Hwang S., Gwon S.Y., Kim M.S., et al. Bacteroides fragilis Toxin Induces IL-8 Secretion in HT29/C1 Cells through Disruption of E-cadherin Junctions // Immune Netw. 2013. Vol.13. №5. P.213–217. DOI: 10.4110/in.2013.13.5.213.
27. Kato N., Liu C.X., Kato H., et al. New subtype of the metalloprotease toxin gene and the incidence of the three Bft subtypes among Bacteroides fragilis isolates in Japan // FEMS Microbiol Lett. 2000. Vol.182. №1– P.171–176.
28. Krinos C.M., Coyne M.J., Weinacht K.G., et al. Extensive surface diversity of a commensal microorganism by multiple DNA inversions // Nature. 2001. Vol. 414. №6863. P. 555–558.
29. Liu C.H., Lee S.M., Vanlare J.M., et al. Regulation of surface architecture by symbiotic bacteria mediates host colonization // Proc Natl Acad Sci USA. 2008. Vol.105. №10 P.3951–3956. DOI: 10.1073/pnas.0709266105.
30. Lobo L.A., Benjamim C.F., Oliveira A.C. The interplay between microbiota and inflammation: lessons from peritonitis and sepsis // Clinical & Translational. Immunology. 2016. №5 P.90. DOI:10.1038/cti.2016.32.
31. Lobo L.A., Jenkins A.L., Jeffrey S. C., Rocha E.R. Expression of Bacteroides fragilis hemolysins in vivo and role of HlyBA in an intra-abdominal infection model // Microbiologyopen. 2013. Vol. 2 №2. P.326–337. DOI: 10.1002/mbo3.76
32. Mazmanian S.K., Liu C.H., Tzianabos A.O., Kasper D.L. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system // Cell. 2005. Vol. 122. P.107–118.
33. Meehan B.M., Malamy M. H. Fumarate reductase is a major contributor to the generation of reactive oxygen species in the anaerobe Bacteroides fragilis // Microbiology. 2012. Vol. 158. P.539–546. DOI:10.1099/mic.0.054403-0.
34. Montravers P., Lepape A., Dubreuil L., et al. Clinical and microbiological profiles of community-acquired and nosocomial intra-abdominal infections: results of the French prospective, observational EBIIA study // The Journal of antimicrobial chemotherapy. 2009. Vol.63. №4. P.85-94. DOI: 10.1093/jac/dkp005.
35. Ngo J.T., Parkins M.D., Gregson D.B., et al. Population-based assessment of the incidence, risk factors, and outcomes of anaerobic bloodstream infections // Infection. 2013. Vol. 41. №1. P.41–48. DOI: 10.1007/s15010-012-0389-4.
36. O'Donoghue EJ, Krachler AM. Mechanisms of outer membrane vesicle entry into host cells // Cell Microbiol. 2016. Vol. 18. №11. P.1508–1517. DOI: 10.1111/cmi.12655.
37. Patrick S., Blakely G.W., Houston S., et al. Twenty-eight divergent polysaccharide loci specifying within- and amongst-strain capsule diversity in three strains of Bacteroides fragilis // Microbiol. 2010. Vol. 156. P.3255–3269. DOI: 10.1099/mic.0.042978-0.
38. Patrick S., Duerden B.I. Gram-negative non-spore forming obligate anaerobes. In: Principles and Practice of Clinical Bacteriology. 2006. Chapter 45. P. 541–556.
39. Prindiville T.P., Sheikh R.A., Cohen S.H., et al. Bacteroides fragilis enterotoxin gene sequences in patients with inflammatory bowel disease // Emerg Infect Dis. 2000. Vol. 6 №2. P.171–174.
40. Pumbwe L., Skilbeck C.A., Nakano V., et al. Bile salts enhance bacterial co-aggregation, bacterial-intestinal epithelial cell adhesion, biofilm formation and antimicrobial resistance of Bacteroides fragilis // Microb Pathog. 2007. Vol. 43. №2–3. P.78–87.
41. Remacle A.G., Shiryaev S.A., Strongin A.Y. Distinct interactions with cellular E-cadherin of the two virulent metalloproteinases encoded by a Bacteroides fragilis pathogenicity island // PLoS One. 2014. Vol. 9. №11. P.e113896. DOI: 10.1371/journal.pone.0113896.
42. Ridlon J.M., Kang D.J., Hylemon P.B. Bile salt biotransformations by human intestinal bacteria // J Lipid Res. 2006. Vol. 47. № 2. P.241–259.
43. Robertson K.P., Smith S.J., Gough M.A., Rocha E.R. Characterization of bacteroides fragilis hemolysins and regulation and synergistic interactions of Hlya and HlyB // Infect. Immuno. 2006. №74. P.2304–2316.
44. Rocha E.R., Smith C.J. Ferritin-like family proteins in the anaerobe Bacteroides fragilis: when an oxygen storm is coming, take your iron to the shelter // BioMetals. 2013. Vol. 26. №4. P.577–591. DOI: 10.1007/s10534-013-9650-2.
45. Rudek W., Haque R.U. Extracellular enzymes of the genus Bacteroides // J Clin Microbiol. 1976. Vol. 4. № 5. P. 458–460.
46. Sampson T.R., Mazmanian S.K. Control of brain development, function, and behavior by the microbiome cell host microbe // Cell Host Microbe. 2016. №17. P. 565–576. DOI: 10.1016/j.chom.2015.04.011
47. Sartelli M., Catena F.L., Ansaloni L., et al. Complicated intra-abdominal infections in a worldwide context: an observational prospective study (CIAOW Study) // World Journal of Emergency Surgery. 2013. №8 P.1. doi.org/10.1186/1749–7922-8-1.
48. Sherwood J.E., Fraser S., Citron D.M., et al. Multi-drug resistant Bacteroides fragilis recovered from blood and severe leg wounds caused by an improvised explosive device (IED) in Afghanistan // Anaerobe. 2011. №17. P.152–155. DOI: 10.1016/j.anaerobe.2011.02.007.
49. Shiryaev S.A., Remacle A.G., Cieplak P., Strongin A.Y. Peptide Sequence Region That is Essential for the Interactions of the Enterotoxigenic Bacteroides fragilis Metalloproteinase II with E-cadherin // J Proteolysis. 2014. Vol. 1. № 1. P.3-14.
50. Simmon K.E., Mirrett S., Reller L.B., Petti C.A. Genotypic diversity of anaerobic isolates from bloodstream infections // J Clin Microbiol. 2008. Vol. 46. №5. P.1596–1601. doi:10.1128/JCM.02469-07.
51. Snydman D.R., Jacobus N.V., McDermott L.A., et al. Lessons learned from the anaerobe survey: historical perspective and review of the most recent data (2005-2007) // Clin Infect Dis. 2010. Vol. 50. № 1. P. 26–33. DOI: 10.1086/647940.
52. Sund C.J., Rocha E.R., Tzianabos A.O., et al. In the bacteroides fragilis transcriptome response to oxygen and H2O2: the role of OxyR and its effect on survival and virulence // Mol. Microbiology. 2008. Vol. 67. P. 129–142.
53. Troy E.B., Kasper D.L. Beneficial effects of Bacteroides fragilis polysaccharides on the immune system // Front Biosci (Landmark Ed). 2010. №15. P. 25–34.
54. Turnbaugh P.J., Ley R.E., Hamady M., et al. The human microbiome project // Nature. 2007. Vol. 449 №7164. P.804–810.
55. Wexler H.M. Bacteroides: the good, the bad, and the nitty-gritty // Clin Microbiol Rev. 2007. Vol. 20. № 4. P.593–621.
56. Zakharzhevskaya N.B., Tsvetkov V.B., Vanyushkina A.A., et al. Interaction of Bacteroides fragilis Toxin with Outer Membrane Vesicles Reveals New Mechanism of Its Secretion and Delivery // Front Cell Infect Microbiol. 2017. Vol. 7. P.2. DOI: 10.3389/fcimb.2017.00002.
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21. Gauzit R., Pean Y., Barth X., et al. Epidemiology, management and prognosis of secondary nonpostoperative peritonitis: a French prospective observational multicenter study // Surg Infect (Larchmt). Vol.10. № 2. P. 119–127. DOI: 10.1089/sur.2007.092.
22. Guzman C.A., Plate M., Pruzzo C. Role of neuraminidase-dependent adherence in Bacteroides fragilis attachment to human epithelial cells // FEMS Microbiol Lett. 1990. №59 (1–2). P. 187–192.
23. Houston S., Blakely G., McDowell A., et al. Binding anddegradation of fibrinogen by Bacteroides fragilis and characterization of a 54 kDa fibrinogen-binding protein // Microbiol. 2010. №156. P.2516–2526. DOI: 10.1099/mic.0.038588-0.
24. Hug L.A., Baker B.J., Anantharaman K., et al. A new view of the tree of life // Nat. Microbiol. 2016. №1. P. 16048. doi: 10.1038/nmicrobiol.2016.48.
25. Husain F., Veeranagouda Y., Hsi J., et al. Two multidrug-resistant clinical isolates of Bacteroides fragilis carry a novel metronidazole resistance nim gene (nimJ) // Antimicrob Agents Chemother. 2013. Vol. 57. P.3767–3774. DOI: 10.1128/AAC.00386-13.
26. Hwang S., Gwon S.Y., Kim M.S., et al. Bacteroides fragilis Toxin Induces IL-8 Secretion in HT29/C1 Cells through Disruption of E-cadherin Junctions // Immune Netw. 2013. Vol.13. №5. P.213–217. DOI: 10.4110/in.2013.13.5.213.
27. Kato N., Liu C.X., Kato H., et al. New subtype of the metalloprotease toxin gene and the incidence of the three Bft subtypes among Bacteroides fragilis isolates in Japan // FEMS Microbiol Lett. 2000. Vol.182. №1– P.171–176.
28. Krinos C.M., Coyne M.J., Weinacht K.G., et al. Extensive surface diversity of a commensal microorganism by multiple DNA inversions // Nature. 2001. Vol. 414. №6863. P. 555–558.
29. Liu C.H., Lee S.M., Vanlare J.M., et al. Regulation of surface architecture by symbiotic bacteria mediates host colonization // Proc Natl Acad Sci USA. 2008. Vol.105. №10 P.3951–3956. DOI: 10.1073/pnas.0709266105.
30. Lobo L.A., Benjamim C.F., Oliveira A.C. The interplay between microbiota and inflammation: lessons from peritonitis and sepsis // Clinical & Translational. Immunology. 2016. №5 P.90. DOI:10.1038/cti.2016.32.
31. Lobo L.A., Jenkins A.L., Jeffrey S. C., Rocha E.R. Expression of Bacteroides fragilis hemolysins in vivo and role of HlyBA in an intra-abdominal infection model // Microbiologyopen. 2013. Vol. 2 №2. P.326–337. DOI: 10.1002/mbo3.76
32. Mazmanian S.K., Liu C.H., Tzianabos A.O., Kasper D.L. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system // Cell. 2005. Vol. 122. P.107–118.
33. Meehan B.M., Malamy M. H. Fumarate reductase is a major contributor to the generation of reactive oxygen species in the anaerobe Bacteroides fragilis // Microbiology. 2012. Vol. 158. P.539–546. DOI:10.1099/mic.0.054403-0.
34. Montravers P., Lepape A., Dubreuil L., et al. Clinical and microbiological profiles of community-acquired and nosocomial intra-abdominal infections: results of the French prospective, observational EBIIA study // The Journal of antimicrobial chemotherapy. 2009. Vol.63. №4. P.85-94. DOI: 10.1093/jac/dkp005.
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36. O'Donoghue EJ, Krachler AM. Mechanisms of outer membrane vesicle entry into host cells // Cell Microbiol. 2016. Vol. 18. №11. P.1508–1517. DOI: 10.1111/cmi.12655.
37. Patrick S., Blakely G.W., Houston S., et al. Twenty-eight divergent polysaccharide loci specifying within- and amongst-strain capsule diversity in three strains of Bacteroides fragilis // Microbiol. 2010. Vol. 156. P.3255–3269. DOI: 10.1099/mic.0.042978-0.
38. Patrick S., Duerden B.I. Gram-negative non-spore forming obligate anaerobes. In: Principles and Practice of Clinical Bacteriology. 2006. Chapter 45. P. 541–556.
39. Prindiville T.P., Sheikh R.A., Cohen S.H., et al. Bacteroides fragilis enterotoxin gene sequences in patients with inflammatory bowel disease // Emerg Infect Dis. 2000. Vol. 6 №2. P.171–174.
40. Pumbwe L., Skilbeck C.A., Nakano V., et al. Bile salts enhance bacterial co-aggregation, bacterial-intestinal epithelial cell adhesion, biofilm formation and antimicrobial resistance of Bacteroides fragilis // Microb Pathog. 2007. Vol. 43. №2–3. P.78–87.
41. Remacle A.G., Shiryaev S.A., Strongin A.Y. Distinct interactions with cellular E-cadherin of the two virulent metalloproteinases encoded by a Bacteroides fragilis pathogenicity island // PLoS One. 2014. Vol. 9. №11. P.e113896. DOI: 10.1371/journal.pone.0113896.
42. Ridlon J.M., Kang D.J., Hylemon P.B. Bile salt biotransformations by human intestinal bacteria // J Lipid Res. 2006. Vol. 47. № 2. P.241–259.
43. Robertson K.P., Smith S.J., Gough M.A., Rocha E.R. Characterization of bacteroides fragilis hemolysins and regulation and synergistic interactions of Hlya and HlyB // Infect. Immuno. 2006. №74. P.2304–2316.
44. Rocha E.R., Smith C.J. Ferritin-like family proteins in the anaerobe Bacteroides fragilis: when an oxygen storm is coming, take your iron to the shelter // BioMetals. 2013. Vol. 26. №4. P.577–591. DOI: 10.1007/s10534-013-9650-2.
45. Rudek W., Haque R.U. Extracellular enzymes of the genus Bacteroides // J Clin Microbiol. 1976. Vol. 4. № 5. P. 458–460.
46. Sampson T.R., Mazmanian S.K. Control of brain development, function, and behavior by the microbiome cell host microbe // Cell Host Microbe. 2016. №17. P. 565–576. DOI: 10.1016/j.chom.2015.04.011
47. Sartelli M., Catena F.L., Ansaloni L., et al. Complicated intra-abdominal infections in a worldwide context: an observational prospective study (CIAOW Study) // World Journal of Emergency Surgery. 2013. №8 P.1. doi.org/10.1186/1749–7922-8-1.
48. Sherwood J.E., Fraser S., Citron D.M., et al. Multi-drug resistant Bacteroides fragilis recovered from blood and severe leg wounds caused by an improvised explosive device (IED) in Afghanistan // Anaerobe. 2011. №17. P.152–155. DOI: 10.1016/j.anaerobe.2011.02.007.
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Published
2019-01-31
How to Cite
ФАДЕЕВА, Татьяна Владимировна et al.
BACTEROIDES FRAGILIS IN THE DEVELOPMENT OF ABDOMINAL SURGICAL INFECTION.
Sibirskij Medicinskij Zurnal (Irkutsk) = Siberian Medical Journal (Irkutsk) 16+, [S.l.], v. 154, n. 3, p. 5-11, jan. 2019.
ISSN 1815-7572. Available at: <http://smj.ismu.baikal.ru/index.php/osn/article/view/301>. Date accessed: 01 jan. 2026.
Issue
Section
Scientific reviews
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
