1887

Journal of Medical Microbiology logo

Volume 73, Issue 7

The state of play of rodent models for the study of infection Open Access

This article is part of the Clostridioides difficile collection.

Abstract

is the most common cause of nosocomial antibiotic-associated diarrhoea and is responsible for a spectrum of diseases characterized by high levels of recurrence and morbidity. In some cases, complications can lead to death. Currently, several types of animal models have been developed to study various aspects of infection (CDI), such as colonization, virulence, transmission and recurrence. These models have also been used to test the role of environmental conditions, such as diet, age and microbiome that modulate infection outcome, and to evaluate several therapeutic strategies. Different rodent models have been used successfully, such as the hamster model and the gnotobiotic and conventional mouse models. These models can be applied to study either the initial CDI infectious process or recurrences. The applications of existing rodent models and their advantages and disadvantages are discussed here.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): animal models , Clostridioides difficile , conventionally reared mice , gnotobiotic mice , hamsters and relapse model
© 2024 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.001857
2024-07-19
2024-09-11
Loading full text...

Full text loading...

/deliver/fulltext/jmm/73/7/jmm001857.html?itemId=/content/journal/jmm/10.1099/jmm.0.001857&mimeType=html&fmt=ahah

References

  1. Lawley TD, Clare S, Walker AW, Goulding D, Stabler RA et al. Antibiotic treatment of clostridium difficile carrier mice triggers a supershedder state, spore-mediated transmission, and severe disease in immunocompromised hosts. Infect Immun 2009; 77:3661–3669 [View Article] [PubMed]
     [Google Scholar]
  2. Price AB, Larson HE, Crow J. Morphology of experimental antibiotic-associated enterocolitis in the hamster: a model for human pseudomembranous colitis and antibiotic-associated diarrhoea. Gut 1979; 20:467–475 [View Article] [PubMed]
     [Google Scholar]
  3. Douce G, Goulding D. Refinement of the hamster model of Clostridium difficile disease. In Mullany P, Roberts AP. eds Clostridium difficile Totowa, NJ: Humana Press; pp 215–227 [View Article]
     [Google Scholar]
  4. Best EL, Freeman J, Wilcox MH. Models for the study of Clostridium difficile infection. Gut Microbes 2012; 3:145–167 [View Article] [PubMed]
     [Google Scholar]
  5. Sambol SP, Tang JK, Merrigan MM, Johnson S, Gerding DN. Infection of hamsters with epidemiologically important strains of Clostridium difficile. J Infect Dis 2001; 183:1760–1766 [View Article] [PubMed]
     [Google Scholar]
  6. Hasan MK, Dhungel BA, Govind R. Characterization of an operon required for growth on cellobiose in Clostridioides difficile. Microbiology 2021; 167:001079 [View Article] [PubMed]
     [Google Scholar]
  7. Small JD. Fatal enterocolitis in hamsters given lincomycin hydrochloride. Lab Anim Care 1968; 18:411–420 [PubMed]
     [Google Scholar]
  8. Larson HE, Borriello SP. Quantitative study of antibiotic-induced susceptibility to Clostridium difficile enterocecitis in hamsters. Antimicrob Agents Chemother 1990; 34:1348–1353 [View Article] [PubMed]
     [Google Scholar]
  9. Merrigan M, Sambol S, Johnson S, Gerding DN. Susceptibility of hamsters to human pathogenic Clostridium difficile strain B1 following clindamycin, ampicillin or ceftriaxone administration. Anaerobe 2003; 9:91–95 [View Article] [PubMed]
     [Google Scholar]
  10. Weiss W, Pulse M, Vickers R. In vivo assessment of SMT19969 in a hamster model of Clostridium difficile infection. Antimicrob Agents Chemother 2014; 58:5714–5718 [View Article] [PubMed]
     [Google Scholar]
  11. Chiari EF, Weiss W, Simon MR, Kiessig ST, Pulse M et al. Oral immunotherapy with human secretory immunoglobulin A improves survival in the hamster model of Clostridioides difficile infection. J Infect Dis 2021; 224:1394–1397 [View Article] [PubMed]
     [Google Scholar]
  12. Burdet C, Sayah-Jeanne S, Nguyen TT, Miossec C, Saint-Lu N et al. Protection of hamsters from mortality by reducing fecal moxifloxacin concentration with DAV131A in a model of moxifloxacin-induced Clostridium difficile colitis. Antimicrob Agents Chemother 2017; 61:e00543-17 [View Article] [PubMed]
     [Google Scholar]
  13. Ghose C, Eugenis I, Edwards AN, Sun X, McBride SM et al. Immunogenicity and protective efficacy of Clostridium difficile spore proteins. Anaerobe 2016; 37:85–95 [View Article] [PubMed]
     [Google Scholar]
  14. Rätsep M, Kõljalg S, Sepp E, Smidt I, Truusalu K et al. A combination of the probiotic and prebiotic product can prevent the germination of Clostridium difficile spores and infection. Anaerobe 2017; 47:94–103 [View Article] [PubMed]
     [Google Scholar]
  15. Diniz AN, Moura LNF, Cruz DSG, Oliveira Junior CA, Figueiredo HCP et al. Characterization of the virulence of three novel clade 2 Clostridioides (Clostridium) difficile strains and a two-year screening in animals and humans in Brazil. PLoS One 2022; 17:e0273013 [View Article] [PubMed]
     [Google Scholar]
  16. Wang Y, Wang S, Bouillaut L, Li C, Duan Z et al. Oral immunization with nontoxigenic Clostridium difficile strains expressing chimeric fragments of TcdA and TcdB elicits protective immunity against C. difficile infection in both mice and hamsters. Infect Immun 2018; 86:e00489-18 [View Article] [PubMed]
     [Google Scholar]
  17. Nale JY, Spencer J, Hargreaves KR, Buckley AM, Trzepiński P et al. Bacteriophage combinations significantly reduce Clostridium difficile growth in vitro and proliferation in vivo. Antimicrob Agents Chemother 2016; 60:968–981 [View Article] [PubMed]
     [Google Scholar]
  18. Zhang B-Z, Cai J, Yu B, Hua Y, Lau CC et al. A DNA vaccine targeting TcdA and TcdB induces protective immunity against Clostridium difficile. BMC Infect Dis 2016; 16:596 [View Article] [PubMed]
     [Google Scholar]
  19. Miezeiewski M, Schnaufer T, Muravsky M, Wang S, Caro-Aguilar I et al. An in vitro culture model to study the dynamics of colonic microbiota in Syrian golden hamsters and their susceptibility to infection with Clostridium difficile. ISME J 2015; 9:321–332 [View Article] [PubMed]
     [Google Scholar]
  20. Wilson KH, Sheagren JN, Freter R. Population dynamics of ingested Clostridium difficile in the gastrointestinal tract of the Syrian hamster. J Infect Dis 1985; 151:355–361 [View Article] [PubMed]
     [Google Scholar]
  21. Abutaleb NS, Seleem MN. In vivo efficacy of auranofin in a hamster model of Clostridioides difficile infection. Sci Rep 2021; 11:7093 [View Article] [PubMed]
     [Google Scholar]
  22. Koon HW, Su B, Xu C, Mussatto CC, Tran DH-N et al. Probiotic Saccharomyces boulardii CNCM I-745 prevents outbreak-associated Clostridium difficile-associated cecal inflammation in hamsters. Am J Physiol Gastrointest Liver Physiol 2016; 311:G610–G623 [View Article] [PubMed]
     [Google Scholar]
  23. Bilverstone TW, Garland M, Cave RJ, Kelly ML, Tholen M et al. The glucosyltransferase activity of C. difficile Toxin B is required for disease pathogenesis. PLoS Pathog 2020; 16:e1008852 [View Article] [PubMed]
     [Google Scholar]
  24. Karyal C, Hughes J, Kelly ML, Luckett JC, Kaye PV et al. Colonisation factor CD0873, an attractive oral vaccine candidate against Clostridioides difficile. Microorganisms 2021; 9:306 [View Article] [PubMed]
     [Google Scholar]
  25. Borriello SP, Ketley JM, Mitchell TJ, Barclay FE, Welch AR 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 1987; 24:53–64 [View Article] [PubMed]
     [Google Scholar]
  26. Hong HA, Ferreira WT, Hosseini S, Anwar S, Hitri K et al. The spore coat protein CotE facilitates host colonization by Clostridium difficile. J Infect Dis 2017; 216:1452–1459 [View Article] [PubMed]
     [Google Scholar]
  27. Trzilova D, Warren MAH, Gadda NC, Williams CL, Tamayo R. Flagellum and toxin phase variation impacts intestinal colonization and disease development in a mouse model of Clostridioides difficile infection. Gut Microbes 2022; 14:2038854 [View Article] [PubMed]
     [Google Scholar]
  28. Simpson M, Bilverstone T, Leslie J, Donlan A, Uddin MJ et al. Clostridioides difficile binary toxin binding component increases virulence in a hamster model. Open Forum Infect Dis 2023; 10:ofad040 [View Article] [PubMed]
     [Google Scholar]
  29. Hu X, Dong R, Huang S, Zeng Y, Zhan W et al. CDBN-YGXZ, a novel small-molecule drug, shows efficacy against Clostridioides difficile infection and recurrence in mouse and hamster infection models. Antimicrob Agents Chemother 2023; 67:e01704-22 [View Article] [PubMed]
     [Google Scholar]
  30. Phan JR, Do DM, Truong MC, Ngo C, Phan JH et al. An aniline-substituted bile salt analog protects both mice and hamsters from multiple Clostridioides difficile strains. Antimicrob Agents Chemother 2022; 66:e01435-21 [View Article]
     [Google Scholar]
  31. Bhute SS, Mefferd CC, Phan JR, Ahmed M, Fox-King AE et al. A high-carbohydrate diet prolongs dysbiosis and Clostridioides difficile carriage and increases delayed mortality in a hamster model of infection. Microbiol Spectr 2022; 10:e01804–21 [View Article]
     [Google Scholar]
  32. Onderdonk AB, Cisneros RL, Bartlett JG. Clostridium difficile in gnotobiotic mice. Infect Immun 1980; 28:277–282 [View Article] [PubMed]
     [Google Scholar]
  33. Vernet A, Corthier G, Dubos-Ramaré F, Parodi AL. Relationship between levels of Clostridium difficile toxin A and toxin B and cecal lesions in gnotobiotic mice. Infect Immun 1989; 57:2123–2127 [View Article] [PubMed]
     [Google Scholar]
  34. Corthier G, Muller MC, Wilkins TD, Lyerly D, L’Haridon R. Protection against experimental pseudomembranous colitis in gnotobiotic mice by use of monoclonal antibodies against Clostridium difficile toxin A. Infect Immun 1991; 59:1192–1195 [View Article] [PubMed]
     [Google Scholar]
  35. Depitre C, Delmee M, Avesani V, L’Haridon R, Roels A et al. Serogroup F strains of Clostridium difficile produce toxin B but not toxin A. J Med Microbiol 1993; 38:434–441 [View Article] [PubMed]
     [Google Scholar]
  36. Corthier G, Dubos F, Raibaud P. Modulation of cytotoxin production by Clostridium difficile in the intestinal tracts of gnotobiotic mice inoculated with various human intestinal bacteria. Appl Environ Microbiol 1985; 49:250–252 [View Article] [PubMed]
     [Google Scholar]
  37. Reeves AE, Koenigsknecht MJ, Bergin IL, Young VB. Suppression of Clostridium difficile in the gastrointestinal tracts of germfree mice inoculated with a murine isolate from the family Lachnospiraceae. Infect Immun 2012; 80:3786–3794 [View Article] [PubMed]
     [Google Scholar]
  38. Girinathan BP, DiBenedetto N, Worley JN, Peltier J, Arrieta-Ortiz ML et al. Invivo commensal control of Clostridioides difficile virulence. Cell Host Microbe 2021; 29:1693–1708 [View Article] [PubMed]
     [Google Scholar]
  39. Ng KM, Ferreyra JA, Higginbottom SK, Lynch JB, Kashyap PC et al. Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature 2013; 502:96–99 [View Article] [PubMed]
     [Google Scholar]
  40. Ferreyra JA, Wu KJ, Hryckowian AJ, Bouley DM, Weimer BC et al. Gut microbiota-produced succinate promotes C. difficile infection after antibiotic treatment or motility disturbance. Cell Host Microbe 2014; 16:770–777 [View Article] [PubMed]
     [Google Scholar]
  41. Spigaglia P, Barketi-Klai A, Collignon A, Mastrantonio P, Barbanti F et al. Surface-layer (S-layer) of human and animal Clostridium difficile strains and their behaviour in adherence to epithelial cells and intestinal colonization. J Med Microbiol 2013; 62:1386–1393 [View Article] [PubMed]
     [Google Scholar]
  42. Kink JA, Williams JA. Antibodies to recombinant Clostridium difficile toxins A and B are an effective treatment and prevent relapse of C. difficile-associated disease in A hamster model of infection. Infect Immun 1998; 66:2018–2025 [View Article] [PubMed]
     [Google Scholar]
  43. Bradshaw WJ, Bruxelle J-F, Kovacs-Simon A, Harmer NJ, Janoir C et al. Molecular features of lipoprotein CD0873: a potential vaccine against the human pathogen Clostridioides difficile. J Biol Chem 2019; 294:15850–15861 [View Article] [PubMed]
     [Google Scholar]
  44. Giordano N, Hastie JL, Smith AD, Foss ED, Gutierrez-Munoz DF et al. Cysteine desulfurase IscS2 plays a role in oxygen resistance in Clostridium difficile. Infect Immun 2018; 86:e00326-18 [View Article] [PubMed]
     [Google Scholar]
  45. Janoir C, Denève C, Bouttier S, Barbut F, Hoys S et al. Adaptive strategies and pathogenesis of Clostridium difficile from in vivo transcriptomics. Infect Immun 2013; 81:3757–3769 [View Article] [PubMed]
     [Google Scholar]
  46. Kansau I, Barketi-Klai A, Monot M, Hoys S, Dupuy B et al. Deciphering adaptation strategies of the epidemic Clostridium difficile 027 strain during infection through in vivo transcriptional analysis. PLoS One 2016; 11:e0158204 [View Article] [PubMed]
     [Google Scholar]
  47. Pruss KM, Sonnenburg JL. C. difficile exploits a host metabolite produced during toxin-mediated disease. Nature 2021; 593:261–265 [View Article] [PubMed]
     [Google Scholar]
  48. Pruss KM, Enam F, Battaglioli E, DeFeo M, Diaz OR et al. Oxidative ornithine metabolism supports non-inflammatory C. difficile colonization. Nat Metab 2022; 4:19–28 [View Article] [PubMed]
     [Google Scholar]
  49. Castex F, Jouvert S, Bastide M, Corthier G. Kinetics of appearance of intestinal lesions in mice mono-associated with a lethal or non-lethal strain of Clostridium difficile. J Med Microbiol 1994; 40:102–109 [View Article] [PubMed]
     [Google Scholar]
  50. Soavelomandroso AP, Gaudin F, Hoys S, Nicolas V, Vedantam G et al. Biofilm structures in a mono-associated mouse model of Clostridium difficile infection. Front Microbiol 2017; 8:2086 [View Article] [PubMed]
     [Google Scholar]
  51. Studer N, Desharnais L, Beutler M, Brugiroux S, Terrazos MA et al. Functional intestinal bile acid 7α-dehydroxylation by Clostridium scindens associated with protection from Clostridium difficile infection in a gnotobiotic mouse model. Front Cell Infect Microbiol 2016; 6:191 [View Article] [PubMed]
     [Google Scholar]
  52. Péchiné S, Janoir C, Boureau H, Gleizes A, Tsapis N et al. Diminished intestinal colonization by Clostridium difficile and immune response in mice after mucosal immunization with surface proteins of Clostridium difficile. Vaccine 2007; 25:3946–3954 [View Article] [PubMed]
     [Google Scholar]
  53. Battaglioli EJ, Hale VL, Chen J, Jeraldo P, Ruiz-Mojica C et al. Clostridioides difficile uses amino acids associated with gut microbial dysbiosis in a subset of patients with diarrhea. Sci Transl Med 2018; 10:eaam7019 [View Article] [PubMed]
     [Google Scholar]
  54. Pu M, Cho JM, Cunningham SA, Behera GK, Becker S et al. Plasmid acquisition alters vancomycin susceptibility in Clostridioides difficile. Gastroenterology 2021; 160:941–945 [View Article] [PubMed]
     [Google Scholar]
  55. Kumar R, Maynard CL, Eipers P, Goldsmith KT, Ptacek T et al. Colonization potential to reconstitute a microbe community in patients detected early after fecal microbe transplant for recurrent C. difficile. BMC Microbiol 2016; 16:5 [View Article] [PubMed]
     [Google Scholar]
  56. Collins J, Auchtung JM, Schaefer L, Eaton KA, Britton RA. Humanized microbiota mice as a model of recurrent Clostridium difficile disease. Microbiome 2015; 3:35 [View Article] [PubMed]
     [Google Scholar]
  57. Hugenholtz F, de Vos WM. Mouse models for human intestinal microbiota research: a critical evaluation. Cell Mol Life Sci 2018; 75:149–160 [View Article] [PubMed]
     [Google Scholar]
  58. Dabard J, Dubos F, Martinet L, Ducluzeau R. Experimental reproduction of neonatal diarrhea in young gnotobiotic hares simultaneously associated with Clostridium difficile and other Clostridium strains. Infect Immun 1979; 24:7–11 [View Article] [PubMed]
     [Google Scholar]
  59. Czuprynski CJ, Johnson WJ, Balish E, Wilkins T. Pseudomembranous colitis in Clostridium difficile-monoassociated rats. Infect Immun 1983; 39:1368–1376 [View Article] [PubMed]
     [Google Scholar]
  60. Schmidt DJ, Beamer G, Tremblay JM, Steele JA, Kim HB et al. A tetraspecific VHH-based neutralizing antibody modifies disease outcome in three animal models of Clostridium difficile infection. Clin Vaccine Immunol 2016; 23:774–784 [View Article] [PubMed]
     [Google Scholar]
  61. Thran M, Pönisch M, Danz H, Horscroft N, Ichtchenko K et al. Co-administration of an effector antibody enhances the half-life and therapeutic potential of RNA-encoded nanobodies. Sci Rep 2023; 13:14632 [View Article] [PubMed]
     [Google Scholar]
  62. Herzog MK-M, Cazzaniga M, Peters A, Shayya N, Beldi L et al. Mouse models for bacterial enteropathogen infections: insights into the role of colonization resistance. Gut Microbes 2023; 15:2172667 [View Article] [PubMed]
     [Google Scholar]
  63. Pavao A, Graham M, Trofimuk O, Delaney ML, Yeliseyev V et al. Protocol for using negative pressure isolator systems to study BSL-2 organisms in gnotobiotic murine models. STAR Protoc 2022; 3:101211 [View Article] [PubMed]
     [Google Scholar]
  64. Smith K, McCoy KD, Macpherson AJ. Use of axenic animals in studying the adaptation of mammals to their commensal intestinal microbiota. Semin Immunol 2007; 19:59–69 [View Article] [PubMed]
     [Google Scholar]
  65. Bhattarai Y, Kashyap PC. Germ-free mice model for studying host-microbial interactions. Methods Mol Biol 2016; 1438:123–135 [View Article] [PubMed]
     [Google Scholar]
  66. Shelby RD, Tengberg N, Conces M, Olson JK, Navarro JB et al. Development of a standardized scoring system to assess a murine model of Clostridium difficile colitis. J Invest Surg 2020; 33:887–895 [View Article] [PubMed]
     [Google Scholar]
  67. Chen X, Katchar K, Goldsmith JD, Nanthakumar N, Cheknis A et al. A mouse model of Clostridium difficile-associated disease. Gastroenterology 2008; 135:1984–1992 [View Article] [PubMed]
     [Google Scholar]
  68. Castro-Córdova P, Díaz-Yáñez F, Muñoz-Miralles J, Gil F, Paredes-Sabja D. Effect of antibiotic to induce Clostridioides difficile-susceptibility and infectious strain in a mouse model of Clostridioides difficile infection and recurrence. Anaerobe 2020; 62:102149 [View Article] [PubMed]
     [Google Scholar]
  69. Pensinger DA, Fisher AT, Dobrila HA, Van Treuren W, Gardner JO et al. Butyrate differentiates permissiveness to Clostridioides difficile infection and influences growth of diverse C. difficile isolates. Infect Immun 2023; 91:e0057022 [View Article] [PubMed]
     [Google Scholar]
  70. Jenior ML, Leslie JL, Young VB, Schloss PD. Clostridium difficile alters the structure and metabolism of distinct cecal microbiomes during initial infection to promote sustained colonization. mSphere 2018; 3:e00261-18 [View Article] [PubMed]
     [Google Scholar]
  71. Reeves AE, Theriot CM, Bergin IL, Huffnagle GB, Schloss PD et al. The interplay between microbiome dynamics and pathogen dynamics in a murine model of Clostridium difficile infection. Gut Microbes 2011; 2:145–158 [View Article] [PubMed]
     [Google Scholar]
  72. Theriot CM, Koumpouras CC, Carlson PE, Bergin II, Aronoff DM et al. Cefoperazone-treated mice as an experimental platform to assess differential virulence of Clostridium difficile strains. Gut Microbes 2011; 2:326–334 [View Article]
     [Google Scholar]
  73. Schubert AM, Sinani H, Schloss PD. Clearance of Clostridioides difficile colonization is associated with antibiotic-specific bacterial changes. mSphere 2021; 6:e01238-20 [View Article]
     [Google Scholar]
  74. Buffie CG, Bucci V, Stein RR, McKenney PT, Ling L et al. Precision microbiome reconstitution restores bile acid mediated resistance to Clostridium difficile. Nature 2015; 517:205–208 [View Article] [PubMed]
     [Google Scholar]
  75. Shin JH, Pawlowski SW, Warren CA. Teaching old mice new tricks: the utility of aged mouse models of C. difficile infection to study pathogenesis and rejuvenate immune response. Gut Microbes 2021; 13:1966255 [View Article] [PubMed]
     [Google Scholar]
  76. Abernathy-Close L, Barron MR, George JM, Dieterle MG, Vendrov KC et al. Intestinal inflammation and altered gut microbiota associated with inflammatory bowel disease render mice susceptible to Clostridioides difficile colonization and infection. mBio 2021; 12:e0273320 [View Article] [PubMed]
     [Google Scholar]
  77. Lee W-T, Wu Y-N, Chen Y-H, Wu S-R, Shih T-M et al. Octahedron iron oxide nanocrystals prohibited Clostridium difficile spore germination and attenuated local and systemic inflammation. Sci Rep 2017; 7:8124 [View Article]
     [Google Scholar]
  78. Tomkovich S, Stough JMA, Bishop L, Schloss PD. The initial gut microbiota and response to antibiotic perturbation influence Clostridioides difficile clearance in mice. mSphere 2020; 5:e00869-20 [View Article] [PubMed]
     [Google Scholar]
  79. Oberkampf M, Hamiot A, Altamirano-Silva P, Bellés-Sancho P, Tremblay YDN et al. c-di-AMP signaling is required for bile salt resistance, osmotolerance, and long-term host colonization by Clostridioides difficile. Sci Signal 2022; 15:eabn8171 [View Article] [PubMed]
     [Google Scholar]
  80. Fletcher JR, Erwin S, Lanzas C, Theriot CM. Shifts in the gut metabolome and Clostridium difficile transcriptome throughout colonization and infection in a mouse model. mSphere 2018; 3:e00089-18 [View Article] [PubMed]
     [Google Scholar]
  81. Fletcher JR, Pike CM, Parsons RJ, Rivera AJ, Foley MH et al. Clostridioides difficile exploits toxin-mediated inflammation to alter the host nutritional landscape and exclude competitors from the gut microbiota. Nat Commun 2021; 12:462 [View Article]
     [Google Scholar]
  82. Theriot CM, Koenigsknecht MJ, Carlson PE, Hatton GE, Nelson AM et al. Antibiotic-induced shifts in the mouse gut microbiome and metabolome increase susceptibility to Clostridium difficile infection. Nat Commun 2014; 5:3114 [View Article] [PubMed]
     [Google Scholar]
  83. Koenigsknecht MJ, Theriot CM, Bergin IL, Schumacher CA, Schloss PD et al. Dynamics and establishment of Clostridium difficile infection in the murine gastrointestinal tract. Infect Immun 2015; 83:934–941 [View Article] [PubMed]
     [Google Scholar]
  84. Li X, Kang Y, Huang Y, Xiao Y, Song L et al. A strain of Bacteroides thetaiotaomicron attenuates colonization of Clostridioides difficile and affects intestinal microbiota and bile acids profile in a mouse model. Biomed Pharmacother 2021; 137:111290 [View Article]
     [Google Scholar]
  85. Foley MH, Walker ME, Stewart AK, O’Flaherty S, Gentry EC et al. Bile salt hydrolases shape the bile acid landscape and restrict Clostridioides difficile growth in the murine gut. Nat Microbiol 2023; 8:611–628 [View Article] [PubMed]
     [Google Scholar]
  86. Wexler AG, Guiberson ER, Beavers WN, Shupe JA, Washington MK et al. Clostridioides difficile infection induces a rapid influx of bile acids into the gut during colonization of the host. Cell Rep 2021; 36:109683 [View Article] [PubMed]
     [Google Scholar]
  87. Hazleton KZ, Martin CG, Orlicky DJ, Arnolds KL, Nusbacher NM et al. Dietary fat promotes antibiotic-induced Clostridioides difficile mortality in mice. NPJ Biofilms Microbiom 2022; 8:15 [View Article] [PubMed]
     [Google Scholar]
  88. Yakabe K, Higashi S, Akiyama M, Mori H, Murakami T et al. Dietary-protein sources modulate host susceptibility to Clostridioides difficile infection through the gut microbiota. Cell Rep 2022; 40:111332 [View Article] [PubMed]
     [Google Scholar]
  89. Hutton ML, Pehlivanoglu H, Vidor CJ, James ML, Thomson MJ et al. Repurposing auranofin as a Clostridioides difficile therapeutic. J Antimicrob Chemother 2019 [View Article]
     [Google Scholar]
  90. De Wolfe TJ, Kates AE, Barko L, Darien BJ, Safdar N. Modified mouse model of Clostridioides difficile infection as a platform for probiotic efficacy studies. Antimicrob Agents Chemother 2019; 63:e00111-19 [View Article] [PubMed]
     [Google Scholar]
  91. Yang J, Meng L, Yang H. Therapeutic effects of bifidobacterium breve YH68 in combination with vancomycin and metronidazole in a primary Clostridioides difficile-infected mouse model. Microbiol Spectr 2022; 10:e0067222 [View Article] [PubMed]
     [Google Scholar]
  92. Larsen IS, Chenaux M, Collins FWJ, Mandic A, Hansen LBS et al. Bacillus velezensis DSM 33864 reduces Clostridioides difficile colonization without disturbing commensal gut microbiota composition. Sci Rep 2023; 13:14941 [View Article] [PubMed]
     [Google Scholar]
  93. Koh E, Hwang IY, Lee HL, De Sotto R, Lee JWJ et al. Engineering probiotics to inhibit Clostridioides difficile infection by dynamic regulation of intestinal metabolism. Nat Commun 2022; 13:3834 [View Article] [PubMed]
     [Google Scholar]
  94. Hirano R, Sakanaka M, Yoshimi K, Sugimoto N, Eguchi S et al. Next-generation prebiotic promotes selective growth of bifidobacteria, suppressing Clostridioides difficile. Gut Microbes 2021; 13:1973835 [View Article] [PubMed]
     [Google Scholar]
  95. Madan R, Petri WA. Immune responses to Clostridium difficile infection. Trends Mol Med 2012; 18:658–666 [View Article] [PubMed]
     [Google Scholar]
  96. Xu B, Wu X, Gong Y, Cao J. IL-27 induces LL-37/CRAMP expression from intestinal epithelial cells: implications for immunotherapy of Clostridioides difficile infection. Gut Microbes 2021; 13:1968258 [View Article] [PubMed]
     [Google Scholar]
  97. Leslie JL, Vendrov KC, Jenior ML, Young VB. The gut microbiota is associated with clearance of Clostridium difficile infection independent of adaptive immunity. mSphere 2019; 4:e00698-18 [View Article] [PubMed]
     [Google Scholar]
  98. Littmann ER, Lee J-J, Denny JE, Alam Z, Maslanka JR et al. Host immunity modulates the efficacy of microbiota transplantation for treatment of Clostridioides difficile infection. Nat Commun 2021; 12:755 [View Article] [PubMed]
     [Google Scholar]
  99. Wang S, Ju X, Heuler J, Zhang K, Duan Z et al. Recombinant fusion protein vaccine containing Clostridioides difficile FliC and FliD protects mice against C. difficile infection. Infect Immun 2023; 91:e0016922 [View Article] [PubMed]
     [Google Scholar]
  100. Sun X, Wang H, Zhang Y, Chen K, Davis B et al. Mouse relapse model of Clostridium difficile infection. Infect Immun 2011; 79:2856–2864 [View Article] [PubMed]
     [Google Scholar]
  101. Elmer GW, McFarland LV. Suppression by Saccharomyces boulardii of toxigenic Clostridium difficile overgrowth after vancomycin treatment in hamsters. Antimicrob Agents Chemother 1987; 31:129–131 [View Article]
     [Google Scholar]
  102. Seekatz AM, Theriot CM, Molloy CT, Wozniak KL, Bergin IL et al. Fecal microbiota transplantation eliminates Clostridium difficile in a murine model of relapsing disease. Infect Immun 2015; 83:3838–3846 [View Article] [PubMed]
     [Google Scholar]
  103. van Prehn J, Reigadas E, Vogelzang EH, Bouza E, Hristea A et al. European Society of Clinical Microbiology and Infectious Diseases: 2021 update on the treatment guidance document for Clostridioides difficile infection in adults. Clin Microbiol Infect 2021; 27:S1–S21 [View Article] [PubMed]
     [Google Scholar]
  104. Louie TJ, Miller MA, Mullane KM, Weiss K, Lentnek A et al. Fidaxomicin versus vancomycin for Clostridium difficile infection. N Engl J Med 2011; 364:422–431 [View Article]
     [Google Scholar]
  105. Warren CA, van Opstal E, Ballard TE, Kennedy A, Wang X et al. Amixicile, a novel inhibitor of pyruvate: ferredoxin oxidoreductase, shows efficacy against Clostridium difficile in a mouse infection model. Antimicrob Agents Chemother 2012; 56:4103–4111 [View Article] [PubMed]
     [Google Scholar]
  106. Abutaleb NS, Seleem MN. Auranofin, at clinically achievable dose, protects mice and prevents recurrence from Clostridioides difficile infection. Sci Rep 2020; 10:7701 [View Article] [PubMed]
     [Google Scholar]
  107. Naclerio GA, Abutaleb NS, Li D, Seleem MN, Sintim HO. Ultrapotent inhibitor of Clostridioides difficile growth, which suppresses recurrence in vivo. J Med Chem 2020; 63:11934–11944
     [Google Scholar]
  108. Deakin LJ, Clare S, Fagan RP, Dawson LF, Pickard DJ et al. The Clostridium difficile spo0A gene is a persistence and transmission factor. Infect Immun 2012; 80:2704–2711 [View Article] [PubMed]
     [Google Scholar]
  109. Passmore IJ, Letertre MPM, Preston MD, Bianconi I, Harrison MA et al. Para-cresol production by Clostridium difficile affects microbial diversity and membrane integrity of Gram-negative bacteria. PLoS Pathog 2018; 14:e1007191 [View Article] [PubMed]
     [Google Scholar]
  110. Hu C, Garey KW. Nonmammalian models to study Clostridioides difficile infection; a systematic review. Anaerobe 2023; 79:102694 [View Article] [PubMed]
     [Google Scholar]
/content/journal/jmm/10.1099/jmm.0.001857
Loading
The state of play of rodent models for the study of Clostridioides difficile infection
J. Med. Microbiol. 73, 001857 (2024); https://doi.org/10.1099/jmm.0.001857
/content/journal/jmm/10.1099/jmm.0.001857
/content/journal/jmm/10.1099/jmm.0.001857
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error