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Clostridium difficile Exposures, Colonization, and the Microbiome: Implications for Prevention

Published online by Cambridge University Press:  19 March 2018

Sara L. Revolinski  and
L. Silvia Munoz-Price
Sara L. Revolinski
Affiliation:
Department of Pharmacy, Froedtert Hospital, Milwaukee, Wisconsin School of Pharmacy, Medical College of Wisconsin, Milwaukee, Wisconsin
L. Silvia Munoz-Price*
Affiliation:
Division of Infectious Diseases, Department of Medicine, Medical College of Wisconsin, Milwaukee, Wisconsin
*
Address correspondence to L. Silvia Munoz-Price, MD, PhD, 9200 W Wisconsin Ave, Milwaukee, WI 53226 (smunozprice@mcw.edu).
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Abstract

New studies have been published regarding the epidemiology of Clostridium difficile in topics such as asymptomatic C. difficile colonization, community-associated C. difficile infection, environmental contamination outside healthcare settings, animal colonization, and the interactions between C. difficile and the gut microbiome. In addition to summarizing these findings, this review offers a perspective on the potential impact of high-throughput sequencing and other potential techniques on the prevention of C. difficile.

Infect Control Hosp Epidemiol 2018;39:596–602

Type
Review Article
Information
Infection Control & Hospital Epidemiology , Volume 39 , Issue 5 , May 2018 , pp. 596 - 602
Copyright
© 2018 by The Society for Healthcare Epidemiology of America. All rights reserved 

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References

REFERENCES

1. Loo, VG, Bourgault, AM, Poirier, L, et al. Host and pathogen factors for Clostridium difficile infection and colonization. N Engl J Med 2011;365:1693–1703.CrossRefGoogle ScholarPubMed
2. Alasmari, F, Seiler, SM, Hink, T, Burnham, CA, Dubberke, ER. Prevalence and risk factors for asymptomatic Clostridium difficile carriage. Clin Infect Dis 2014;59:216–222.Google Scholar
3. Furuya-Kanamori, L, Clements, AC, Foster, NF, et al. Asymptomatic Clostridium difficile colonization in two Australian tertiary hospitals, 2012–2014: prospective, repeated cross-sectional study. Clin Microbiol Infect 2017;23:48.e1–48.e7.Google Scholar
4. Pires, D, Prendki, V, Renzi, G, et al. Low frequency of asymptomatic carriage of toxigenic Clostridium difficile in an acute care geriatric hospital: prospective cohort study in Switzerland. Antimicrob Resist Infect Control 2016;5:24.Google Scholar
5. Blixt, T, Gradel, KO, Homann, C, et al. Asymptomatic carriers contribute to nosocomial Clostridium difficile infection: a cohort study of 4,508 patients. Gastroenterology 2017;152:1031–1041.Google Scholar
6. Zacharioudakis, IM, Zervou, FN, Pliakos, EE, Ziakas, PD, Mylonakis, E. Colonization with toxinogenic C. difficile upon hospital admission, and risk of infection: a systematic review and meta-analysis. Am J Gastroenterol 2015;110:381–390.Google Scholar
7. Kamboj, M, Sheahan, A, Sun, J, et al. Transmission of Clostridium difficile during hospitalization for allogeneic stem cell transplant. Infect Control Hosp Epidemiol 2016;37:8–15.CrossRefGoogle ScholarPubMed
8. Bruminhent, J, Wang, ZX, Hu, C, et al. Clostridium difficile colonization and disease in patients undergoing hematopoietic stem cell transplantation. Biol Blood Marrow Transplant 2014;20:1329–1334.CrossRefGoogle ScholarPubMed
9. Jain, T, Croswell, C, Urday-Cornejo, V, et al. Clostridium difficile colonization in hematopoietic stem cell transplant recipients: a prospective study of the epidemiology and outcomes involving toxigenic and nontoxigenic strains. Biol Blood Marrow Transplant 2016;22:157–163.Google Scholar
10. Cannon, CM, Musuuza, JS, Barker, AK, et al. Risk of Clostridium difficile infection in hematology-oncology patients colonized with toxigenic C. difficile . Infect Control Hosp Epidemiol 2017;38:718–720.Google Scholar
11. Gerding, DN, Meyer, T, Lee, C, et al. Administration of spores of nontoxigenic Clostridium difficile strain M3 for prevention of recurrent C. difficile infection: a randomized clinical trial. JAMA 2015;313:1719–1727.Google Scholar
12. Longtin, Y, Paquet-Bolduc, B, Gilca, R, et al. Effect of detecting and isolating Clostridium difficile carriers at hospital admission on the incidence of C. difficile infections: a quasi-experimental controlled study. JAMA Intern Med 2016;176:796–804.Google Scholar
13. Eyre, DW, Griffiths, D, Vaughan, A, et al. Asymptomatic Clostridium difficile colonisation and onward transmission. PLoS One 2013;8:e78445.Google Scholar
14. Eyre, DW, Fawley, WN, Best, EL, et al. Comparison of multilocus variable-number tandem-repeat analysis and whole-genome sequencing for investigation of Clostridium difficile transmission. J Clin Microbiol 2013;51:4141–4149.Google Scholar
15. Didelot, X, Eyre, DW, Cule, M, et al. Microevolutionary analysis of Clostridium difficile genomes to investigate transmission. Genome Biol 2012;13:R118.Google Scholar
16. Eyre, DW, Cule, ML, Wilson, DJ, et al. Diverse sources of C. difficile infection identified on whole-genome sequencing. N Engl J Med 2013;369:1195–1205.Google Scholar
17. Khanna, S, Pardi, DS, Aronson, SL, et al. The epidemiology of community-acquired Clostridium difficile infection: a population-based study. Am J Gastroenterol 2012;107:89–95.CrossRefGoogle ScholarPubMed
18. Lessa, FC, Winston, LG, McDonald, LC. Burden of Clostridium difficile infection in the United States. N Engl J Med 2015;372:2369–2370.Google Scholar
19. Lessa, FC, Mu, Y, Winston, LG, et al. Determinants of Clostridium difficile infection incidence across diverse United States geographic locations. Open Forum Infect Dis 2014;1:ofu048.Google Scholar
20. Kotila, SM, Mentula, S, Ollgren, J, Virolainen-Julkunen, A, Lyytikainen, O. Community- and healthcare-associated Clostridium difficile infections, Finland, 2008–2013. Emerg Infect Dis 2016;22:1747–1753.Google Scholar
21. Furuya-Kanamori, L, Yakob, L, Riley, TV, et al. Community-acquired Clostridium difficile infection, Queensland, Australia. Emerg Infect Dis 2016;22:1659–1661.Google Scholar
22. Eyre, DW, Tracey, L, Elliott, B, et al. Emergence and spread of predominantly community-onset Clostridium difficile PCR ribotype 244 infection in Australia, 2010 to 2012. Euro Surveill 2015;20:21059.CrossRefGoogle ScholarPubMed
23. Fawley, WN, Davies, KA, Morris, T, Parnell, P, Howe, R, Wilcox, MH. Enhanced surveillance of Clostridium difficile infection occurring outside hospital, England, 2011 to 2013. Euro Surveill 2016;21(29): doi: 10.2807/1560-7917.ES.2016.21.29.30295.Google Scholar
24. Naggie, S, Miller, BA, Zuzak, KB, et al. A case-control study of community-associated Clostridium difficile infection: no role for proton pump inhibitors. Am J Med 2011;124:276–277.Google Scholar
25. Kuntz, JL, Chrischilles, EA, Pendergast, JF, Herwaldt, LA, Polgreen, PM. Incidence of and risk factors for community-associated Clostridium difficile infection: a nested case-control study. BMC Infect Dis 2011;11:194.Google Scholar
26. Wilcox, MH, Mooney, L, Bendall, R, Settle, CD, Fawley, WN. A case-control study of community-associated Clostridium difficile infection. J Antimicrob Chemother 2008;62:388–396.Google Scholar
27. Deshpande, A, Pasupuleti, V, Thota, P, et al. Community-associated Clostridium difficile infection and antibiotics: a meta-analysis. J Antimicrob Chemother 2013;68:1951–1961.Google Scholar
28. Chitnis, AS, Holzbauer, SM, Belflower, RM, et al. Epidemiology of community-associated Clostridium difficile infection, 2009 through 2011. JAMA Intern Med 2013;173:1359–1367.Google Scholar
29. Kim, KH, Fekety, R, Batts, DH, et al. Isolation of Clostridium difficile from the environment and contacts of patients with antibiotic-associated colitis. J Infect Dis 1981;143:42–50.Google Scholar
30. Sethi, AK, Al-Nassir, WN, Nerandzic, MM, Bobulsky, GS, Donskey, CJ. Persistence of skin contamination and environmental shedding of Clostridium difficile during and after treatment of C. difficile infection. Infect Control Hosp Epidemiol 2010;31:21–27.Google Scholar
31. Sethi, AK, Al-Nassir, WN, Nerandzic, MM, Donskey, CJ. Skin and environmental contamination with vancomycin-resistant Enterococci in patients receiving oral metronidazole or oral vancomycin treatment for Clostridium difficile-associated disease. Infect Control Hosp Epidemiol 2009;30:13–17.Google Scholar
32. Pepin, J, Gonzales, M, Valiquette, L. Risk of secondary cases of Clostridium difficile infection among household contacts of index cases. J Infect 2012;64:387–390.Google Scholar
33. Loo, VG, Brassard, P, Miller, MA. Household transmission of Clostridium difficile to family members and domestic pets. Infect Control Hosp Epidemiol 2016;37:1342–1348.Google Scholar
34. Stoesser, N, Eyre, DW, Quan, TP, et al. Epidemiology of Clostridium difficile in infants in Oxfordshire, UK: risk factors for colonization and carriage, and genetic overlap with regional C. difficile infection strains. PLoS One 2017;12:e0182307.Google Scholar
35. Anderson, DJ, Rojas, LF, Watson, S, et al. Identification of novel risk factors for community-acquired Clostridium difficile infection using spatial statistics and geographic information system analyses. PLoS One 2017;12:e0176285.Google Scholar
36. Fry, PR, Thakur, S, Abley, M, Gebreyes, WA. Antimicrobial resistance, toxinotype, and genotypic profiling of Clostridium difficile isolates of swine origin. J Clin Microbiol 2012;50:2366–2372.Google Scholar
37. Knetsch, CW, Connor, TR, Mutreja, A, et al. Whole-genome sequencing reveals potential spread of Clostridium difficile between humans and farm animals in the Netherlands, 2002 to 2011. Euro Surveill 2014;19:20954.Google Scholar
38. Keessen, EC, Harmanus, C, Dohmen, W, Kuijper, EJ, Lipman, LJ. Clostridium difficile infection associated with pig farms. Emerg Infect Dis 2013;19:1032–1034.Google Scholar
39. Zidaric, V, Zemljic, M, Janezic, S, Kocuvan, A, Rupnik, M. High diversity of Clostridium difficile genotypes isolated from a single poultry farm producing replacement laying hens. Anaerobe 2008;14:325–327.Google Scholar
40. Rodriguez-Palacios, A, Stampfli, HR, Duffield, T, et al. Clostridium difficile PCR ribotypes in calves, Canada. Emerg Infect Dis 2006;12:1730–1736.Google Scholar
41. Rodriguez-Palacios, A, Staempfli, HR, Duffield, T, Weese, JS. Clostridium difficile in retail ground meat, Canada. Emerg Infect Dis 2007;13:485–487.Google Scholar
42. Stone, NE, Sidak-Loftis, LC, Sahl, JW, et al. More than 50% of Clostridium difficile isolates from pet dogs in Flagstaff, USA, carry toxigenic genotypes. PLoS One 2016;11:e0164504.Google Scholar
43. Orden, C, Neila, C, Blanco, JL, et al. Recreational sandboxes for children and dogs can be a source of epidemic ribotypes of Clostridium difficile . Zoonoses Public Health 2018;65:88–95.Google Scholar
44. Rodriguez, C, Taminiau, B, van, BJ, Delmee, M, Daube, G. Clostridium difficile in food and animals: a comprehensive review. Adv Exp Med Biol 2016;932:65–92.Google Scholar
45. Rodriguez-Palacios, A, Ilic, S, LeJeune, JT. Clostridium difficile with moxifloxacin/clindamycin resistance in vegetables in Ohio, USA, and prevalence meta-analysis. J Pathog 2014;2014:158601.Google Scholar
46. al, SN, Brazier, JS. The distribution of Clostridium difficile in the environment of South Wales. J Med Microbiol 1996;45:133–137.Google Scholar
47. Kotila, SM, Pitkanen, T, Brazier, J, et al. Clostridium difficile contamination of public tap water distribution system during a waterborne outbreak in Finland. Scand J Public Health 2013;41:541–545.Google Scholar
48. Britton, RA, Young, VB. Role of the intestinal microbiota in resistance to colonization by Clostridium difficile . Gastroenterology 2014;146:1547–1553.Google Scholar
49. Britton, RA, Young, VB. Interaction between the intestinal microbiota and host in Clostridium difficile colonization resistance. Trends Microbiol 2012;20:313–319.Google Scholar
50. Buffie, CG, Pamer, EG. Microbiota-mediated colonization resistance against intestinal pathogens. Nat Rev Immunol 2013;13:790–801.Google Scholar
51. Lynch, SV, Pedersen, O. The human intestinal microbiome in health and disease. N Engl J Med 2016;375:2369–2379.Google Scholar
52. Young, VB. The role of the microbiome in human health and disease: an introduction for clinicians. BMJ 2017;356:j831.Google Scholar
53. Schubert, AM, Rogers, MA, Ring, C, et al. Microbiome data distinguish patients with Clostridium difficile infection and non-C. difficile-associated diarrhea from healthy controls. MBio 2014;5:e01021–14.Google Scholar
54. Zhang, L, Dong, D, Jiang, C, Li, Z, Wang, X, Peng, Y. Insight into alteration of gut microbiota in Clostridium difficile infection and asymptomatic C. difficile colonization. Anaerobe 2015;34:1–7.Google Scholar
55. Buffie, CG, Bucci, V, Stein, RR, et al. Precision microbiome reconstitution restores bile acid mediated resistance to Clostridium difficile . Nature 2015;517:205–208.CrossRefGoogle ScholarPubMed
56. Studer, N, Desharnais, L, Beutler, M, et al. Functional intestinal bile acid 7alpha-dehydroxylation by Clostridium scindens associated with protection from Clostridium difficile infection in a gnotobiotic mouse model. Front Cell Infect Microbiol 2016;6:191.CrossRefGoogle Scholar
57. Chang, JY, Antonopoulos, DA, Kalra, A, et al. Decreased diversity of the fecal microbiome in recurrent Clostridium difficile-associated diarrhea. J Infect Dis 2008;197:435–438.Google Scholar
58. Knecht, H, Neulinger, SC, Heinsen, FA, et al. Effects of beta-lactam antibiotics and fluoroquinolones on human gut microbiota in relation to Clostridium difficile associated diarrhea. PLoS One 2014;9:e89417.Google Scholar
59. Lewis, BB, Buffie, CG, Carter, RA, et al. Loss of microbiota-mediated colonization resistance to Clostridium difficile infection with oral vancomycin compared with metronidazole. J Infect Dis 2015;212:1656–1665.Google Scholar
60. Abujamel, T, Cadnum, JL, Jury, LA, et al. Defining the vulnerable period for re-establishment of Clostridium difficile colonization after treatment of C. difficile infection with oral vancomycin or metronidazole. PLoS One 2013;8:e76269.Google Scholar
61. Taur, Y, Jenq, RR, Perales, MA, et al. The effects of intestinal tract bacterial diversity on mortality following allogeneic hematopoietic stem cell transplantation. Blood 2014;124:1174–1182.Google Scholar
62. Ross, CL, Spinler, JK, Savidge, TC. Structural and functional changes within the gut microbiota and susceptibility to Clostridium difficile infection. Anaerobe 2016;41:37–43.Google Scholar
63. Theriot, CM, Koenigsknecht, MJ, Carlson, PE Jr, et al. Antibiotic-induced shifts in the mouse gut microbiome and metabolome increase susceptibility to Clostridium difficile infection. Nat Commun 2014;5:3114.Google Scholar
64. Jump, RL, Polinkovsky, A, Hurless, K, et al. Metabolomics analysis identifies intestinal microbiota-derived biomarkers of colonization resistance in clindamycin-treated mice. PLoS One 2014;9:e101267.Google Scholar
65. Allegretti, JR, Kearney, S, Li, N, et al. Recurrent Clostridium difficile infection associates with distinct bile acid and microbiome profiles. Aliment Pharmacol Ther 2016;43:1142–1153.Google Scholar
66. Weingarden, AR, Chen, C, Bobr, A, et al. Microbiota transplantation restores normal fecal bile acid composition in recurrent Clostridium difficile infection. Am J Physiol Gastrointest Liver Physiol 2014;306:G310–G319.Google Scholar
67. Seekatz, AM, Aas, J, Gessert, CE, et al. Recovery of the gut microbiome following fecal microbiota transplantation. MBio 2014;5:e00893–14.Google Scholar
68. Perez-Cobas, AE, Gosalbes, MJ, Friedrichs, A, et al. Gut microbiota disturbance during antibiotic therapy: a multiomic approach. Gut 2013;62:1591–1601.Google Scholar
69. Crofts, TS, Gasparrini, AJ, Dantas, G. Next-generation approaches to understand and combat the antibiotic resistome. Nat Rev Microbiol 2017;15:422–434.CrossRefGoogle ScholarPubMed
70. Halpin, AL, de Man, TJ, Kraft, CS, et al. Intestinal microbiome disruption in patients in a long-term acute care hospital: a case for development of microbiome disruption indices to improve infection prevention. Am J Infect Control 2016;44:830–836.Google Scholar
71. Borriello, SP, Barclay, FE. An in-vitro model of colonisation resistance to Clostridium difficile infection. J Med Microbiol 1986;21:299–309.Google Scholar
72. Obrenovich, ME, Tima, M, Polinkovsky, A, Zhang, R, Emancipator, SN, Donskey, CJ. Targeted metabolomics analysis identifies intestinal microbiota-derived urinary biomarkers of colonization resistance in antibiotic-treated mice. Antimicrob Agents Chemother 2017;61(8):pii e00477–17.Google Scholar
73. Lawes, T, Lopez-Lozano, JM, Nebot, CA, et al. Effect of a national 4C antibiotic stewardship intervention on the clinical and molecular epidemiology of Clostridium difficile infections in a region of Scotland: a nonlinear time-series analysis. Lancet Infect Dis 2017;17:194–206.Google Scholar
74. Dingle, KE, Didelot, X, Quan, TP, et al. Effects of control interventions on Clostridium difficile infection in England: an observational study. Lancet Infect Dis 2017;17:411–421.Google Scholar
75. Revolinski, SL, Wainaina, N, Graham, MB, Munoz-Price, LS. Vertical antimicrobial stewardship to reduce C. difficile colitis in colonized patients. In: Program and abstracts of the Spring Meeting of the Society for Healthcare Epidemiology of America (SHEA); May 18–20, 2016; Atlanta, GA. Abstract 8236.Google Scholar