Clinical implications of antibiotic impact on gastrointestinal microbiota and Clostridium difficile infection

Expert Review of Gastroenterology and Hepatology

Volumn 10, Issue 10, 2016, Pages 1145-1152

  Khanna, Sahil ^a   Pardi, Darrell S ^a  

^a MAYO CLINIC   (United States)

Author keywords

antibiotic associated diarrhea; antibiotics; Clostridium difficile associated diarrhea; Clostridium difficile infection; microbiome; microbiota; stewardship

Indexed keywords

ANTIBIOTIC AGENT; BETA LACTAM ANTIBIOTIC; BETA LACTAMASE INHIBITOR; CARBAPENEM DERIVATIVE; CEPHALOSPORIN DERIVATIVE; CLARITHROMYCIN; CLINDAMYCIN; FIDAXOMICIN; LINCOSAMIDE; MACROLIDE; METRONIDAZOLE; PENICILLIN DERIVATIVE; PLACEBO; POLYPEPTIDE ANTIBIOTIC AGENT; PROBIOTIC AGENT; QUINOLINE DERIVED ANTIINFECTIVE AGENT; RIFAXIMIN; VANCOMYCIN;

ACTINOBACTERIA; AEROBIC BACTERIUM; ANAEROBIC BACTERIUM; ANTIBIOTIC ASSOCIATED DIARRHEA; ANTIBIOTIC THERAPY; BACTERIAL COLONIZATION; BACTEROIDETES; CLOSTRIDIUM DIFFICILE INFECTION; DISEASE ASSOCIATION; DRUG EFFICACY; DYSBIOSIS; ENTEROBACTERIACEAE; ENTEROCOCCUS; FECAL MICROBIOTA TRANSPLANTATION; FIRMICUTES; HELICOBACTER INFECTION; HUMAN; INCIDENCE; INFECTION RISK; INTESTINE FLORA; LONG TERM CARE; PROTEOBACTERIA; REVIEW; RISK FACTOR; SHORT COURSE THERAPY; SPECIES COMPOSITION;

EID: 84961204918     PISSN: 17474124     EISSN: 17474132     Source Type: Journal    
DOI: 10.1586/17474124.2016.1158097     Document Type: Review

References (93)

1. H.Tlaskalová-Hogenová, R.Stepánková, H.Kozáková, et al. The role of gut microbiota (commensal bacteria) and the mucosal barrier in the pathogenesis of inflammatory and autoimmune diseases and cancer:contribution of germ-free and gnotobiotic animal models of human diseases. Cell Mol Immunol. 2011;8:110–120.
2. M.Blaser Antibiotic overuse:stop the killing of beneficial bacteria. Nature. 2011;476:393–394.
3. I.Sekirov, S.L.Russell, L.C.Antunes, et al. Gut microbiota in health and disease. Physiol Rev. 2010;90:859–904.
4. J.Qin, R.Li, J.Raes, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010;464:59–65.
5. M.Rajilić-Stojanović, W.M.de Vos. The first 1000 cultured species of the human gastrointestinal microbiota. FEMS Microbiol Rev. 2014;38:996–1047.• This review provides perspective on the growing knowledge of the GI microbiota.
6. C.Jernberg, S.Löfmark, C.Edlund, et al. Long-term impacts of antibiotic exposure on the human intestinal microbiota. Microbiology. 2010;156:3216–3223.
7. J.G.Bartlett, D.N.Gerding. Clinical recognition and diagnosis of Clostridium difficile infection. Clin Infect Dis. 2008;46(Suppl 1):S12S18.
8. H.E.Jakobsson, C.Jernberg, A.F.Andersson, et al. Short-term antibiotic treatment has differing long-term impacts on the human throat and gut microbiome. PLoS One. 2010;5:e9836.
9. C.Jernberg, S.Löfmark, C.Edlund, et al. Long-term ecological impacts of antibiotic administration on the human intestinal microbiota. ISME J. 2007;1:56–66.• This paper provides insights on long-term impacts of antibiotic exposure.
10. V.Liévin-Le Moal, A.L.Servin. The front line of enteric host defense against unwelcome intrusion of harmful microorganisms:mucins, antimicrobial peptides, and microbiota. Clin Microbiol Rev. 2006;19:315–337.• This is a seminal review on host defense and its complex interactions with enteric pathogens.
11. M.G.Dominguez-Bello, M.J.Blaser, R.E.Ley, et al. Development of the human gastrointestinal microbiota and insights from high-throughput sequencing. Gastroenterology. 2011;140:1713–1719.
12. D.Mariat, O.Firmesse, F.Levenez, et al. The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BMC Microbiol. 2009;9:123.
13. A.W.Walker, J.D.Sanderson, C.Churcher, et al. High-throughput clone library analysis of the mucosa-associated microbiota reveals dysbiosis and differences between inflamed and non-inflamed regions of the intestine in inflammatory bowel disease. BMC Microbiol. 2011;11:7.
14. A.Vrieze, N.E.Van, F.Holleman, et al. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology. 2012;143:913–916.
15. P.J.Turnbaugh, V.K.Ridaura, J.J.Faith, et al. The effect of diet on the human gut microbiome:a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med. 2009;1:6ra14.
16. R.E.Ley, P.J.Turnbaugh, S.Klein, et al. Microbial ecology:human gut microbes associated with obesity. Nature. 2006;444:1022–1023.
17. P.Moayyedi, M.G.Surette, P.T.Kim, et al. Fecal microbiota transplantation induces remission in patients with active ulcerative colitis in a randomized controlled trial. Gastroenterology. 2015;149:102–109.
18. E.B.Hollister, C.Gao, J.Versalovic. Compositional and functional features of the gastrointestinal microbiome and their effects on human health. Gastroenterology. 2014;146:1449–1458.
19. A.K.Benson, S.A.Kelly, R.Legge, et al. Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proc Natl Acad Sci U S A. 2010;107:18933–18938.
20. A.Bleich, A.K.Hansen. Time to include the gut microbiota in the hygienic standardisation of laboratory rodents. Comp Immunol Microbiol Infect Dis. 2012;35:81–92.
21. J.Hansen, A.Gulati, R.B.Sartor. The role of mucosal immunity and host genetics in defining intestinal commensal bacteria. Curr Opin Gastroenterol. 2010;26:564–571.
22. A.Spor, O.Koren, R.Ley. Unravelling the effects of the environment and host genotype on the gut microbiome. Nat Rev Microbiol. 2011;9:279–290.
23. S.Tims, C.Derom, D.M.Jonkers, et al. Microbiota conservation and BMI signatures in adult monozygotic twins. ISME J. 2013;7:707–717.
24. P.J.Turnbaugh, M.Hamady, T.Yatsunenko, et al. A core gut microbiome in obese and lean twins. Nature. 2009;457:480–484.
25. J.P.Van de Merwe, J.H.Stegeman, M.P.Hazenberg. The resident faecal flora is determined by genetic characteristics of the host. Implications for Crohn’s disease? Antonie Van Leeuwenhoek. 1983;49:119–124.
26. E.G.Zoetendal, A.D.L.Akkermans, W.M.Akkermans-van Vliet, et al. The host genotype affects the bacterial community in the human gastrointestinal tract. Microb Ecol Health D. 2001;13:129–134.
27. C.A.Edwards, A.M.Parrett. Intestinal flora during the first months of life:new perspectives. Br J Nutr. 2002;88(Suppl. 1):S11–S18.
28. A.M.Zivkovic, J.B.German, C.B.Lebrilla, et al. Human milk glycobiome and its impact on the infant gastrointestinal microbiota. Proc Natl Acad Sci U S A. 2011;108(Suppl 1):4653–4658.
29. Z.Xu, R.Knight. Dietary effects on human gut microbiome diversity. Br J Nutr. 2015;113(Suppl 1):S1S5.
30. G.D.Wu, F.D.Bushmanc, J.D.Lewis. Diet, the human gut microbiota, and IBD. Anaerobe. 2013;24:117–120.
31. I.Martínez, C.E.Muller, J.Walter. Long-term temporal analysis of the human fecal microbiota revealed a stable core of dominant bacterial species. PLoS One. 2013;8:e69621.
32. P.B.Eckburg, E.M.Bik, C.N.Bernstein, et al. Diversity of the human intestinal microbial flora. Science. 2005;308:1635–1638.
33. D.N.Frank, A.L.St Amand, R.A.Feldman, et al. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A. 2007;104:13780–13785.
34. J.Gerritsen, H.Smidt, G.T.Rijkers, et al. Intestinal microbiota in human health and disease:the impact of probiotics. Genes Nutr. 2011;6:209–240.
35. S.C.Bischoff. ‘Gut health’:a new objective in medicine? BMC Med. 2011;9:24.
36. F.Rafii, J.B.Sutherland, C.E.Cerniglia. Effects of treatment with antimicrobial agents on the human colonic microflora. Ther Clin Risk Manag. 2008;4:1343–1358.• This manuscript provides insights on impacts of antibiotic exposure on the microbiota.
37. M.F.De La Cochetière, T.Durand, P.Lepage, et al. Resilience of the dominant human fecal microbiota upon short-course antibiotic challenge. J Clin Microbiol. 2005;43:5588–5592.
38. M.Sjölund, K.Wreiber, D.I.Andersson, et al. Long-term persistence of resistant Enterococcus species after antibiotics to eradicate Helicobacter pylori. Ann Intern Med. 2003;139:483–487.
39. A.Sullivan, C.Edlund, C.E.Nord. Effect of antimicrobial agents on the ecological balance of human microflora. Lancet Infect Dis. 2001;1:101–114.
40. S.Löfmark, C.Jernberg, J.K.Jansson, et al. Clindamycin-induced enrichment and long-term persistence of resistant Bacteroides spp. and resistance genes. J Antimicrob Chemother. 2006;58:1160–1167.
41. M.Lindgren, S.Löfmark, C.Edlund, et al. Prolonged impact of a one-week course of clindamycin on Enterococcus spp. in human normal microbiota. Scand J Infect Dis. 2009;41:215–219.
42. S.D.Nyberg, M.Österblad, A.J.Hakanen, et al. Long-term antimicrobial resistance in Escherichia coli from human intestinal microbiota after administration of clindamycin. Scand J Infect Dis. 2007;39:514–520.
43. M.Sjölund, E.Tano, M.J.Blaser, et al. Persistence of resistant Staphylococcus epidermidis after single course of clarithromycin. Emerg Infect Dis. 2005;11:1389–1393.
44. J.Garau, D.P.Nicolau, B.Wullt, et al. Antibiotic stewardship challenges in the management of community-acquired infections for prevention of escalating antibiotic resistance. J Global Antimicrob Resist. 2014;2:245–253.
45. S.S.Oberoi, C.Dhingra, G.Sharma, et al. Antibiotics in dental practice:how justified are we. Int Dent J. 2015;65:4–10.
46. B.P.Willing, S.L.Russell, B.B.Finlay. Shifting the balance:antibiotic effects on host-microbiota mutualism. Nat Rev Microbiol. 2011;9:233–243.
47. L.Dethlefsen, S.Huse, M.L.Sogin, et al. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol. 2008;6:e280.
48. L.Dethlefsen, D.A.Relman. Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc Natl Acad Sci U S A. 2011;108(Suppl 1):4554–4561.
49. P.D.Cotter, C.Stanton, R.P.Ross, et al. The impact of antibiotics on the gut microbiota as revealed by high throughput DNA sequencing. Discov Med. 2012;13:193–199.
50. F.C.Lessa, C.V.Gould, L.C.McDonald. Current status of Clostridium difficile infection epidemiology. Clin Infect Dis. 2012;55(Suppl 2):S65S70.
51. L.V.McFarland. Antibiotic-associated diarrhea:epidemiology, trends and treatment. Future Microbiol. 2008;3:563–578.
52. J.G.Bartlett, T.W.Chang, M.Gurwith, et al. Antibiotic-associated pseudomembranous colitis due to toxin-producing clostridia. N Engl J Med. 1978;298:531–534.
53. S.Khanna, D.S.Pardi. Clostridium difficile infection:new insights into management. Mayo Clin Proc. 2012;87:1106–1117.
54. S.Khanna, D.S.Pardi, S.L.Aronson, et al. The epidemiology of community-acquired Clostridium difficile infection:a population-based study. Am J Gastroenterol. 2012;107:89–95.
55. F.C.Lessa, Y.Mu, W.M.Bamberg, et al. Burden of Clostridium difficile infection in the United States. N Engl J Med. 2015;372:825–834.•• The incidence and severity of Clostridium difficile infection continue to increase, resulting in a major public health threat.
56. S.S.Magill, J.R.Edwards, W.Bamberg, et al. Multistate point-prevalence survey of health care-associated infections. N Engl J Med. 2014;370:1198–1208.
57. F.Barbut, A.Richard, K.Hamadi, et al. Epidemiology of recurrences or reinfections of Clostridium difficile-associated diarrhea. J Clin Microbiol. 2000;38:2386–2388.
58. J.Pepin, L.Valiquette, M.E.Alary, et al. Clostridium difficile-associated diarrhea in a region of Quebec from 1991 to 2003:a changing pattern of disease severity. CMAJ. 2004;171:466–472.
59. J.Pepin, N.Saheb, M.A.Coulombe, et al. Emergence of fluoroquinolones as the predominant risk factor for Clostridium difficile-associated diarrhea:a cohort study during an epidemic in Quebec. Clin Infect Dis. 2005;41:1254–1260.
60. J.Freeman, M.P.Bauer, S.D.Baines, et al. The changing epidemiology of Clostridium difficile infections. Clin Microbiol Rev. 2010;23:529–549.
61. G.E.Bignardi. Risk factors for Clostridium difficile infection. J Hosp Infect. 1998;40:1–15.
62. F.J.Tedesco, R.W.Barton, D.H.Alpers. Clindamycin-associated colitis. A prospective study. Ann Intern Med. 1974;81:429–433.
63. J.J.Marr, M.D.Sans, F.J.Tedesco. Bacterial studies of Clindamycin-associated colitis. A preliminary report. Gastroenterology. 1975;69:352–358.
64. S.L.Gorbach. Antibiotics and Clostridium difficile. N Engl J Med. 1999;341:1690–1691.
65. V.G.Loo, L.Poirier, M.A.Miller, et al. A predominantly clonal multi-institutional outbreak of Clostridium difficile-associated diarrhea with high morbidity and mortality. N Engl J Med. 2005;353:2442–2449.
66. R.Gaynes, D.Rimland, E.Killum, et al. Outbreak of Clostridium difficile infection in a long-term care facility:association with gatifloxacin use. Clin Infect Dis. 2004;38:640–645.
67. V.Stevens, G.Dumyati, L.S.Fine, et al. Cumulative antibiotic exposures over time and the risk of Clostridium difficile infection. Clin Infect Dis. 2011;53:42–48.
68. A.Deshpande, V.Pasupuleti, P.Thota, et al. Community-associated Clostridium difficile infection and antibiotics:a meta-analysis. J Antimicrob Chemother. 2013;68:1951–1961.
69. S.H.Cohen, D.N.Gerding, S.Johnson, et al. Clinical practice guidelines for Clostridium difficile infection in adults:2010 update by the society for healthcare epidemiology of America (SHEA) and the infectious diseases society of America (IDSA). Infect Control Hosp Epidemiol. 2010;31:431–455.
70. K.Z.Vardakas, K.A.Polyzos, K.Patouni, et al. Treatment failure and recurrence of Clostridium difficile infection following treatment with vancomycin or metronidazole:a systematic review of the evidence. Int J Antimicrob Agents. 2012;40:1–8.
71. T.Abujamel, J.L.Cadnum, L.A.Jury, 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.
72. D.F.Newton, S.Macfarlane, G.T.Macfarlane. Effects of antibiotics on bacterial species composition and metabolic activities in chemostats containing defined populations of human gut microorganisms. Antimicrob Agents Chemother. 2013;57:2016–2025.
73. I.Brook, H.M.Wexler, E.J.Goldstein. Antianaerobic antimicrobials:spectrum and susceptibility testing. Clin Microbiol Rev. 2013;26:526–546.
74. G.W.Tannock, K.Munro, C.Taylor, et al. A new macrocyclic antibiotic, fidaxomicin (OPT-80), causes less alteration to the bowel microbiota of Clostridium difficile-infected patients than does vancomycin. Microbiology. 2010;156:3354–3359.
75. M.M.Nerandzic, K.Mullane, M.A.Miller, et al. Reduced acquisition and overgrowth of vancomycin-resistant enterococci and Candida species in patients treated with fidaxomicin versus vancomycin for Clostridium difficile infection. Clin Infect Dis. 2012;55(Suppl 2):S121S126.
76. T.J.Louie, J.Emery, W.Krulicki, et al. OPT-80 eliminates Clostridium difficile and is sparing of bacteroides species during treatment of C. difficile infection. Antimicrob Agents Chemother. 2009;53:261–263.
77. T.J.Louie, K.Cannon, B.Byrne, et al. Fidaxomicin preserves the intestinal microbiome during and after treatment of Clostridium difficile infection (CDI) and reduces both toxin reexpression and recurrence of CDI. Clin Infect Dis. 2012;55(Suppl 2):S132S142.
78. T.J.Louie, M.A.Miller, K.M.Mullane, et al. Fidaxomicin versus vancomycin for Clostridium difficile infection. N Engl J Med. 2011;364:422–431.
79. H.L.DuPont, Z.D.Jiang, P.C.Okhuysen, et al. A randomized, double-blind, placebo-controlled trial of rifaximin to prevent travelers’ diarrhea. Ann Intern Med. 2005;142:805–812.
80. S.R.Curry, J.W.Marsh, K.A.Shutt, et al. High frequency of rifampin resistance identified in an epidemic Clostridium difficile clone from a large teaching hospital. Clin Infect Dis. 2009;48:425–429.
81. W.N.Al-Nassir, A.K.Sethi, Y.Li, et al. Both oral metronidazole and oral vancomycin promote persistent overgrowth of vancomycin-resistant enterococci during treatment of Clostridium difficile-associated disease. Antimicrob Agents Chemother. 2008;52:2403–2406.
82. A.K.Sethi, W.N.Al-Nassir, M.M.Nerandzic, et al. 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.
83. C.Caffarelli, F.Cardinale, C.Povesi-Dascola, et al. Use of probiotics in pediatric infectious diseases. Expert Rev Anti Infect Ther. 2015;13:1517–1535.
84. S.Chatterjee, P.Kar, T.Das, et al. Randomised placebo-controlled double blind multicentric trial on efficacy and safety of Lactobacillus acidophilus LA-5 and Bifidobacterium BB-12 for prevention of antibiotic-associated diarrhoea. J Assoc Physicians India. 2013;61:708–712.
85. C.G.Dietrich, T.Kottmann, M.Alavi. Commercially available probiotic drinks containing Lactobacillus casei DN-114001 reduce antibiotic-associated diarrhea. World J Gastroenterol. 2014;20:15837–15844.
86. I.Issa, R.Moucari. Probiotics for antibiotic-associated diarrhea:do we have a verdict? World J Gastroenterol. 2014;20:17788–17795.
87. S.Johnson. Recurrent Clostridium difficile infection:a review of risk factors, treatments, and outcomes. J Infect. 2009;58:403–410.
88. I.Youngster, J.Sauk, C.Pindar, et al. Fecal microbiota transplant for relapsing Clostridium difficile infection using a frozen inoculum from unrelated donors:a randomized, open-label, controlled pilot study. Clin Infect Dis. 2014;58:1515–1522.
89. E.Van Nood, A.Vrieze, M.Nieuwdorp, et al. Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med. 2013;368:407–415.•• Report from a clinical trial concluding that fecal microbiota transplantation was more effective than vancomycin for recurrent CDI.
90. C.R.Kelly, C.Ihunnah, M.Fischer, et al. Fecal microbiota transplant for treatment of Clostridium difficile infection in immunocompromised patients. Am J Gastroenterol. 2014;109:1065–1071.
91. B.E.Hirsch, N.Saraiya, K.Poeth, et al. Effectiveness of fecal-derived microbiota transfer using orally administered capsules for recurrent Clostridium difficile infection. BMC Infect Dis. 2015;15:191.
92. A.Ponte, R.Pinho, M.Mota, et al. Initial experience with fecal microbiota transplantation in Clostridium difficile infection - transplant protocol and preliminary results. Rev Esp Enferm Dig. 2015;107:402–407.
93. Y.A.Ghouri, D.M.Richards, E.F.Rahimi, et al. Systematic review of randomized controlled trials of probiotics, prebiotics, and synbiotics in inflammatory bowel disease. Clin Exp Gastroenterol. 2014;7:473–487.