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Review

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

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Pages 1145-1152 | Received 30 Oct 2015, Accepted 22 Feb 2016, Published online: 16 Mar 2016

References

  • Tlaskalová-Hogenová H, Stepánková R, Kozáková H, 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.
  • Blaser M. Antibiotic overuse: stop the killing of beneficial bacteria. Nature. 2011;476:393–394.
  • Sekirov I, Russell SL, Antunes LC, et al. Gut microbiota in health and disease. Physiol Rev. 2010;90:859–904.
  • Qin J, Li R, Raes J, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010;464:59–65.
  • Rajilić-Stojanović M, de Vos WM. The first 1000 cultured species of the human gastrointestinal microbiota. FEMS Microbiol Rev. 2014;38:996–1047.
  • Jernberg C, Löfmark S, Edlund C, et al. Long-term impacts of antibiotic exposure on the human intestinal microbiota. Microbiology. 2010;156:3216–3223.
  • Bartlett JG, Gerding DN. Clinical recognition and diagnosis of Clostridium difficile infection. Clin Infect Dis. 2008;46(Suppl 1):S12S18.
  • Jakobsson HE, Jernberg C, Andersson AF, et al. Short-term antibiotic treatment has differing long-term impacts on the human throat and gut microbiome. PLoS One. 2010;5:e9836.
  • Jernberg C, Löfmark S, Edlund C, et al. Long-term ecological impacts of antibiotic administration on the human intestinal microbiota. ISME J. 2007;1:56–66.
  • Liévin-Le Moal V, Servin AL. 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.
  • Dominguez-Bello MG, Blaser MJ, Ley RE, et al. Development of the human gastrointestinal microbiota and insights from high-throughput sequencing. Gastroenterology. 2011;140:1713–1719.
  • Mariat D, Firmesse O, Levenez F, et al. The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BMC Microbiol. 2009;9:123.
  • Walker AW, Sanderson JD, Churcher C, 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.
  • Vrieze A, Van NE, Holleman F, et al. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology. 2012;143:913–916.
  • Turnbaugh PJ, Ridaura VK, Faith JJ, et al. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med. 2009;1:6ra14.
  • Ley RE, Turnbaugh PJ, Klein S, et al. Microbial ecology: human gut microbes associated with obesity. Nature. 2006;444:1022–1023.
  • Moayyedi P, Surette MG, Kim PT, et al. Fecal microbiota transplantation induces remission in patients with active ulcerative colitis in a randomized controlled trial. Gastroenterology. 2015;149:102–109.
  • Hollister EB, Gao C, Versalovic J. Compositional and functional features of the gastrointestinal microbiome and their effects on human health. Gastroenterology. 2014;146:1449–1458.
  • Benson AK, Kelly SA, Legge R, 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.
  • Bleich A, Hansen AK. Time to include the gut microbiota in the hygienic standardisation of laboratory rodents. Comp Immunol Microbiol Infect Dis. 2012;35:81–92.
  • Hansen J, Gulati A, Sartor RB. The role of mucosal immunity and host genetics in defining intestinal commensal bacteria. Curr Opin Gastroenterol. 2010;26:564–571.
  • Spor A, Koren O, Ley R. Unravelling the effects of the environment and host genotype on the gut microbiome. Nat Rev Microbiol. 2011;9:279–290.
  • Tims S, Derom C, Jonkers DM, et al. Microbiota conservation and BMI signatures in adult monozygotic twins. ISME J. 2013;7:707–717.
  • Turnbaugh PJ, Hamady M, Yatsunenko T, et al. A core gut microbiome in obese and lean twins. Nature. 2009;457:480–484.
  • Van de Merwe JP, Stegeman JH, Hazenberg MP. The resident faecal flora is determined by genetic characteristics of the host. Implications for Crohn’s disease? Antonie Van Leeuwenhoek. 1983;49:119–124.
  • Zoetendal EG, Akkermans ADL, Akkermans-van Vliet WM, et al. The host genotype affects the bacterial community in the human gastrointestinal tract. Microb Ecol Health D. 2001;13:129–134.
  • Edwards CA, Parrett AM. Intestinal flora during the first months of life: new perspectives. Br J Nutr. 2002;88(Suppl. 1):S11–S18.
  • Zivkovic AM, German JB, Lebrilla CB, 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.
  • Xu Z, Knight R. Dietary effects on human gut microbiome diversity. Br J Nutr. 2015;113(Suppl 1):S1S5.
  • Wu GD, Bushmanc FD, Lewis JD. Diet, the human gut microbiota, and IBD. Anaerobe. 2013;24:117–120.
  • Martínez I, Muller CE, Walter J. Long-term temporal analysis of the human fecal microbiota revealed a stable core of dominant bacterial species. PLoS One. 2013;8:e69621.
  • Eckburg PB, Bik EM, Bernstein CN, et al. Diversity of the human intestinal microbial flora. Science. 2005;308:1635–1638.
  • Frank DN, St Amand AL, Feldman RA, 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.
  • Gerritsen J, Smidt H, Rijkers GT, et al. Intestinal microbiota in human health and disease: the impact of probiotics. Genes Nutr. 2011;6:209–240.
  • Bischoff SC. ‘Gut health’: a new objective in medicine? BMC Med. 2011;9:24.
  • Rafii F, Sutherland JB, Cerniglia CE. Effects of treatment with antimicrobial agents on the human colonic microflora. Ther Clin Risk Manag. 2008;4:1343–1358.
  • De La Cochetière MF, Durand T, Lepage P, et al. Resilience of the dominant human fecal microbiota upon short-course antibiotic challenge. J Clin Microbiol. 2005;43:5588–5592.
  • Sjölund M, Wreiber K, Andersson DI, et al. Long-term persistence of resistant Enterococcus species after antibiotics to eradicate Helicobacter pylori. Ann Intern Med. 2003;139:483–487.
  • Sullivan A, Edlund C, Nord CE. Effect of antimicrobial agents on the ecological balance of human microflora. Lancet Infect Dis. 2001;1:101–114.
  • Löfmark S, Jernberg C, Jansson JK, et al. Clindamycin-induced enrichment and long-term persistence of resistant Bacteroides spp. and resistance genes. J Antimicrob Chemother. 2006;58:1160–1167.
  • Lindgren M, Löfmark S, Edlund C, 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.
  • Nyberg SD, Österblad M, Hakanen AJ, 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.
  • Sjölund M, Tano E, Blaser MJ, et al. Persistence of resistant Staphylococcus epidermidis after single course of clarithromycin. Emerg Infect Dis. 2005;11:1389–1393.
  • Garau J, Nicolau DP, Wullt B, 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.
  • Oberoi SS, Dhingra C, Sharma G, et al. Antibiotics in dental practice: how justified are we. Int Dent J. 2015;65:4–10.
  • Willing BP, Russell SL, Finlay BB. Shifting the balance: antibiotic effects on host-microbiota mutualism. Nat Rev Microbiol. 2011;9:233–243.
  • Dethlefsen L, Huse S, Sogin ML, 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.
  • Dethlefsen L, Relman DA. 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.
  • Cotter PD, Stanton C, Ross RP, et al. The impact of antibiotics on the gut microbiota as revealed by high throughput DNA sequencing. Discov Med. 2012;13:193–199.
  • Lessa FC, Gould CV, McDonald LC. Current status of Clostridium difficile infection epidemiology. Clin Infect Dis. 2012;55(Suppl 2):S65S70.
  • McFarland LV. Antibiotic-associated diarrhea: epidemiology, trends and treatment. Future Microbiol. 2008;3:563–578.
  • Bartlett JG, Chang TW, Gurwith M, et al. Antibiotic-associated pseudomembranous colitis due to toxin-producing clostridia. N Engl J Med. 1978;298:531–534.
  • Khanna S, Pardi DS. Clostridium difficile infection: new insights into management. Mayo Clin Proc. 2012;87:1106–1117.
  • 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.
  • Lessa FC, Mu Y, Bamberg WM, et al. Burden of Clostridium difficile infection in the United States. N Engl J Med. 2015;372:825–834.
  • Magill SS, Edwards JR, Bamberg W, et al. Multistate point-prevalence survey of health care-associated infections. N Engl J Med. 2014;370:1198–1208.
  • Barbut F, Richard A, Hamadi K, et al. Epidemiology of recurrences or reinfections of Clostridium difficile-associated diarrhea. J Clin Microbiol. 2000;38:2386–2388.
  • Pepin J, Valiquette L, Alary ME, 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.
  • Pepin J, Saheb N, Coulombe MA, 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.
  • Freeman J, Bauer MP, Baines SD, et al. The changing epidemiology of Clostridium difficile infections. Clin Microbiol Rev. 2010;23:529–549.
  • Bignardi GE. Risk factors for Clostridium difficile infection. J Hosp Infect. 1998;40:1–15.
  • Tedesco FJ, Barton RW, Alpers DH. Clindamycin-associated colitis. A prospective study. Ann Intern Med. 1974;81:429–433.
  • Marr JJ, Sans MD, Tedesco FJ. Bacterial studies of Clindamycin-associated colitis. A preliminary report. Gastroenterology. 1975;69:352–358.
  • Gorbach SL. Antibiotics and Clostridium difficile. N Engl J Med. 1999;341:1690–1691.
  • Loo VG, Poirier L, Miller MA, 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.
  • Gaynes R, Rimland D, Killum E, et al. Outbreak of Clostridium difficile infection in a long-term care facility: association with gatifloxacin use. Clin Infect Dis. 2004;38:640–645.
  • Stevens V, Dumyati G, Fine LS, et al. Cumulative antibiotic exposures over time and the risk of Clostridium difficile infection. Clin Infect Dis. 2011;53:42–48.
  • 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.
  • Cohen SH, Gerding DN, Johnson S, 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.
  • Vardakas KZ, Polyzos KA, Patouni K, 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.
  • 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.
  • Newton DF, Macfarlane S, Macfarlane GT. 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.
  • Brook I, Wexler HM, Goldstein EJ. Antianaerobic antimicrobials: spectrum and susceptibility testing. Clin Microbiol Rev. 2013;26:526–546.
  • Tannock GW, Munro K, Taylor C, 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.
  • Nerandzic MM, Mullane K, Miller MA, 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.
  • Louie TJ, Emery J, Krulicki W, 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.
  • Louie TJ, Cannon K, Byrne B, 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.
  • Louie TJ, Miller MA, Mullane KM, et al. Fidaxomicin versus vancomycin for Clostridium difficile infection. N Engl J Med. 2011;364:422–431.
  • DuPont HL, Jiang ZD, Okhuysen PC, et al. A randomized, double-blind, placebo-controlled trial of rifaximin to prevent travelers’ diarrhea. Ann Intern Med. 2005;142:805–812.
  • Curry SR, Marsh JW, Shutt KA, 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.
  • Al-Nassir WN, Sethi AK, Li Y, 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.
  • Sethi AK, Al-Nassir WN, Nerandzic MM, 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.
  • Caffarelli C, Cardinale F, Povesi-Dascola C, et al. Use of probiotics in pediatric infectious diseases. Expert Rev Anti Infect Ther. 2015;13:1517–1535.
  • Chatterjee S, Kar P, Das T, 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.
  • Dietrich CG, Kottmann T, Alavi M. Commercially available probiotic drinks containing Lactobacillus casei DN-114001 reduce antibiotic-associated diarrhea. World J Gastroenterol. 2014;20:15837–15844.
  • Issa I, Moucari R. Probiotics for antibiotic-associated diarrhea: do we have a verdict? World J Gastroenterol. 2014;20:17788–17795.
  • Johnson S. Recurrent Clostridium difficile infection: a review of risk factors, treatments, and outcomes. J Infect. 2009;58:403–410.
  • Youngster I, Sauk J, Pindar C, 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.
  • Van Nood E, Vrieze A, Nieuwdorp M, et al. Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med. 2013;368:407–415.
  • Kelly CR, Ihunnah C, Fischer M, et al. Fecal microbiota transplant for treatment of Clostridium difficile infection in immunocompromised patients. Am J Gastroenterol. 2014;109:1065–1071.
  • Hirsch BE, Saraiya N, Poeth K, et al. Effectiveness of fecal-derived microbiota transfer using orally administered capsules for recurrent Clostridium difficile infection. BMC Infect Dis. 2015;15:191.
  • Ponte A, Pinho R, Mota M, 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.
  • Ghouri YA, Richards DM, Rahimi EF, et al. Systematic review of randomized controlled trials of probiotics, prebiotics, and synbiotics in inflammatory bowel disease. Clin Exp Gastroenterol. 2014;7:473–487.

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