Oral probiotic combination of lactobacillus and bifidobacterium alters the gastrointestinal microbiota during antibiotic treatment for clostridium difficile infection

PLoS ONE

Volumn 13, Issue 9, 2018, Pages

  De Wolfe, T J ^a,b   Eggers, S ^b   Barker, A K ^b   Kates, A E ^b,c   Dill McFarland, K A ^d   Suen, G ^d   Safdar, N ^b,c  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c WILLIAM S MIDDLETON MEMORIAL VETERANS HOSPITAL   (United States)

^d UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; FIDAXOMICIN; IRON COMPLEX; METRONIDAZOLE; PROBIOTIC AGENT; RNA 16S; VANCOMYCIN; ANTIINFECTIVE AGENT;

ANTIBIOTIC THERAPY; ARTICLE; BIFIDOBACTERIUM; BIFIDOBACTERIUM ANIMALIS; CLINICAL ARTICLE; CLOSTRIDIUM DIFFICILE INFECTION; CONTROLLED STUDY; FECES ANALYSIS; HUMAN; INTESTINE FLORA; LACTOBACILLUS; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS PARACASEI; MICROBIAL COMMUNITY; NONHUMAN; RNA SEQUENCE; SEQUENCE ANALYSIS; CLOSTRIDIUM INFECTION; DRUG EFFECT; ORAL DRUG ADMINISTRATION; PHYSIOLOGY;

ADMINISTRATION, ORAL; ANTI-BACTERIAL AGENTS; BIFIDOBACTERIUM; CLOSTRIDIUM INFECTIONS; GASTROINTESTINAL MICROBIOME; HUMANS; LACTOBACILLUS; PROBIOTICS;

EID: 85054081768     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0204253     Document Type: Article

References (48)

1. Miller BA, Chen LF, Sexton DJ, Anderson DJ. Comparison of the burdens of hospital-onset, healthcare facility-associated Clostridium difficile infection and of healthcare-associated infection due to methicillin-resistant Staphylococcus aureus in community hospitals. Infect Control Hosp Epidemiol. 2011; 32: 387–390. https://doi.org/10.1086/659156 PMID: 21460491
2. McDonald LC, Owings M, Jernigan DB. Clostridium difficile infection in patients discharged from US short-stay hospitals, 1996–2003. Emerg Infect Dis. 2006; 12: 409–415. https://doi.org/10.3201/eid1203.051064 PMID: 16704777
3. Lessa FC, Mu Y, Bamberg WM, Beldavs ZG, Dumyati GK, Dunn JR, et al. Burden of Clostridium difficile infection in the United States. N Engl J Med. 2015; 372: 825–834. https://doi.org/10.1056/NEJMoa1408913 PMID: 25714160
4. Centers for Disease Control and Prevention. Antibiotic resistance threats in the United States, 2013 [Internet]. 2013 pp. 1–114. https://www.cdc.gov/drugresistance/pdf/ar-threats-2013-508.pdf
5. Department of Veterans Affairs. VHA Directive 1031: Antimicrobial Stewardship Programs. 2014;0: 1–9. https://www.va.gov/vhapublications/ViewPublication.asp?pub_ID=2964
6. Butler M, Olson A, Drekonja D, Shaukat A, Schwehr N, Shippee N, et al. Early diagnosis, prevention, and treatment of Clostridium difficile: update. Rockville (MD): Agency for Healthcare Research and Quality (US); 2016.
7. Britton RA, Young VB. Role of the intestinal microbiota in resistance to colonization by Clostridium difficile. Gastroenterology. 2014; 146: 1547–1553. https://doi.org/10.1053/j.gastro.2014.01.059 PMID: 24503131
8. Sebaihia M, Wren BW, Mullany P, Fairweather NF, Minton N, Stabler R, et al. The multidrug-resistant human pathogen Clostridium difficile has a highly mobile, mosaic genome. Nat Genet. 2006; 38: 779–786. https://doi.org/10.1038/ng1830 PMID: 16804543
9. Mathur H, Rea MC, Cotter PD, Ross RP, Hill C. The potential for emerging therapeutic options for Clostridium difficile infection. Gut Microbes. 2014; 5: 696–710. https://doi.org/10.4161/19490976.2014. 983768 PMID: 25564777
10. Olson MM, Shanholtzer CJ, Lee JT, Gerding DN. Ten years of prospective Clostridium difficile-associated disease surveillance and treatment at the Minneapolis VA medical center, 1982–1991. Infect Control Hosp Epidemiol. 1994; 15: 371–381. https://doi.org/10.2307/30145589 PMID: 7632199
11. Miller M. The fascination with probiotics for Clostridium difficile infection: lack of evidence for prophylactic or therapeutic efficacy. Anaerobe. Elsevier Ltd; 2009; 15: 281–284. https://doi.org/10.1016/j.anaerobe.2009.08.005 PMID: 19699309
12. Barker AK, Duster M, Valentine S, Hess T, Archbald-Pannone L, Guerrant R, et al. A randomized controlled trial of probiotics for Clostridium difficile infection in adults (PICO). Journal of Antimicrobial Chemotherapy. 2017; 72: 1–4.
13. Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Applied and Environmental Microbiology. 2013; 79: 5112–5120. https://doi.org/10.1128/AEM.01043-13 PMID: 23793624
14. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology. 2009; 75: 7537–7541. https://doi.org/10.1128/AEM.01541-09 PMID: 19801464
15. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, et al. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Research. 2007; 35: 7188–7196. https://doi.org/10.1093/nar/gkm864 PMID: 17947321
16. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Applied and Environmental Microbiology. 2006; 72: 5069–5072. https://doi.org/10.1128/AEM.03006-05 PMID: 16820507
17. Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy. Applied and Environmental Microbiology. 2007; 73: 5261–5267. https://doi.org/10.1128/AEM.00062-07 PMID: 17586664
18. R Core Team. R: a language and environment for statistical computing [Internet]. Vienna; 2017. https://www.R-project.org/
19. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, et al. vegan: community ecology package. 2017;0: 1–292. https://CRAN.R-project.org/package=vegan
20. Noguchi K, Gel YR, Brunner E, 2012. nparLD: an R software package for the nonparametric analysis of longitudinal data in factorial experiments. Journal of Statistical Software.
21. Kanehisa M, Goto S. KEGG: Kyoto encyclopedia of genes and genomes. Oxford University Press; 2000.
22. Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M. KEGG as a reference resource for gene and protein annotation. Nucleic Acids Research. 2016; 44: D457–D462. https://doi.org/10.1093/nar/gkv1070 PMID: 26476454
23. Kanehisa M, Furumichi M, Tanabe M, Sato Y, Morishima K. KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Research. 2017; 45: D353–D361. https://doi.org/10.1093/nar/gkw1092 PMID: 27899662
24. Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol. Nature Publishing Group; 2013; 31: 814–821. https://doi.org/10.1038/nbt.2676 PMID: 23975157
25. Abubucker S, Segata N, Goll J, Schubert AM, Izard J, Cantarel BL, et al. Metabolic reconstruction for metagenomic data and its application to the human microbiome. Eisen JA, editor. PLoS Comput Biol. 2012; 8: e1002358–17. https://doi.org/10.1371/journal.pcbi.1002358 PMID: 22719234
26. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, et al. Metagenomic biomarker discovery and explanation. Genome Biol. BioMed Central Ltd; 2011; 12: R60. https://doi.org/10.1186/gb-2011-12-6-r60 PMID: 21702898
27. Goldenberg JZ, Ma S, Saxton JD. Probiotics for the prevention of Clostridium difficile-associated diarrhea in adults and children. Cochrane Database of Systematic Reviews. 2013. https://doi.org/10.1002/14651858.CD006095.pub3 PMID: 23728658
28. Sanders ME. Probiotics and microbiota composition. BMC Medicine. BMC Medicine; 2016; 14: 1–3.
29. Kristensen NB, Bryrup T, Allin KH, Nielsen T, Hansen TH, Pedersen O. Alterations in fecal microbiota composition by probiotic supplementation in healthy adults: a systematic review of randomized controlled trials. Genome Med. Genome Medicine; 2016; 8: 1–11.
30. Cammarota G, Ianiro G, Bibbò S, Gasbarrini A. Gut microbiota modulation: probiotics, antibiotics or fecal microbiota transplantation? Intern Emerg Med. 2014; 9: 365–373. https://doi.org/10.1007/s11739-014-1069-4 PMID: 24664520
31. Tannock GW, Munro K, Harmsen HJ, Welling GW, Smart J, Gopal PK. Analysis of the fecal microflora of human subjects consuming a probiotic product containing Lactobacillus rhamnosus DR20. Applied and Environmental Microbiology. 2000; 66: 2578–2588. PMID: 10831441
32. Grehan MJ, Borody TJ, Leis SM, Campbell J, Mitchell H, Wettstein A. Durable alteration of the colonic microbiota by the administration of donor fecal flora. J Clin Gastroenterol. 2010; 44: 551–561. https://doi.org/10.1097/MCG.0b013e3181e5d06b PMID: 20716985
33. Bassis CM, Theriot CM, Young VB. Alteration of the Murine Gastrointestinal Microbiota by Tigecycline Leads to Increased Susceptibility to Clostridium difficile Infection. Antimicrob Agents Chemother. 2014; 58: 2767–2774. https://doi.org/10.1128/AAC.02262-13 PMID: 24590475
34. Weingarden AR, Chen C, Bobr A, Yao D, Lu Y, Nelson VM, et al. Microbiota transplantation restores normal fecal bile acid composition in recurrent Clostridium difficileinfection. AJP: Gastrointestinal and Liver Physiology. 2014; 306: G310–G319. https://doi.org/10.1152/ajpgi.00282.2013 PMID: 24284963
35. Engelbrektson A, Korzenik JR, Pittler A, Sanders ME, Klaenhammer TR, Leyer G, et al. Probiotics to minimize the disruption of faecal microbiota in healthy subjects undergoing antibiotic therapy. Journal of Medical Microbiology. 2009; 58: 663–670. https://doi.org/10.1099/jmm.0.47615-0 PMID: 19369530
36. Rolfe RD, Helebian S, Finegold SM. Bacterial Interference Between Clostridium-Difficile and Normal Fecal Flora. J Infect Dis. 1981; 143: 470–475. PMID: 6785366
37. Abujamel T, Cadnum JL, Jury LA, Sunkesula VCK, Kundrapu S, Jump RL, et al. Defining the vulnerable period for re-establishment of Clostridium difficile colonization after treatment of C. difficile infection with oral vancomycin or metronidazole. Paredes-Sabja D, editor. PLoS ONE. 2013; 8: e76269. https://doi.org/10.1371/journal.pone.0076269 PMID: 24098459
38. Dabard J, Bridonneau C, Phillipe C, Anglade P, Molle D, Nardi M, et al. Ruminococcin A, a new lantibiotic produced by a Ruminococcus gnavus strain isolated from human feces. Applied and Environmental Microbiology. American Society for Microbiology (ASM); 2001; 67: 4111–4118. https://doi.org/10.1128/AEM.67.9.4111-4118.2001
39. Antharam VC, Li EC, Ishmael A, Sharma A, Mai V, Rand KH, et al. Intestinal dysbiosis and depletion of butyrogenic bacteria in Clostridium difficile infection and nosocomial diarrhea. J Clin Microbiol. 2013; 51: 2884–2892. https://doi.org/10.1128/JCM.00845-13 PMID: 23804381
40. Petrof EO, Gloor GB, Vanner SJ, Weese SJ, Carter D, Daigneault MC, et al. Stool substitute transplant therapy for the eradication of Clostridium difficile infection: “RePOOPulating” the gut. Microbiome. 2013; 1: 1–1.
41. McNulty NP, Yatsunenko T, Hsiao A, Faith JJ, Muegge BD, Goodman AL, et al. The impact of a consortium of fermented milk strains on the gut microbiome of gnotobiotic mice and monozygotic twins. Sci Transl Med. 2011; 3: 1–26. https://doi.org/10.1126/scitranslmed.3002701 PMID: 22030749
42. Brown JS, Holden DW. Iron acquisition by Gram-positive bacterial pathogens. Microbes and Infection. 2002; 4: 1149–1156. https://doi.org/10.1016/S1286-4579(02)01640-4 PMID: 12361915
43. Mendez C, Salas JA. The role of ABC transporters in antibiotic-producing organisms: drug secretion and resistance mechanisms. Res Microbiol. 2001; 152: 341–350. https://doi.org/10.1016/S0923-2508 (01)01205-0 PMID: 11421281
44. Wilson DN. Ribosome-targeting antibiotics and mechanisms of bacterial resistance. Nat Rev Micro. Nature Publishing Group; 2014; 12: 35–48. https://doi.org/10.1038/nrmicro3155 PMID: 24336183
45. David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. Nature Publishing Group; 2014; 505: 559–563. https://doi.org/10.1038/nature12820 PMID: 24336217
46. Jackson MA, Verdi S, Maxan M-E, Shin CM, Zierer J, Bowyer RCE, et al. Gut microbiota associations with common diseases and prescription medications in a population-based cohort. Nat Comms. Springer US; 2018; 1–8. https://doi.org/10.1038/s41467-018-05184-7 PMID: 29985401
47. Louie TJ, Cannon K, Byrne B, Emery J, Ward L, Eyben M, 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. Clinical Infectious Diseases. 2012; 55: S132–S142. https://doi.org/10.1093/cid/cis338 PMID: 22752862
48. Schubert AM, Sinani H, Schloss PD. Antibiotic-induced alterations of the murine gut microbiota and subsequent effects on colonization resistance against Clostridium difficile. mBio. 2015; 6: e00974–15–10. https://doi.org/10.1128/mBio.00974-15 PMID: 26173701