Prolonged use of a proton pump inhibitor reduces microbial diversity: Implications for Clostridium difficile susceptibility

Microbiome

Volumn 2, Issue 1, 2014, Pages

  Seto, Charlie T ^a,b   Jeraldo, Patricio ^b,c   Orenstein, Robert ^d   Chia, Nicholas ^a,b,e   DiBaise, John K ^d  

^a UNIVERSITY OF MINNESOTA   (United States)

^b MAYO CLINIC   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^d MAYO CLINIC   (United States)

^e MAYO GRADUATE SCHOOL   (United States)

Author keywords

Clostridium difficile; Gut microbiome; Proton pump inhibitor

Indexed keywords

OMEPRAZOLE; RNA 16S;

ADULT; ANTIBIOTIC SENSITIVITY; ARTICLE; CLINICAL ARTICLE; CLINICAL TRIAL; CLOSTRIDIUM BUTYRICUM; CLOSTRIDIUM DIFFICILE INFECTION; CLOSTRIDIUM PERFRINGENS; CONTROLLED STUDY; DNA EXTRACTION; FEMALE; HIGH THROUGHPUT SEQUENCING; HUMAN; LONG TERM EXPOSURE; MALE; MICROBIAL DIVERSITY; MULTIDIMENSIONAL SCALING; OBSERVATIONAL STUDY; PEPTOCLOSTRIDIUM DIFFICILE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUESTIONNAIRE;

CLOSTRIDIUM DIFFICILE;

EID: 84931284624     PISSN: None     EISSN: 20492618     Source Type: Journal    
DOI: 10.1186/2049-2618-2-42     Document Type: Article

References (56)

1. Peery AF, Dellon ES, Lund J, Crockett SD, McGowan CE, Bulsiewicz WJ, Gangarosa LM, Thiny MT, Stizenberg K, Morgan DR, Ringel Y, Kim HP, Dibonaventura MD, Carroll CF, Allen JK, Cook SF, Sandler RS, Kappelman MD, Shaheen NJ. Burden of gastrointestinal disease in the United States: 2012 update. Gastroenterology 2012, 143:1179-1187. e1171-1173, 10.1053/j.gastro.2012.08.002, 3480553, 22885331.
2. AstraZeneca Annual Report and Form 20-F Information 2013. [http://www.astrazeneca-annualreports.com/2013/_assets/pdfs/Strategic_report.pdf].
3. Lindberg P, Brändström A, Wallmark B, Mattsson H, Rikner L, Hoffmann KJ. Omeprazole: the first proton pump inhibitor. Med Res Rev 1990, 10(1):1-54. 10.1002/med.2610100102, 2404184.
4. Sarzynski E, Puttarajappa C, Xie Y, Grover M, Laird-Fick H. Association between proton pump inhibitor use and anemia: a retrospective cohort study. Dig Dis Sci 2011, 56(8):2349-2353. 10.1007/s10620-011-1589-y, 21318590.
5. Lam JR, Schneider JL, Zhao W, Corley DA. Proton pump inhibitor and histamine 2 receptor antagonist use and vitamin B12 deficiency. JAMA 2013, 310(22):2435-2442. 10.1001/jama.2013.280490, 24327038.
6. Howden C. Vitamin B12 levels during prolonged treatment with proton pump inhibitors. J Clin Gastroenterol 2000, 30(1):29-33. 10.1097/00004836-200001000-00006, 10636207.
7. Florentin M, Elisaf MS. Proton pump inhibitor-induced hypomagnesemia: a new challenge. World J Nephrol 2012, 1(6):151-154. 10.5527/wjn.v1.i6.151, 3782221, 24175253.
8. Yu EW, Blackwell T, Ensrud KE, Hillier TA, Lane NE, Orwoll E, Bauer DC. Acid-suppressive medications and risk of bone loss and fracture in older adults. Calcif Tissue Int 2008, 83(4):251-259. 10.1007/s00223-008-9170-1, 2596870, 18813868.
9. de Vries F, Cooper AL, Cockle SM, van Staa TP, Cooper C. Fracture risk in patients receiving acid-suppressant medication alone and in combination with bisphosphonates. Osteoporos Int 2009, 20(12):1989-1998. 10.1007/s00198-009-0891-4, 19333676.
10. Lo W-K, Chan WW. Proton pump inhibitor use and the risk of small intestinal bacterial overgrowth: a meta-analysis. Clin Gastroenterol Hepatol 2013, 11:483-490. 10.1016/j.cgh.2012.12.011, 23270866.
11. Lombardo L, Foti M, Ruggia O, Chiecchio A. Increased incidence of small intestinal bacterial overgrowth during proton pump inhibitor therapy. Clin Gastroenterol Hepatol 2010, 8(6):504-508. 10.1016/j.cgh.2009.12.022, 20060064.
12. Ali T, Roberts DN, Tierney WM. Long-term safety concerns with proton pump inhibitors. Am J Med 2009, 122(10):896-903. 10.1016/j.amjmed.2009.04.014, 19786155.
13. Sheen E, Triadafilopoulos G. Adverse effects of long-term proton pump inhibitor therapy. Dig Dis Sci 2011, 56(4):931-950. 10.1007/s10620-010-1560-3, 21365243.
14. Chitnis AS, Holzbauer SM, Belflower RM, Winston LG, Bamberg WM, Lyons C, Farley MM, Dumyati GK, Wilson LE, Beldavs ZG, Dunn JR, Gould LG, MacCannell DR, Gerding DN, McDonald LC, Lessa FC. Epidemiology of community-associated Clostridium difficile infection, 2009 through 2011. JAMA Intern Med 2013, 173:1359-1367. 10.1001/jamainternmed.2013.7056, 23780507.
15. Barletta JF, El-Ibiary SY, Davis LE, Nguyen B, Raney CR. Proton pump inhibitors and the risk for hospital-acquired Clostridium difficile infection. Mayo Clin Proc 2013, 88:1085-1090. 10.1016/j.mayocp.2013.07.004, 24012413.
16. Freedberg DE, Salmasian H, Friedman C, Abrams JA. Proton pump inhibitors and risk for recurrent Clostridium difficile infection among inpatients. Am J Gastroenterol 2013, 108:1794-1801. 10.1038/ajg.2013.333, 3966060, 24060760.
17. Janarthanan S, Ditah I, Adler DG, Ehrinpreis MN. Clostridium difficile-associated diarrhea and proton pump inhibitor therapy: a meta-analysis. Am J Gastroenterol 2012, 107:1001-1010. 10.1038/ajg.2012.179, 22710578.
18. Kim JW, Lee KL, Jeong JB, Kim BG, Shin S, Kim JS, Jung HC, Song IS. Proton pump inhibitors as a risk factor for recurrence of Clostridium-difficile-associated diarrhea. World J Gastroenterol 2010, 16:3573-3577. 10.3748/wjg.v16.i28.3573, 2909558, 20653067.
19. Kwok CS, Arthur AK, Anibueze CI, Singh S, Cavallazzi R, Loke YK. Risk of Clostridium difficile infection with acid suppressing drugs and antibiotics: a meta-analysis. Am J Gastroenterol 2012, 107:1011-1019. 10.1038/ajg.2012.108, 22525304.
20. FDA FDA Drug Safety Communication: Clostridium difficile-associated diarrhea can be associated with stomach acid drugs known as proton pump inhibitors (PPIs). 2012, United States, FDA.
21. Rao A, Jump RL, Pultz NJ, Pultz MJ, Donskey CJ. In vitro killing of nosocomial pathogens by acid and acidified nitrite. Antimicrob Agents Chemother 2006, 50:3901-3904. 10.1128/AAC.01506-05, 1635176, 17065628.
22. Britton RA, Young VB. Role of the intestinal microbiota in resistance to colonization by Clostridium difficile. Gastroenterology 2014, 146:1547-1553. 10.1053/j.gastro.2014.01.059, 24503131.
23. Antharam VC, Li EC, Ishmael A, Sharma A, Mai V, Rand KH, Wang GP. Intestinal dysbiosis and depletion of butyrogenic bacteria in Clostridium difficile infection and nosocomial diarrhea. J Clin Microbiol 2013, 51(9):2884-2892. 10.1128/JCM.00845-13, 3754663, 23804381.
24. Chang JY, Antonopoulos DA, Kalra A, Tonelli A, Khalife WT, Schmidt TM, Young VB. Decreased diversity of the fecal microbiome in recurrent Clostridium difficile-associated diarrhea. J Infect Dis 2008, 197:435-438. 10.1086/525047, 18199029.
25. Schubert AM, Rogers MA, Ring C, Mogle J, Petrosino JP, Young VB, Aronoff DM, Schloss PD. Microbiome data distinguish patients with Clostridium difficile infection and non-C. difficile-associated diarrhea from healthy controls. MBio 2014, 5(3):e01021-14. 4010826, 24803517.
26. Kanno T, Matsuki T, Oka M, Utsunomiya H, Inada K, Magari H, Inoue I, Maekita T, Ueda K, Enomoto S, Iguchi M, Yanaoka K, Tamai H, Akimoto S, Nomoto K, Tanaka R, Ichinose M. Gastric acid reduction leads to an alteration in lower intestinal microflora. Biochem Biophys Res Commun 2009, 381:666-670. 10.1016/j.bbrc.2009.02.109, 19248769.
27. Wallace JL, Syer S, Denou E, De Palma G, Vong L, McKnight W, Jury J, Bolla M, Bercik P, Collins SM, Verdu E, Ongini E. Proton pump inhibitors exacerbate NSAID-induced small intestinal injury by inducing dysbiosis. Gastroenterology 2011, 141:1314-1322. 10.1053/j.gastro.2011.06.075, 21745447.
28. Langille MG, Zaneveld J, Caporaso G, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Thurber RLV, Knight R, Beiko RG, Huttenhower C. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 2013, 31:814-821. 10.1038/nbt.2676, 3819121, 23975157.
29. 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(7):e69621. 10.1371/journal.pone.0069621, 3712949, 23874976.
30. Garcia-Mazcorro JF, Suchodolski JS, Jones KR, Clark-Price SC, Dowd SE, Minamoto Y, Markel M, Steiner JM, Dossin O. Effect of the proton pump inhibitor omeprazole on the gastrointestinal bacterial microbiota of healthy dogs. FEMS Microbiol Ecol 2012, 80:624-636. 10.1111/j.1574-6941.2012.01331.x, 22324305.
31. Jonkers D, Stobberingh E, Stockbrugger R. Omeprazole inhibits growth of Gram-positive and Gram-negative bacteria including Helicobacter pylori in vitro. J Antimicrob Chemother 1996, 37:145-150.
32. Pérez-Cobas AE, Artacho A, Ott SJ, Moya A, Gosalbes MJ, Latorre A. Structural and functional changes in the gut microbiota associated to Clostridium difficile infection. Front Microbiol 2014, 5:335. 4163665, 25309515.
33. Chen X, Katchar K, Goldsmith JD, Nanthakumar N, Cheknis A, Gerding DN, Kelly CP. A mouse model of Clostridium difficile-associated disease. Gastroenterology 2008, 135(6):1984-1992. 10.1053/j.gastro.2008.09.002, 18848941.
34. Ng KM, Ferreyra JA, Higginbottom SK, Lynch JB, Kashyap PC, Gopinath S, Naidu N, Choudhury B, Weimer BC, Monack DM, Sonnenburg JL. Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature 2013, 502(7469):96-99. 10.1038/nature12503, 3825626, 23995682.
35. Yamamoto-Osaki T, Kamiya S, Sawamura S, Kai M, Ozawa A. Growth inhibition of Clostridium difficile by intestinal flora of infant faeces in continuous flow culture. J Med Microbiol 1994, 40(3):179-187. 10.1099/00222615-40-3-179, 8114067.
36. Wilson KH, Perini F. Role of competition for nutrients in suppression of Clostridium difficile by the colonic microflora. Infect Immun 1988, 56:2610-2614. 259619, 3417352.
37. Kanehisa M. Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 2000, 28:27-30. 10.1093/nar/28.1.27, 102409, 10592173.
38. Sorg J, Sonenshein AL. Bile salts and glycine as cogerminants for Clostridium difficile spores. J Bacteriol 2008, 190(7):2505-2512. 10.1128/JB.01765-07, 2293200, 18245298.
39. Yamakawa K, Kamiya S, Meng XQ, Karasawa T, Nakamura S. Toxin production by Clostridium difficile in a defined medium with limited amino acids. J Med Microbiol 1994, 41:319-323. 10.1099/00222615-41-5-319, 7966203.
40. Howerton A, Ramirez N, Abel-Santos E. Mapping interactions between germinants and Clostridium difficile spores. J Bacteriol 2011, 193(1):274-282. 10.1128/JB.00980-10, 3019946, 20971909.
41. Theisen J, Nehra D, Citron D, Johansson J, Hagen JA, Crookes PF, DeMeester SR, Bremner CG, DeMeester TR, Peters JH. Suppression of gastric acid secretion in patients with gastroesophageal reflux disease results in gastric bacterial overgrowth and deconjugation of bile acids. J Gastrointest Surg 2000, 4:50-54. 10.1016/S1091-255X(00)80032-3, 10631362.
42. Sorg JA, Sonenshein A. Inhibiting the initiation of Clostridium difficile spore germination using analogs of chenodeoxycholic acid, a bile acid. J Bacteriol 2010, 192(19):4983-4990. 10.1128/JB.00610-10, 2944524, 20675492.
43. Giel JL, Sorg J, Sonenshein AL, Zhu J. Metabolism of bile salts in mice influences spore germination in Clostridium difficile. PLoS One 2010, 5(1):e8740. 10.1371/journal.pone.0008740, 2806926, 20090901.
44. Nerandzic MM, Pultz MJ, Donskey CJ. Examination of potential mechanisms to explain the association between proton pump inhibitors and Clostridium difficile infection. Antimicrob Agents Chemother 2009, 53:4133-4137. 10.1128/AAC.00252-09, 2764230, 19667292.
45. Stewart DB, Hegarty JP. Correlation between virulence gene expression and proton pump inhibitors and ambient pH in Clostridium difficile: results of an in vitro study. J Med Microbiol 2013, 62:1517-1523. 10.1099/jmm.0.059709-0, 23800596.
46. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 2012, 6(8):1621-1624. 10.1038/ismej.2012.8, 3400413, 22402401.
47. Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R, Mills DA, Caporaso JG. Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods 2013, 10:57-59. 3531572, 23202435.
48. Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 2013, 10:996-998. 10.1038/nmeth.2604, 23955772.
49. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 2006, 72:5069-5072. 10.1128/AEM.03006-05, 1489311, 16820507.
50. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 2009, 75:7537-7541. 10.1128/AEM.01541-09, 2786419, 19801464.
51. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. QIIME allows analysis of high-throughput community sequencing data g. Nat Methods 2010, 7:335-336. 10.1038/nmeth.f.303, 3156573, 20383131.
52. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 2013, 41(D1):D590-D596. 10.1093/nar/gks1219, 3531112, 23193283.
53. Knights D, Kuczynski J, Charlson ES, Zaneveld J, Mozer MC, Collman RG, Bushman FD, Knight R, Kelley ST. Bayesian community-wide culture-independent microbial source tracking. Nat Methods 2011, 8:761-763. 10.1038/nmeth.1650, 3791591, 21765408.
54. Faith DP, Minchin PR, Belbin L. Compositional dissimilarity as a robust measure of ecological distance. Vegetatio 1987, 69:57-68.
55. Ramette A. Multivariate analyses in microbial ecology. FEMS Microbiol Ecol 2007, 62(2):142-160. 10.1111/j.1574-6941.2007.00375.x, 2121141, 17892477.
56. Meyer D, Dimitriadou E, Hornik K, Weingessel K, Leisch L. e1071: Misc Functions of the Department of Statistics (e1071), TU Wien. R package version 1.6-3 2014,