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Published in: Digestive Diseases and Sciences 11/2018

Open Access 01-11-2018 | Original Article

Gut Microbiota Composition Before and After Use of Proton Pump Inhibitors

Authors: Mariko Hojo, Takashi Asahara, Akihito Nagahara, Tsutomu Takeda, Kohei Matsumoto, Hiroya Ueyama, Kenshi Matsumoto, Daisuke Asaoka, Takuya Takahashi, Koji Nomoto, Yuichiro Yamashiro, Sumio Watanabe

Published in: Digestive Diseases and Sciences | Issue 11/2018

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Abstract

Background

Recently, problems associated with proton pump inhibitor (PPI) use have begun to surface. PPIs influence the gut microbiota; therefore, PPI use may increase the risk of enteric infections and cause bacterial translocation. In this study, we investigated fecal microbiota composition, fecal organic acid concentrations and pH, and gut bacteria in the blood of the same patients before and after PPI use.

Methods

Twenty patients with reflux esophagitis based on endoscopic examination received 8 weeks of treatment with PPIs. To analyze fecal microbiota composition and gut bacteria in blood and organic acid concentrations, 16S and 23S rRNA-targeted quantitative RT-PCR and high-performance liquid chromatography were conducted.

Results

Lactobacillus species were significantly increased at both 4 and 8 weeks after PPI treatment compared with bacterial counts before treatment (P = 0.011 and P = 0.002, respectively). Among Lactobacillus spp., counts of the L. gasseri subgroup, L. fermentum, the L. reuteri subgroup, and the L. ruminis subgroup were significantly increased at 4 and 8 weeks after treatment compared with counts before treatment. Streptococcus species were also significantly increased at 4 and 8 weeks after PPI treatment compared with counts before treatment (P < 0.01 and P < 0.001, respectively). There was no significant difference in the total organic acid concentrations before and after PPI treatment. Detection rates of bacteria in blood before and after PPI treatment were 22 and 28%, respectively, with no significant differences.

Conclusions

Our quantitative RT-PCR results showed that gut dysbiosis was caused by PPI use, corroborating previous results obtained by metagenomic analysis.
Literature
1.
go back to reference Savarino E, Zentilin P, Marabotto E, et al. Overweight is a risk factor for both erosive and non-erosive reflux disease. Dig Liver Dis. 2011;43:940–945.CrossRef Savarino E, Zentilin P, Marabotto E, et al. Overweight is a risk factor for both erosive and non-erosive reflux disease. Dig Liver Dis. 2011;43:940–945.CrossRef
2.
go back to reference Nakajima S, Nishiyama Y, Yamaoka M, Yasuoka T, Cho E. Changes in the prevalence of Helicobacter pylori infection and gastrointestinal diseases in the past 17 years. J Gastroenterol Hepatol. 2010;25(Suppl 1):S99–S110.CrossRef Nakajima S, Nishiyama Y, Yamaoka M, Yasuoka T, Cho E. Changes in the prevalence of Helicobacter pylori infection and gastrointestinal diseases in the past 17 years. J Gastroenterol Hepatol. 2010;25(Suppl 1):S99–S110.CrossRef
3.
go back to reference Robinson M. Review article: the pharmacodynamics and pharmacokinetics of proton pump inhibitors–overview and clinical implications. Aliment Pharmacol Ther. 2004;20(Suppl 6):1–10.CrossRef Robinson M. Review article: the pharmacodynamics and pharmacokinetics of proton pump inhibitors–overview and clinical implications. Aliment Pharmacol Ther. 2004;20(Suppl 6):1–10.CrossRef
4.
go back to reference Wolff T, Miller T, Ko S. Aspirin for the primary prevention of cardiovascular events: an update of the evidence for the U.S. Preventive Services Task Force. Ann Intern Med. 2009;150:405–410.CrossRef Wolff T, Miller T, Ko S. Aspirin for the primary prevention of cardiovascular events: an update of the evidence for the U.S. Preventive Services Task Force. Ann Intern Med. 2009;150:405–410.CrossRef
5.
go back to reference Mo C, Sun G, Lu ML, et al. Proton pump inhibitors in prevention of low-dose aspirin-associated upper gastrointestinal injuries. World J Gastroenterol. 2015;21:5382–5392.CrossRef Mo C, Sun G, Lu ML, et al. Proton pump inhibitors in prevention of low-dose aspirin-associated upper gastrointestinal injuries. World J Gastroenterol. 2015;21:5382–5392.CrossRef
6.
go back to reference Fife D, Barancik JI. Northeastern Ohio Trauma Study III: incidence of fractures. Ann Emerg Med. 1985;14:244–248.CrossRef Fife D, Barancik JI. Northeastern Ohio Trauma Study III: incidence of fractures. Ann Emerg Med. 1985;14:244–248.CrossRef
7.
go back to reference Hassett G, Hart DJ, Manek NJ, Doyle DV, Spector TD. Risk factors for progression of lumbar spine disc degeneration: the Chingford Study. Arthritis Rheum. 2003;48:3112–3117.CrossRef Hassett G, Hart DJ, Manek NJ, Doyle DV, Spector TD. Risk factors for progression of lumbar spine disc degeneration: the Chingford Study. Arthritis Rheum. 2003;48:3112–3117.CrossRef
8.
go back to reference Singh G, Triadafilopoulos G. Appropriate choice of proton pump inhibitor therapy in the prevention and management of NSAID-related gastrointestinal damage. Int J Clin Pract. 2005;59:1210–1217.CrossRef Singh G, Triadafilopoulos G. Appropriate choice of proton pump inhibitor therapy in the prevention and management of NSAID-related gastrointestinal damage. Int J Clin Pract. 2005;59:1210–1217.CrossRef
9.
go back to reference Wilde MI, McTavish D. Omeprazole. An update of its pharmacology and therapeutic use in acid-related disorders. Drugs. 1994;48:91–132.CrossRef Wilde MI, McTavish D. Omeprazole. An update of its pharmacology and therapeutic use in acid-related disorders. Drugs. 1994;48:91–132.CrossRef
10.
go back to reference Carswell CI, Goa KL. Rabeprazole: an update of its use in acid-related disorders. Drugs. 2001;61:2327–2356.CrossRef Carswell CI, Goa KL. Rabeprazole: an update of its use in acid-related disorders. Drugs. 2001;61:2327–2356.CrossRef
11.
go back to reference Insogna KL. The effect of proton pump-inhibiting drugs on mineral metabolism. Am J Gastroenterol. 2009;104(Suppl 2):S2–S4.CrossRef Insogna KL. The effect of proton pump-inhibiting drugs on mineral metabolism. Am J Gastroenterol. 2009;104(Suppl 2):S2–S4.CrossRef
12.
go back to reference Leonard J, Marshall JK, Moayyedi P. Systematic review of the risk of enteric infection in patients taking acid suppression Am J Gastroenterol.. 2007;102:2047–2056. (quiz 2057).PubMed Leonard J, Marshall JK, Moayyedi P. Systematic review of the risk of enteric infection in patients taking acid suppression Am J Gastroenterol.. 2007;102:2047–2056. (quiz 2057).PubMed
13.
go back to reference Naito Y, Kashiwagi K, Takagi T, Andoh A, Inoue R. Intestinal dysbiosis secondary to proton-pump inhibitor use. Digestion. 2018;97:195–204.CrossRef Naito Y, Kashiwagi K, Takagi T, Andoh A, Inoue R. Intestinal dysbiosis secondary to proton-pump inhibitor use. Digestion. 2018;97:195–204.CrossRef
14.
go back to reference Freedberg DE, Lebwohl B, Abrams JA. The impact of proton pump inhibitors on the human gastrointestinal microbiome. Clin Lab Med. 2014;34:771–785.CrossRef Freedberg DE, Lebwohl B, Abrams JA. The impact of proton pump inhibitors on the human gastrointestinal microbiome. Clin Lab Med. 2014;34:771–785.CrossRef
15.
go back to reference Lombardo L, Foti M, Ruggia O, Chiecchio A. Increased incidence of small intestinal bacterial overgrowth during proton pump inhibitor therapy. Clin Gastroenterol Hepatol. 2010;8:504–508.CrossRef Lombardo L, Foti M, Ruggia O, Chiecchio A. Increased incidence of small intestinal bacterial overgrowth during proton pump inhibitor therapy. Clin Gastroenterol Hepatol. 2010;8:504–508.CrossRef
16.
go back to reference de Vos M, De Vroey B, Garcia BG, et al. Role of proton pump inhibitors in the occurrence and the prognosis of spontaneous bacterial peritonitis in cirrhotic patients with ascites. Liver Int. 2013;33:1316–1323.CrossRef de Vos M, De Vroey B, Garcia BG, et al. Role of proton pump inhibitors in the occurrence and the prognosis of spontaneous bacterial peritonitis in cirrhotic patients with ascites. Liver Int. 2013;33:1316–1323.CrossRef
17.
go back to reference Wang YP, Liu CJ, Chen TJ, Lin YT, Fung CP. Proton pump inhibitor use significantly increases the risk of cryptogenic liver abscess: a population-based study. Aliment Pharmacol Ther. 2015;41:1175–1181.CrossRef Wang YP, Liu CJ, Chen TJ, Lin YT, Fung CP. Proton pump inhibitor use significantly increases the risk of cryptogenic liver abscess: a population-based study. Aliment Pharmacol Ther. 2015;41:1175–1181.CrossRef
18.
go back to reference Kamada N, Chen GY, Inohara N, Nunez G. Control of pathogens and pathobionts by the gut microbiota. Nat Immunol. 2013;14:685–690.CrossRef Kamada N, Chen GY, Inohara N, Nunez G. Control of pathogens and pathobionts by the gut microbiota. Nat Immunol. 2013;14:685–690.CrossRef
19.
go back to reference Jackson MA, Goodrich JK, Maxan ME, et al. Proton pump inhibitors alter the composition of the gut microbiota. Gut. 2016;65:749–756.CrossRef Jackson MA, Goodrich JK, Maxan ME, et al. Proton pump inhibitors alter the composition of the gut microbiota. Gut. 2016;65:749–756.CrossRef
20.
go back to reference Imhann F, Bonder MJ, Vich Vila A, et al. Proton pump inhibitors affect the gut microbiome. Gut. 2016;65:740–748.CrossRef Imhann F, Bonder MJ, Vich Vila A, et al. Proton pump inhibitors affect the gut microbiome. Gut. 2016;65:740–748.CrossRef
21.
go back to reference Takagi T, Naito Y, Inoue R, et al. The influence of long-term use of proton pump inhibitors on the gut microbiota: an age-sex-matched case-control study. J Clin Biochem Nutr. 2018;62:100–105.CrossRef Takagi T, Naito Y, Inoue R, et al. The influence of long-term use of proton pump inhibitors on the gut microbiota: an age-sex-matched case-control study. J Clin Biochem Nutr. 2018;62:100–105.CrossRef
22.
go back to reference Otsuka T, Sugimoto M, Inoue R, et al. Influence of potassium-competitive acid blocker on the gut microbiome of Helicobacter pylori-negative healthy individuals. Gut. 2017;66:1723–1725.CrossRef Otsuka T, Sugimoto M, Inoue R, et al. Influence of potassium-competitive acid blocker on the gut microbiome of Helicobacter pylori-negative healthy individuals. Gut. 2017;66:1723–1725.CrossRef
23.
go back to reference Freedberg DE, Toussaint NC, Chen SP, et al. Proton pump inhibitors alter specific taxa in the human gastrointestinal microbiome: a crossover trial. Gastroenterology. 2015;149:e889. Freedberg DE, Toussaint NC, Chen SP, et al. Proton pump inhibitors alter specific taxa in the human gastrointestinal microbiome: a crossover trial. Gastroenterology. 2015;149:e889.
24.
go back to reference Berg RD. Bacterial translocation from the gastrointestinal tract. Adv Exp Med Biol. 1999;473:11–30.CrossRef Berg RD. Bacterial translocation from the gastrointestinal tract. Adv Exp Med Biol. 1999;473:11–30.CrossRef
25.
go back to reference Mortensen FV, Nielsen H, Mulvany MJ, Hessov I. Short chain fatty acids dilate isolated human colonic resistance arteries. Gut. 1990;31:1391–1394.CrossRef Mortensen FV, Nielsen H, Mulvany MJ, Hessov I. Short chain fatty acids dilate isolated human colonic resistance arteries. Gut. 1990;31:1391–1394.CrossRef
26.
go back to reference Scheppach W, Bartram P, Richter A, et al. Effect of short-chain fatty acids on the human colonic mucosa in vitro. JPEN J Parenter Enteral Nutr. 1992;16:43–48.CrossRef Scheppach W, Bartram P, Richter A, et al. Effect of short-chain fatty acids on the human colonic mucosa in vitro. JPEN J Parenter Enteral Nutr. 1992;16:43–48.CrossRef
27.
go back to reference Kamath PS, Hoepfner MT, Phillips SF. Short-chain fatty acids stimulate motility of the canine ileum. Am J Physiol. 1987;253:G427–G433.PubMed Kamath PS, Hoepfner MT, Phillips SF. Short-chain fatty acids stimulate motility of the canine ileum. Am J Physiol. 1987;253:G427–G433.PubMed
28.
go back to reference Umesaki Y, Yajima T, Yokokura T, Mutai M. Effect of organic acid absorption on bicarbonate transport in rat colon. Pflugers Arch. 1979;379:43–47.CrossRef Umesaki Y, Yajima T, Yokokura T, Mutai M. Effect of organic acid absorption on bicarbonate transport in rat colon. Pflugers Arch. 1979;379:43–47.CrossRef
29.
go back to reference Chapman MA. The role of the colonic flora in maintaining a healthy large bowel mucosa. nn R Coll Surg Engl. 2001;83:75–80. Chapman MA. The role of the colonic flora in maintaining a healthy large bowel mucosa. nn R Coll Surg Engl. 2001;83:75–80.
30.
go back to reference Tana C, Umesaki Y, Imaoka A, Handa T, Kanazawa M, Fukudo S. Altered profiles of intestinal microbiota and organic acids may be the origin of symptoms in irritable bowel syndrome. Neurogastroenterol Motil. 2010;22:e114–e515. Tana C, Umesaki Y, Imaoka A, Handa T, Kanazawa M, Fukudo S. Altered profiles of intestinal microbiota and organic acids may be the origin of symptoms in irritable bowel syndrome. Neurogastroenterol Motil. 2010;22:e114–e515.
31.
go back to reference Lundell LR, Dent J, Bennett JR, et al. Endoscopic assessment of oesophagitis: clinical and functional correlates and further validation of the Los Angeles classification. Gut. 1999;45:172–180.CrossRef Lundell LR, Dent J, Bennett JR, et al. Endoscopic assessment of oesophagitis: clinical and functional correlates and further validation of the Los Angeles classification. Gut. 1999;45:172–180.CrossRef
32.
go back to reference Matsuda K, Tsuji H, Asahara T, Kado Y, Nomoto K. Sensitive quantitative detection of commensal bacteria by rRNA-targeted reverse transcription-PCR. Appl Environ Microbiol. 2007;73:32–39.CrossRef Matsuda K, Tsuji H, Asahara T, Kado Y, Nomoto K. Sensitive quantitative detection of commensal bacteria by rRNA-targeted reverse transcription-PCR. Appl Environ Microbiol. 2007;73:32–39.CrossRef
33.
go back to reference Matsuda K, Tsuji H, Asahara T, Matsumoto K, Takada T, Nomoto K. Establishment of an analytical system for the human fecal microbiota, based on reverse transcription-quantitative PCR targeting of multicopy rRNA molecules. Appl Environ Microbiol. 2009;75:1961–1969.CrossRef Matsuda K, Tsuji H, Asahara T, Matsumoto K, Takada T, Nomoto K. Establishment of an analytical system for the human fecal microbiota, based on reverse transcription-quantitative PCR targeting of multicopy rRNA molecules. Appl Environ Microbiol. 2009;75:1961–1969.CrossRef
34.
go back to reference Sakaguchi S, Saito M, Tsuji H, et al. Bacterial rRNA-targeted reverse transcription-PCR used to identify pathogens responsible for fever with neutropenia. J Clin Microbiol. 2010;48:1624–1628.CrossRef Sakaguchi S, Saito M, Tsuji H, et al. Bacterial rRNA-targeted reverse transcription-PCR used to identify pathogens responsible for fever with neutropenia. J Clin Microbiol. 2010;48:1624–1628.CrossRef
35.
go back to reference Ohigashi S, Sudo K, Kobayashi D, et al. Changes of the intestinal microbiota, short chain fatty acids, and fecal pH in patients with colorectal cancer. Dig Dis Sci. 2013;58:1717–1726.CrossRef Ohigashi S, Sudo K, Kobayashi D, et al. Changes of the intestinal microbiota, short chain fatty acids, and fecal pH in patients with colorectal cancer. Dig Dis Sci. 2013;58:1717–1726.CrossRef
36.
go back to reference Sato J, Kanazawa A, Ikeda F, et al. Gut dysbiosis and detection of “live gut bacteria” in blood of Japanese patients with type 2 diabetes. Diabetes Care. 2014;37:2343–2350.CrossRef Sato J, Kanazawa A, Ikeda F, et al. Gut dysbiosis and detection of “live gut bacteria” in blood of Japanese patients with type 2 diabetes. Diabetes Care. 2014;37:2343–2350.CrossRef
37.
go back to reference Matsuda K, Tsuji H, Asahara T, et al. Sensitive quantification of Clostridium difficile cells by reverse transcription-quantitative PCR targeting rRNA molecules. Appl Environ Microbiol. 2012;78:5111–5118.CrossRef Matsuda K, Tsuji H, Asahara T, et al. Sensitive quantification of Clostridium difficile cells by reverse transcription-quantitative PCR targeting rRNA molecules. Appl Environ Microbiol. 2012;78:5111–5118.CrossRef
38.
go back to reference Matsuki T, Watanabe K, Fujimoto J, et al. Development of 16S rRNA-gene-targeted group-specific primers for the detection and identification of predominant bacteria in human feces. Appl Environ Microbiol. 2002;68:5445–5451.CrossRef Matsuki T, Watanabe K, Fujimoto J, et al. Development of 16S rRNA-gene-targeted group-specific primers for the detection and identification of predominant bacteria in human feces. Appl Environ Microbiol. 2002;68:5445–5451.CrossRef
39.
go back to reference Matsuki T, Watanabe K, Fujimoto J, Takada T, Tanaka R. Use of 16S rRNA gene-targeted group-specific primers for real-time PCR analysis of predominant bacteria in human feces. Appl Environ Microbiol. 2004;70:7220–7228.CrossRef Matsuki T, Watanabe K, Fujimoto J, Takada T, Tanaka R. Use of 16S rRNA gene-targeted group-specific primers for real-time PCR analysis of predominant bacteria in human feces. Appl Environ Microbiol. 2004;70:7220–7228.CrossRef
40.
go back to reference Suzuki Y, Ikeda K, Sakuma K, et al. Association between Yogurt Consumption and Intestinal Microbiota in Healthy Young Adults Differs by Host Gender. Front Microbiol. 2017;8:847.CrossRef Suzuki Y, Ikeda K, Sakuma K, et al. Association between Yogurt Consumption and Intestinal Microbiota in Healthy Young Adults Differs by Host Gender. Front Microbiol. 2017;8:847.CrossRef
41.
go back to reference Morita C, Tsuji H, Hata T, et al. Gut dysbiosis in patients with anorexia nervosa. PLoS ONE. 2015;10:e0145274.CrossRef Morita C, Tsuji H, Hata T, et al. Gut dysbiosis in patients with anorexia nervosa. PLoS ONE. 2015;10:e0145274.CrossRef
42.
go back to reference Turnbaugh PJ, Hamady M, Yatsunenko T, et al. A core gut microbiome in obese and lean twins. Nature. 2009;457:480–484.CrossRef Turnbaugh PJ, Hamady M, Yatsunenko T, et al. A core gut microbiome in obese and lean twins. Nature. 2009;457:480–484.CrossRef
43.
go back to reference Qin J, Li Y, Cai Z, et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature. 2012;490:55–60.CrossRef Qin J, Li Y, Cai Z, et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature. 2012;490:55–60.CrossRef
44.
go back to reference Howden CW, Hunt RH. Relationship between gastric secretion and infection. Gut. 1987;28:96–107.CrossRef Howden CW, Hunt RH. Relationship between gastric secretion and infection. Gut. 1987;28:96–107.CrossRef
45.
go back to reference Kaci G, Goudercourt D, Dennin V, et al. Anti-inflammatory properties of Streptococcus salivarius, a commensal bacterium of the oral cavity and digestive tract. Appl Environ Microbiol. 2014;80:928–934.CrossRef Kaci G, Goudercourt D, Dennin V, et al. Anti-inflammatory properties of Streptococcus salivarius, a commensal bacterium of the oral cavity and digestive tract. Appl Environ Microbiol. 2014;80:928–934.CrossRef
46.
go back to reference Do T, Jolley KA, Maiden MC, et al. Population structure of Streptococcus oralis. Microbiology (Read Engl). 2009;155:2593–2602.CrossRef Do T, Jolley KA, Maiden MC, et al. Population structure of Streptococcus oralis. Microbiology (Read Engl). 2009;155:2593–2602.CrossRef
47.
go back to reference Xu HB, Wang HD, Li CH, et al. Proton pump inhibitor use and risk of spontaneous bacterial peritonitis in cirrhotic patients: a systematic review and meta-analysis. Genet Mol Res.. 2015;14:7490–7501.CrossRef Xu HB, Wang HD, Li CH, et al. Proton pump inhibitor use and risk of spontaneous bacterial peritonitis in cirrhotic patients: a systematic review and meta-analysis. Genet Mol Res.. 2015;14:7490–7501.CrossRef
48.
go back to reference Zhou SJ, Wang SQ, Ma YY, et al. Association of proton pump inhibitors with the occurrence of gut-derived bacteraemia in patients with haematological malignancy after chemotherapy. Hematology (Amst Neth). 2016;21:332–337.CrossRef Zhou SJ, Wang SQ, Ma YY, et al. Association of proton pump inhibitors with the occurrence of gut-derived bacteraemia in patients with haematological malignancy after chemotherapy. Hematology (Amst Neth). 2016;21:332–337.CrossRef
49.
go back to reference Ramamoorthy SL, Lee JK, Mintz Y, et al. The impact of proton-pump inhibitors on intraperitoneal sepsis: a word of caution for transgastric NOTES procedures. Surg Endosc. 2010;24:16–20.CrossRef Ramamoorthy SL, Lee JK, Mintz Y, et al. The impact of proton-pump inhibitors on intraperitoneal sepsis: a word of caution for transgastric NOTES procedures. Surg Endosc. 2010;24:16–20.CrossRef
50.
go back to reference Engen PA, Green SJ, Voigt RM, Forsyth CB, Keshavarzian A. The gastrointestinal microbiome: alcohol effects on the composition of intestinal microbiota. Alcohol Res. 2015;37:223–236.PubMedPubMedCentral Engen PA, Green SJ, Voigt RM, Forsyth CB, Keshavarzian A. The gastrointestinal microbiome: alcohol effects on the composition of intestinal microbiota. Alcohol Res. 2015;37:223–236.PubMedPubMedCentral
51.
go back to reference Selle K, Klaenhammer TR. Genomic and phenotypic evidence for probiotic influences of Lactobacillus gasseri on human health. FEMS Microbiol Rev. 2013;37:915–935.CrossRef Selle K, Klaenhammer TR. Genomic and phenotypic evidence for probiotic influences of Lactobacillus gasseri on human health. FEMS Microbiol Rev. 2013;37:915–935.CrossRef
52.
go back to reference Varma P, Dinesh KR, Menon KK, Biswas R. Lactobacillus fermentum isolated from human colonic mucosal biopsy inhibits the growth and adhesion of enteric and foodborne pathogens. J Food Sci. 2010;75:M546–M551.CrossRef Varma P, Dinesh KR, Menon KK, Biswas R. Lactobacillus fermentum isolated from human colonic mucosal biopsy inhibits the growth and adhesion of enteric and foodborne pathogens. J Food Sci. 2010;75:M546–M551.CrossRef
53.
go back to reference Thomas CM, Hong T, van Pijkeren JP, et al. Histamine derived from probiotic Lactobacillus reuteri suppresses TNF via modulation of PKA and ERK signaling. PloS one. 2012;7:e31951.CrossRef Thomas CM, Hong T, van Pijkeren JP, et al. Histamine derived from probiotic Lactobacillus reuteri suppresses TNF via modulation of PKA and ERK signaling. PloS one. 2012;7:e31951.CrossRef
54.
go back to reference Taweechotipatr M, Iyer C, Spinler JK, Versalovic J, Tumwasorn S. Lactobacillus saerimneri and Lactobacillus ruminis: novel human-derived probiotic strains with immunomodulatory activities. FEMS Microbiol Lett. 2009;293:65–72.CrossRef Taweechotipatr M, Iyer C, Spinler JK, Versalovic J, Tumwasorn S. Lactobacillus saerimneri and Lactobacillus ruminis: novel human-derived probiotic strains with immunomodulatory activities. FEMS Microbiol Lett. 2009;293:65–72.CrossRef
55.
go back to reference Sherid M, Samo S, Sulaiman S, Husein H, Sifuentes H, Sridhar S. Liver abscess and bacteremia caused by Lactobacillus: role of probiotics? Case report and review of the literature. BMC Gastroenterol. 2016;16:138.CrossRef Sherid M, Samo S, Sulaiman S, Husein H, Sifuentes H, Sridhar S. Liver abscess and bacteremia caused by Lactobacillus: role of probiotics? Case report and review of the literature. BMC Gastroenterol. 2016;16:138.CrossRef
57.
go back to reference Hasegawa S, Goto S, Tsuji H, et al. Intestinal dysbiosis and lowered serum lipopolysaccharide-binding protein in Parkinson’s disease. PloS one. 2015;10:e0142164.CrossRef Hasegawa S, Goto S, Tsuji H, et al. Intestinal dysbiosis and lowered serum lipopolysaccharide-binding protein in Parkinson’s disease. PloS one. 2015;10:e0142164.CrossRef
58.
go back to reference Fijan S. Microorganisms with claimed probiotic properties: an overview of recent literature. Int J Environ Res Public Health. 2014;11:4745–4767.CrossRef Fijan S. Microorganisms with claimed probiotic properties: an overview of recent literature. Int J Environ Res Public Health. 2014;11:4745–4767.CrossRef
59.
go back to reference Papizadeh M, Rohani M, Nahrevanian H, Javadi A, Pourshafie MR. Probiotic characters of Bifidobacterium and Lactobacillus are a result of the ongoing gene acquisition and genome minimization evolutionary trends. Microb. Pathog. 2017;111:118–131.CrossRef Papizadeh M, Rohani M, Nahrevanian H, Javadi A, Pourshafie MR. Probiotic characters of Bifidobacterium and Lactobacillus are a result of the ongoing gene acquisition and genome minimization evolutionary trends. Microb. Pathog. 2017;111:118–131.CrossRef
Metadata
Title
Gut Microbiota Composition Before and After Use of Proton Pump Inhibitors
Authors
Mariko Hojo
Takashi Asahara
Akihito Nagahara
Tsutomu Takeda
Kohei Matsumoto
Hiroya Ueyama
Kenshi Matsumoto
Daisuke Asaoka
Takuya Takahashi
Koji Nomoto
Yuichiro Yamashiro
Sumio Watanabe
Publication date
01-11-2018
Publisher
Springer US
Published in
Digestive Diseases and Sciences / Issue 11/2018
Print ISSN: 0163-2116
Electronic ISSN: 1573-2568
DOI
https://doi.org/10.1007/s10620-018-5122-4

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