Probiotics in Functional Dyspepsia
Abstract
:1. Introduction
2. Materials and Methods
3. Probiotics as a Potential Treatment for FD
4. The Evidence
4.1. Data from Cohort Studies
Study—Ref | Country | FD Diagnosis | Probiotic (Type/Duration) | Primary Outcome |
---|---|---|---|---|
Cohort Studies | ||||
Ianiro et al. [28] | Italy | Rome III | Lactobacillus reuterii 100 billion/g (0.04 g), Lactobacillus rhamnosus GG 350 billion/g (0.1143 g), Saccharomyces boulardi 20 billion/g (0.08 g), vitamin B6 hydrochloride (0.00102 g), inositol (0.025 g), silica (0.01255 g); Q10 coenzyme (25 mg)—7 days | Control in symptoms by using Rome III criteria |
Nakae et al. [29] | Japan | Rome III | One hundred and eighteen grams of yogurt containing 109 colony-forming units of Lactobacillus gasseri OLL2716 (LG21) (LG21 yogurt) every day for 12 weeks | Symptoms of GERD (FSSG) questionnaire |
Igarashi et al. [30] | Japan | Rome III | One hundred and eighteen grams of yogurt containing 109 colony-forming units (CFUs) of Lactobacillus gasseri OLL2716 (LG21) (LG21 yogurt) every day for 12 weeks | Symptoms of GERD (FSSG) questionnaire |
Drago et al. [31] | Italy | Rome IV | Lacticaseibacillus rhamnosus LR04 (DSM 16605), Lactiplantibacillus pentosus LPS01 (DSM 21980), Lactiplantibacillus plantarum LP01 (LMG P-21021), and Lactobacillus delbrueckii subsp. Delbruekii LDD01 (DMS 22106) for 30 days in four groups: (1) probiotics alone, (2) probiotics plus proton-pump inhibitors, (3) probiotics plus prokinetics, and (4) probiotic plus antacid | Presence of specific clinical symptoms associated with PDS (postprandial filling and early satiety) and EPS (epigastric pain and epigastric burning) at study beginning (T0) and study end (T1) |
Sun et al. [32] | China | Rome IV | One hundred milliliters (2 bottles/d, 100 mL/bottle) of beverage containing Lactobacillus paracasei LC-37 for 4 weeks | Change in digestive symptom scores at baseline, after 14 and 28 days of treatment |
Randomized Controlled Trials | ||||
Kim et al. [33] | USA | Rome II | Four grams of probiotics: 50 million CFU (six species): Lactobacillus acidophilus, Bifidobacterium bifidum, Bacillus subtilis, Lactobacillus bulgaricus, Lactobacillus lactis, and Bacillus lichenformis once a day >12 weeks | Gastrointestinal Quality of Life Index (GIQLI) improvement |
Ohtsu et al. [34] | Japan | Rome III | Eighty-five grams of yogurt containing Lactobacillus gasseri OLL2716 (L. gasseri OLL2716—amount of L. gasseri OLL2716 per unit of yogurt: 10 9 CFU or higher) for 12 weeks | Global assessment (impression of effect of the 12-week test food intake on gastric symptoms) |
Wauters et al. [35] | Belgium | Rome IV | Bacillus coagulans MY01 and Bacillus subtilis MY02, 2·5 × 109 colony-forming units per capsule, taken twice per day with meals for 8 weeks and open-label extension phase of 8 weeks | Proportion of clinical responders; decrease of at least 0·7 in PDS score at week 8 in FD with baseline PDS scores of 1 or more (at least mild symptom scores) on the LPDS diary in the entire cohort (on and off proton-pump inhibitors) |
4.2. Data from Randomized Controlled Trials (RCT)
4.3. Data from Meta-Analysis
5. Critical Appraisal and Future Directions
6. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
- Enck, P.; Azpiroz, F.; Boeckxstaens, G.; Elsenbruch, S.; Feinle-Bisset, C.; Holtmann, G.; Lackner, J.M.; Ronkainen, J.; Schemann, M.; Stengel, A.; et al. Functional dyspepsia. Nat. Rev. Dis. Prim. 2017, 3, 17081. [Google Scholar] [CrossRef]
- Stanghellini, V.; Chan, F.K.; Hasler, W.L.; Malagelada, J.R.; Suzuki, H.; Tack, J.; Talley, N.J. Gastroduodenal Disorders. Gastroenterology 2016, 150, 1380–1392. [Google Scholar] [CrossRef] [PubMed]
- Wauters, L.; Dickman, R.; Drug, V.; Mulak, A.; Serra, J.; Enck, P.; Tack, J.; Group, E.F.C.; Accarino, A.; Barbara, G.; et al. United European Gastroenterology (UEG) and European Society for Neurogastroenterology and Motility (ESNM) consensus on functional dyspepsia. United Eur. Gastroenterol. J. 2021, 9, 307–331. [Google Scholar] [CrossRef] [PubMed]
- Wauters, L.; Talley, N.J.; Walker, M.M.; Tack, J.; Vanuytsel, T. Novel concepts in the pathophysiology and treatment of functional dyspepsia. Gut 2020, 69, 591–600. [Google Scholar] [CrossRef]
- Moayyedi, P.; Lacy, B.E.; Andrews, C.N.; Enns, R.A.; Howden, C.W.; Vakil, N. ACG and CAG Clinical Guideline: Management of Dyspepsia. Am. J. Gastroenterol. 2017, 112, 988–1013. [Google Scholar] [CrossRef] [PubMed]
- Tack, J.; Carbone, F. Functional dyspepsia and gastroparesis. Curr. Opin. Gastroenterol. 2017, 33, 446–454. [Google Scholar] [CrossRef]
- Tziatzios, G.; Gkolfakis, P.; Papanikolaou, I.S.; Mathur, R.; Pimentel, M.; Giamarellos-Bourboulis, E.J.; Triantafyllou, K. Gut Microbiota Dysbiosis in Functional Dyspepsia. Microorganisms 2020, 8, 691. [Google Scholar] [CrossRef]
- Talley, N.J. What Causes Functional Gastrointestinal Disorders? A Proposed Disease Model. Am. J. Gastroenterol. 2020, 115, 41–48. [Google Scholar] [CrossRef]
- Ford, A.C.; Quigley, E.M.; Lacy, B.E.; Lembo, A.J.; Saito, Y.A.; Schiller, L.R.; Soffer, E.E.; Spiegel, B.M.; Moayyedi, P. Efficacy of prebiotics, probiotics, and synbiotics in irritable bowel syndrome and chronic idiopathic constipation: Systematic review and meta-analysis. Am. J. Gastroenterol. 2014, 109, 1547–1561. [Google Scholar] [CrossRef]
- Ukena, S.N.; Singh, A.; Dringenberg, U.; Engelhardt, R.; Seidler, U.; Hansen, W.; Bleich, A.; Bruder, D.; Franzke, A.; Rogler, G.; et al. Probiotic Escherichia coli Nissle 1917 inhibits leaky gut by enhancing mucosal integrity. PLoS ONE 2007, 2, e1308. [Google Scholar] [CrossRef]
- Hosseini, A.; Nikfar, S.; Abdollahi, M. Probiotics use to treat irritable bowel syndrome. Expert Opin. Biol. Ther. 2012, 12, 1323–1334. [Google Scholar] [CrossRef] [PubMed]
- Pimentel, M.; Lembo, A. Microbiome and Its Role in Irritable Bowel Syndrome. Dig. Dis. Sci. 2020, 65, 829–839. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- O’Mahony, L.; McCarthy, J.; Kelly, P.; Hurley, G.; Luo, F.; Chen, K.; O’Sullivan, G.C.; Kiely, B.; Collins, J.K.; Shanahan, F.; et al. Lactobacillus and bifidobacterium in irritable bowel syndrome: Symptom responses and relationship to cytokine profiles. Gastroenterology 2005, 128, 541–551. [Google Scholar] [CrossRef]
- Rousseaux, C.; Thuru, X.; Gelot, A.; Barnich, N.; Neut, C.; Dubuquoy, L.; Dubuquoy, C.; Merour, E.; Geboes, K.; Chamaillard, M.; et al. Lactobacillus acidophilus modulates intestinal pain and induces opioid and cannabinoid receptors. Nat. Med. 2007, 13, 35–37. [Google Scholar] [CrossRef]
- Zhang, J.; Wu, H.M.; Wang, X.; Xie, J.; Li, X.; Ma, J.; Wang, F.; Tang, X. Efficacy of prebiotics and probiotics for functional dyspepsia: A systematic review and meta-analysis. Medicine 2020, 99, e19107. [Google Scholar] [CrossRef]
- Gudina, E.J.; Teixeira, J.A.; Rodrigues, L.R. Isolation and functional characterization of a biosurfactant produced by Lactobacillus paracasei. Colloids Surf. B Biointerfaces 2010, 76, 298–304. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vanheel, H.; Vicario, M.; Vanuytsel, T.; Van Oudenhove, L.; Martinez, C.; Keita, A.V.; Pardon, N.; Santos, J.; Soderholm, J.D.; Tack, J.; et al. Impaired duodenal mucosal integrity and low-grade inflammation in functional dyspepsia. Gut 2014, 63, 262–271. [Google Scholar] [CrossRef] [PubMed]
- Patel, R.M.; Myers, L.S.; Kurundkar, A.R.; Maheshwari, A.; Nusrat, A.; Lin, P.W. Probiotic bacteria induce maturation of intestinal claudin 3 expression and barrier function. Am. J. Pathol. 2012, 180, 626–635. [Google Scholar] [CrossRef] [Green Version]
- Caviglia, G.P.; Rosso, C.; Ribaldone, D.G.; Dughera, F.; Fagoonee, S.; Astegiano, M.; Pellicano, R. Physiopathology of intestinal barrier and the role of zonulin. Minerva Biotecnol. 2019, 31, 83–92. [Google Scholar] [CrossRef]
- Kaji, I.; Iwanaga, T.; Watanabe, M.; Guth, P.H.; Engel, E.; Kaunitz, J.D.; Akiba, Y. SCFA transport in rat duodenum. Am. J. Physiol. Gastrointest. Liver Physiol. 2015, 308, G188–G197. [Google Scholar] [CrossRef]
- Camilleri, M. Peripheral mechanisms in irritable bowel syndrome. N. Engl. J. Med. 2012, 367, 1626–1635. [Google Scholar] [CrossRef] [PubMed]
- Dalile, B.; Van Oudenhove, L.; Vervliet, B.; Verbeke, K. The role of short-chain fatty acids in microbiota-gut-brain communication. Nat. Rev. Gastroenterol. Hepatol. 2019, 16, 461–478. [Google Scholar] [CrossRef] [PubMed]
- Yano, J.M.; Yu, K.; Donaldson, G.P.; Shastri, G.G.; Ann, P.; Ma, L.; Nagler, C.R.; Ismagilov, R.F.; Mazmanian, S.K.; Hsiao, E.Y. Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis. Cell 2015, 161, 264–276. [Google Scholar] [CrossRef] [Green Version]
- Simren, M.; Tornblom, H.; Palsson, O.S.; van Tilburg, M.A.L.; Van Oudenhove, L.; Tack, J.; Whitehead, W.E. Visceral hypersensitivity is associated with GI symptom severity in functional GI disorders: Consistent findings from five different patient cohorts. Gut 2018, 67, 255–262. [Google Scholar] [CrossRef] [PubMed]
- Burns, G.; Carroll, G.; Mathe, A.; Horvat, J.; Foster, P.; Walker, M.M.; Talley, N.J.; Keely, S. Evidence for Local and Systemic Immune Activation in Functional Dyspepsia and the Irritable Bowel Syndrome: A Systematic Review. Am. J. Gastroenterol. 2019, 114, 429–436. [Google Scholar] [CrossRef] [PubMed]
- Anitha, M.; Vijay-Kumar, M.; Sitaraman, S.V.; Gewirtz, A.T.; Srinivasan, S. Gut microbial products regulate murine gastrointestinal motility via Toll-like receptor 4 signaling. Gastroenterology 2012, 143, 1006–1016.e1004. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wu, R.Y.; Maattanen, P.; Napper, S.; Scruten, E.; Li, B.; Koike, Y.; Johnson-Henry, K.C.; Pierro, A.; Rossi, L.; Botts, S.R.; et al. Non-digestible oligosaccharides directly regulate host kinome to modulate host inflammatory responses without alterations in the gut microbiota. Microbiome 2017, 5, 135. [Google Scholar] [CrossRef] [Green Version]
- Ianiro, G.; Pizzoferrato, M.; Franceschi, F.; Tarullo, A.; Luisi, T.; Gasbarrini, G. Effect of an extra-virgin olive oil enriched with probiotics or antioxidants on functional dyspepsia: A pilot study. Eur. Rev. Med. Pharmacol. Sci. 2013, 17, 2085–2090. [Google Scholar]
- Nakae, H.; Tsuda, A.; Matsuoka, T.; Mine, T.; Koga, Y. Gastric microbiota in the functional dyspepsia patients treated with probiotic yogurt. BMJ Open Gastroenterol. 2016, 3, e000109. [Google Scholar] [CrossRef] [Green Version]
- Igarashi, M.; Nakae, H.; Matsuoka, T.; Takahashi, S.; Hisada, T.; Tomita, J.; Koga, Y. Alteration in the gastric microbiota and its restoration by probiotics in patients with functional dyspepsia. BMJ Open Gastroenterol. 2017, 4, e000144. [Google Scholar] [CrossRef]
- Drago, L.; Meroni, G.; Pistone, D.; Pasquale, L.; Milazzo, G.; Monica, F.; Aragona, S.; Ficano, L.; Vassallo, R.; Gastrobiota, G. Evaluation of main functional dyspepsia symptoms after probiotic administration in patients receiving conventional pharmacological therapies. J. Int. Med. Res. 2021, 49, 300060520982657. [Google Scholar] [CrossRef]
- Sun, E.; Zhang, X.; Zhao, Y.; Li, J.; Sun, J.; Mu, Z.; Wang, R. Beverages containing Lactobacillus paracasei LC-37 improved functional dyspepsia through regulation of the intestinal microbiota and their metabolites. J. Dairy Sci. 2021, 104, 6389–6398. [Google Scholar] [CrossRef] [PubMed]
- Kim, S.L.; Hilli, L.; Orlowski, J.; Kupperman, J.L.; Baral, M.; Waters, R.F. Efficacy of probiotics and nutrients in functional gastrointestinal disorders: A preliminary clinical trial. Dig. Dis. Sci. 2006, 51, 2134–2144. [Google Scholar] [CrossRef] [PubMed]
- Ohtsu, T.; Takagi, A.; Uemura, N.; Inoue, K.; Sekino, H.; Kawashima, A.; Uchida, M.; Koga, Y. The Ameliorating Effect of Lactobacillus gasseri OLL2716 on Functional Dyspepsia in Helicobacter pylori-Uninfected Individuals: A Randomized Controlled Study. Digestion 2017, 96, 92–102. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wauters, L.; Slaets, H.; De Paepe, K.; Ceulemans, M.; Wetzels, S.; Geboers, K.; Toth, J.; Thys, W.; Dybajlo, R.; Walgraeve, D.; et al. Efficacy and safety of spore-forming probiotics in the treatment of functional dyspepsia: A pilot randomised, double-blind, placebo-controlled trial. Lancet Gastroenterol. Hepatol. 2021, 6, 784–792. [Google Scholar] [CrossRef]
- Tziatzios, G.; Giamarellos-Bourboulis, E.J.; Papanikolaou, I.S.; Pimentel, M.; Dimitriadis, G.D.; Triantafyllou, K. Is small intestinal bacterial overgrowth involved in the pathogenesis of functional dyspepsia? Med. Hypotheses 2017, 106, 26–32. [Google Scholar] [CrossRef]
- Tziatzios, G.; Gkolfakis, P.; Papanikolaou, I.S.; Mathur, R.; Pimentel, M.; Damoraki, G.; Giamarellos-Bourboulis, E.J.; Dimitriadis, G.; Triantafyllou, K. High prevalence of small intestinal bacterial overgrowth among functional dyspepsia patients. Dig. Dis. 2020, 39, 382–390. [Google Scholar] [CrossRef]
- Sugano, K.; Tack, J.; Kuipers, E.J.; Graham, D.Y.; El-Omar, E.M.; Miura, S.; Haruma, K.; Asaka, M.; Uemura, N.; Malfertheiner, P.; et al. Kyoto global consensus report on Helicobacter pylori gastritis. Gut 2015, 64, 1353–1367. [Google Scholar] [CrossRef]
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Tziatzios, G.; Gkolfakis, P.; Leite, G.; Mathur, R.; Damoraki, G.; Giamarellos-Bourboulis, E.J.; Triantafyllou, K. Probiotics in Functional Dyspepsia. Microorganisms 2023, 11, 351. https://doi.org/10.3390/microorganisms11020351
Tziatzios G, Gkolfakis P, Leite G, Mathur R, Damoraki G, Giamarellos-Bourboulis EJ, Triantafyllou K. Probiotics in Functional Dyspepsia. Microorganisms. 2023; 11(2):351. https://doi.org/10.3390/microorganisms11020351
Chicago/Turabian StyleTziatzios, Georgios, Paraskevas Gkolfakis, Gabriela Leite, Ruchi Mathur, Georgia Damoraki, Evangelos J. Giamarellos-Bourboulis, and Konstantinos Triantafyllou. 2023. "Probiotics in Functional Dyspepsia" Microorganisms 11, no. 2: 351. https://doi.org/10.3390/microorganisms11020351