Probiotics in Autoimmune and Inflammatory Disorders
Abstract
:1. History of Probiotics
1.1. Recognized Benefits in the 1900s
1.2. Expanded Role in Infants and in Patients with Gastroinestinal Disorders (2000–Present)
2. Effects of Probiotics in High-Risk Populations with Immune Dysregulation and Autoimmune Diseases
3. Mechanism of Action of Probiotics
4. “Polarization” within the Medical Community Regarding the Use of Probiotics
5. The Future of Probiotics
Author Contributions
Funding
Conflicts of Interest
References
- McFarland, L.V. From yaks to yogurt: The history, development, and current use of probiotics. Clin. Infect. Dis. 2015, 60, S85–S90. [Google Scholar] [CrossRef] [PubMed]
- Guo, X.; Long, R.; Kreuzer, M.; Ding, L.; Shang, Z.; Zhang, Y.; Yang, Y.; Cui, G. Importance of functional ingredients in yak milk-derived food on health of Tibetan nomads living under high-altitude stress: A review. Crit. Rev. Food Sci. Nutr. 2014, 54, 292–302. [Google Scholar] [CrossRef] [PubMed]
- Curtis, R.I. Salted fish products in ancient medicine. J. Hist. Med. Allied Sci. 1984, 39, 430–445. [Google Scholar] [CrossRef] [PubMed]
- Fisberg, M.; Machado, R. History of yogurt and current patterns of consumption. Nutr. Rev. 2015, 73, 4–7. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gasbarrini, G.; Bonvicini, F.; Gramenzi, A. Probiotics History. J. Clin. Gastroenterol. 2016, 50, S116–S119. [Google Scholar] [CrossRef] [PubMed]
- Schultz, M. Clinical use of E. coli Nissle 1917 in inflammatory bowel disease. Inflamm. Bowel. Dis. 2008, 14, 1012–1018. [Google Scholar] [CrossRef] [PubMed]
- Guarino, A.; Guandalini, S.; Lo, V.A. Probiotics for Prevention and Treatment of Diarrhea. J. Clin. Gastroenterol. 2015, 49, S37–S45. [Google Scholar] [CrossRef] [PubMed]
- Alfaleh, K.; Bassler, D. Probiotics for prevention of necrotizing enterocolitis in preterm infants. Cochrane Database Syst. Rev. 2008, CD005496. [Google Scholar] [CrossRef]
- Thomas, J.P.; Raine, T.; Reddy, S.; Belteki, G. Probiotics for the prevention of necrotising enterocolitis in very low-birth-weight infants: A meta-analysis and systematic review. Acta Paediatr. 2017, 106, 1729–1741. [Google Scholar] [CrossRef] [PubMed]
- Chang, H.Y.; Chen, J.H.; Chang, J.H.; Lin, H.C.; Lin, C.Y.; Peng, C.C. Multiple strains probiotics appear to be the most effective probiotics in the prevention of necrotizing enterocolitis and mortality: An updated meta-analysis. PLoS ONE 2017, 12, e0171579. [Google Scholar] [CrossRef] [PubMed]
- Aceti, A.; Gori, D.; Barone, G.; Callegari, M.L.; Di, M.A.; Fantini, M.P.; Indrio, F.; Maggio, L.; Meneghin, F.; Morelli, L.; et al. Probiotics for prevention of necrotizing enterocolitis in preterm infants: Systematic review and meta-analysis. Ital. J. Pediatr. 2015, 41, 89–109. [Google Scholar] [CrossRef] [PubMed]
- Aceti, A.; Maggio, L.; Beghetti, I.; Gori, D.; Barone, G.; Callegari, M.L.; Fantini, M.P.; Indrio, F.; Meneghin, F.; Morelli, L.; et al. Probiotics Prevent Late-Onset Sepsis in Human Milk-Fed, Very Low Birth Weight Preterm Infants: Systematic Review and Meta-Analysis. Nutrients 2017, 9, 904–925. [Google Scholar] [CrossRef] [PubMed]
- Khailova, L.; Dvorak, K.; Arganbright, K.M.; Halpern, M.D.; Kinouchi, T.; Yajima, M.; Dvorak, B. Bifidobacterium bifidum improves intestinal integrity in a rat model of necrotizing enterocolitis. Am. J. Physiol. Gastrointest. Liver Physiol. 2009, 297, G940–G949. [Google Scholar] [CrossRef] [PubMed]
- Good, M.; Sodhi, C.P.; Ozolek, J.A.; Buck, R.H.; Goehring, K.C.; Thomas, D.L.; Vikram, A.; Bibby, K.; Morowitz, M.J.; Firek, B.; et al. Lactobacillus rhamnosus HN001 decreases the severity of necrotizing enterocolitis in neonatal mice and preterm piglets: Evidence in mice for a role of TLR9. Am. J. Physiol. Gastrointest. Liver Physiol. 2014, 306, G1021–G1032. [Google Scholar] [CrossRef] [PubMed]
- Hoang, T.K.; He, B.; Wang, T.; Tran, D.Q.; Rhoads, J.M.; Liu, Y. Protective effect of Lactobacillus reuteri DSM 17938 against experimental necrotizing enterocolitis is mediated by Toll-like receptor 2. Am. J. Physiol. Gastrointest. Liver Physiol. 2018, 315, G231–G240. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.; Fatheree, N.Y.; Dingle, B.M.; Tran, D.Q.; Rhoads, M. Lactobacillus reuteri DSM 17938 changes the frequency of Foxp3+ regulatory T cells in the intestine and mesenteric lymph node in experimental necrotizing enterocolitis. PLoS ONE 2013, 8, e56547. [Google Scholar] [CrossRef] [PubMed]
- Simren, M.; Palsson, O.S.; Whitehead, W.E. Update on Rome IV Criteria for Colorectal Disorders: Implications for Clinical Practice. Curr. Gastroenterol. Rep. 2017, 19, 15–23. [Google Scholar] [CrossRef] [PubMed]
- Pozuelo, M.; Panda, S.; Santiago, A.; Mendez, S.; Accarino, A.; Santos, J.; Guarner, F.; Azpiroz, F.; Manichanh, C. Reduction of butyrate- and methane-producing microorganisms in patients with Irritable Bowel Syndrome. Sci. Rep. 2015, 5, 12693–12705. [Google Scholar] [CrossRef] [PubMed]
- 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] [PubMed]
- Zhang, Y.; Li, L.; Guo, C.; Mu, D.; Feng, B.; Zuo, X.; Li, Y. Effects of probiotic type, dose and treatment duration on irritable bowel syndrome diagnosed by Rome III criteria: A meta-analysis. BMC Gastroenterol. 2016, 16, 62–73. [Google Scholar] [CrossRef] [PubMed]
- Wessel, M.A.; Cobb, J.C.; Jackson, E.B.; Harris, G.S., Jr.; Detwiler, A.C. Paroxysmal fussing in infancy, sometimes called colic. Pediatrics 1954, 14, 421–435. [Google Scholar] [PubMed]
- de Weerth, C.; Fuentes, S.; Puylaert, P.; de Vos, W.M. Intestinal microbiota of infants with colic: Development and specific signatures. Pediatrics 2013, 131, e550–e558. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rhoads, J.M.; Fatheree, N.Y.; Norori, J.; Liu, Y.; Lucke, J.F.; Tyson, J.E.; Ferris, M.J. Altered fecal microflora and increased fecal calprotectin in infants with colic. J. Pediatr. 2009, 155, 823–828. [Google Scholar] [CrossRef] [PubMed]
- Savino, F.; Cordisco, L.; Tarasco, V.; Calabrese, R.; Palumeri, E.; Matteuzzi, D. Molecular identification of coliform bacteria from colicky breastfed infants. Acta Paediatr. 2009, 98, 1582–1588. [Google Scholar] [CrossRef] [PubMed]
- Rhoads, J.M.; Collins, J.; Fatheree, N.Y.; Hashmi, S.S.; Taylor, C.M.; Luo, M.; Hoang, T.K.; Gleason, W.A.; Van Arsdall, M.R.; Navarro, F.; et al. Infant Colic Represents Gut Inflammation and Dysbiosis. J. Pediatr. 2018. [Google Scholar] [CrossRef] [PubMed]
- Harb, T.; Matsuyama, M.; David, M.; Hill, R.J. Infant Colic-What works: A Systematic Review of Interventions for Breast-fed Infants. J. Pediatr. Gastroenterol. Nutr. 2016, 62, 668–686. [Google Scholar] [CrossRef] [PubMed]
- Sung, V.; D’Amico, F.; Cabana, M.D.; Chau, K.; Koren, G.; Savino, F.; Szajewska, H.; Deshpande, G.; Dupont, C.; Indrio, F.; et al. Lactobacillus reuteri to Treat Infant Colic: A Meta-analysis. Pediatrics 2018, 141, e20171811. [Google Scholar] [CrossRef] [PubMed]
- Xu, M.; Wang, J.; Wang, N.; Sun, F.; Wang, L.; Liu, X.H. The Efficacy and Safety of the Probiotic Bacterium Lactobacillus reuteri DSM 17938 for Infantile Colic: A Meta-Analysis of Randomized Controlled Trials. PLoS ONE 2015, 10, e0141445. [Google Scholar] [CrossRef] [PubMed]
- Maldonado, J.; Canabate, F.; Sempere, L.; Vela, F.; Sanchez, A.R.; Narbona, E.; Lopez-Huertas, E.; Geerlings, A.; Valero, A.D.; Olivares, M.; et al. Human milk probiotic Lactobacillus fermentum CECT5716 reduces the incidence of gastrointestinal and upper respiratory tract infections in infants. J. Pediatr. Gastroenterol. Nutr. 2012, 54, 55–61. [Google Scholar] [CrossRef] [PubMed]
- Rautava, S.; Salminen, S.; Isolauri, E. Specific probiotics in reducing the risk of acute infections in infancy—A randomised, double-blind, placebo-controlled study. Br. J. Nutr. 2009, 101, 1722–1726. [Google Scholar] [CrossRef] [PubMed]
- Smith, T.J.; Rigassio-Radler, D.; Denmark, R.; Haley, T.; Touger-Decker, R. Effect of Lactobacillus rhamnosus LGG(R) and Bifidobacterium animalis ssp. lactis BB-12(R) on health-related quality of life in college students affected by upper respiratory infections. Br. J. Nutr. 2013, 109, 1999–2007. [Google Scholar] [CrossRef] [PubMed]
- Taipale, T.; Pienihakkinen, K.; Isolauri, E.; Larsen, C.; Brockmann, E.; Alanen, P.; Jokela, J.; Soderling, E. Bifidobacterium animalis subsp. lactis BB-12 in reducing the risk of infections in infancy. Br. J. Nutr. 2011, 105, 409–416. [Google Scholar] [CrossRef] [PubMed]
- Nocerino, R.; Paparo, L.; Terrin, G.; Pezzella, V.; Amoroso, A.; Cosenza, L.; Cecere, G.; De, M.G.; Micillo, M.; Albano, F.; et al. Cow’s milk and rice fermented with Lactobacillus paracasei CBA L74 prevent infectious diseases in children: A randomized controlled trial. Clin. Nutr. 2017, 36, 118–125. [Google Scholar] [CrossRef] [PubMed]
- Villena, J.; Barbieri, N.; Salva, S.; Herrera, M.; Alvarez, S. Enhanced immune response to pneumococcal infection in malnourished mice nasally treated with heat-killed Lactobacillus casei. Microbiol. Immunol. 2009, 53, 636–646. [Google Scholar] [CrossRef] [PubMed]
- Ishizaki, A.; Bi, X.; Nguyen, L.V.; Matsuda, K.; Pham, H.V.; Phan, C.T.T.; Khu, D.T.K.; Ichimura, H. Effects of Short-Term Probiotic Ingestion on Immune Profiles and Microbial Translocation among HIV-1-Infected Vietnamese Children. Int. J Mol. Sci. 2017, 18, E2185. [Google Scholar] [CrossRef] [PubMed]
- McCulloch, J.; Lydyard, P.M.; Rook, G.A. Rheumatoid arthritis: How well do the theories fit the evidence? Clin. Exp. Immunol. 1993, 92, 1–6. [Google Scholar] [CrossRef] [PubMed]
- Mohammed, A.T.; Khattab, M.; Ahmed, A.M.; Turk, T.; Sakr, N.; Khalil, M.; Abdelhalim, M.; Sawaf, B.; Hirayama, K.; Huy, N.T. The therapeutic effect of probiotics on rheumatoid arthritis: A systematic review and meta-analysis of randomized control trials. Clin. Rheumatol. 2017, 36, 2697–2707. [Google Scholar] [CrossRef] [PubMed]
- de Oliveira, G.L.V.; Leite, A.Z.; Higuchi, B.S.; Gonzaga, M.I.; Mariano, V.S. Intestinal dysbiosis and probiotic applications in autoimmune diseases. Immunology 2017, 152, 1–12. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Eerola, E.; Mottonen, T.; Hannonen, P.; Luukkainen, R.; Kantola, I.; Vuori, K.; Tuominen, J.; Toivanen, P. Intestinal flora in early rheumatoid arthritis. Br. J Rheumatol. 1994, 33, 1030–1038. [Google Scholar] [CrossRef] [PubMed]
- Brusca, S.B.; Abramson, S.B.; Scher, J.U. Microbiome and mucosal inflammation as extra-articular triggers for rheumatoid arthritis and autoimmunity. Curr. Opin. Rheumatol. 2014, 26, 101–107. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dorozynska, I.; Majewska-Szczepanik, M.; Marcinska, K.; Szczepanik, M. Partial depletion of natural gut flora by antibiotic aggravates collagen induced arthritis (CIA) in mice. Pharmacol. Rep. 2014, 66, 250–255. [Google Scholar] [CrossRef] [PubMed]
- Hatakka, K.; Martio, J.; Korpela, M.; Herranen, M.; Poussa, T.; Laasanen, T.; Saxelin, M.; Vapaatalo, H.; Moilanen, E.; Korpela, R. Effects of probiotic therapy on the activity and activation of mild rheumatoid arthritis—A pilot study. Scand. J. Rheumatol. 2003, 32, 211–215. [Google Scholar] [CrossRef] [PubMed]
- Zamani, B.; Golkar, H.R.; Farshbaf, S.; Emadi-Baygi, M.; Tajabadi-Ebrahimi, M.; Jafari, P.; Akhavan, R.; Taghizadeh, M.; Memarzadeh, M.R.; Asemi, Z. Clinical and metabolic response to probiotic supplementation in patients with rheumatoid arthritis: A randomized, double-blind, placebo-controlled trial. Int. J. Rheum. Dis. 2016, 19, 869–879. [Google Scholar] [CrossRef] [PubMed]
- Chen, J.; Wright, K.; Davis, J.M.; Jeraldo, P.; Marietta, E.V.; Murray, J.; Nelson, H.; Matteson, E.L.; Taneja, V. An expansion of rare lineage intestinal microbes characterizes rheumatoid arthritis. Genome Med. 2016, 8, 43–57. [Google Scholar] [CrossRef] [PubMed]
- Alipour, B.; Homayouni-Rad, A.; Vaghef-Mehrabany, E.; Sharif, S.K.; Vaghef-Mehrabany, L.; Asghari-Jafarabadi, M.; Nakhjavani, M.R.; Mohtadi-Nia, J. Effects of Lactobacillus casei supplementation on disease activity and inflammatory cytokines in rheumatoid arthritis patients: A randomized double-blind clinical trial. Int. J. Rheum. Dis. 2014, 17, 519–527. [Google Scholar] [PubMed]
- Liu, X.; Zou, Q.; Zeng, B.; Fang, Y.; Wei, H. Analysis of fecal Lactobacillus community structure in patients with early rheumatoid arthritis. Curr. Microbiol. 2013, 67, 170–176. [Google Scholar] [CrossRef] [PubMed]
- Rahman, A.; Isenberg, D.A. Systemic lupus erythematosus. N. Engl. J. Med. 2008, 358, 929–939. [Google Scholar] [CrossRef] [PubMed]
- Stevens, K.M. The Aetiology of Systemic Lupus Erythematosus. Lancet 1964, 2, 506–508. [Google Scholar] [CrossRef]
- Lopez, P.; de, P.B.; Rodriguez-Carrio, J.; Hevia, A.; Sanchez, B.; Margolles, A.; Suarez, A. Th17 responses and natural IgM antibodies are related to gut microbiota composition in systemic lupus erythematosus patients. Sci. Rep. 2016, 6, 24072. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Esmaeili, S.A.; Mahmoudi, M.; Momtazi, A.A.; Sahebkar, A.; Doulabi, H.; Rastin, M. Tolerogenic probiotics: Potential immunoregulators in Systemic Lupus Erythematosus. J. Cell. Physiol. 2017, 232, 1994–2007. [Google Scholar] [CrossRef] [PubMed]
- Mu, Q.; Zhang, H.; Liao, X.; Lin, K.; Liu, H.; Edwards, M.R.; Ahmed, S.A.; Yuan, R.; Li, L.; Cecere, T.E.; et al. Control of lupus nephritis by changes of gut microbiota. Microbiome 2017, 5, 73. [Google Scholar] [CrossRef] [PubMed]
- Tzang, B.S.; Liu, C.H.; Hsu, K.C.; Chen, Y.H.; Huang, C.Y.; Hsu, T.C. Effects of oral Lactobacillus administration on antioxidant activities and CD4+CD25+forkhead box P3 (FoxP3)+ T cells in NZB/W F1 mice. Br. J. Nutr. 2017, 118, 333–342. [Google Scholar] [CrossRef] [PubMed]
- Esmaeili, S.A.; Mahmoudi, M.; Rezaieyazdi, Z.; Sahebari, M.; Tabasi, N.; Sahebkar, A.; Rastin, M. Generation of tolerogenic dendritic cells using Lactobacillus rhamnosus and Lactobacillus delbrueckii as tolerogenic probiotics. J. Cell. Biochem. 2018, 119, 7865–7872. [Google Scholar] [CrossRef] [PubMed]
- Frech, T.M.; Khanna, D.; Maranian, P.; Frech, E.J.; Sawitzke, A.D.; Murtaugh, M.A. Probiotics for the treatment of systemic sclerosis-associated gastrointestinal bloating/ distention. Clin. Exp. Rheumatol. 2011, 29, S22–S25. [Google Scholar] [PubMed]
- Rohr, M.; Narasimhulu, C.A.; Sharma, D.; Doomra, M.; Riad, A.; Naser, S.; Parthasarathy, S. Inflammatory Diseases of the Gut. J. Med. Food 2018, 21, 113–126. [Google Scholar] [CrossRef] [PubMed]
- Shen, J.; Zuo, Z.X.; Mao, A.P. Effect of probiotics on inducing remission and maintaining therapy in ulcerative colitis, Crohn’s disease, and pouchitis: Meta-analysis of randomized controlled trials. Inflamm. Bowel. Dis. 2014, 20, 21–35. [Google Scholar] [CrossRef] [PubMed]
- Derwa, Y.; Gracie, D.J.; Hamlin, P.J.; Ford, A.C. Systematic review with meta-analysis: The efficacy of probiotics in inflammatory bowel disease. Aliment. Pharmacol. Ther. 2017, 46, 389–400. [Google Scholar] [CrossRef] [PubMed]
- Shen, Z.H.; Zhu, C.X.; Quan, Y.S.; Yang, Z.Y.; Wu, S.; Luo, W.W.; Tan, B.; Wang, X.Y. Relationship between intestinal microbiota and ulcerative colitis: Mechanisms and clinical application of probiotics and fecal microbiota transplantation. World J. Gastroenterol. 2018, 24, 5–14. [Google Scholar] [CrossRef] [PubMed]
- Ganji-Arjenaki, M.; Rafieian-Kopaei, M. Probiotics are a good choice in remission of inflammatory bowel diseases: A meta analysis and systematic review. J. Cell. Physiol. 2018, 233, 2091–2103. [Google Scholar] [CrossRef] [PubMed]
- Goverman, J. Autoimmune T cell responses in the central nervous system. Nat. Rev. Immunol. 2009, 9, 393–407. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nylander, A.; Hafler, D.A. Multiple sclerosis. J. Clin. Investig. 2012, 122, 1180–1188. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- McFarland, H.F.; Martin, R. Multiple sclerosis: A complicated picture of autoimmunity. Nat. Immunol. 2007, 8, 913–919. [Google Scholar] [CrossRef] [PubMed]
- Berer, K.; Mues, M.; Koutrolos, M.; Rasbi, Z.A.; Boziki, M.; Johner, C.; Wekerle, H.; Krishnamoorthy, G. Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination. Nature 2011, 479, 538–541. [Google Scholar] [CrossRef] [PubMed]
- Chen, J.; Chia, N.; Kalari, K.R.; Yao, J.Z.; Novotna, M.; Soldan, M.M.; Luckey, D.H.; Marietta, E.V.; Jeraldo, P.R.; Chen, X.; et al. Multiple sclerosis patients have a distinct gut microbiota compared to healthy controls. Sci. Rep. 2016, 6, 28484. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jangi, S.; Gandhi, R.; Cox, L.M.; Li, N.; von, G.F.; Yan, R.; Patel, B.; Mazzola, M.A.; Liu, S.; Glanz, B.L.; et al. Alterations of the human gut microbiome in multiple sclerosis. Nat. Commun. 2016, 7, 12015. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Newland, P.K.; Heitkemper, M.; Zhou, Y. The Emerging Role of the Gut Microbiome in Adult Patients with Multiple Sclerosis. J. Neurosci. Nurs. 2016, 48, 358–364. [Google Scholar] [CrossRef] [PubMed]
- Ochoa-Reparaz, J.; Mielcarz, D.W.; Ditrio, L.E.; Burroughs, A.R.; Foureau, D.M.; Haque-Begum, S.; Kasper, L.H. Role of gut commensal microflora in the development of experimental autoimmune encephalomyelitis. J. Immunol. 2009, 183, 6041–6050. [Google Scholar] [CrossRef] [PubMed]
- Yokote, H.; Miyake, S.; Croxford, J.L.; Oki, S.; Mizusawa, H.; Yamamura, T. NKT cell-dependent amelioration of a mouse model of multiple sclerosis by altering gut flora. Am. J. Pathol. 2008, 173, 1714–1723. [Google Scholar] [CrossRef] [PubMed]
- He, B.; Hoang, T.K.; Tian, X.; Taylor, C.M.; Blanchard, E.; Luo, M.; Bhattacharjee, M.B.; Lindsey, J.M.; Tran, D.Q.; J Marc Rhoads, J.M.; et al. Lactobacillus reuteri reduces the severity of experimental autoimmune encephalomyelitis in mice by modulating gut microbiota. Front Immunol. 2018. under review. [Google Scholar]
- Kouchaki, E.; Tamtaji, O.R.; Salami, M.; Bahmani, F.; Daneshvar, K.R.; Akbari, E.; Tajabadi-Ebrahimi, M.; Jafari, P.; Asemi, Z. Clinical and metabolic response to probiotic supplementation in patients with multiple sclerosis: A randomized, double-blind, placebo-controlled trial. Clin. Nutr. 2017, 36, 1245–1249. [Google Scholar] [CrossRef] [PubMed]
- Pessione, E. Lactic acid bacteria contribution to gut microbiota complexity: Lights and shadows. Front. Cell. Infect. Microbiol. 2012, 2, 86. [Google Scholar] [CrossRef] [PubMed]
- Louis, P.; Flint, H.J. Formation of propionate and butyrate by the human colonic microbiota. Environ. Microbiol. 2017, 19, 29–41. [Google Scholar] [CrossRef] [PubMed]
- Macfarlane, S.; Macfarlane, G.T. Regulation of short-chain fatty acid production. Proc. Nutr. Soc. 2003, 62, 67–72. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sivieri, K.; Morales, M.L.; Adorno, M.A.; Sakamoto, I.K.; Saad, S.M.; Rossi, E.A. Lactobacillus acidophilus CRL 1014 improved "gut health" in the SHIME reactor. BMC Gastroenterol. 2013, 13, 100. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- LeBlanc, J.G.; Chain, F.; Martin, R.; Bermudez-Humaran, L.G.; Courau, S.; Langella, P. Beneficial effects on host energy metabolism of short-chain fatty acids and vitamins produced by commensal and probiotic bacteria. Microb. Cell Fact. 2017, 16, 79. [Google Scholar] [CrossRef] [PubMed]
- Canani, R.B.; Costanzo, M.D.; Leone, L.; Pedata, M.; Meli, R.; Calignano, A. Potential beneficial effects of butyrate in intestinal and extraintestinal diseases. World J Gastroenterol. 2011, 17, 1519–1528. [Google Scholar] [CrossRef] [PubMed]
- Keku, T.O.; Dulal, S.; Deveaux, A.; Jovov, B.; Han, X. The gastrointestinal microbiota and colorectal cancer. Am. J. Physiol. Gastrointest. Liver Physiol. 2015, 308, G351–G363. [Google Scholar] [CrossRef] [PubMed]
- Dass, N.B.; John, A.K.; Bassil, A.K.; Crumbley, C.W.; Shehee, W.R.; Maurio, F.P.; Moore, G.B.; Taylor, C.M.; Sanger, G.J. The relationship between the effects of short-chain fatty acids on intestinal motility in vitro and GPR43 receptor activation. Neurogastroenterol. Motil. 2007, 19, 66–74. [Google Scholar] [CrossRef] [PubMed]
- Kuwahara, A. Contributions of colonic short-chain Fatty Acid receptors in energy homeostasis. Front. Endocrinol. (Lausanne) 2014, 5, 144. [Google Scholar] [CrossRef] [PubMed]
- Vinolo, M.A.; Rodrigues, H.G.; Hatanaka, E.; Sato, F.T.; Sampaio, S.C.; Curi, R. Suppressive effect of short-chain fatty acids on production of proinflammatory mediators by neutrophils. J. Nutr. Biochem. 2011, 22, 849–855. [Google Scholar] [CrossRef] [PubMed]
- Park, J.S.; Lee, E.J.; Lee, J.C.; Kim, W.K.; Kim, H.S. Anti-inflammatory effects of short chain fatty acids in IFN-gamma-stimulated RAW 264.7 murine macrophage cells: Involvement of NF-kappaB and ERK signaling pathways. Int. Immunopharmacol. 2007, 7, 70–77. [Google Scholar] [CrossRef] [PubMed]
- Kespohl, M.; Vachharajani, N.; Luu, M.; Harb, H.; Pautz, S.; Wolff, S.; Sillner, N.; Walker, A.; Schmitt-Kopplin, P.; Boettger, T.; et al. The Microbial Metabolite Butyrate Induces Expression of Th1-Associated Factors in CD4(+) T Cells. Front Immunol. 2017, 8, 1036. [Google Scholar] [CrossRef] [PubMed]
- Bianchetti, D.G.A.M.; Amelio, G.S.; Lava, S.A.G.; Bianchetti, M.G.; Simonetti, G.D.; Agostoni, C.; Fossali, E.F.; Milani, G.P. D-lactic acidosis in humans: Systematic literature review. Pediatr. Nephrol. 2018, 33, 673–681. [Google Scholar] [CrossRef] [PubMed]
- Cahova, M.; Bratova, M.; Wohl, P. Parenteral Nutrition-Associated Liver Disease: The Role of the Gut Microbiota. Nutrients 2017, 9, 987. [Google Scholar] [CrossRef] [PubMed]
- Mayeur, C.; Gratadoux, J.J.; Bridonneau, C.; Chegdani, F.; Larroque, B.; Kapel, N.; Corcos, O.; Thomas, M.; Joly, F. Faecal D/L lactate ratio is a metabolic signature of microbiota imbalance in patients with short bowel syndrome. PLoS ONE 2013, 8, e54335. [Google Scholar] [CrossRef] [PubMed]
- Hubbard, T.D.; Murray, I.A.; Bisson, W.H.; Lahoti, T.S.; Gowda, K.; Amin, S.G.; Patterson, A.D.; Perdew, G.H. Adaptation of the human aryl hydrocarbon receptor to sense microbiota-derived indoles. Sci. Rep. 2015, 5, 12689. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gao, J.; Xu, K.; Liu, H.; Liu, G.; Bai, M.; Peng, C.; Li, T.; Yin, Y. Impact of the Gut Microbiota on Intestinal Immunity Mediated by Tryptophan Metabolism. Front. Cell. Infect. Microbiol. 2018, 8, 13. [Google Scholar] [CrossRef] [PubMed]
- Korecka, A.; Dona, A.; Lahiri, S.; Tett, A.J.; Al-Asmakh, M.; Braniste, V.; D’Arienzo, R.; Abbaspour, A.; Reichardt, N.; Fujii-Kuriyama, Y.; et al. Bidirectional communication between the Aryl hydrocarbon Receptor (AhR) and the microbiome tunes host metabolism. NPJ Biofilms Microbiomes 2016, 2, 16014. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Benson, J.M.; Shepherd, D.M. Aryl hydrocarbon receptor activation by TCDD reduces inflammation associated with Crohn’s disease. Toxicol. Sci. 2011, 120, 68–78. [Google Scholar] [CrossRef] [PubMed]
- Sutter, C.H.; Bodreddigari, S.; Campion, C.; Wible, R.S.; Sutter, T.R. 2,3,7,8-Tetrachlorodibenzo-p-dioxin increases the expression of genes in the human epidermal differentiation complex and accelerates epidermal barrier formation. Toxicol. Sci. 2011, 124, 128–137. [Google Scholar] [CrossRef] [PubMed]
- Shi, L.Z.; Faith, N.G.; Nakayama, Y.; Suresh, M.; Steinberg, H.; Czuprynski, C.J. The aryl hydrocarbon receptor is required for optimal resistance to Listeria monocytogenes infection in mice. J. Immunol. 2007, 179, 6952–6962. [Google Scholar] [CrossRef] [PubMed]
- Behnsen, J.; Jellbauer, S.; Wong, C.P.; Edwards, R.A.; George, M.D.; Ouyang, W.; Raffatellu, M. The cytokine IL-22 promotes pathogen colonization by suppressing related commensal bacteria. Immunity 2014, 40, 262–273. [Google Scholar] [CrossRef] [PubMed]
- Venkatesh, M.; Mukherjee, S.; Wang, H.; Li, H.; Sun, K.; Benechet, A.P.; Qiu, Z.; Maher, L.; Redinbo, M.R.; Phillips, R.S.; et al. Symbiotic bacterial metabolites regulate gastrointestinal barrier function via the xenobiotic sensor PXR and Toll-like receptor 4. Immunity 2014, 41, 296–310. [Google Scholar] [CrossRef] [PubMed]
- Desbonnet, L.; Garrett, L.; Clarke, G.; Bienenstock, J.; Dinan, T.G. The probiotic Bifidobacteria infantis: An assessment of potential antidepressant properties in the rat. J. Psychiatr. Res. 2008, 43, 164–174. [Google Scholar] [CrossRef] [PubMed]
- Zelante, T.; Iannitti, R.G.; Cunha, C.; De, L.A.; Giovannini, G.; Pieraccini, G.; Zecchi, R.; D’Angelo, C.; Massi-Benedetti, C.; Fallarino, F.; et al. Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22. Immunity 2013, 39, 372–385. [Google Scholar] [CrossRef] [PubMed]
- Heldin, C.H.; Moustakas, A. Role of Smads in TGFbeta signaling. Cell Tissue Res. 2012, 347, 21–36. [Google Scholar] [CrossRef] [PubMed]
- Tran, D.Q. TGF-beta: The sword, the wand, and the shield of FOXP3(+) regulatory T cells. J. Mol. Cell Biol. 2012, 4, 29–37. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.; Tran, D.Q.; Fatheree, N.Y.; Marc, R.J. Lactobacillus reuteri DSM 17938 differentially modulates effector memory T cells and Foxp3+ regulatory T cells in a mouse model of necrotizing enterocolitis. Am. J. Physiol. Gastrointest. Liver Physiol. 2014, 307, G177–G186. [Google Scholar] [CrossRef] [PubMed]
- Sakai, F.; Hosoya, T.; Ono-Ohmachi, A.; Ukibe, K.; Ogawa, A.; Moriya, T.; Kadooka, Y.; Shiozaki, T.; Nakagawa, H.; Nakayama, Y.; et al. Lactobacillus gasseri SBT2055 induces TGF-beta expression in dendritic cells and activates TLR2 signal to produce IgA in the small intestine. PLoS ONE 2014, 9, e105370. [Google Scholar] [CrossRef] [PubMed]
- Barletta, B.; Rossi, G.; Schiavi, E.; Butteroni, C.; Corinti, S.; Boirivant, M.; Di, F.G. Probiotic VSL#3-induced TGF-beta ameliorates food allergy inflammation in a mouse model of peanut sensitization through the induction of regulatory T cells in the gut mucosa. Mol. Nutr. Food Res. 2013, 57, 2233–2244. [Google Scholar] [PubMed]
- Fujii, T.; Ohtsuka, Y.; Lee, T.; Kudo, T.; Shoji, H.; Sato, H.; Nagata, S.; Shimizu, T.; Yamashiro, Y. Bifidobacterium breve enhances transforming growth factor beta1 signaling by regulating Smad7 expression in preterm infants. J. Pediatr. Gastroenterol. Nutr. 2006, 43, 83–88. [Google Scholar] [CrossRef] [PubMed]
- Huang, I.F.; Lin, I.C.; Liu, P.F.; Cheng, M.F.; Liu, Y.C.; Hsieh, Y.D.; Chen, J.J.; Chen, C.L.; Chang, H.W.; Shu, C.W. Lactobacillus acidophilus attenuates Salmonella-induced intestinal inflammation via TGF-beta signaling. BMC Microbiol. 2015, 15, 203. [Google Scholar] [CrossRef] [PubMed]
- He, B.; Hoang, T.K.; Wang, T.; Ferris, M.; Taylor, C.M.; Tian, X.; Luo, M.; Tran, D.Q.; Zhou, J.; Tatevian, N.; et al. Resetting microbiota by Lactobacillus reuteri inhibits T reg deficiency-induced autoimmunity via adenosine A2A receptors. J. Exp. Med. 2017, 214, 107–123. [Google Scholar] [CrossRef] [PubMed]
- He, B.; Hoang, T.K.; Tran, D.Q.; Rhoads, J.M.; Liu, Y. Adenosine A2A Receptor Deletion Blocks the Beneficial Effects of Lactobacillus reuteri in Regulatory T-Deficient Scurfy Mice. Front. Immunol. 2017, 8, 1680. [Google Scholar] [CrossRef] [PubMed]
- Hannibal, M.C.; Torgerson, T. IPEX Syndrome. Available online: http://www.ncbi.nlm.nih.gov/books/NBK1118/ (accessed on 12 October 2018).
- Frei, R.; Ferstl, R.; Konieczna, P.; Ziegler, M.; Simon, T.; Rugeles, T.M.; Mailand, S.; Watanabe, T.; Lauener, R.; Akdis, C.A.; et al. Histamine receptor 2 modifies dendritic cell responses to microbial ligands. J. Allergy Clin. Immunol. 2013, 132, 194–204. [Google Scholar] [CrossRef] [PubMed]
- Ganesh, B.P.; Hall, A.; Ayyaswamy, S.; Nelson, J.W.; Fultz, R.; Major, A.; Haag, A.; Esparza, M.; Lugo, M.; Venable, S.; et al. Diacylglycerol kinase synthesized by commensal Lactobacillus reuteri diminishes protein kinase C phosphorylation and histamine-mediated signaling in the mammalian intestinal epithelium. Mucosal. Immunol. 2018, 11, 380. [Google Scholar] [CrossRef] [PubMed]
- Ferstl, R.; Frei, R.; Schiavi, E.; Konieczna, P.; Barcik, W.; Ziegler, M.; Lauener, R.P.; Chassard, C.; Lacroix, C.; Akdis, C.A.; et al. Histamine receptor 2 is a key influence in immune responses to intestinal histamine-secreting microbes. J. Allergy Clin. Immunol. 2014, 134, 744–746. [Google Scholar] [CrossRef] [PubMed]
- Thomas, C.M.; Hong, T.; van Pijkeren, J.P.; Hemarajata, P.; Trinh, D.V.; Hu, W.; Britton, R.A.; Kalkum, M.; Versalovic, J. Histamine derived from probiotic Lactobacillus reuteri suppresses TNF via modulation of PKA and ERK signaling. PLoS ONE 2012, 7, e31951. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gao, C.; Major, A.; Rendon, D.; Lugo, M.; Jackson, V.; Shi, Z.; Mori-Akiyama, Y.; Versalovic, J. Histamine H2 Receptor-Mediated Suppression of Intestinal Inflammation by Probiotic Lactobacillus reuteri. MBio. 2015, 6, e01358–e01415. [Google Scholar] [CrossRef] [PubMed]
- Gao, C.; Ganesh, B.P.; Shi, Z.; Shah, R.R.; Fultz, R.; Major, A.; Venable, S.; Lugo, M.; Hoch, K.; Chen, X.; et al. Gut Microbe-Mediated Suppression of Inflammation-Associated Colon Carcinogenesis by Luminal Histamine Production. Am. J. Pathol. 2017, 187, 2323–2336. [Google Scholar] [CrossRef] [PubMed]
- NIH/National Center for Complementary and Integrative Health. Probiotics: In Depth. Available online: http://nccih.nih.gov/health/probiotics/introduction.htm (accessed on 10 September 2018).
- CDC/Centers for Disease Control and Prevention. Fatal Gastrointestinal Mucormycosis in an Infant Following Use of Contaminated ABC Dophilus Powder from Solgar Inc. Available online: http://www.cdc.gov/fungal/outbreaks/rhizopus-investigation.html (accessed on 10 September 2018).
- Sun, J.; Marwah, G.; Westgarth, M.; Buys, N.; Ellwood, D.; Gray, P.H. Effects of Probiotics on Necrotizing Enterocolitis, Sepsis, Intraventricular Hemorrhage, Mortality, Length of Hospital Stay, and Weight Gain in Very Preterm Infants: A Meta-Analysis. Adv. Nutr. 2017, 8, 749–763. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, G.Q.; Hu, H.J.; Liu, C.Y.; Shakya, S.; Li, Z.Y. Probiotics for Preventing Late-Onset Sepsis in Preterm Neonates: A PRISMA-Compliant Systematic Review and Meta-Analysis of Randomized Controlled Trials. Medicine (Baltimore) 2016, 95, e2581. [Google Scholar] [CrossRef] [PubMed]
- Arumugam, S.; Lau, C.S.; Chamberlain, R.S. Probiotics and Synbiotics Decrease Postoperative Sepsis in Elective Gastrointestinal Surgical Patients: A Meta-Analysis. J. Gastrointest. Surg. 2016, 20, 1123–1131. [Google Scholar] [CrossRef] [PubMed]
- Sender, R.; Fuchs, S.; Milo, R. Revised Estimates for the Number of Human and Bacteria Cells in the Body. PLoS Biol. 2016, 14, e1002533. [Google Scholar] [CrossRef] [PubMed]
- Lim, J.Y.; Yoon, J.; Hovde, C.J. A brief overview of Escherichia coli O157:H7 and its plasmid O157. J. Microbiol. Biotechnol. 2010, 20, 5–14. [Google Scholar] [PubMed]
- Larsen, C.N.; Nielsen, S.; Kaestel, P.; Brockmann, E.; Bennedsen, M.; Christensen, H.R.; Eskesen, D.C.; Jacobsen, B.L.; Michaelsen, K.F. Dose-response study of probiotic bacteria Bifidobacterium animalis subsp lactis BB-12 and Lactobacillus paracasei subsp paracasei CRL-341 in healthy young adults. Eur. J. Clin. Nutr. 2006, 60, 1284–1293. [Google Scholar] [CrossRef] [PubMed]
- Dommels, Y.E.; Kemperman, R.A.; Zebregs, Y.E.; Draaisma, R.B.; Jol, A.; Wolvers, D.A.; Vaughan, E.E.; Albers, R. Survival of Lactobacillus reuteri DSM 17938 and Lactobacillus rhamnosus GG in the human gastrointestinal tract with daily consumption of a low-fat probiotic spread. Appl. Environ. Microbiol. 2009, 75, 6198–6204. [Google Scholar] [CrossRef] [PubMed]
- Songisepp, E.; Kals, J.; Kullisaar, T.; Mandar, R.; Hutt, P.; Zilmer, M.; Mikelsaar, M. Evaluation of the functional efficacy of an antioxidative probiotic in healthy volunteers. Nutr. J. 2005, 4, 22. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fatheree, N.Y.; Liu, Y.; Ferris, M.; Van, A.M.; McMurtry, V.; Zozaya, M.; Cai, C.; Rahbar, M.H.; Hessabi, M.; Vu, T.; et al. Hypoallergenic formula with Lactobacillus rhamnosus GG for babies with colic: A pilot study of recruitment, retention, and fecal biomarkers. World J. Gastrointest. Pathophysiol. 2016, 7, 160–170. [Google Scholar] [CrossRef] [PubMed]
- Mangalat, N.; Liu, Y.; Fatheree, N.Y.; Ferris, M.J.; Van Arsdall, M.R.; Chen, Z.; Rahbar, M.H.; Gleason, W.A.; Norori, J.; Tran, D.Q.; et al. Safety and tolerability of Lactobacillus reuteri DSM 17938 and effects on biomarkers in healthy adults: Results from a randomized masked trial. PLoS ONE 2012, 7, e43910. [Google Scholar] [CrossRef] [PubMed]
- Schouten, J.N.; Van der Ende, M.E.; Koeter, T.; Rossing, H.H.; Komuta, M.; Verheij, J.; van der Valk, M.; Hansen, B.E.; Janssen, H.L. Risk factors and outcome of HIV-associated idiopathic noncirrhotic portal hypertension. Aliment. Pharmacol. Ther. 2012, 36, 875–885. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fatheree, N.Y.; Liu, Y.; Taylor, C.M.; Hoang, T.K.; Cai, C.; Rahbar, M.H.; Hessabi, M.; Ferris, M.; McMurtry, V.; Wong, C.; et al. Lactobacillus reuteri for Infants with Colic: A Double-Blind, Placebo-Controlled, Randomized Clinical Trial. J. Pediatr. 2017, 191, 170–178. [Google Scholar] [CrossRef] [PubMed]
- Sedgwick, P.; Marston, L. How to read a funnel plot in a meta-analysis. BMJ 2015, 351, h4718. [Google Scholar] [CrossRef] [PubMed]
- Athalye-Jape, G.; Rao, S.; Patole, S. Effects of probiotics on experimental necrotizing enterocolitis: A systematic review and meta-analysis. Pediatr. Res. 2018, 83, 16–22. [Google Scholar] [CrossRef] [PubMed]
- Moayyedi, P.; Ford, A.C.; Talley, N.J.; Cremonini, F.; Foxx-Orenstein, A.E.; Brandt, L.J.; Quigley, E.M. The efficacy of probiotics in the treatment of irritable bowel syndrome: A systematic review. Gut 2010, 59, 325–332. [Google Scholar] [CrossRef] [PubMed]
- Si, X.B.; Lan, Y.; Qiao, L. A meta-analysis of randomized controlled trials of bismuth-containing quadruple therapy combined with probiotic supplement for eradication of Helicobacter pylori. Zhonghua Nei Ke Za Zhi 2017, 56, 752–759. (In Chinese) [Google Scholar] [PubMed]
- Gutierrez-Castrellon, P.; Indrio, F.; Bolio-Galvis, A.; Jimenez-Gutierrez, C.; Jimenez-Escobar, I.; Lopez-Velazquez, G. Efficacy of Lactobacillus reuteri DSM 17938 for infantile colic: Systematic review with network meta-analysis. Medicine (Baltimore) 2017, 96, e9375. [Google Scholar] [CrossRef] [PubMed]
- Salari, P.; Nikfar, S.; Abdollahi, M. A meta-analysis and systematic review on the effect of probiotics in acute diarrhea. Inflamm. Allergy Drug Targets 2012, 11, 3–14. [Google Scholar] [CrossRef] [PubMed]
- Ladas, E.J.; Bhatia, M.; Chen, L.; Sandler, E.; Petrovic, A.; Berman, D.M.; Hamblin, F.; Gates, M.; Hawks, R.; Sung, L.; et al. The safety and feasibility of probiotics in children and adolescents undergoing hematopoietic cell transplantation. Bone Marrow Transplant. 2016, 51, 262–266. [Google Scholar] [CrossRef] [PubMed]
- Liu, Z.H.; Huang, M.J.; Zhang, X.W.; Wang, L.; Huang, N.Q.; Peng, H.; Lan, P.; Peng, J.S.; Yang, Z.; Xia, Y.; et al. The effects of perioperative probiotic treatment on serum zonulin concentration and subsequent postoperative infectious complications after colorectal cancer surgery: A double-center and double-blind randomized clinical trial. Am. J. Clin. Nutr. 2013, 97, 117–126. [Google Scholar] [CrossRef] [PubMed]
- Stiksrud, B.; Nowak, P.; Nwosu, F.C.; Kvale, D.; Thalme, A.; Sonnerborg, A.; Ueland, P.M.; Holm, K.; Birkeland, S.E.; Dahm, A.E.; et al. Reduced Levels of D-dimer and Changes in Gut Microbiota Composition After Probiotic Intervention in HIV-Infected Individuals on Stable ART. J. Acquir. Immune. Defic. Syndr. 2015, 70, 329–337. [Google Scholar] [CrossRef] [PubMed]
- Tan, C.K.; Said, S.; Rajandram, R.; Wang, Z.; Roslani, A.C.; Chin, K.F. Pre-surgical Administration of Microbial Cell Preparation in Colorectal Cancer Patients: A Randomized Controlled Trial. World J. Surg. 2016, 40, 1985–1992. [Google Scholar] [CrossRef] [PubMed]
- Van den Nieuwboer, M.; Brummer, R.J.; Guarner, F.; Morelli, L.; Cabana, M.; Claasen, E. The administration of probiotics and synbiotics in immune compromised adults: Is it safe? Benef. Microbes 2015, 6, 3–17. [Google Scholar] [CrossRef] [PubMed]
- Guarino, A.; Lo, V.A.; Dias, J.A.; Berkley, J.A.; Boey, C.; Bruzzese, D.; Cohen, M.B.; Cruchet, S.; Liguoro, I.; Salazar-Lindo, E.; et al. Universal recommendations for the management of acute diarrhea in non-malnourished children. J. Pediatr. Gastroenterol. Nutr. 2018. [Google Scholar] [CrossRef] [PubMed]
- Parker, M.W.; Schaffzin, J.K.; Lo, V.A.; Yau, C.; Vonderhaar, K.; Guiot, A.; Brinkman, W.B.; White, C.M.; Simmons, J.M.; Gerhardt, W.E.; et al. Rapid adoption of Lactobacillus rhamnosus GG for acute gastroenteritis. Pediatrics 2013, 131, S96–S102. [Google Scholar] [CrossRef] [PubMed]
- Yi, S.H.; Jernigan, J.A.; McDonald, L.C. Prevalence of probiotic use among inpatients: A descriptive study of 145 U.S. hospitals. Am. J. Infect. Control 2016, 44, 548–553. [Google Scholar] [CrossRef] [PubMed]
- Sleator, R.D. Designer probiotics: Development and applications in gastrointestinal health. World J. Gastrointest. Pathophysiol. 2015, 6, 73–78. [Google Scholar] [CrossRef] [PubMed]
- Olson, J.K.; Navarro, J.B.; Allen, J.M.; McCulloh, C.J.; Mashburn-Warren, L.; Wang, Y.; Varaljay, V.A.; Bailey, M.T.; Goodman, S.D.; Besner, G.E. An enhanced Lactobacillus reuteri biofilm formulation that increases protection against experimental necrotizing enterocolitis. Am. J. Physiol. Gastrointest. Liver Physiol. 2018, 315, G408–G419. [Google Scholar] [CrossRef] [PubMed]
© 2018 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Liu, Y.; Alookaran, J.J.; Rhoads, J.M. Probiotics in Autoimmune and Inflammatory Disorders. Nutrients 2018, 10, 1537. https://doi.org/10.3390/nu10101537
Liu Y, Alookaran JJ, Rhoads JM. Probiotics in Autoimmune and Inflammatory Disorders. Nutrients. 2018; 10(10):1537. https://doi.org/10.3390/nu10101537
Chicago/Turabian StyleLiu, Yuying, Jane J. Alookaran, and J. Marc Rhoads. 2018. "Probiotics in Autoimmune and Inflammatory Disorders" Nutrients 10, no. 10: 1537. https://doi.org/10.3390/nu10101537
APA StyleLiu, Y., Alookaran, J. J., & Rhoads, J. M. (2018). Probiotics in Autoimmune and Inflammatory Disorders. Nutrients, 10(10), 1537. https://doi.org/10.3390/nu10101537