Effects of a Postbiotic and Prebiotic Mixture on Suckling Rats’ Microbiota and Immunity
Abstract
:1. Introduction
2. Materials and Methods
2.1. Animals
2.2. Experimental Design and Sample Collection
2.3. pH of Stools and Stomach Content
2.4. Quantification of Immunoglobulins
2.5. Gene Expression Analysis
2.6. Microbiota Composition
2.7. Quantification of Short-Chain Fatty Acids in the Cecal Content
2.8. Statistical Analysis
3. Results
3.1. Growth and Morphometry
3.2. Fecal and Stomach Content Variables
3.3. Immunoglobulins in Plasma
3.4. Gene Expression
3.5. Microbiota
3.6. Cecal SCFA Production
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Acknowledgments
Conflicts of Interest
References
- Ballard, O.; Morrow, A.L. Human milk composition: Nutrients and bioactive factors. Pediatr. Clin. N. Am. 2013, 60, 49–74. [Google Scholar] [CrossRef] [Green Version]
- Salminen, S.; Stahl, B.; Vinderola, G.; Szajewska, H. Infant formula supplemented with biotics: Current knowledge and future perspectives. Nutrients 2020, 12, 1952. [Google Scholar] [CrossRef] [PubMed]
- Martin, C.R.; Ling, P.-R.; Blackburn, G.L. Review of infant feeding: Key features of breast milk and infant formula. Nutrients 2016, 8, 279. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Szajewska, H.; Skórka, A.; Pieścik-Lech, M. Fermented infant formulas without live bacteria: A systematic review. Eur. J. Nucl. Med. Mol. Imaging 2015, 174, 1413–1420. [Google Scholar] [CrossRef]
- Suárez, J.E. Microbiota autóctona, probióticos y prebióticos. Nutr. Hosp. 2015, 31, 3–9. [Google Scholar] [CrossRef]
- Gibson, G.R.; Hutkins, R.; Sanders, M.E.; Prescott, S.L.; Reimer, R.A.; Salminen, S.J.; Scott, K.; Stanton, C.; Swanson, K.S.; Cani, P.D.; et al. Expert consensus document: The international scientific association for probiotics and prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat. Rev. Gastroenterol. Hepatol. 2017, 14, 491–502. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Marques, T.M.; Wall, R.; Ross, R.; Fitzgerald, G.F.; Ryan, C.A.; Stanton, C. Programming infant gut microbiota: Influence of dietary and environmental factors. Curr. Opin. Biotechnol. 2010, 21, 149–156. [Google Scholar] [CrossRef] [PubMed]
- Veereman-Wauters, G.; Staelens, S.; Van de Broek, H.; Plaskie, K.; Wesling, F.; Roger, L.; McCartney, A.; Assam, P. Physiological and bifidogenic effects of prebiotic supplements in infant formulae. J. Pediatr. Gastroenterol. Nutr. 2011, 52, 763–771. [Google Scholar] [CrossRef]
- Moro, G.; Minoli, I.; Mosca, M.; Fanaro, S.; Jelinek, J.; Stahl, B.; Boehm, G. Dosage-related bifidogenic effects of galacto- and fructooligosaccharides in formula-fed term infants. J. Pediatr. Gastroenterol. Nutr. 2002, 34, 291–295. [Google Scholar] [CrossRef]
- Rigo-Adrover, M.; Saldaña-Ruíz, S.; Van Limpt, K.; Knipping, K.; Garssen, J.; Knol, J.; Franch, A.; Castell, M.; Pérez-Cano, F.J. A combination of scGOS/lcFOS with bifidobacterium breve M-16V protects suckling rats from rotavirus gastroenteritis. Eur. J. Nutr. 2016, 56, 1657–1670. [Google Scholar] [CrossRef]
- Arslanoglu, S.; Moro, G.E.; Schmitt, J.; Tandoi, L.; Rizzardi, S.; Boehm, G. Early dietary intervention with a mixture of prebiotic oligosaccharides reduces the incidence of allergic manifestations and infections during the first two years of life. J. Nutr. 2008, 138, 1091–1095. [Google Scholar] [CrossRef]
- Azagra-Boronat, I.; Massot-Cladera, M.; Knipping, K.; Land, B.V.; Stahl, B.; Garssen, J.; Rodríguez-Lagunas, M.J.; Franch, À.; Castell, M.; Pérez-Cano, F.J. Supplementation with 2′-FL and scGOS/lcFOS ameliorates rotavirus-induced diarrhea in suckling rats. Front. Cell. Infect. Microbiol. 2018, 8, 372. [Google Scholar] [CrossRef]
- Bruzzese, E.; Volpicelli, M.; Squeglia, V.; Bruzzese, D.; Salvini, F.; Bisceglia, M.; Lionetti, P.; Cinquetti, M.; Iacono, G.; Amarri, S.; et al. A formula containing galacto- and fructo-oligosaccharides prevents intestinal and extra-intestinal infections: An observational study. Clin. Nutr. 2009, 28, 156–161. [Google Scholar] [CrossRef] [Green Version]
- Grathwohl, D. Early supplementation of prebiotic oligosaccharides protects formula-fed infants against infections during the first six months of life. J. Nutr. 2008, 138, 1520. [Google Scholar] [CrossRef] [Green Version]
- Rigo-Adrover, M.; Perez-Berezo, T.; Ramos-Romero, S.; van Limpt, K.; Knipping, K.; Garssen, J.; Knol, J.; Franch, À.; Castell, M.; Pérez-Cano, F.J. A fermented milk concentrate and a combination of short-chain galacto-oligosaccharides/long-chain fructo-oligosaccharides/pectin-derived acidic oligosaccharides protect suckling rats from rotavirus gastroenteritis. Br. J. Nutr. 2017, 117, 209–217. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Osborn, D.A.; Shin, J.K.H. Prebiotics in infants for prevention of allergic disease and food allergy. Cochrane Database Syst. Rev. 2013. [Google Scholar] [CrossRef]
- Fernández, L.; Langa, S.; Martin, V.; Maldonado, A.; Jiménez, E.; Martín, R.; Rodríguez, J.M. The human milk microbiota: Origin and potential roles in health and disease. Pharmacol. Res. 2013, 69, 1–10. [Google Scholar] [CrossRef]
- Pineiro, M.; Stanton, C. Probiotic bacteria: Legislative framework—Requirements to evidence basis. J. Nutr. 2007, 137, 850S–853S. [Google Scholar] [CrossRef] [PubMed]
- FAO; WHO. Guidelines for the Evaluation of Probiotics in Food; WHO: Geneva, Switzerland, 2002; pp. 1–11. [Google Scholar]
- Soccol, C.R.; Vandenberghe, L.P.D.S.; Spier, M.R.; Medeiros, A.B.P.; Yamaguishi, C.T.; De Dea Lindner, J.; Pandey, A.; Thomaz-Soccol, V. The Potential of probiotics: A review. Food Technol. Biotechnol. 2010, 48, 413–434. [Google Scholar]
- Wegh, C.A.M.; Geerlings, S.Y.; Knol, J.; Roeselers, G.; Belzer, C. Postbiotics and their potential applications in early life nutrition and beyond. Int. J. Mol. Sci. 2019, 20, 4673. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vieira, A.T.; Fukumori, C.; Ferreira, C.M. New insights into therapeutic strategies for gut microbiota modulation in inflammatory diseases. Clin. Transl. Immunol. 2016, 5, e87. [Google Scholar] [CrossRef] [PubMed]
- Walsh, C.; Guinane, C.; O’Toole, P.; Cotter, P.D. Beneficial modulation of the gut microbiota. FEBS Lett. 2014, 588, 4120–4130. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xiang, Q.; Wu, X.; Pan, Y.; Wang, L.; Cui, C.; Guo, Y.; Zhu, L.; Peng, J.; Wei, H. Early-life intervention using fecal microbiota combined with probiotics promotes gut microbiota maturation, regulates immune system development, and alleviates weaning stress in piglets. Int. J. Mol. Sci. 2020, 21, 503. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Broom, L.J.; Kogut, M.H. The role of the gut microbiome in shaping the immune system of chickens. Veter- Immunol. Immunopathol. 2018, 204, 44–51. [Google Scholar] [CrossRef] [PubMed]
- Salminen, S.; Collado, M.C.; Endo, A.; Hill, C.; Lebeer, S.; Quigley, E.M.M.; Sanders, M.E.; Shamir, R.; Swann, J.R.; Szajewska, H.; et al. The international scientific association of probiotics and prebiotics (ISAPP) consensus statement on the definition and scope of postbiotics. Nat. Rev. Gastroenterol. Hepatol. 2021, 1–19. [Google Scholar] [CrossRef]
- Malagón-Rojas, J.N.; Mantziari, A.; Salminen, S.; Szajewska, H. Postbiotics for preventing and treating common infectious diseases in children: A systematic review. Nutrients 2020, 12, 389. [Google Scholar] [CrossRef] [Green Version]
- Chuah, L.-O.; Foo, H.L.; Loh, T.C.; Alitheen, N.B.M.; Yeap, S.K.; Mutalib, N.E.A.; Rahim, R.A.; Yusoff, K. Postbiotic metabolites produced by Lactobacillus plantarum strains exert selective cytotoxicity effects on cancer cells. BMC Complement. Altern. Med. 2019, 19, 1–12. [Google Scholar] [CrossRef] [Green Version]
- Kareem, K.Y.; Loh, T.C.; Foo, H.L.; Asmara, S.A.; Akit, H. Influence of postbiotic RG14 and inulin combination on cecal microbiota, organic acid concentration, and cytokine expression in broiler chickens. Poult. Sci. 2017, 96, 966–975. [Google Scholar] [CrossRef] [PubMed]
- De Almada, C.N.; Almada, C.N.; Martinez, R.C.R.; Sant’Ana, A.S. Paraprobiotics: Evidences on their ability to modify biological responses, inactivation methods and perspectives on their application in foods. Trends Food Sci. Technol. 2016, 58, 96–114. [Google Scholar] [CrossRef]
- Aguilar-Toalá, J.E.; Varela, R.G.; Garcia, H.; Mata-Haro, V.; González-Córdova, A.; Vallejo-Cordoba, B.; Hernández-Mendoza, A. Postbiotics: An evolving term within the functional foods field. Trends Food Sci. Technol. 2018, 75, 105–114. [Google Scholar] [CrossRef]
- Compare, D.; Rocco, A.; Coccoli, P.; Angrisani, D.; Sgamato, C.; Iovine, B.; Salvatore, U.; Nardone, G. Lactobacillus casei DG and its postbiotic reduce the inflammatory mucosal response: An ex-vivo organ culture model of post-infectious irritable bowel syndrome. BMC Gastroenterol. 2017, 17, 53. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Simeoli, R.; Raso, G.M.; Pirozzi, C.; Lama, A.; Santoro, A.; Russo, R.; Montero-Melendez, T.; Canani, R.B.; Calignano, A.; Perretti, M.; et al. An orally administered butyrate-releasing derivative reduces neutrophil recruitment and inflammation in dextran sulphate sodium-induced murine colitis. Br. J. Pharmacol. 2017, 174, 1484–1496. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Popović, N.; Djokić, J.; Brdaric, E.; Dinic, M.; Terzić-Vidojević, A.; Golić, N.; Veljović, K. The influence of heat-killed enterococcus faecium BGPAS1-3 on the tight junction protein expression and immune function in differentiated caco-2 cells infected with listeria monocytogenes ATCC 19111. Front. Microbiol. 2019, 10, 412. [Google Scholar] [CrossRef]
- Gao, J.; Li, Y.; Wan, Y.; Hu, T.; Liu, L.; Yang, S.; Gong, Z.; Zeng, Q.; Wei, Y.; Yang, W.; et al. A novel postbiotic from lactobacillus rhamnosus gg with a beneficial effect on intestinal barrier function. Front. Microbiol. 2019, 10, 477. [Google Scholar] [CrossRef] [Green Version]
- Dunand, E.; Burns, P.; Binetti, A.; Bergamini, C.V.; Peralta, G.H.; Forzani, L.; Reinheimer, J.; Vinderola, G. Postbiotics produced at laboratory and industrial level as potential functional food ingredients with the capacity to protect mice against salmonella infection. J. Appl. Microbiol. 2019, 127, 219–229. [Google Scholar] [CrossRef]
- Brial, F.; Le Lay, A.; Dumas, M.-E.; Gauguier, D. Implication of gut microbiota metabolites in cardiovascular and metabolic diseases. Cell. Mol. Life Sci. 2018, 75, 3977–3990. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Maguire, M.; Maguire, G. Gut dysbiosis, leaky gut, and intestinal epithelial proliferation in neurological disorders: Towards the development of a new therapeutic using amino acids, prebiotics, probiotics, and postbiotics. Rev. Neurosci. 2018, 30, 179–201. [Google Scholar] [CrossRef]
- Reeves, P.G.; Nielsen, F.H.; Fahey, G.C., Jr. AIN-93 Purified diets for laboratory rodents: Final report of the american institute of nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J. Nutr. 1993, 123, 1939–1951. [Google Scholar] [CrossRef]
- Azagra-Boronat, I.; Massot-Cladera, M.; Mayneris-Perxachs, J.; Knipping, K.; Land, B.V.; Tims, S.; Stahl, B.; Garssen, J.; Franch, À.; Castell, M.; et al. Immunomodulatory and prebiotic effects of 2′-fucosyllactose in suckling rats. Front. Immunol. 2019, 10, 1773. [Google Scholar] [CrossRef] [Green Version]
- Rigo-Adrover, M.D.M.; Knipping, K.; Garssen, J.; Van Limpt, K.; Knol, J.; Franch, À.; Castell, M.; Rodríguez-Lagunas, M.J.; Pérez-Cano, F.J. Prevention of rotavirus diarrhea in suckling rats by a specific fermented milk concentrate with prebiotic mixture. Nutrients 2019, 11, 189. [Google Scholar] [CrossRef] [Green Version]
- Rigo-Adrover, M.D.M.; Van Limpt, K.; Knipping, K.; Garssen, J.; Knol, J.; Costabile, A.; Franch, À.; Castell, M.; Pérez-Cano, F.J. Preventive effect of a synbiotic combination of galacto- and fructooligosaccharides mixture with bifidobacterium breve M-16V in a model of multiple rotavirus infections. Front. Immunol. 2018, 9, 1318. [Google Scholar] [CrossRef] [Green Version]
- Ayechu-Muruzabal, V.; Xiao, L.; Wehkamp, T.; van Ark, I.; Hoogendoorn, E.; Leusink-Muis, T.; Folkerts, G.; Garssen, J.; Willemsen, L.; Land, B.V. A fermented milk matrix containing postbiotics supports Th1- and Th17-type immunity In Vitro and modulates the influenza-specific vaccination response In Vivo in association with altered serum galectin ratios. Vaccines 2021, 9, 254. [Google Scholar] [CrossRef] [PubMed]
- Abrahamse, E.; Huybers, S.; Alles, M.S.; Renes, I.B.; Knol, J.; Bouritius, H.; Ludwig, T. Fermented infant formula increases ileal protein digestibility and reduces ileal proteolytic activity compared with standard and hydrolyzed infant formulas in piglets. J. Nutr. 2015, 145, 1423–1428. [Google Scholar] [CrossRef] [Green Version]
- Vandenplas, Y.; De Halleux, V.; Arciszewska, M.; Lach, P.; Pokhylko, V.; Klymenko, V.; Schoen, S.; Abrahamse-Berkeveld, M.A.; Mulder, K.; Rubio, R.P.; et al. A partly fermented infant formula with postbiotics including 3′-GL, specific oligosaccharides, 2′-FL, and milk fat supports adequate growth, is safe and well-tolerated in healthy term infants: A double-blind, randomised, controlled, multi-country trial. Nutrients 2020, 12, 3560. [Google Scholar] [CrossRef]
- Rodriguez-Herrera, A.; Mulder, K.; Bouritius, H.; Rubio, R.; Muñoz, A.; Agosti, M.; Lista, G.; Corvaglia, L.; Ludwig, T.; Abrahamse-Berkeveld, M.; et al. Gastrointestinal tolerance, growth and safety of a partly fermented formula with specific prebiotics in healthy infants: A double-blind, randomized, controlled trial. Nutrients 2019, 11, 1530. [Google Scholar] [CrossRef] [Green Version]
- Azagra-Boronat, I.; Massot-Cladera, M.; Knipping, K.; Land, B.V.; Tims, S.; Stahl, B.; Knol, J.; Garssen, J.; Franch, À.; Castell, M. Oligosaccharides modulate rotavirus-associated dysbiosis and TLR gene expression in neonatal rats. Cells 2019, 8, 876. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Livak, K.J.; Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative pcr and the 2−ΔΔCT method. Methods 2001, 25, 402–408. [Google Scholar] [CrossRef] [PubMed]
- Wang, Q.; Garrity, G.M.; Tiedje, J.M.; Cole, J.R. Naive bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 2007, 73, 5261–5267. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Anderson, M.J.; Walsh, D.C.I. Permanova, anosim, and the mantel test in the face of heterogeneous dispersions: What null hypothesis are you testing? Ecol. Monogr. 2013, 83, 557–574. [Google Scholar] [CrossRef]
- Mandal, S.; Van Treuren, W.; White, R.A.; Eggesbø, M.A.; Knight, R.T.; Peddada, S.D. Analysis of composition of microbiomes: A novel method for studying microbial composition. Microb. Ecol. Health Dis. 2015, 26, 27663. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Béghin, L.; Tims, S.; Roelofs, M.; Rougé, C.; Oozeer, R.; Rakza, T.; Chirico, G.; Roeselers, G.; Knol, J.; Rozé, J.C.; et al. Fermented infant formula (with Bifidobacterium breve C50 and Streptococcus thermophilus O65) with prebiotic oligosaccharides is safe and modulates the gut microbiota towards a microbiota closer to that of breastfed infants. Clin. Nutr. 2021, 40, 778–787. [Google Scholar] [CrossRef]
- Toca, M.D.C.; Burgos, F.; Fernández, A.; Giglio, N.; Orsi, M.; Sosa, P.; Tabacco, O.; Ursino, F.; Ussher, F.; Vinderola, G. Gut ecosystem during infancy: The role of “biotics”. Arch. Argent. Pediatr. 2020, 118, 278–285. [Google Scholar] [CrossRef]
- Vandenplas, Y.; De Greef, E.; Veereman, G. Prebiotics in infant formula. Gut Microbes 2015, 5, 681–687. [Google Scholar] [CrossRef] [Green Version]
- Vandenplas, Y.; Zakharova, I.; Dmitrieva, Y. Oligosaccharides in infant formula: More evidence to validate the role of prebiotics. Br. J. Nutr. 2015, 113, 1339–1344. [Google Scholar] [CrossRef] [Green Version]
- Morel, F.B.; Oozeer, R.; Piloquet, H.; Moyon, T.; Pagniez, A.; Knol, J.; Darmaun, D.; Michel, C. Preweaning modulation of intestinal microbiota by oligosaccharides or amoxicillin can contribute to programming of adult microbiota in rats. Nutrients 2015, 31, 515–522. [Google Scholar] [CrossRef] [PubMed]
- Huet, F.; Abrahamse-Berkeveld, M.; Tims, S.; Simeoni, U.; Beley, G.; Savagner, C.; Vandenplas, Y.; Hourihane, J.O. Partly Fermented infant formulae with specific oligosaccharides support adequate infant growth and are well-tolerated. J. Pediatr. Gastroenterol. Nutr. 2016, 63, e43–e53. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bryk, G.; Coronel, M.Z.; Lugones, C.; Mandalunis, P.; Rio, M.E.; Gualtieri, A.F.; De Portela, M.L.P.M.; Zeni, S.N. Effect of a mixture of GOS/FOS® on calcium absorption and retention during recovery from protein malnutrition: Experimental model in growing rats. Eur. J. Nutr. 2015, 55, 2445–2458. [Google Scholar] [CrossRef]
- Bryk, G.; Coronel, M.Z.; Pellegrini, G.G.; Mandalunis, P.; Rio, M.E.; De Portela, M.L.P.M.; Zeni, S.N. Effect of a combination GOS/FOS® prebiotic mixture and interaction with calcium intake on mineral absorption and bone parameters in growing rats. Eur. J. Nutr. 2015, 54, 913–923. [Google Scholar] [CrossRef]
- Abrams, S.A.; Griffin, I.J.; Hawthorne, K.M.; Liang, L.; Gunn, S.K.; Darlington, G.; Ellis, K.J. A combination of prebiotic short- and long-chain inulin-type fructans enhances calcium absorption and bone mineralization in young adolescents. Am. J. Clin. Nutr. 2005, 82, 471–476. [Google Scholar] [CrossRef] [PubMed]
- Rao, S.; Srinivasjois, R.; Patole, S. Prebiotic supplementation in full-term neonates. Arch. Pediatr. Adolesc. Med. 2009, 163, 755–764. [Google Scholar] [CrossRef] [Green Version]
- Beasley, D.; Koltz, A.M.; Lambert, J.E.; Fierer, N.; Dunn, R. The evolution of stomach acidity and its relevance to the human microbiome. PLoS ONE 2015, 10, e0134116. [Google Scholar] [CrossRef] [PubMed]
- Penagos Paniagua, M.J.; Pérez, R.D.B.; Cruz, M.D.L.L.G.; Benítez, J.M.Z. El Sistema inmune del recién nacido. alergia, asma e inmunol. Pediátricas 2003, 12, 18–23. [Google Scholar]
- Van Hoffen, E.; Ruiter, B.; Faber, J.; M’Rabet, L.; Knol, E.; Stahl, B.; Arslanoglu, S.; Moro, G.; Boehm, G.; Garssen, J. A specific mixture of short-chain galacto-oligosaccharides and long-chain fructo-oligosaccharides induces a beneficial immunoglobulin profile in infants at high risk for allergy. Allergy 2009, 64, 484–487. [Google Scholar] [CrossRef]
- Kim, J.J.; Khan, W.I. Goblet cells and mucins: Role in innate defense in enteric infections. Pathogens 2013, 2, 55–70. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dharmani, P.; Srivastava, V.; Kissoon-Singh, V.; Chadee, K. Role of intestinal mucins in innate host defense mechanisms against pathogens. J. Innate Immun. 2008, 1, 123–135. [Google Scholar] [CrossRef] [PubMed]
- Okazaki, Y.; Katayama, T. Consumption of non-digestible oligosaccharides elevates colonic alkaline phosphatase activity by up-regulating the expression ofIAP-I, with increased mucins and microbial fermentation in rats fed a high-fat diet. Br. J. Nutr. 2019, 121, 146–154. [Google Scholar] [CrossRef]
- Leforestier, G.; Blais, A.; Blachier, F.; Marsset-Baglieri, A.; Davila, A.-M.; Perrin, E.; Tomé, D. Effects of galacto-oligosaccharide ingestion on the mucosa-associated mucins and sucrase activity in the small intestine of mice. Eur. J. Nutr. 2009, 48, 457–464. [Google Scholar] [CrossRef]
- Van Herreweghen, F.; De Paepe, K.; Roume, H.; Kerckhof, F.-M.; Van De Wiele, T. Mucin degradation niche as a driver of microbiome composition and Akkermansia muciniphila abundance in a dynamic gut model is donor independent. FEMS Microbiol. Ecol. 2018, 94, 1–13. [Google Scholar] [CrossRef] [Green Version]
- Suzuki, T. Regulation of the intestinal barrier by nutrients: The role of tight junctions. Anim. Sci. J. 2020, 91, e13357. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Alizadeh, A.; Akbari, P.; DiFilippo, E.; Schols, H.A.; Ulfman, L.H.; Schoterman, M.H.C.; Garssen, J.; Fink-Gremmels, J.; Braber, S. The piglet as a model for studying dietary components in infant diets: Effects of galacto-oligosaccharides on intestinal functions. Br. J. Nutr. 2016, 115, 605–618. [Google Scholar] [CrossRef] [Green Version]
- Kaisho, T.; Akira, S. Toll-like receptor function and signaling. J. Allergy Clin. Immunol. 2006, 117, 979–987. [Google Scholar] [CrossRef]
- Schokker, D.; Fledderus, J.; Jansen, R.; Vastenhouw, S.A.; De Bree, F.M.; Smits, M.A.; Jansman, A.A.J.M. Supplementation of fructooligosaccharides to suckling piglets affects intestinal microbiota colonization and immune development. J. Anim. Sci. 2018, 96, 2139–2153. [Google Scholar] [CrossRef] [PubMed]
- Geerlings, S.Y.; Kostopoulos, I.; De Vos, W.M.; Belzer, C. Akkermansia muciniphila in the human gastrointestinal tract: When, where, and how? Microorganisms 2018, 6, 75. [Google Scholar] [CrossRef] [Green Version]
- Nishiwaki, H.; Ito, M.; Ms, T.I.; Hamaguchi, T.; Maeda, T.; Kashihara, K.; Tsuboi, Y.; Ueyama, J.; Shimamura, T.; Mori, H.; et al. Meta-analysis of gut dysbiosis in parkinson’s disease. Mov. Disord. 2020, 35, 1626–1635. [Google Scholar] [CrossRef]
- Zhou, K. Strategies to promote abundance of Akkermansia muciniphila, an emerging probiotics in the gut, evidence from dietary intervention studies. J. Funct. Foods 2017, 33, 194–201. [Google Scholar] [CrossRef]
- Shin, N.R.; Lee, J.C.; Lee, H.Y.; Kim, M.S.; Whon, T.W.; Lee, M.S.; Bae, J.W. An increase in the Akkermansia spp. population induced by metformin treatment improves glucose homeostasis in diet-induced obese mice. Gut 2014, 63, 727–735. [Google Scholar] [CrossRef] [Green Version]
- Everard, A.; Belzer, C.; Geurts, L.; Ouwerkerk, J.P.; Druart, C.; Bindels, L.B.; Guiot, Y.; Derrien, M.; Muccioli, G.G.; Delzenne, N.M.; et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc. Natl. Acad. Sci. USA 2013, 110, 9066–9071. [Google Scholar] [CrossRef] [Green Version]
- Doumatey, A.P.; Adeyemo, A.; Zhou, J.; Lei, L.; Adebamowo, S.N.; Adebamowo, C.; Rotimi, C.N. Gut microbiome profiles are associated with type 2 diabetes in urban Africans. Front. Cell. Infect. Microbiol. 2020, 10, 63. [Google Scholar] [CrossRef] [Green Version]
- Yu, M.; Jia, H.; Zhou, C.; Yang, Y.; Zhao, Y.; Yang, M.; Zou, Z. Variations in gut microbiota and fecal metabolic phenotype associated with depression by 16S rRNA gene sequencing and LC/MS-based metabolomics. J. Pharm. Biomed. Anal. 2017, 138, 231–239. [Google Scholar] [CrossRef] [PubMed]
- Tian, S.; Wang, J.; Yu, H.; Wang, J.; Zhu, W. Changes in ileal microbial composition and microbial metabolism by an early-life galacto-oligosaccharides intervention in a neonatal porcine model. Nutrients 2019, 11, 1753. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Han, C.; Dai, Y.; Liu, B.; Wang, L.; Wang, J.; Zhang, J. Diversity analysis of intestinal microflora between healthy and diarrheal neonatal piglets from the same litter in different regions. Anaerobe 2019, 55, 136–141. [Google Scholar] [CrossRef] [PubMed]
- Ben, X.-M.; Li, J.; Feng, Z.-T.; Shi, S.-Y.; Lu, Y.-D.; Chen, R.; Zhou, X.-Y. Low level of galacto-oligosaccharide in infant formula stimulates growth of intestinal Bifidobacteria and Lactobacilli. World J. Gastroenterol. 2008, 14, 6564–6568. [Google Scholar] [CrossRef] [PubMed]
- Song, X.; Zhong, L.; Lyu, N.; Liu, F.; Li, B.; Hao, Y.; Xue, Y.; Li, J.; Feng, Y.; Ma, Y.; et al. Inulin can alleviate metabolism disorders in ob/ob mice by partially restoring leptin-related pathways mediated by gut microbiota. Genom. Proteom. Bioinform. 2019, 17, 64–75. [Google Scholar] [CrossRef] [PubMed]
- Hu, X.; Ouyang, S.; Xie, Y.; Gong, Z.; Du, J. Characterizing the gut microbiota in patients with chronic kidney disease. Postgrad. Med. 2020, 132, 495–505. [Google Scholar] [CrossRef] [PubMed]
- Kang, X.; Zhan, L.-B.; Lu, X.-G.; Song, J.-B.; Zhong, Y.; Wang, Y.; Yang, Y.-L.; Fan, Z.-W.; Jiang, X.Z.; Sun, R. Characteristics of gastric microbiota in gk rats with spontaneous diabetes: A comparative study. Diabetes Metab. Syndr. Obes. Targets Ther. 2020, 13, 1435–1447. [Google Scholar] [CrossRef]
- Cao, W.; Chin, Y.; Chen, X.; Mi, Y.; Xue, C.; Wang, Y.; Tang, Q. The role of gut microbiota in the resistance to obesity in mice fed a high fat diet. Int. J. Food Sci. Nutr. 2019, 71, 453–463. [Google Scholar] [CrossRef] [PubMed]
- Hua, Y.; Fan, R.; Zhao, L.; Tong, C.; Qian, X.; Zhang, M.; Xiao, R.; Ma, W. Trans-fatty acids alter the gut microbiota in high-fat-diet-induced obese rats. Br. J. Nutr. 2020, 124, 1251–1263. [Google Scholar] [CrossRef] [PubMed]
- Haange, S.-B.; Jehmlich, N.; Hoffmann, M.; Weber, K.; Lehmann, J.; Von Bergen, M.; Slanina, U. Disease development is accompanied by changes in bacterial protein abundance and functions in a refined model of dextran sulfate sodium (DSS)-induced colitis. J. Proteome Res. 2019, 18, 1774–1786. [Google Scholar] [CrossRef]
- Youssef, O.; Lahti, L.; Kokkola, A.; Karla, T.; Tikkanen, M.; Ehsan, H.; Carpelan-Holmström, M.; Koskensalo, S.; Böhling, T.; Rautelin, H.; et al. Stool microbiota composition differs in patients with stomach, colon, and rectal neoplasms. Dig. Dis. Sci. 2018, 63, 2950–2958. [Google Scholar] [CrossRef] [Green Version]
- Liang, J.Q.; Li, T.; Nakatsu, G.; Chen, Y.-X.; Yau, T.O.; Chu, E.; Wong, S.; Szeto, C.H.; Ng, S.C.; Chan, F.K.L.; et al. A novel faecal Lachnoclostridium marker for the non-invasive diagnosis of colorectal adenoma and cancer. Gut 2020, 69, 1248–1257. [Google Scholar] [CrossRef] [Green Version]
- Li, N.; Huang, S.; Jiang, L.; Dai, Z.; Li, T.; Han, D.; Wang, J. Characterization of the early life microbiota development and predominant Lactobacillus Species at distinct gut segments of low- and normal-birth-weight piglets. Front. Microbiol. 2019, 10, 797. [Google Scholar] [CrossRef]
- Zhang, Y.; Chen, L.; Hu, M.; Kim, J.J.; Lin, R.; Xu, J.; Fan, L.; Qi, Y.; Wang, L.; Liu, W.; et al. Dietary type 2 resistant starch improves systemic inflammation and intestinal permeability by modulating microbiota and metabolites in aged mice on high-fat diet. Aging 2020, 12, 9173–9187. [Google Scholar] [CrossRef]
- Ju, T.; Kong, J.Y.; Stothard, P.; Willing, B.P. Defining the role of Parasutterella, a previously uncharacterized member of the core gut microbiota. ISME J. 2019, 13, 1520–1534. [Google Scholar] [CrossRef]
- 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] [Green Version]
- Liu, L.; He, Y.; Wang, K.; Miao, J.L.; Zheng, Z. Metagenomics approach to the intestinal microbiome structure and function in high fat diet-induced obesity in mice fed with conjugated linoleic acid (CLA). Food Funct. 2020, 11, 9729–9739. [Google Scholar] [CrossRef] [PubMed]
- Cheng, M.; Zhang, X.; Miao, Y.; Cao, J.; Wu, Z.; Weng, P. The modulatory effect of (-)-epigallocatechin 3-O-(3-O-methyl) gallate (EGCG3″Me) on intestinal microbiota of high fat diet-induced obesity mice model. Food Res. Int. 2017, 92, 9–16. [Google Scholar] [CrossRef] [PubMed]
- Wüst, P.K.; Horn, M.A.; Drake, H.L. Clostridiaceae and Enterobacteriaceae as active fermenters in earthworm gut content. ISME J. 2010, 5, 92–106. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, Y.-T.; Zeng, Y.; Li, J.; Zhao, X.-Y.; Yi, Y.; Gou, M.; Kamagata, Y.; Narihiro, T.; Nobu, M.K.; Tang, Y.-Q. Novel syntrophic isovalerate-degrading bacteria and their energetic cooperation with methanogens in methanogenic chemostats. Environ. Sci. Technol. 2020, 54, 9618–9628. [Google Scholar] [CrossRef] [PubMed]
- Petrognani, C.; Boon, N.; Ganigué, R. Production of isobutyric acid from methanol by Clostridium luticellarii. Green Chem. 2020, 22, 8389–8402. [Google Scholar] [CrossRef]
REF | PRE | POST | P+P | |
---|---|---|---|---|
Naso-anal (Body, cm) | 9.10 ± 0.16 | 9.44 ± 0.10 | 9.38 ± 0.10 | 9.75 ± 0.07 *# φ |
Anus-tail (Tail, cm) | 4.78 ± 0.11 | 4.58 ± 0.07 | 5.00 ± 0.07 # | 4.99 ± 0.07 # |
Naso-tail (cm) | 13.88 ± 0.24 | 14.03 ± 0.16 | 14.38 ± 0.08 | 14.74 ± 0.13 *# φ |
Body/Tail length ratio | 1.91 ± 0.03 | 2.06 ± 0.02 * | 1.88 ± 0.04 # | 1.96 ± 0.02 # |
Body mass index (g/cm2) | 0.32 ± 0.01 | 0.32 ± 0.00 | 0.33 ± 0.01 # | 0.34 ± 0.00 # |
Lee index (g0.33/cm, ×1000) | 327.35 ± 2.53 | 321.97 ± 1.00 * | 329.16 ± 2.78 | 327.21 ± 1.42 # |
Spleen/BW ratio (%) | 0.43 ± 0.03 | 0.47 ± 0.02 | 0.47 ± 0.02 | 0.49 ± 0.02 |
Thymus/BW ratio (%) | 0.45 ± 0.01 | 0.44 ± 0.01 | 0.45 ± 0.01 | 0.45 ± 0.01 |
Liver/BW ratio (%) | 3.40 ± 0.05 | 3.47 ± 0.06 | 3.42 ± 0.10 | 3.54 ± 0.08 * |
Large int./BW ratio (%) | 0.60 ± 0.01 | 0.71 ± 0.02 * | 0.57 ± 0.02 # | 0.68 ± 0.02 * φ |
Small int./BW ratio (%) | 3.48 ± 0.09 | 5.32 ± 0.09 * | 3.45 ± 0.07 # | 5.06 ± 0.15 * φ |
Large int. length/BW (cm/g) | 24.91 ± 1.48 | 22.78 ± 0.77 | 21.63 ± 1.28 | 20.41 ± 0.54 *# |
Small int. length/BW (cm/g) | 134.96 ± 6.49 | 142.73 ± 6.53 | 127.35 ± 2.86 # | 120.41 ± 5.72 # |
Stomach/BW ratio (%) | 0.76 ± 0.02 | 0.75 ± 0.02 | 0.70 ± 0.01 # | 0.71 ± 0.01 |
Ig (µg/mL) | REF | PRE | POST | P+P |
---|---|---|---|---|
IgG | 3117.81 ± 271.58 | 2968.14 ± 194.43 | 2341.86 ± 202.01 * | 1985.85 ± 110.81 *# |
(98.64 ± 0.04%) | (98.52 ± 0.03% *) | (98.47 ± 0.06% *) | (98.41 ± 0.05% *) | |
IgG1 | 260.53 ± 25.42 | 208.69 ± 14.56 | 142.05 ± 15.73 *# | 130.10 ± 8.56 *# |
(8.97 ± 1.06%) | (7.02 ± 0.11%) | (6.07 ± 0.42%) | (6.56 ± 0.23%) | |
IgG2a | 551.53 ± 38.91 | 499.33 ± 28.96 | 394.47 ± 31.40 *# | 363.66 ± 19.07 *# |
(18.01 ± 0.65%) | (17.35 ± 1.27%) | (17.01 ± 0.79%) | (18.49 ± 0.69%) | |
IgG2b | 1193.30 ± 109.62 | 1255.98 ± 93.37 | 813.73 ± 78.19 *# | 758.59 ± 46.86 *# |
(38.12 ± 0.45%) | (42.11 ± 0.65% *) | (34.61 ± 0.66% *#) | (38.15 ± 0.88% #φ) | |
IgG2c | 1112.44 ± 131.36 | 1004.12 ± 84.37 | 991.60 ± 87.20 | 733.49 ± 52.67 *#φ |
(34.91 ± 1.21%) | (33.52 ± 0.94%) | (42.30 ± 0.35% *#) | (36.79 ± 1.39% φ) | |
IgM | 23.02 ± 1.55 | 26.86 ± 2.18 | 23.21 ± 3.14 | 20.46 ± 1.23 # |
(0.74 ± 0.02%) | (0.89 ± 0.03% *) | (0.96 ± 0.07% *) | (1.02 ± 0.04% *#) | |
IgA | 18.97 ± 1.05 | 17.68 ± 0.76 | 13.30 ± 0.81 *# | 11.61 ± 0.96 *# |
(0.62 ± 0.02%) | (0.6 ± 0.02%) | (0.57 ± 0.02%) | (0.57 ± 0.02%) | |
Th1/Th2 ratio a | 2.81 ± 0.20 | 3.20 ± 0.22 * | 3.34 ± 0.08 * | 3.03 ± 0.14 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 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 (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Morales-Ferré, C.; Azagra-Boronat, I.; Massot-Cladera, M.; Tims, S.; Knipping, K.; Garssen, J.; Knol, J.; Franch, À.; Castell, M.; Rodríguez-Lagunas, M.J.; et al. Effects of a Postbiotic and Prebiotic Mixture on Suckling Rats’ Microbiota and Immunity. Nutrients 2021, 13, 2975. https://doi.org/10.3390/nu13092975
Morales-Ferré C, Azagra-Boronat I, Massot-Cladera M, Tims S, Knipping K, Garssen J, Knol J, Franch À, Castell M, Rodríguez-Lagunas MJ, et al. Effects of a Postbiotic and Prebiotic Mixture on Suckling Rats’ Microbiota and Immunity. Nutrients. 2021; 13(9):2975. https://doi.org/10.3390/nu13092975
Chicago/Turabian StyleMorales-Ferré, Carla, Ignasi Azagra-Boronat, Malén Massot-Cladera, Sebastian Tims, Karen Knipping, Johan Garssen, Jan Knol, Àngels Franch, Margarida Castell, María J. Rodríguez-Lagunas, and et al. 2021. "Effects of a Postbiotic and Prebiotic Mixture on Suckling Rats’ Microbiota and Immunity" Nutrients 13, no. 9: 2975. https://doi.org/10.3390/nu13092975