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The Changes of Colonic Bacterial Composition and Bacterial Metabolism Induced by an Early Food Introduction in a Neonatal Porcine Model

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Abstract

The impact of an early food introduction on the microbiota composition and microbial metabolism in colon was investigated using a new-born piglet model. At day 4 after birth, 10 litters of piglets were randomly allocated to a sow-rearing group (SR group) and a milk-replacer supplementing group (MRS group) (n = 5). A commercial milk replacer was given to the suckling piglets in the MRS group from the 4th day to the 28th day. Pyrosequencing of the V3–V4 region of the 16S rRNA genes showed that the milk replacer supplementation significantly decreased the relative abundance of Lactobacillus, Clostridium XI, Blautia, Clostridium sensustricto and Escherichia (p = 0.08) in the colon of the piglets, but significantly increased the relative abundance of Paraprevotella on the 28th day. In addition, the abundance of Rumminococcus, Clostridium XlVa, Succiniclasticum, Clostridium IV tended to increase in the MRS group. The concentrations of acetate, propionate, butyrate, valerate and branch-chain fatty acids (BCFAs) in the colonic digesta increased with the milk replacer supplementary in the MRS group. In addition, the milk replacer supplementary increased the expression level of Toll-like receptor 4 (TLR4), but decreased the expression level of interleukin-6 (IL-6) in the colonic mucosa of the piglets. In conclusion, an early food introduction can influence the gut bacterial composition and metabolism, and may further affect the intestinal health by modifying the gene transcription related to the colonic function. These findings may provide some guidelines for the early nutrition supplementation for infants during the lactation period.

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References

  1. Salone LR, Vann WF Jr, Dee DL (2013) Breastfeeding: an overview of oral and general health benefits. J Am Dent Assoc 144:143–151

    Article  PubMed  Google Scholar 

  2. Walker A (2010) Breast milk as the gold standard for protective nutrients. J Pediatr 156:s3-7. https://doi.org/10.1016/j.jpeds.2009.11.021

    PubMed  Google Scholar 

  3. Kramer MS, Kakuma R (2004) The optimal duration of exclusive breastfeeding: a systematic review. Adv Exp Med Biol 554:63–77

    Article  PubMed  Google Scholar 

  4. Colen CG, Ramey DM (2014) Is breast truly best? Estimating the effects of breastfeeding on long-term child health and wellbeing in the United States using sibling comparisons. Soc Sci Med 109:55–65. https://doi.org/10.1016/j.socscimed. 2014.01.027

    Article  PubMed  PubMed Central  Google Scholar 

  5. Le Huerou-Luron I, Blat S, Boudry G (2010) Breast- v. formula-feeding: impacts on the digestive tract and immediate and long-term health effects. Nutr Res Rev 23:23–36. https://doi.org/10.1017/S0954422410000065

    Article  PubMed  Google Scholar 

  6. Pang WW, Aris IM, Fok D, Soh SE, Chua MC, Lim SB, Saw SM, Kwek K, Gluckman PD, Godfrey KM, van Dam RM, Kramer MS, Chong YS (2016) Determinants of breastfeeding practices and success in a multi-ethnic Asian population. Birth 43:68–77. https://doi.org/10.1111/birt.12206

    Article  PubMed  Google Scholar 

  7. Victora CG, Bahl R, Barros AJD, França GVA, Horton S, Krasevec J, Murch S, Sankar MJ, Walker N, Rollins NC (2016) Breastfeeding in the 21st century: epidemiology, mechanisms, and lifelong effect. Lancet 387:475–490. https://doi.org/10.1016/s0140-6736(15)01024-7

    Article  PubMed  Google Scholar 

  8. Fallani M, Amarri S, Uusijarvi A, Adam R, Khanna S, Aguilera M, Gil A, Vieites JM, Norin E, Young D, Scott JA, Dore J, Edwards CA (2011) Determinants of the human infant intestinal microbiota after the introduction of first complementary foods in infant samples from five European centres. Microbiology 157:1385–1392. https://doi.org/10.1099/mic.0.042143-0

    Article  CAS  PubMed  Google Scholar 

  9. Issaka AI, Agho KE, Page AN, Burns P, Stevens GJ, Dibley MJ (2014) Determinants of early introduction of solid, semi-solid or soft foods among infants aged 3–5 months in four Anglophone West African countries. Nutrients 6:2602–2618. https://doi.org/10.3390/nu6072602

    Article  PubMed  PubMed Central  Google Scholar 

  10. Penny ME, Creed-Kanashiro HM, Robert RC, Narro MR, Caulfield LE, Black RE (2005) Effectiveness of an educational intervention delivered through the health services to improve nutrition in young children: a cluster-randomised controlled trial. Lancet 365:1863–1872. https://doi.org/10.1016/s0140-6736(05)66426-4

    Article  PubMed  Google Scholar 

  11. Poroyko V, White JR, Wang M, Donovan S, Alverdy J, Liu DC, Morowitz MJ (2010) Gut microbial gene expression in mother-fed and formula-fed piglets. PLoS ONE 5:e12459. https://doi.org/10.1371/journal.pone.0012459

    Article  PubMed  PubMed Central  Google Scholar 

  12. De Lange CFM, Pluske J, Gong J, Nyachoti CM (2010) Strategic use of feed ingredients and feed additives to stimulate gut health and development in young pigs. Livest Sci 134(1–3):124–134. https://doi.org/10.1016/j.livsci.2010.06.117

    Article  Google Scholar 

  13. Kamitsuka MD, Horton MK, Williams MA (2000) The incidence of necrotizing enterocolitis after introducing standardized feeding schedules for infants between 1250 and 2500 grams and less than 35 weeks of gestation. Pediatrics 105:379–383

    Article  CAS  PubMed  Google Scholar 

  14. Caulfield LE, Huffman SL, Piwoz EG (1999) Interventions to improve intake of complementary foods by infants 6 to 12 months of age in developing countries: impact on growth and on the prevalence of malnutrition and potential contribution to child survival. Food Nutr Bull 20:183–200

    Article  Google Scholar 

  15. Schroeder DG, Martorell R, Floras R (1999) Infant and child growth and fatness and fat distribution in guatemalan adults. Am J Epidemiol 149:177–185

    Article  CAS  PubMed  Google Scholar 

  16. Kim HB, Isaacson RE (2015) The pig gut microbial diversity: understanding the pig gut microbial ecology through the next generation high throughput sequencing. Vet Microbiol 177:242–251. https://doi.org/10.1016/j.vetmic.2015.03.014

    Article  CAS  PubMed  Google Scholar 

  17. Sekirov I, Russell SL, Antunes LC, Finlay BB (2010) Gut microbiota in health and disease. Physiol Rev 90:859–904. https://doi.org/10.1152/physrev.00045.2009.-Gut

    Article  CAS  PubMed  Google Scholar 

  18. Tan H, O’Toole PW (2015) Impact of diet on the human intestinal microbiota. Curr Opin Food Sci 2:71–77. doi.https://doi.org/10.1016/j.cofs.2015.01.005

    Article  Google Scholar 

  19. Duncan SH, Lobley GE, Holtrop G, Ince J, Johnstone AM, Louis P, Flint HJ (2008) Human colonic microbiota associated with diet, obesity and weight loss. Int J Obes (Lond) 32:1720–1724. https://doi.org/10.1038/ijo.2008.155

    Article  CAS  Google Scholar 

  20. Russell SL, Gold MJ, Hartmann M, Willing BP, Thorson L, Wlodarska M, Gill N, Blanchet MR, Mohn WW, McNagny KM, Finlay BB (2012) Early life antibiotic-driven changes in microbiota enhance susceptibility to allergic asthma. EMBO Rep 13:440–447. https://doi.org/10.1038/embor.2012.32

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Zoetendal EG, Akkermans ADL, Vos WMD (1998) Temperature Gradient Gel Electrophoresis Analysis of 16S rRNA from Human Fecal Samples Reveals Stable and Host-Specific Communities of Active Bacteria. Appl Environ Microbiol 64:3854–3859

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R (2012) Ultra-high-throughput microbial community analysis on the illumina hiSeq and miSeq platforms. ISME J 6:1621–1624. https://doi.org/10.1038/ismej.2012.8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Sun Y, Zhou L, Fang L, Su Y, Zhu W (2015) Responses in colonic microbial community and gene expression of pigs to a long-term high resistant starch diet. Front Microbiol 6:877. https://doi.org/10.3389/fmicb.2015.00877

    PubMed  PubMed Central  Google Scholar 

  24. Mao S, Zhang R, Wang D, Zhu W (2012) The diversity of the fecal bacterial community and its relationship with the concentration of volatile fatty acids in the feces during subacute rumen acidosis in dairy cows. BMC Vet Res 8:237. https://doi.org/10.1186/1746-6148-8-237

    Article  PubMed  PubMed Central  Google Scholar 

  25. Nyachoti CM, Omogbenigun FO, Rademacher M, Blank G (2006) Performance responses and indicators of gastrointestinal health in early-weaned pigs fed low-protein amino acid-supplemented diets. J Anim Sci 84:125–134

    Article  CAS  PubMed  Google Scholar 

  26. Zhang CJ, Yu M, Yang YX, Mu CL, Su Y, Zhu WY (2016) Differential effect of early antibiotic intervention on bacterial fermentation patterns and mucosal gene expression in the colon of pigs under diets with different protein levels. Appl Microbiol Biotechnol 101:1–13

    Google Scholar 

  27. Herfel TM, Jacobi SK, Lin X, Fellner V, Walker DC, Jouni ZE, Odle J (2011) Polydextrose enrichment of infant formula demonstrates prebiotic characteristics by altering intestinal microbiota, organic acid concentrations, and cytokine expression in suckling piglets. J Nutr 141:2139–2145. https://doi.org/10.3945/jn.111.143727

    Article  CAS  PubMed  Google Scholar 

  28. Huh SY, Rifas-Shiman SL, Taveras EM, Oken E, Gillman MW (2011) Timing of solid food introduction and risk of obesity in preschool-aged children. Pediatrics 127:e544-551. https://doi.org/10.1542/peds.2010-0740

    Article  Google Scholar 

  29. Kuo AA, Inkelas M, Slusser WM, Maidenberg M, Halfon N (2011) Introduction of solid food to young infants. Matern Child Health J 15:1185–1194. https://doi.org/10.1007/s10995-010-0669-5

    Article  PubMed  Google Scholar 

  30. Lin HY, Chang JH, Chung MY, Lin HC (2014) Prevention of necrotizing enterocolitis in preterm very low birth weight infants: is it feasible? J Formos Med Assoc 113:490–497. https://doi.org/10.1016/j.jfma.2013.03.010

    Article  PubMed  Google Scholar 

  31. Blaut M (2015) Gut microbiota and energy balance: role in obesity. Proc Nutr Soc 74:227–234. https://doi.org/10.1017/S0029665114001700

    Article  CAS  PubMed  Google Scholar 

  32. De Vadder F, Kovatcheva-Datchary P, Goncalves D, Vinera J, Zitoun C, Duchampt A, Backhed F, Mithieux G (2014) Microbiota-generated metabolites promote metabolic benefits via gut-brain neural circuits. Cell 156:84–96. https://doi.org/10.1016/j.cell.2013.12.016

    Article  PubMed  Google Scholar 

  33. Lin HV, Frassetto A, Kowalik EJ, Nawrocki AR, Lu MM, Kosinski JR, Hubert JA, Szeto D, Yao X, Forrest G, Marsh DJ (2012) Butyrate and propionate protect against diet-induced obesity and regulate gut hormones via free fatty acid receptor 3-independent mechanisms. PLoS ONE 7:e35240. https://doi.org/10.1371/journal.pone.0035240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Chen H, Mao X, He J, Yu B, Huang Z, Yu J, Zheng P, Chen D (2013) Dietary fibre affects intestinal mucosal barrier function and regulates intestinal bacteria in weaning piglets. Br J Nutr 110:1837–1848. https://doi.org/10.1017/S0007114513001293

    Article  CAS  PubMed  Google Scholar 

  35. Howard MD, Gordon DT, Pace LW, Garleb KA, Kerley MS (1995) Effects of dietary supplementation with fructooligosaccharides on colonic microbiota populations and epithelial cell proliferation in neonatal pigs. J Pediatr Gastroenterol Nutr 21:297–303

    Article  CAS  PubMed  Google Scholar 

  36. Lopetuso LR, Scaldaferri F, Petito V, Gasbarrini A (2013) Commensal Clostridia: leading players in the maintenance of gut homeostasis. Gut Pathog 5:23. https://doi.org/10.1186/1757-4749-5-23

    Article  PubMed  PubMed Central  Google Scholar 

  37. Martinez I, Kim J, Duffy PR, Schlegel VL, Walter J (2010) Resistant Starches Types 2 and 4 Have Differential Effects on the Composition of the Fecal Microbiota in Human Subjects. PLoS ONE 5:e15046. https://doi.org/10.1371/journal.pone.0015046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Pryde SE, Duncan SH, Hold GL, Stewart CS, Flint HJ (2002) The microbiology of butyrate formation in the human colon. FEMS Microbiol Lett 217:133–139

    Article  CAS  PubMed  Google Scholar 

  39. Singhal A, Farooqi IS, O’ Rahilly S, Cole TJ, Fewtrell M, Lucas A (2002) Early nutrition and leptin concentrations in later life. Am J Clin Nutr 75:993–999

    Article  CAS  PubMed  Google Scholar 

  40. Walker AW, Ince J, Duncan SH, Webster LM, Holtrop G, Ze X, Brown D, Stares MD, Scott P, Bergerat A, Louis P, McIntosh F, Johnstone AM, Lobley GE, Parkhill J, Flint HJ (2011) Dominant and diet-responsive groups of bacteria within the human colonic microbtioa. ISME J 5:220–230. https://doi.org/10.1038/ismej.2010.118

    Article  CAS  PubMed  Google Scholar 

  41. Kanengoni AT, Chimonyo M, Tasara T, Cormican P, Chapwanya A, Ndimba BK, Dzama K (2015) A comparison of faecal microbial populations of South African Windsnyer-type indigenous pigs (SAWIP) and Large White x Landrace (LW × LR) crosses fed diets containing ensiled maize cobs. FEMS Microbiol Lett 362:fnv100. https://doi.org/10.1093/femsle/fnv100

    Article  PubMed  Google Scholar 

  42. Shi C, Wang J, Zhu Y, Niu Q, Wang J (2017) Effects of early supplementary feeding milk replacer on post weaning piglets’ diarrhea frequency, bacterial community and metabolites. Anim Husb Vet Med 49:51–57

    Google Scholar 

  43. Penders J, Thijs C, Vink C, Stelma FF, Snijders B, Kummeling I, van den Brandt PA, Stobberingh EE (2006) Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics 118:511–521

    Article  PubMed  Google Scholar 

  44. Drissi F, Raoult D, Merhej V (2016) Metabolic role of lactobacilli in weight modification in humans and animals. Microb Pathog. https://doi.org/10.1016/j.micpath.2016.03.006

    PubMed  Google Scholar 

  45. Grummer-Strawn LM, Scanlon KS, Fein SB (2008) Infant feeding and feeding transitions during the first year of life. Pediatrics 122:S36-42. https://doi.org/10.1542/peds.2008-1315d

    Article  PubMed  Google Scholar 

  46. Macfarlane S, Cleary S, Bahrami B, Reynolds N, Macfarlane GT (2013) Synbiotic consumption changes the metabolism and composition of the gut microbiota in older people and modifies inflammatory processes: a randomised, double-blind, placebo-controlled crossover study. Aliment Pharmacol Ther 38:804–816. https://doi.org/10.1111/apt.12453

    Article  CAS  PubMed  Google Scholar 

  47. Miquel S, Martín R, Rossi O, Bermúdez-Humarán LG, Chatel JM, Soko H, Thomas M, Wells JM, Langella P (2013) Faecalibacterium prausnitzii and human intestinal health. Curr Opin Microbiol 16:255–261. https://doi.org/10.1016/j.mib.2013.06.003

    Article  CAS  PubMed  Google Scholar 

  48. Cassir N, Simeoni U, La Scola B (2016) Gut microbiota and the pathogenesis of necrotizing enterocolitis in preterm neonates. Future Microbiol 11:273–292. https://doi.org/10.2217/fmb.15.136

    Article  CAS  PubMed  Google Scholar 

  49. Aufreiter S, Kim JH, O’Connor DL (2011) Dietary oligosaccharides increase colonic weight and the amount but not concentration of bacterially synthesized folate in the colon of piglets. J Nutr 141:366–372. https://doi.org/10.3945/jn.110.135343

    Article  CAS  PubMed  Google Scholar 

  50. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA (2005) Diversity of the human intestinal microbial flora. Science 308:1635–1638. https://doi.org/10.1126/science.1110591

    Article  PubMed  PubMed Central  Google Scholar 

  51. Jacobi SK, Odle J (2012) Nutritional factors influencing intestinal health of the neonate. Adv Nutr 3:687–696. https://doi.org/10.3945/an.112.002683

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermudez-Humaran LG, Gratadoux JJ, Blugeon S, Bridonneau C, Furet JP, Corthier G, Grangette C, Vasquez N, Pochart P, Trugnan G, Thomas G, Blottiere HM, Dore J, Marteau P, Seksik P, Langella P (2008) Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci USA 105:16731–16736. https://doi.org/10.1073/pnas.0804812105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Dheer R, Santaolalla R, Davies JM, Lang JK, Phillips MC, Pastorini C, Vazquez- Pertejo MT, Abreu MT (2016) Intestinal epithelial toll-like receptor 4 signaling affects epithelial function and colonic microbiota and promotes a risk for transmissible colitis. Infect Immun 84:798–810. https://doi.org/10.1128/IAI.01374-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Fukata M, Michelsen KS, Eri R, Thomas LS, Hu B, Lukasek K, Nast CC, Lechago J, Xu R, Naiki Y, Soliman A, Arditi M, Abreu MT (2005) Toll-like receptor-4 is required for intestinal response to epithelial injury and limiting bacterial translocation in a murine model of acute colitis. Am J Physiol Gastrointest Liver Physiol 288:G1055-1065. https://doi.org/10.1152/ajpgi.00328.2004

    Article  Google Scholar 

  55. Hooper LV, Littman DR, Macpherson AJ (2012) Interactions between the microbiota and the immune system. Science 336:1268–1273. https://doi.org/10.1126/science.1223490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors thank National Center for International Research on Animal Gut Nutrition for financial support. This study was supported by National Key R&D Program of China 2017YFD0500505 and the Fundamental Research Funds for the Central Universities, China (KYZ201722).

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Shi, C., Zhu, Y., Niu, Q. et al. The Changes of Colonic Bacterial Composition and Bacterial Metabolism Induced by an Early Food Introduction in a Neonatal Porcine Model. Curr Microbiol 75, 745–751 (2018). https://doi.org/10.1007/s00284-018-1442-z

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