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Use of pigs as a potential model for research into dietary modulation of the human gut microbiota

  • Sonja N. Heinritz (a1), Rainer Mosenthin (a1) and Eva Weiss (a1)


The human intestinal microbial ecosystem plays an important role in maintaining health. A multitude of diseases including diarrhoea, gastrointestinal inflammatory disorders, such as necrotising enterocolitis (NEC) of neonates, and obesity are linked to microbial composition and metabolic activity. Therefore, research on possible dietary strategies influencing microbial composition and activity, both preventive and curative, is being accomplished. Interest has focused on pre- and probiotics that stimulate the intestinal production of beneficial bacterial metabolites such as butyrate, and beneficially affect microbial composition. The suitability of an animal model to study dietary linked diseases is of much concern. The physiological similarity between humans and pigs in terms of digestive and associated metabolic processes places the pig in a superior position over other non-primate models. Furthermore, the pig is a human-sized omnivorous animal with comparable nutritional requirements, and shows similarities to the human intestinal microbial ecosystem. Also, the pig has been used as a model to assess microbiota–health interactions, since pigs exhibit similar syndromes to humans, such as NEC and partly weanling diarrhoea. In contrast, when using rodent models to study diet–microbiota–health interactions, differences between rodents and humans have to be considered. For example, studies with mice and human subjects assessing possible relationships between the composition and metabolic activity of the gut microbiota and the development of obesity have shown inconsistencies in results between studies. The present review displays the similarities and differences in intestinal microbial ecology between humans and pigs, scrutinising the pig as a potential animal model, with regard to possible health effects.

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*Corresponding author: Dr Eva Weiss, fax +49 711 459 22421, email


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1Turnbaugh, PJ, Ley, RE, Mahowald, MA, et al. (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444, 10271031.
2Guo, X, Xia, X, Tang, R, et al. (2008) Development of a real-time PCR method for Firmicutes and Bacteroidetes in faeces and its application to quantify intestinal population of obese and lean pigs. Lett Appl Microbiol 47, 367373.
3Ley, RE, Backhed, F, Turnbaugh, P, et al. (2005) Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A 102, 1107011075.
4Schwiertz, A, Gruhl, B, Löbnitz, M, et al. (2003) Development of the intestinal bacterial composition in hospitalized preterm infants in comparison with breast-fed, full-term infants. Pediatr Res 54, 393399.
5Magne, F, Hachelaf, W, Suau, A, et al. (2006) A longitudinal study of infant faecal microbiota during weaning. FEMS Microbiol Ecol 58, 563571.
6Govers, MJAP, Gannon, NJ, Dunshea, FR, et al. (1999) Wheat bran affects the site of fermentation of resistant starch and luminal indexes related to colon cancer risk: a study in pigs. Gut 45, 840847.
7Duncan, SH, Lobley, GE, Holtrop, G, et al. (2008) Human colonic microbiota associated with diet, obesity and weight loss. Int J Obes 32, 17201724.
8Schrezenmeir, J & de Vrese, M (2001) Probiotics, prebiotics, and synbiotics – approaching a definition. Am J Clin Nutr 73, 361S364S.
9Marik, PE (2012) Colonic flora, probiotics, obesity and diabetes. Front Endocrin 3, 87.
10Gibson, GR & Roberfroid, MB (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 125, 14011412.
11Houpt, AK, Houpt, R & Pond, WG (1979) The pig as a model for the study of obesity and of control of food intake: a review. Yale J Biol Med 52, 307329.
12Graham, H & Aman, P (1987) The pig as a model in dietary fibre digestion studies. Scand J Gastroenterol 22, 5561.
13Van Soest, PJ, Jeraci, J, Fosse, T, et al. (1982) Comparative fermentation of fibre in man and other animals. In Fibre in Human and Animal Nutrition, Bulletin no. 20, pp. 7580 [Wallace, G and Bell, L, editors]. Wellington: The Royal Society of New Zealand.
14Brooks, SP, McAllister, M, Sandoz, M, et al. (2003) Culture-independent phylogenetic analysis of the faecal flora of the rat. Can J Microbiol 49, 589601.
15Manichanh, C, Reeder, J, Gibert, P, et al. (2010) Reshaping the gut microbiome with bacterial transplantation and antibiotic intake. Genome Res 20, 14111419.
16Tomas, J, Langella, P & Cherbuy, C (2012) The intestinal microbiota in the rat model: major breakthroughs from new technologies. Anim Health Res Rev 13, 5463.
17Lay, C, Rigottier-Gois, L, Holmstrom, K, et al. (2005) Colonic microbiota signatures across five northern European countries. Appl Environ Microbiol 71, 41534155.
18Dalby, AB, Frank, DN, St Amand, AL, et al. (2006) Culture-independent analysis of indomethacin induced alterations in the rat gastrointestinal microbiota. Appl Environ Microbiol 72, 67076715.
19Delroisse, JM, Boulvin, AL, Parmentier, I, et al. (2008) Quantification of Bifidobacterium spp. and Lactobacillus spp. in rat fecal samples by real-time PCR. Res Microbiol 163, 663670.
20Oli, MW, Petschow, BW & Buddington, RK (1998) Evaluation of fructooligosaccharide supplementation of oral electrolyte solutions for treatment of diarrhoea: recovery of the intestinal bacteria. Dig Dis Sci 43, 138147.
21Andersen, AD, Mølbak, L, Thymann, T, et al. (2011) Dietary long-chain n-3 PUFA, gut microbiota and fatmass in early postnatal piglet development – exploring a potential interplay. Prostaglandins Leukot Essent Fatty Acids 85, 345351.
22Leser, TD, Amernuvor, JZ & Jensen, TK (2002) Culture-independent analysis of gut bacteria: the pig gastrointestinal tract microbiota revisited. Appl Environ Microbiol 68, 673690.
23Miller, ER & Ullrey, DE (1987) The pig as a model for human nutrition. Annu Rev Nutr 7, 361382.
24Baker, DH (2008) Animal models in nutrition research. J Nutr 138, 391396.
25Puiman, P & Stoll, B (2008) Animal models to study neonatal nutrition in humans. Curr Opin Clin Nutr Metab Care 11, 601606.
26Kien, CL, Ailabouni, AH, Murray, RD, et al. (1997) Technical note: pig model for studying nutrient assimilation by the intestine and colon. J Anim Sci 75, 21612164.
27Labib, S, Erb, A, Kraus, M, et al. (2004) The pig caecum model: a suitable tool to study the intestinal metabolism of flavonoids. Mol Nutr Food Res 48, 326332.
28Emmans, GC & Kyriazakis, I (1999) Growth and body composition. In A Quantitative Biology of the Pig, pp. 181198 [Kyriazakis, I, editor]. Wallingford: CAB International.
29Mochizuki, S & Makita, T (1998) Differences in intestinal length between specific-pathogen-free (SPF) and conventional swine. J Vet Med Sci 60, 545548.
30Van Rens, BTTM & Van Der Lende, T (2002) Litter size and piglet traits of gilts with different prolactin receptor genotypes. Theriogenology 57, 883893.
31Patterson, JK, Lei, XG & Miller, DD (2008) The pig as an experimental model for elucidating the mechanisms governing dietary influence on mineral absorption. Exp Biol Med 233, 651664.
32Rispat, G, Slaoui, M, Weber, D, et al. (1993) Haematological and plasma biochemical values for healthy Yucatan micropigs. Lab Anim Sci 27, 368373.
33Guilloteau, P, Zabielski, R, Hammon, HM, et al. (2010) Nutritional programming of gastrointestinal tract development. Is the pig a good model for man? Nutr Res Rev 23, 422.
34Ehle, FR, Jeraci, JL, Robertson, JB, et al. (1982) The influence of dietary fiber on digestibility, rate of passage and gastrointestinal fermentation in pigs. J Anim Sci 55, 10711081.
35Rérat, A, Fiszlewicz, M, Giusi, A, et al. (1987) Influence of meal frequency on postprandial variations in the production and absorption of volatile fatty acids in the digestive tract of conscious pigs. Anim Sci 64, 448456.
36Argenzio, RA & Stevens, CE (1984) The large intestine bowel – a supplementary rumen. Proc Nutr Soc 43, 1323.
37von Engelhardt, W, Bartels, J, Kirschberger, S, et al. (1998) Role of short-chain fatty acids in the hind gut. Vet Q 20, 5259.
38Allison, C & Macfarlane, T (1989) Influence of pH, nutrient availability and growth rate on amine production by Bacteroides fragilis and Clostridium perfringens. Appl Environ Microbiol 55, 28942898.
39Cummings, JH & Englyst, HN (1987) Fermentation in the human large intestine and the available substrates. Am J Clin Nutr 4, 12431255.
40Louis, P, Scott, KP, Duncan, SH, et al. (2007) Understanding the effects of diet on bacterial metabolism in the large intestine. J Appl Microbiol 102, 11971208.
41Wright, RS, Anderson, JW & Bridges, SR (1990) Propionate inhibits hepatocyte lipid synthesis. Exp Biol Med 195, 2629.
42Vogt, JA, Pencharz, PB & Wolever, TMS (2004) l-Rhamnose increases serum propionate in humans. Am J Clin Nutr 80, 8994.
43Pryde, SE, Duncan, SH, Hold, GL, et al. (2002) The microbiology of butyrate formation in the human colon. FEMS Microbiol Lett 17, 133139.
44Aminov, RI, Walker, AW, Duncan, SH, et al. (2006) Molecular diversity, cultivation, and improved detection by fluorescent in situ hybridization of a dominant group of human gut bacteria related to Roseburia spp. or Eubacterium rectale. Appl Anim Ethol 72, 63716376.
45Asahara, T, Shimizu, K, Nomoto, K, et al. (2001) Antibacterial effect of fermented milk containing Bifidobacterium breve, Bifidobacterium bifidum and Lactobacillus acidophilus against indigenous Escherichia coli infection in mice. Microb Ecol Health Dis 13, 1624.
46Zoetendal, EG, Akkermans, ADL & de Vos, WM (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, 38543859.
47Zoetendal, EG, von Wright, A, Vilpponen-Salmela, T, et al. (2002) Mucosa-associated bacteria in the human gastrointestinal tract are uniformly distributed along the colon and differ from the community recovered from feces. Appl Environ Microbiol 68, 34013407.
48Zoetendal, EG, Vaughan, EE & de Vos, WM (2006) A microbial world within us. Mol Microbiol 6, 16391650.
49Zoetendal, EG, Rajilic-Stojanovic, M & de Vos, WM (2008) High throughput diversity and functionality analysis of the gastrointestinal tract microbiota. Gut 57, 16051615.
50Sghir, A, Gramet, G, Suau, A, et al. (2000) Quantification of bacterial groups within human fecal flora by oligonucleotide probe hybridization. Appl Environ Microbiol 6, 22632266.
51Doré, J & Corthier, G (2010) The human intestinal microbiota. Gastroenterol Clin Biol 34, S7S15.
52Harmsen, HJ, Raangs, GC, He, T, et al. (2002) Extensive set of 16S rRNA-based probes for detection of bacteria in human feces. Appl Environ Microbiol 6, 29822990.
53Rigottier-Gois, L, Bourhis, AG, Gramet, G, et al. (2003) Fluorescent hybridisation combined with flow cytometry and hybridisation of total RNA to analyse the composition of microbial communities in human faeces using 16S rRNA probes. FEMS Microbiol Ecol 43, 237245.
54Flint, HJ, Duncan, SH, Scott, KP, et al. (2007) Interactions and competition within the microbial community of the human colon: links between diet and health. Environ Microbiol 9, 11011111.
55Playne, M (1994) Probiotic foods. Food Aust 46, 362364.
56Lay, C, Sutren, M, Rochet, V, et al. (2005) Design and validation of 16S rRNA probes to enumerate members of the Clostridium leptum subgroup in human faecal microbiota. Environ Microbiol 7, 933946.
57Mueller, S, Saunier, K, Hanisch, C, et al. (2006) Differences in fecal microbiota in different European study populations in relation to age, gender, and country: a cross-sectional study. Appl Environ Microbiol 72, 10271033.
58Reuter, G (2001) The Lactobacillus and Bifidobacterium microflora of the human intestine: composition and succession. Curr Issues Intest Microbiol 2, 4353.
59Fallani, M, Young, D, Scott, J, et al. (2010) The intestinal microbiota of 6-week-old infants across Europe: geographic influence beyond delivery mode, breastfeeding and antibiotics. J Pediatr Gastroenterol Nutr 51, 7784.
60Moore, WEC, Moore, LVH, Cato, EP, et al. (1987) Effect of high-fiber and high-oil diets on the fecal flora of swine. Appl Environ Microbiol 53, 16381644.
61Stewart, CS (1997) Microorganisms in hindgut fermentors. In Gastrointestinal Microbiology, vol. 2, pp. 142186 [Mackie, RI, White, BA and Isaacson, RE, editors]. New York: Chapman and Hall.
62Gaskins, HR (2001) Intestinal bacteria and their influence on swine growth. In Swine Nutrition, pp. 585608 [Lewis, AJ and Southern, LL, editors]. Boca Raton: CRC Press.
63Jensen, BB (2001) Possible ways of modifying type and amount of products from microbial fermentation in the gut. In Gut Environment of Pigs, pp. 181200 [Piva, A, Bach Knudsen, KE and Lindberg, JE, editors]. Nottingham: Nottingham University Press.
64van der Klis, JD & Jansman, AJM (2002) Optimising nutrient digestion, absorption and gut barrier function in monogastrics: reality or illusion? In Nutrition and Health of the Gastrointestinal Tract, pp. 1536 [Blok, MC, Vahl, HA, de Lange, L, van de Braak, AE, Hemke, G and Hessing, M, editors]. Wageningen: Wageningen Academic Publishers.
65Hopwood, DE & Hampson, DJ (2003) Interactions between the intestinal microflora, diet and diarrhoea, and their influences on piglet health in the immediate post-weaning period. In Weaning the Pig: Concepts and Consequences, pp. 199218 [Pluske, JR, Le Dividich, J and Verstegen, MWA, editors]. Wageningen: Wageningen Academic Publishers.
66Kim, HB, Borewicz, K, White, BA, et al. (2011) Longitudinal investigation of the age-related bacterial diversity in the feces of commercial pigs. Vet Microbiol 153, 124133.
67Petri, D, Hill, JE & Van Kessel, AG (2010) Microbial succession in the gastrointestinal tract (GIT) of the preweaned pig. Livest Sci 133, 107109.
68Pieper, R, Janczyk, P, Zeyner, A, et al. (2008) Ecophysiology of the total and Lactobacillus communities in the terminal small intestine of weaning piglets. Microb Ecol 56, 474483.
69Loh, G, Eberhard, M, Brunner, RM, et al. (2006) Inulin alters the intestinal microbiota and short-chain fatty acid concentrations in growing pigs regardless of their basal diet. J Nutr 136, 11981202.
70Mikkelsen, LL, Bendixen, C, Jakobsen, M, et al. (2003) Enumeration of bifidobacteria in gastrointestinal samples from piglets. Appl Environ Microbiol 69, 654658.
71Simpson, PJ, Stanton, C, Fitzgerald, GF, et al. (2003) Genomic diversity and relatedness of bifidobacteria isolated from a porcine cecum. J Bacteriol 185, 25712581.
72Krause, DO, Easter, RA, White, BA, et al. (1995) Effect of weaning diet on the ecology of adherent lactobacilli in the gastrointestinal tract of the pig. J Anim Sci 73, 23472354.
73Leser, TD, Lindecrona, RH, Jensen, TK, et al. (2000) Changes in bacterial community structure in the colon of pigs fed different experimental diets and after infection with Brachyspira hyodysenteriae. Appl Environ Microbiol 66, 32903296.
74Mariat, D, Firmesse, O, Levenez, F, et al. (2009) The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BMC Microbiol 9, 123.
75Hooper, LV, Littman, DR & Macpherson, AJ (2012) Interactions between the microbiota and the immune system. Science 336, 12681273.
76Bezirtzoglou, E (1997) The intestinal microflora during the first weeks of life. Anaerobe 3, 173177.
77Gronlund, MM, Lehtonen, OP, Eerola, E, et al. (1999) Fecal microflora in healthy infants born by different methods of delivery: permanent changes in intestinal flora after cesarean delivery. J Pediatr Gastroenterol Nutr 28, 1925.
78Penders, J, Thijs, C, Vink, C, et al. (2006) Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics 118, 511521.
79Susick, EK, Putnam, M, Bermudez, DM, et al. (2012) Longitudinal study comparing the dynamics of Clostridium difficile in conventional and antimicrobial free pigs at farm and slaughter. Vet Microbiol 157, 172178.
80Heavey, PM & Rowland, IR (1999) The gut microbiology of the developing infant: microbiology and metabolism. Microbiol Ecol Health Dis 11, 7583.
81Yoshioka, H, Iseki, K & Fujita, K (1983) Development and differences of intestinal flora in the neonatal period in breast-fed and bottle-fed infants. Pediatrics 72, 317321.
82Kunz, C & Rudloff, S (1993) Biological functions of oligosaccharides in human milk. Acta Paediatr 82, 903912.
83Newburg, DS (1999) Human milk glycoconjugates that inhibit pathogens. Curr Med Chem 6, 117127.
84Langendijk, PS, Schut, F, Jansen, GJ, et al. (1995) Quantitative fluorescence in situ hybridisation of Bifidobacterium spp. with genus-specific 16S rRNA-targeted probes and its application in fecal samples. Appl Environ Microbiol 61, 30693075.
85Heikkilä, MP & Saris, PEJ (2003) Inhibition of Staphylococcus aureus by the commensal bacteria of human milk. J Appl Microbiol 95, 471478.
86West, PA, Hewitt, JH & Murphy, OM (1979) Influence of methods of collection and storage on the bacteriology of human milk. J Appl Microbiol 46, 269277.
87Kirjavainen, PV, Apostolou, E, Arvola, T, et al. (2001) Characterizing the composition of intestinal microflora as a prospective treatment target in infant allergic disease. FEMS Immunol Med Microbiol 32, 17.
88Favier, C, Vaughan, EE, De Vos, WM, et al. (2002) Molecular monitoring of succession of bacterial communities in human neonates. Appl Environ Microbiol 68, 219226.
89Pieper, R, Janczyk, P, Schumann, R, et al. (2006) The intestinal microflora of piglets around weaning with emphasis on lactobacilli. Arch Zootech 9, 2840.
90Montagne, L, Arturo-Schaan, M, Le Floc'h, N, et al. (2010) Effect of sanitary conditions and dietary fibre on the adaptation of gut microbiota after weaning. Livest Sci 133, 113116.
91Thangaraju, M, Cresci, GA, Liu, K, et al. (2009) GPR109A is a G-proteincoupled receptor for the bacterial fermentation product butyrate and functions as a tumor suppressor in colon. Cancer Res 69, 28262832.
92Duncan, SH, Louis, P & Flint, HJ (2004) Lactate-utilizing bacteria, isolated from human feces, that produce butyrate as a major fermentation product. Appl Environ Microbiol 70, 58105817.
93Watson, TS & Bertram, JM (1983) Some observations on mother–infant interactions in the pig (Sus scrofa). Appl Anim Ethol 9, 253.
94Gleed, PT & Sansom, BF (1982) Ingestion of iron in sow's feces by piglets reared in farrowing crates with slatted floors. Br J Nutr 47, 113117.
95Schmidt, B, Mulder, IE, Musk, CC, et al. (2011) Establishment of normal gut microbiota is compromised under excessive hygiene conditions. PLoS ONE 6, e28284.
96Lunney, JK (2007) Advances in swine biomedical model genomics. Int J Biol Sci 3, 179184.
97Lamendella, R, Domingo, JW, Ghosh, S, et al. (2011) Comparative fecal metagenomics unveils unique functional capacity of the swine gut. BMC Microbiol 11, 103.
98Nabuurs, MJA (1998) Weaning piglets as a model for studying pathophysiology of diarrhoea. Vet Q 20, 4245.
99Fujiwara, S, Hashiba, H, Hirota, T, et al. (1997) Proteinaceous factor(s) in culture supernatant fluids of bifidobacteria which prevents the binding of enterotoxigenic Escherichia coli to gangliotetraosylceramide. Appl Environ Microbiol 63, 506512.
100Gordon, JE, Chitkara, ID & Wyon, JB (1963) Weanling diarrhoea. Am J Med Sci 245, 129160.
101Nabuurs, MJA, van Zijderveld, FG & de Leeuw, PW (1993) Clinical and microbiological field studies in the Netherlands of diarrhoea in pigs at weaning. Res Vet Sci 55, 7077.
102Nataro, JP & Kaper, JB (1998) Diarrhoeagenic Escherichia coli. Clin Microbiol Rev 11, 142201.
103Gaastra, W & de Graaf, FK (1982) Host-specific fimbrial adhesions of noninvasive enterotoxigenic Escherichia coli strains. Microbiol Rev 46, 129161.
104de Zoysa, I, Rea, M & Martines, J (1991) Why promote breast-feeding in diarrhoeal disease control programmes? Health Policy Plan 6, 371379.
105Newburg, DS (2005) Innate immunity and human milk. J Nutr 135, 13081312.
106Lara-Villoslada, F, Olivares, M, Sierra, S, et al. (2007) Beneficial effects of probiotic bacteria isolated from breast milk. Br J Nutr 98, Suppl. 1, S96S100.
107Wagstrom, EA, Yoon, KJ & Zimmerman, JJ (2000) Immune components in porcine mammary secretions. Viral Immunol 13, 383397.
108Martín, R, Delgado, S, Maldonado, A, et al. (2009) Isolation of lactobacilli from sow milk and evaluation of their probiotic potential. J Dairy Res 76, 418425.
109Cummins, AG, Steele, TW, LaBrooy, JT, et al. (1988) Maturation of the rat small intestine at weaning: changes in epithelial cell kinetics, bacterial flora, and mucosal immune activity. Gut 29, 16721679.
110Pluske, JR, Hampson, DJ & Williams, IH (1997) Factors influencing the structure and function of the small intestine in the weaned pig: a review. Livest Prod Sci 51, 215236.
111Lecce, JG, Clare, DA, Balsbaugh, RK, et al. (1983) Effect of dietary regimen on rotavirus–Escherichia coli weanling diarrhoea of piglets. J Clin Microbiol 17, 689695.
112Parashar, UD, Bresee, JS, Gentsch, JR, et al. (1998) Rotavirus. Emerg Infect Dis 4, 561570.
113Parashar, UD, Gibson, C, Bresee, JS, et al. (2006) Rotavirus and severe childhood diarrhoea. Emerg Infect Dis 12, 304306.
114Ramig, RF (2004) Pathogenesis of intestinal and systemic rotavirus infection. J Virol 78, 1021310220.
115Shu, Q, Freeman, Q & Harsharnjit, SG (2001) Probiotic treatment using Bifidobacterium lactis HN019 reduces weanling diarrhoea associated with rotavirus and Escherichia coli infection in a piglet model. J Pediatr Gastroenterol Nutr 33, 171177.
116Gill, HS & Guarner, F (2004) Probiotics and human health: a clinical perspective. Postgrad Med J 80, 516526.
117Lallès, JP, Bosi, P, Smidt, H, et al. (2007) Nutritional management of gut health in pigs around weaning. Proc Nutr Soc 66, 260268.
118Szajewska, H & Mrukowicz, JZ (2001) Probiotics in the treatment and prevention of acute infectious diarrhoea in infants and children: a systematic review of published randomized, double-blind, placebo-controlled trials. J Pediatr Gastroenterol Nutr 33, S17S25.
119Gill, HS, Rutherford, KJ, Prasad, J, et al. (2000) Enhancement of natural and acquired immunity by Lactobacillus rhamnosus (HN001), Lactobacillus acidophilus (HN017) and Bifidobacterium lactis (HN019). Br J Nutr 83, 167176.
120Arunachalam, K, Gill, HS & Chandra, RK (2000) Enhancement of natural immune function by dietary consumption of Bifidobacterium lactis (HN019). Eur J Clin Nutr 54, 263267.
121Schroeder, B, Duncker, S, Barth, S, et al. (2006) Preventive effects of the probiotic Escherichia coli strain Nissle 1917 on acute secretory diarrhoea in a pig model of intestinal infection. Dig Dis Sci 51, 724731.
122Eisenberg, PG (1993) Causes of diarrhea in tube-fed patients: a comprehensive approach to diagnosis and management. Nutr Clin Pract 8, 119123.
123Brown, DR, Overend, MF & Treder, BG (1990) Neurohormonal regulation of ion transport in the porcine distal jejunum. Actions of somatostatin-14 and its natural and synthetic homologs. J Pharmacol Exp Ther 252, 126134.
124Eto, B, Boisset, M & Desjeux, JF (1996) Sodium fluoride inhibits the antisecretory effect of peptide YY and its analog in rabbit jejunum. Arch Physiol Biochem 104, 180184.
125Cermak, R, Follmer, U & Wolffram, S (1998) Dietary flavonol quercetin induces chloride secretion in rat colon. Am J Physiol 275, G1166G1172.
126Patterson, JK, Yasuda, K, Welch, RM, et al. (2010) Supplemental dietary inulin of variable chain lengths alters intestinal bacterial populations in young pigs. J Nutr 140, 21582161.
127Buddington, RK, Williams, CH, Chen, S, et al. (1996) A dietary supplement of neosugar alters the fecal flora and decrease s activities of some reductive enzymes in human subjects. Am J Clin Nutr 63, 709716.
128Donovan, SM, Wang, M, Li, M, et al. (2012) Host–microbe interactions in the neonatal intestine: role of human milk oligosaccharides. Adv Nutr 3, 450S455S.
129Herfel, TM, Jacobi, SK, Lin, X, et al. (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, 21392145.
130Herfel, TM, Jacobi, SK, Lin, X, et al. (2009) Safety evaluation of polydextrose in infant formula using a suckling piglet model. Food Chem Toxicol 47, 15301537.
131Kien, CL, Chang, JC, Cooper, JR, et al. (2004) Effects of prefeeding a prebiotic on diarrhoea and colonic cell proliferation in piglets fed lactulose. J Parenter Enteral Nutr 28, 2226.
132Kien, CL, Murray, RD, Qualman, SJ, et al. (1999) Lactulose feeding in piglets: a model for persistent diarrhoea and colitis induced by severe sugar malabsorption. Dig Dis Sci 44, 14761484.
133Flourie, B, Briet, F, Florent, C, et al. (1993) Can diarrhoea induced by lactulose be reduced by prolonged ingestion of lactulose? Am J Clin Nutr 58, 369375.
134Torrallardona, D, Conde, MR, Badiola, I, et al. (2003) Effect of fishmeal replacement with spray-dried animal plasma and colistin on intestinal structure, intestinal microbiology, and performance of weanling pigs challenged with Escherichia coli K99. J Anim Sci 81, 12201226.
135Toda, M, Okubo, S, Ikagai, H, et al. (1992) The protective activity of tea catechins against experimental-infection by Vibrio cholerae. Microbiol Immunol 36, 9991001.
136Ishihara, N, Chu, DC, Akachi, S, et al. (2001) Improvement of intestinal microflora balance and prevention of digestive and respiratory organ diseases in calves by green tea extracts. Livest Prod Sci 68, 217229.
137Bruins, MJ, Cermak, R, Kiers, JL, et al. (2006) In vivo and in vitro effects of tea extracts on enterotoxigenic Escherichia coli-induced intestinal fluid loss in animal models. J Pediatr Gastroenterol Nutr 43, 459469.
138Terada, A, Hara, H, Nakajyo, S, et al. (1993) Effect of supplements of tea polyphenols on the cecal flora and cecal metabolites of chicks. Microb Ecol Health Dis 6, 39.
139Hara, H, Orita, N, Hatano, S, et al. (1995) Effect of tea polyphenols on fecal flora and fecal metabolic products of pigs. J Vet Med Sci 57, 4549.
140Ishihara, N & Akachi, S (1997) Green tea extract as a remedy for diarrhoea in farm-raised calves. In Chemistry and Applications of Green Tea, pp. 137144 [Yamamoto, T, Juneja, LR, Chu, DC and Kim, M, editors]. Boca Raton: CRC Press LLC.
141Hara, Y (1997) Influence of tea catechins on the digestive tract. J Cell Biochem Suppl 27, 5258.
142Friedman, M (2007) Overview of antibacterial, antitoxin, antiviral, and antifungal activities of tea flavonoids and teas. Mol Nutr Food Res 51, 116134.
143Neilands, JB (1995) Siderophores – structure and function of microbial iron transport compounds. J Biol Chem 270, 2672326726.
144Bruins, MJ, Vente-Spreeuwenberg, MAM, Smits, CH, et al. (2011) Black tea reduces diarrhoea prevalence but decreases growth performance in enterotoxigenic Escherichia coli-infected post-weaning piglets. Anim Physiol Anim Nutr 95, 388398.
145Ngure, FM, Wanyoko, JK, Mahungu, SM, et al. (2009) Catechins depletion patterns in relation to theaflavin and thearubigins formation. Food Chem 115, 814.
146Neu, J & Weiss, MD (1999) Necrotizing enterocolitis: pathophysiology and prevention. J Parenter Enteral Nutr 23, S13S17.
147Sangild, PT (2006) Gut responses to enteral nutrition in preterm infants and animals. Exp Biol Med (Maywood) 231, 16951711.
148Neu, J (1996) Necrotizing enterocolitis – the search for a unifying pathogenic theory leading to prevention. Pediatr Clin North Am 43, 409432.
149Travadi, JN, Patole, SK & Simmer, K (2003) Gastric pneumatosis in neonates: revisited. J Paediatr Child Health 39, 560562.
150Lee, JS & Polin, RA (2003) Treatment and prevention of necrotizing enterocolitis. Semin Neonatol 8, 449459.
151Siggers, RH, Siggers, J, Thymann, T, et al. (2011) Nutritional modulation of the gut microbiota and immune system in preterm neonates susceptible to necrotizing enterocolitis. J Nutr Biochem 22, 511521.
152Hoy, CM, Wood, CM, Hawkey, PM, et al. (2000) Duodenal microflora in very-low-birth-weight neonates and relation to necrotizing enterocolitis. J Clin Microbiol 38, 45394547.
153de la Cochetiere, MF, Piloquet, H, des Robert, C, et al. (2004) Early intestinal bacterial colonization and necrotizing enterocolitis in premature infants: the putative role of Clostridium. Pediatr Res 56, 366370.
154Jiang, P, Sangild, PT, Siggers, RH, et al. (2010) Bacterial colonization affects the intestinal proteome of preterm pigs susceptible to necrotizing enterocolitis. Neonatology 99, 280288.
155Cilieborg, MS, Boye, M, Molbak, L, et al. (2011) Preterm birth and necrotizing enterocolitis alter gut colonization in pigs. Pediatr Res 69, 1016.
156Sangild, PT, Siggers, RH, Schmidt, M, et al. (2006) Diet and colonization-dependent intestinal dysfunction predisposes to necrotizing enterocolitis in preterm pigs. Gastroenterology 130, 17761792.
157Darragh, AJ & Moughan, PJ (1995) The three-week-old piglet as a model animal for studying protein digestion in human infants. J Pediatr Gastroenterol Nutr 21, 387393.
158Bjornvad, CR, Thymann, T, Deutz, NE, et al. (2008) Enteral feeding induces diet-dependent mucosal dysfunction, bacterial proliferation, and necrotizing enterocolitis in preterm pigs on parenteral nutrition. Am J Physiol Gastrointest Liver Physiol 295, G1092G1103.
159Siggers, RH, Siggers, J, Boye, M, et al. (2008) Early administration of probiotics alters bacterial colonization and limits diet-induced gut dysfunction and severity of necrotizing enterocolitis in preterm pigs. J Nutr 138, 14371444.
160Braegger, CHP (2009) Probiotika bei Früh- und Neugeborenen (Probiotics in premature and newborn). In Probiotika, Präbiotika und Synbiotika (Probiotics, Prebiotics and Synbiotics), pp. 283288 [Bischoff, SC, editor]. Stuttgart: Georg Thieme Verlag KG.
161Westerbeek, EAM, van den Berg, A & Lafeber, HN (2006) The intestinal bacterial colonisation in preterm infants: a review of the literature. Clin Nutr 25, 361368.
162Claud, EC & Walker, WA (2001) Hypothesis: inappropriate colonization of the premature intestine can cause neonatal necrotizing enterocolitis. FASEB J 15, 13981403.
163Lin, J (2004) Too much short chain fatty acids cause neonatal necrotizing enterocolitis. Med Hypotheses 62, 291293.
164Peng, LY, He, ZJ, Chen, W, et al. (2007) Effects of butyrate on intestinal barrier function in a Caco-2 cell monolayer model of intestinal barrier. Pediatr Res 61, 3741.
165Dierick, NA, Decuypere, JA, Molly, K, et al. (2002) The combined use of triacylglycerols containing medium-chain fatty acids (MCFAs) and exogenous lipolytic enzymes as an alternative for nutritional antibiotics in piglet nutrition I. In vitro screening of the release of MCFAs from selected fat sources by selected exogenous lipolytic enzymes under simulated pig gastric conditions and their effects on the gut flora of piglets. Livest Prod Sci 75, 129142.
166Zentek, J, Buchheit-Renko, S, Manner, K, et al. (2012) Intestinal concentrations of free and encapsulated dietary medium-chain fatty acids and effects on gastric microbial ecology and bacterial metabolic products in the digestive tract of piglets. Arch Anim Nutr 66, 1426.
167Clark, DA, Thompson, JE, Weiner, LB, et al. (1985) Necrotizing enterocolitis: intraluminal biochemistry in human neonates and a rabbit model. Pediatr Res 19, 919921.
168Lin, J, Nafday, SM, Chauvin, SN, et al. (2002) Variable effects of short chain fatty acids and lactic acid in inducing intestinal mucosal injury in newborn rats. J Pediatr Gastroenterol Nutr 35, 545550.
169Pender, SF, Quinn, JJ & Sanderson, IR (2000) Butyrate upregulates stromelysin-1 production by intestinal mesenchymal cells. Am J Physiol Gastrointest Liver Physiol 279, G918G924.
170Butel, MJ, Roland, N, Hibert, A, et al. (1998) Clostridial pathogenicity in experimental necrotising enterocolitis in gnotobiotic quails and protective role of bifidobacteria. J Med Microbiol 47, 391399.
171Bin-Nun, A, Bromiker, R, Wilschanski, M, et al. (2005) Oral probiotics prevent necrotizing enterocolitis in very low birth weight neonates. J Pediatr 147, 192196.
172Lin, HC, Su, BH, Chen, AC, et al. (2005) Oral probiotics reduce the incidence and severity of necrotizing enterocolitis in very low birth weight infants. Pediatrics 115, 14.
173Hoyos, AB (1999) Reduced incidence of necrotizing enterocolitis associated with enteral administration of Lactobacillus acidophilus and Bifidobacterium infantis to neonates in an intensive care unit. Int J Infect Dis 3, 197202.
174Cilieborg, MS, Thymann, T, Siggers, R, et al. (2011) The incidence of necrotizing enterocolitis is increased following probiotic administration to preterm pigs. J Nutr 14, 223230.
175Land, MH, Rouster-Stevens, K, Woods, CR, et al. (2005) Lactobacillus sepsis associated with probiotic therapy. Pediatrics 115, 178181.
176Ohishi, A, Takahashi, S, Ito, Y, et al. (2010) Bifidobacterium septicemia associated with postoperative probiotic therapy in a neonate with omphalocele. J Pediatr 156, 679681.
177Wagner, RD, Warner, T, Roberts, L, et al. (1997) Colonization of congenitally immunodeficient mice with probiotic bacteria. Infect Immun 65, 33453351.
178Cilieborg, MS, Boye, M & Sangild, PT (2012) Bacterial colonization and gut development in preterm neonates. Early Hum Dev 88, S41S49.
179World Health Organization (2012) Obesity and overweight: key facts (accessed accessed January 2013).
180Fleissner, CK, Huebel, N, Abd El-Bary, MM, et al. (2010) Absence of intestinal microbiota does not protect mice from diet-induced obesity. Br J Nutr 104, 919929.
181Greiner, T & Bäckhed, F (2011) Effects of the gut microbiota on obesity and glucose homeostasis. Trends Endocrinol Metab 22, 117123.
182Schwiertz, A, Taras, D, Schafer, K, et al. (2010) Microbiota and SCFA in lean and overweight healthy subjects. Obesity 18, 190195.
183Nadal, I, Santacruz, A, Marcos, A, et al. (2009) Shifts in clostridia, Bacteroides and immunoglobulin-coating fecal bacteria associated with weight loss in obese adolescents. Int J Obes (Lond) 33, 758767.
184Turnbaugh, PJ, Hamady, M, Yatsunenko, T, et al. (2009) A core gut microbiome in obese and lean twins. Nature 457, 480484.
185Kalliomäki, M, Collado, MC, Salminen, S, et al. (2008) Early differences in fecal microbiota composition in children may predict overweight. Am J Clin Nutr 87, 534538.
186Arner, P (2005) Resistin: yet another adipokine tells us that men are not mice. Diabetologia 48, 22032205.
187Torres-Rovira, L, Astiz, S, Caro, A, et al. (2012) Diet-induced swine model with obesity/leptin resistance for the study of metabolic syndrome and type 2 diabetes. Scientific World Journal 2012, 510149.
188O'Hea, EK & Leveille, GA (1969) Significance of adipose tissue and liver as sites of fatty acid synthesis in the pig and the efficiency of utilization of various substrates for lipogenesis. J Nutr 99, 338344.
189Letexier, D, Pinteur, C, Large, V, et al. (2003) Comparison of the expression and activity of the lipogenic pathway in human and rat adipose tissue. J Lipid Res 44, 21272134.
190Mitchell, AD (2007) Impact of research with cattle, pigs, and sheep on nutritional concepts: body composition and growth. J Nutr 137, 711714.
191Ley, RE, Turnbaugh, PJ, Klein, S, et al. (2006) Microbial ecology: human gut microbes associated with obesity. Nature 444, 10221023.
192Pedersen, R, Ingerslev, HC, Sturek, M, et al. (2013) Characterisation of gut microbiota in Ossabaw and Göttingen minipigs as models of obesity and metabolic syndrome. PLOS ONE 8, e56612.
193Luo, Y, Su, Y, Wright, ADG, et al. (2012) Lean breed Landrace pigs harbor fecal methanogens at higher diversity and density than obese breed Erhualian pigs. Archaea 2012, 605289.
194Johnson, KA & Johnson, DE (1995) Methane emissions from cattle. J Anim Sci 73, 24832492.
195Armougom, F, Henry, M & Vialettes, B (2009) Monitoring bacterial community of human gut microbiota reveals an increase in Lactobacillus in obese patients and methanogens in anorexic patients. PLoS ONE 4, e7125.
196He, Q, Ren, P & Kong, X (2012) Comparison of serum metabolite compositions between obese and lean growing pigs using an NMR-based metabonomic approach. J Nutr Biochem 23, 133139.
197Rezzi, S, Ramadan, Z, Fay, LB, et al. (2007) Nutritional metabonomics: applications and perspectives. J Proteome Res 6, 513525.
198Li, M, Wang, B, Zhang, M, et al. (2008) Symbiotic gut microbes modulate human metabolic phenotypes. Proc Natl Acad Sci U S A 105, 21172122.
199Varel, VH, Pond, WG, Pekas, JC, et al. (1982) Influence of high-fibre diet on bacterial populations in gastrointestinal tracts of obese- and lean genotype pigs. Appl Environ Microbiol 44, 107112.
200Abrams, SA, Griffin, IJ, Hawthorne, KM, et al. (2007) Effect of prebiotic supplementation and calcium intake on body mass index. J Pediatr 151, 293298.
201Kadooka, Y, Sato, M, Imaizumi, K, et al. (2010) Regulation of abdominal adiposity by probiotics (Lactobacillus gasseri SBT2055) in adults with obese tendencies in a randomized controlled trial. Eur J Clin Nutr 64, 636643.
202Cani, PD, Neyrinck, AM, Fava, F, et al. (2007) Selective increases of bifidobacteria in gut microbiota improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia 50, 23742383.
203An, HM, Park, SY, Lee, DK, et al. (2011) Antiobesity and lipid-lowering effects of Bifidobacterium spp. in high fat diet-induced obese rats. Lipids Health Dis 10, 116.
204Luoto, R, Kalliomaki, M, Laitinen, K, et al. (2010) The impact of perinatal probiotic intervention on the development of overweight and obesity: follow-up study from birth to 10 years. Int J Obes (Lond) 34, 15311537.
205Turnbaugh, PJ, Baeckhed, F, Fulton, L, et al. (2008) Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 3, 213223.
206Wall, R, Ross, RP, Shanahan, F, et al. (2009) Metabolic activity of the enteric microbiota influences the fatty acid composition of murine and porcine liver and adipose tissues. Am J Clin Nutr 89, 13931401.
207Nagao, K, Inoue, N, Wang, YM, et al. (2005) Dietary conjugated linoleic acid alleviates nonalcoholic fatty liver disease in Zucker (fa/fa) rats. J Nutr 135, 913.
208Loguercio, C, Federico, A, Tuccillo, C, et al. (2005) Beneficial effects of a probiotic VSL#3 on parameters of liver dysfunction in chronic liver diseases. J Clin Gastroenterol 39, 540543.
209Baillie, RA, Takada, R, Nakamura, M, et al. (1999) Coordinate induction of peroxisomal acyl-CoA oxidase and UCP-3 by dietary fish oil: a mechanism for decreased body fat deposition. Prostaglandins Leukot Essent Fatty Acids 60, 351356.
210Huber, J, Loffler, M, Bilban, M, et al. (2007) Prevention of high-fat diet-induced adipose tissue remodeling in obese diabetic mice by n-3 polyunsaturated fatty acids. Int J Obes 31, 10041013.
211Kabir, M, Skurnik, G, Naour, N, et al. (2007) Treatment for 2 mo with n-3 polyunsaturated fatty acids reduces adiposity and some atherogenic factors but does not improve insulin sensitivity in women with type 2 diabetes: a randomized controlled study. Am J Clin Nutr 86, 16701679.
212Hill, AM, Buckley, JD, Murphy, KJ, et al. (2007) Combining fish-oil supplements with regular aerobic exercise improves body composition and cardiovascular disease risk factors. Am J Clin Nutr 85, 12671274.
213Kratz, M, Callahan, HS & Yang, PY (2009) Dietary n-3-polyunsaturated fatty acids and energy balance in overweight or moderately obese men and women: a randomized controlled trial. Nutr Metab 6, 2431.
214Nielsen, S, Nielsen, DS, Lauritzen, L, et al. (2007) Impact of diet on the intestinal microbiota in 10-month-old infants. J Pediatr Gastroenterol Nutr 44, 613618.
215Bayerdorffer, EH, Oertel, N, Lehn, G, et al. (1989) Topographic association between active gastritis and Campylobacter pylori colonisation. J Clin Pathol 42, 834839.
216Graham, GY (1989) Campylobacter pylori and peptic ulcer disease. Gastroenterology 96, 615625.
217Kusters, JG, van Vliet, AHM & Kuipers, EJ (2006) Pathogenesis of Helicobacter pylori infection. Clin Microbiol Rev 19, 449490.
218Oozeer, R, Goupil-Feuillerat, N, Alpert, CA, et al. (2002) Lactobacillus casei is able to survive and initiate protein synthesis during its transit in the digestive tract of human flora-associated mice. Appl Environ Microbiol 68, 35703574.
219Gerard, P, Beguet, F, Lepercq, P, et al. (2004) Gnotobiotic rats harboring human intestinal microbiota as a model for studying cholesterol-to-coprostanol conversion. FEMS Microbiol Ecol 47, 337343.
220Pang, X, Hua, X, Yang, Q, et al. (2007) Inter-species transplantation of gut microbiota from human to pigs. ISME J 1, 156162.
221Che, C, Pang, X, Hua, X, et al. (2009) Effects of human fecal flora on intestinal morphology and mucosal immunity in human flora-associated piglet. Scand J Immunol 69, 223233.
222Shen, J, Zhang, B, Wei, H, et al. (2010) Assessment of the modulating effects of fructo-oligosaccharides on fecal microbiota using human flora-associated piglets. Arch Microbiol 192, 959968.
223Groenen, MAM, Archibald, AL, Uenishi, H, et al. (2012) Pig genomes provide insight into porcine demography and evolution. Nature 491, 393398.
224Anonymous (1997) Consensus meeting on cereals, fiber and colorectal and breast cancers. ECP Consensus Panel on Cereals and Cancer. Eur J Cancer Prev 6, 512514.
225Weisburger, JH, Reddy, BS, Rose, DP, et al. (1993) Protective mechanisms of dietary fibers in nutritional carcinogenesis. Basic Life Sci 61, 4563.
226Velazquez, OC, Seto, RW, Bain, AM, et al. (1997) Deoxycholate inhibits in vivo butyrate-mediated BrDU labeling of the colonic crypt. J Surg Res 69, 344348.
227Le Gall, M, Serena, A, Jørgensen, H, et al. (2009) The role of whole wheat grain and wheat and rye ingredients on the digestion and fermentation processes in the gut – a model experiment with pigs. Br J Nutr 102, 15901600.



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