Effects of Cocoa Husk Feeding on the Composition of Swine Intestinal Microbiota

Journal of Agricultural and Food Chemistry

Volumn 64, Issue 10, 2016, Pages 2046-2052

  Magistrelli, Damiano ^a   Zanchi, Raffaella ^a   Malagutti, Luca ^a   Galassi, Gianluca ^a   Canzi, Enrica ^a   Rosi, Fabia ^a  

^a UNIVERSITY OF MILAN   (Italy)

Author keywords

cocoa husks; intestinal microbiota; pigs; polyphenols

Indexed keywords

FLUORESCENCE MICROSCOPY; MAMMALS; NUTRITION;

DIETARY FIBERS; FEED EFFICIENCIES; FLUORESCENCE IN SITU HYBRIDIZATION; MICROBIAL COMPOSITION; MICROBIAL POPULATIONS; MICROBIOTAS; PIGS; POLYPHENOLS;

COCOA;

ANALYSIS; ANIMAL; ANIMAL FOOD; BACTERIUM; CACAO; CHEMISTRY; CLASSIFICATION; GENETICS; INTESTINE; INTESTINE FLORA; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; PIG;

ANIMAL FEED; ANIMALS; BACTERIA; CACAO; GASTROINTESTINAL MICROBIOME; INTESTINES; SWINE;

EID: 84961780832     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.5b05732     Document Type: Article

References (56)

1. Laparra, J. M.; Sanz, Y. Interactions of gut microbiota with functional food components and nutraceuticals Pharmacol. Res. 2010, 61, 219-225 10.1016/j.phrs.2009.11.001
2. Gibson, G. R.; Probert, H. M.; Van Loo, J.; Rastall, R. A.; Roberfroid, M. B. Dietary modulation of the human colonic microbiota: Updating the concept of prebiotics Nutr. Res. Rev. 2004, 17, 259-275 10.1079/NRR200479
3. Etxeberria, U.; Fernández-Quintela, A.; Milagro, F. I.; Aguirre, L.; Martínez, J. A.; Portillo, M. P. Impact of polyphenols and polyphenol-rich dietary sources on gut microbiota composition J. Agric. Food Chem. 2013, 61, 9517-9533 10.1021/jf402506c
4. Larrosa, M.; Luceri, C.; Vivoli, E.; Pagliuca, C.; Lodovici, M.; Moneti, G.; Dolara, P. Polyphenol metabolites from colonic microbiota exert anti-inflammatory activity on different inflammation models Mol. Nutr. Food Res. 2009, 53, 1044-1054 10.1002/mnfr.200800446
5. Kemperman, R. A.; Bolca, S.; Roger, L. C.; Vaughan, E. E. Novel approaches for analysing gut microbes and dietary polyphenols: Challenges and opportunities Microbiology 2010, 156, 3224-3231 10.1099/mic.0.042127-0
6. Lee, H. C.; Jenner, A. M.; Low, C. S.; Lee, Y. K. Effect of tea phenolics and their aromatic fecal bacterial metabolites on intestinal microbiota Res. Microbiol. 2006, 157, 876-884 10.1016/j.resmic.2006.07.004
7. Zanchi, R.; Canzi, E.; Molteni, L.; Scozzoli, M. Effect of Camellia sinensis L. whole plant extract on piglet intestinal ecosystem Ann. Microbiol. 2008, 58, 147-152 10.1007/BF03179459
8. Lecumberri, E.; Mateos, R.; Izquierdo-Pulido, M.; Rupérez, P.; Goya, L.; Bravo, L. Dietary fibre composition, antioxidant capacity and physico-chemical properties of a fibre-rich product from cocoa (Theobroma cacao L.) Food Chem. 2007, 104, 948-954 10.1016/j.foodchem.2006.12.054
9. Beckett, S. T. Traditional chocolate making. In Industrial Chocolate Manufacture and Use, 4 th ed.; Beckett, S. T., Ed.; Wiley: Chichester, UK, 2009; pp 1-9.
10. Magistrelli, D.; Malagutti, L.; Rosi, F. Cocoa husks feeding improves some indices of health and welfare of pigs Indian J. Res. 2014, 3 (7) 210-213 http://worldwidejournals.com/paripex/viewinhtml.php?val=MjU0NA==&b1= D. Magistrelli, L. Malagutti, F. Rosi&k=D. Magistrelli, L. Malagutti, F. Rosi
11. Magistrelli, D.; Malagutti, L.; Galassi, G.; Rosi, F. Cocoa husks in diets of Italian heavy pigs J. Anim. Sci. 2012, 90 (Suppl. 4) 230-232 10.2527/jas.53970
12. Tuohy, K. M.; Conterno, L.; Gasperotti, M.; Viola, R. Up-regulating the human intestinal microbiome using whole plant foods, polyphenols, and/or fiber J. Agric. Food Chem. 2012, 60, 8776-8782 10.1021/jf2053959
13. Bähr, A.; Wolf, E. Domestic animal models for biomedical research Reprod. Dom. Anim. 2012, 47 (Suppl. 4) 59-71 10.1111/j.1439-0531.2012.02056.x
14. Furet, J. P.; Firmesse, O.; Gourmelon, M.; Bridonneau, C.; Tap, J.; Mondot, S.; Doré, J.; Corthier, G. Comparative assessment of human and farm animal fecal microbiota using real-time quantitative PCR FEMS Microbiol. Ecol. 2009, 68, 351-362 10.1111/j.1574-6941.2009.00671.x
15. Lee, J. E.; Lee, S.; Sung, J.; Ko, G. P. Analysis of human and animal fecal microbiota for microbial source tracking ISME J. 2011, 5, 362-365 10.1038/ismej.2010.120
16. Ferrando, R.; Blum, J. C. LAlimentation des Animaux Monogastriques: Porc, Lapin, Volaille, 2 nd ed.; INRA: Paris, France, 1989.
17. Burndred, F. Food safety in chocolate manufacture and processing. In Industrial Chocolate Manufacture and Use, 4 th ed.; Beckett, S. T., Ed.; Wiley: Chichester, UK, 2009; pp 530-550.
18. AOAC. Official Methods of Analysis, 15 th ed.; Association of Official Analytical Chemists International: Gaithersburg, MD, USA, 1995.
19. Mertens, D. R. Gravimetric determination of amylase-treated neutral detergent fiber in feeds using refluxing in beakers or crucibles: Collaborative study J. AOAC 2002, 85, 1217-1240
20. Van Soest, P. J.; Robertson, J. B.; Lewis, B. A. Methods of dietary fiber, neutral detergent fiber and non-polysaccharides in relation to animal nutrition J. Dairy Sci. 1991, 74, 3583-3597 10.3168/jds.S0022-0302(91)78551-2
21. Budini, R.; Tonelli, D.; Girotti, S. Analysis of total phenols using the Prussian Blue method J. Agric. Food Chem. 1980, 28, 1236-1238 10.1021/jf60232a056
22. Amann, R. I.; Ludwig, W.; Schleifer, K. H. Phylogenetic identification and in-situ detection of individual microbial-cells without cultivation Microbiol. Rev. 1995, 59, 143-169
23. Daims, H.; Bruhl, A.; Amann, R.; Schleifer, K. H.; Wagner, M. The domain-specific probe EUB338 is insufficient for the detection of all bacteria: Development and evaluation of a more comprehensive probe set Syst. Appl. Microbiol. 1999, 22, 434-444 10.1016/S0723-2020(99)80053-8
24. Wallner, G.; Amann, R.; Beisker, W. Optimizing fluorescent in situ hybridization with ribosomal-RNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms Cytometry 1993, 14, 136-143 10.1002/cyto.990140205
25. Harmsen, H. J. M.; Elfferich, P.; Schut, F.; Welling, G. W. A 16S rRNA-targeted probe for detection of lactobacilli and enterococci in fecal samples by fluorescent in situ hybridisation Microb. Ecol. Health Dis. 1999, 11, 3-12 10.3402/mehd.v11i1.7876
26. Manz, W.; Amann, R.; Ludwig, W. Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum cytophaga-flavobacter-bacteroides in the natural environment Microbiology 1996, 142, 1097-1106 10.1099/13500872-142-5-1097
27. Langendijk, P. S.; Schut, F.; Jansen, G. J.; Raangs, G. C.; Kamphuis, G. R.; Wilkinson, M. H.; Welling, G. W. Quantitative fluorescence in situ hybridization of Bifidobacterium spp. with genus-specific 16S rRNA-targeted probes and its application in fecal samples Appl. Environ. Microbiol. 1995, 61, 3069-3075
28. Franks, A. H.; Harmsen, H. J.; Raangs, G. C.; Jansen, G. J.; Schut, F.; Welling, G. W. Variations of bacterial populations in human feces measured by fluorescent in situ hybridization with group-specific 16S rRNA-targeted oligonucleotide probes Appl. Environ. Microbiol. 1998, 64, 3336-3345
29. Kempf, V. A.; Trebesius, K.; Autenrieth, I. B. Fluorescent in situ hybridization allows rapid identification of microorganisms in blood cultures J. Clin. Microbiol. 2000, 38, 830-838
30. Poulsen, L. K.; Lan, F.; Kristensen, C. S.; Hobolth, P.; Molin, S.; Krogfelt, K. A. Spatial distribution of Escherichia coli in the mouse large intestine inferred from rRNA in situ hybridization Infect. Immun. 1994, 62, 5191-5194
31. Suau, A.; Rochet, V.; Sghir, A.; Gramet, G.; Brewaeys, S.; Sutren, M.; Rigottier-Gois, L.; Doré, J. Fusobacterium prausnitzii and related species represent a dominant group within the human fecal flora Syst. Appl. Microbiol. 2001, 24, 139-145 10.1078/0723-2020-00015
32. Kim, H. B.; Borewicz, K.; White, B. A.; Singer, R. S.; Sreevatsan, S.; Tu, Z. J.; Isaacson, R. E. Longitudinal investigation of the age-related bacterial diversity in the feces of commercial pigs Vet. Microbiol. 2011, 153, 124-133 10.1016/j.vetmic.2011.05.021
33. Guarner, F.; Schaafsma, G. J. Probiotics Int. J. Food Microbiol. 1998, 39, 237-238 10.1016/S0168-1605(97)00136-0
34. Collins, M. D.; Gibson, G. R. Probiotics, prebiotics, and synbiotics: Approaches for modulating the microbial ecology of the gut Am. J. Clin. Nutr. 1999, 69 (Suppl.) 1052S-1057S
35. Ljungh, A.; Wadström, T. Lactic acid bacteria as probiotics Curr. Issues Intest. Microbiol. 2006, 7, 73-90
36. Sasaki, M.; Klapproth, J. M. A. The role of bacteria in the pathogenesis of ulcerative colitis. J. Signal Transduction 2012, 704953, 6 pp. 10.1155/2012/704953.
37. Foulquié Moreno, M. R.; Sarantinopoulos, P.; Tsakalidou, E.; De Vuyst, L. The role and application of enterococci in food and health Int. J. Food Microbiol. 2006, 106, 1-24 10.1016/j.ijfoodmicro.2005.06.026
38. Jin, L. Z.; Marquardt, R. R.; Zhao, X. A Strain of Enterococcus faecium (18C23) inhibits adhesion of enterotoxigenic Escherichia coli K88 to porcine small intestine mucus Appl. Environ. Microbiol. 2000, 66, 4200-4204 10.1128/AEM.66.10.4200-4204.2000
39. Teixeira, L. M.; Carvalho, M. d G. S.; Espinola, M. M. B.; Steigerwalt, A. G.; Douglas, M. P.; Brenner, D. J.; Facklam, R. R. Enterococcus porcinus sp. nov. and Enterococcus ratti sp. nov., associated with enteric disorders in animals Int. J. Syst. Evol. Microbiol. 2001, 51, 1737-1743 10.1099/00207713-51-5-1737
40. Vancanneyt, M.; Snauwaert, C.; Cleenwerck, I.; Baele, M.; Descheemaeker, P.; Goossens, H.; Pot, B.; Vandamme, P.; Swings, J.; Haesebrouck, F.; Devriese, L. A. Enterococcus villorum sp. nov., an enteroadherent bacterium associated with diarrhoea in piglets Int. J. Syst. Evol. Microbiol. 2001, 51, 393-400 10.1099/00207713-51-2-393
41. Balish, E.; Warner, T. Enterococcus faecalis induces inflammatory bowel disease in interleukin-10 knockout mice Am. J. Pathol. 2002, 160, 2253-2257 10.1016/S0002-9440(10)61172-8
42. Collado, M. C.; Sanz, Y. Characterization of the gastrointestinal mucosa-associated microbiota of pigs and chickens using culture-based and molecular methodologies J. Food Prot. 2007, 12, 2708-2934
43. Hatheway, C. L. Toxigenic Clostridia Clin. Microbiol. Rev. 1990, 3, 66-98
44. Swidsinski, A.; Loening-Baucke, V.; Herber, A. Mucosal flora in Crohns disease and ulcerative colitis-an overview J. Physiol. Pharmacol. 2009, 60 (Suppl. 6) 61-71
45. Wu, G. D.; Bushmanc, F. D.; Lewis, J. D. Diet, the human gut microbiota, and IBD Anaerobe 2013, 24, 117-120 10.1016/j.anaerobe.2013.03.011
46. Hooper, L. V.; Midtvedt, T.; Gordon, J. I. How host-microbial interactions shape the nutrient environment of the mammalian intestine Annu. Rev. Nutr. 2002, 22, 283-307 10.1146/annurev.nutr.22.011602.092259
47. Wrzosek, L.; Miquel, S.; Noordine, M. L.; Bouet, S.; Chevalier-Curt, M. J.; Robert, V.; Philippe, C.; Bridonneau, C.; Cherbuy, C.; Robbe-Masselot, C.; Langella, P.; Thomas, M. Bacteroides thetaiotaomicron and Faecalibacterium prausnitzii influence the production of mucus glycans and the development of goblet cells in the colonic epithelium of a gnotobiotic model rodent BMC Biol. 2013, 11, 61-73 10.1186/1741-7007-11-61
48. van Limpt, C.; Crienen, A.; Vriesema, A.; Knol, J. Effect of colonic short chain fatty acids and pH on the growth of pathogens and gut commensals. Book of Abstracts of the 24th International Congress of Pediatrics; Cancun, Mexico, 2004; p 487.
49. Massot-Cladera, M.; Pérez-Berezo, T.; Franch, A.; Castell, M.; Pérez-Cano, F. J. Cocoa modulatory effect on rat faecal microbiota and colonic crosstalk Arch. Biochem. Biophys. 2012, 527, 105-112 10.1016/j.abb.2012.05.015
50. Ivarsson, E. Chicory (Cichorium intybus L) as fibre source in pig diets: Effects on digestibility, gut microbiota and performance. Doctoral thesis 19, Acta Universitatis Agriculturae Sueciae, 2012, (http://pub.epsilon.slu.se/8693/1/ivarsson-emma-120416.pdf).
51. Leser, T. D.; Amenuvor, J. Z.; Jensen, T. K.; Lindecrona, R. H.; Boye, M.; Møller, K. Culture-independent analysis of gut bacteria: The pig gastrointestinal tract microbiota revisited Appl. Environ. Microbiol. 2002, 68, 673-690 10.1128/AEM.68.2.673-690.2002
52. Sokol, H.; Seksik, P.; Furet, J. P.; Firmesse, O.; Nion-Larmurier, I.; Beaugerie, L.; Cosnes, J.; Corthier, G.; Marteau, P.; Doré, J. Low counts of Faecalibacterium prausnitzii in colitis microbiota Inflamm. Bowel Dis. 2009, 15, 1183-1189 10.1002/ibd.20903
53. Pryde, S. E.; Duncan, S. H.; Hold, G. L.; Stewart, C. S.; Flint, H. J. The microbiology of butyrate formation in the human colon FEMS Microbiol. Lett. 2002, 217, 133-139 10.1111/j.1574-6968.2002.tb11467.x
54. Karlsson, F.; Tremaroli, V.; Nielsen, J.; Bäckhed, F. Assessing the human gut microbiota in metabolic diseases Diabetes 2013, 62, 3341-3349 10.2337/db13-0844
55. Ley, R. E.; Turnbaugh, P. J.; Klein, S.; Gordon, J. I. Microbial ecology: Human gut microbes associated with obesity Nature 2006, 444, 1022-1023 10.1038/4441022a
56. Magistrelli, D.; Galassi, G.; Crovetto, G. M.; Rosi, F. Influence of high levels of beet pulp in the diet on endocrine/metabolic traits, slaughter dressing percentage, and ham quality in Italian heavy pigs Ital. J. Anim. Sci. 2010, 8, 37-49 10.4081/ijas.2009.37