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The effect of a diet with fructan-rich chicory roots on intestinal helminths and microbiota with special focus on Bifidobacteria and Campylobacter in piglets around weaning

Published online by Cambridge University Press:  04 January 2011

A. N. Jensen ,
H. Mejer ,
L. Mølbak ,
M. Langkjær ,
T. K. Jensen ,
Ø. Angen ,
T. Martinussen ,
K. Klitgaard ,
D. L. Baggesen  and
S. M. Thamsborg
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A. N. Jensen*
Affiliation:
Division of Microbiology and Risk Assessment, National Food Institute, Technical University of Denmark, Bülowsvej 27, DK-1790 Copenhagen V, Denmark
H. Mejer
Affiliation:
Department of Veterinary Disease Biology, Faculty of Life Sciences, University of Copenhagen, Dyrlægevej 100, DK-1870 Frederiksberg C, Denmark
L. Mølbak
Affiliation:
Division of Veterinary Diagnostics and Research, National Veterinary Institute, Technical University of Denmark, Bülowsvej 27, DK-1790 Copenhagen V, Denmark
M. Langkjær
Affiliation:
Department of Veterinary Disease Biology, Faculty of Life Sciences, University of Copenhagen, Dyrlægevej 100, DK-1870 Frederiksberg C, Denmark
T. K. Jensen
Affiliation:
Division of Veterinary Diagnostics and Research, National Veterinary Institute, Technical University of Denmark, Bülowsvej 27, DK-1790 Copenhagen V, Denmark
Ø. Angen
Affiliation:
Division of Veterinary Diagnostics and Research, National Veterinary Institute, Technical University of Denmark, Bülowsvej 27, DK-1790 Copenhagen V, Denmark
T. Martinussen
Affiliation:
Research Unit of Statistics, University of Southern Denmark, J. B. Winsløws Vej, 5000 Odense C, Denmark
K. Klitgaard
Affiliation:
Division of Veterinary Diagnostics and Research, National Veterinary Institute, Technical University of Denmark, Bülowsvej 27, DK-1790 Copenhagen V, Denmark
D. L. Baggesen
Affiliation:
Division of Microbiology and Risk Assessment, National Food Institute, Technical University of Denmark, Bülowsvej 27, DK-1790 Copenhagen V, Denmark
S. M. Thamsborg
Affiliation:
Department of Veterinary Disease Biology, Faculty of Life Sciences, University of Copenhagen, Dyrlægevej 100, DK-1870 Frederiksberg C, Denmark
A. Roepstorff
Affiliation:
Department of Veterinary Disease Biology, Faculty of Life Sciences, University of Copenhagen, Dyrlægevej 100, DK-1870 Frederiksberg C, Denmark
*
†E-mail: [email protected]
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Abstract

The restrictions on the use of antibiotic and anthelmintic treatments in organic pig farming necessitate alternative non-medical control strategies. Therefore, the antibiotic and parasite-reducing effect of a fructan-rich (prebiotic) diet of dried chicory was investigated in free-ranging piglets. Approximately half of 67 piglets from nine litters were experimentally infected with Ascaris suum and Trichuris suis in the suckling period (1 to 7 weeks of age) and 58 of the piglets were challenged daily with Eschericiacoli O138:F8 for 9 days after weaning to induce weaning diarrhoea. The litters were fed either chicory (30% dry matter) or a control diet. The effect of chicory on intestinal helminths, intestinal microbiota, especially Bifidobacteria and Campylobacter spp. and E. coli post-weaning diarrhoea was assessed. The weight gain of the piglets was not impaired significantly by chicory. The intestinal A. suum worm burden was reduced by 64% (P = 0.034) in the chicory-fed piglets, whereas these same piglets had 63% more T. suis worms (P = 0.016). Feeding with chicory elicited no changes among the main bacterial groups in ileum according to terminal restriction fragment length polymorphism analysis. However, the terminal-restriction fragment (T-RF) 208 bp, which may belong to Lachnospiraceae, was stimulated by the chicory feed (P = 0.03), and T-RF 370 bp that matches Enterobacter belonging to the Enterobacteria was reduced (P = 0.004). In addition, chicory increased the level of Bifidobacteria (P = 0.001) and the faecal Campylobacter excretion level was transitorily reduced in chicory-fed piglets at 7 weeks of age (P = 0.029). Unfortunately, it was not possible to assess the effect of chicory on post-weaning diarrhoea as it did not develop. In conclusion, feeding piglets chicory around the time of weaning caused complex changes of the microbiota and parasite communities within the intestinal tract, and feeding piglets chicory may therefore serve as an animal-friendly strategy to control pathogens.

Keywords

Ascaris suumCampylobacterchicoryTrichuris suisBifidobacteriumweaningdiarrhoea
Type
Full Paper
Information
animal , Volume 5 , Issue 6 , June 2011 , pp. 851 - 860
Copyright
Copyright © The Animal Consortium 2011

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References

Bach Knudsen, KE, Hessov, I 1995. Recovery of inulin from Jerusalem artichoke (Helianthus tuberosus L.) in the small intestine of man. British Journal of Nutrition 74, 101–113.Google Scholar
Bosscher, D, Loo, JV, Franck, A 2006. Inulin and oligofructose as prebiotics in the prevention of intestinal infections and diseases. Nutrition Research Reviews 19, 216–226.CrossRefGoogle ScholarPubMed
Delroisse, JM, Boulvin, AL, Parmentier, I, Dauphin, RD, Vandenbol, M, Portetelle, D 2008. Quantification of Bifidobacterium spp. and Lactobacillus spp. in rat fecal samples by real-time PCR. Microbiological Research 163, 663–670.CrossRefGoogle ScholarPubMed
Diggle, PJ, Liang, KY, Zeger, SL 1994. Analysis of longitudinal data. Oxford University Press, Oxford, UK.Google Scholar
Duncan, SH, Aminov, RI, Scott, KP, Louis, P, Stanton, TB, Flint, HJ 2006. Proposal of Roseburia faecis sp. nov., Roseburia hominis sp. nov. and Roseburia inulinivorans sp. nov., based on isolates from human faeces. International Journal of Systematic and Evolutionary Microbiology 56, 2437–2441.Google Scholar
Falony, G, Vlachou, A, Verbrugghe, K, De Vuyst, L 2006. Cross-feeding between Bifidobacterium longum BB536 and acetate-converting, butyrate-producing colon bacteria during growth on oligofructose. Applied and Environmental Microbiology 72, 7835–7841.CrossRefGoogle ScholarPubMed
Frydendahl, K, Imberechts, H, Lehmann, S 2001. Automated 5’ nuclease assay for detection of virulence factors in porcine Escherichia coli. Molecular and Cellular Probes 15, 151–160.Google Scholar
Frydendahl, K, Kåre Jensen, T, Strodl Andersen, J, Fredholm, M, Evans, G 2003. Association between the porcine Escherichia coli F18 receptor genotype and phenotype and susceptibility to colonisation and post-weaning diarrhoea caused by E. coli O138:F18. Veterinary Microbiology 93, 39–51.Google Scholar
Gibson, GR, Wang, X 1994. Regulatory effects of bifidobacteria on the growth of other colonic bacteria. The Journal of Applied Bacteriology 77, 412–420.Google Scholar
Grizard, D, Barthomeuf, C 1999. Non-digestible oligosaccharides used as prebiotic agents: mode of production and beneficial effects on animal and human health. Reproduction Nutrition Development 39, 563–588.CrossRefGoogle ScholarPubMed
Halas, D, Hansen, CF, Hampson, DJ, Mullan, BP, Wilsen, RH, Pluske, JR 2009. Effect of dietary supplementation with inulin and/or benzoic acid on the incidence and severity of post-weaning diarrhoea in weaner pigs after experimental challenge with enterotoxigenic Echerichia coli. Archives of Animal Nutrition 63, 267–280.CrossRefGoogle ScholarPubMed
Hale, OM, Stewart, TB 1979. Influence of an experimental infection of Trichuris suis on performance of pigs. Journal of Animal Science 49, 1000–1005.CrossRefGoogle ScholarPubMed
Hale, OM, Stewart, TB, Marti, OG 1985. Influence of an experimental infection of Ascaris suum on performance of pigs. Journal of Animal Science 60, 220–225.Google Scholar
Hansen, LL, Mejer, H, Thamsborg, SM, Byrne, DV, Roepstorff, A, Karlsson, AH, Hansen-Møller, J, Jensen, MT, Tuomola, M 2006. Influence of chicory roots (Cichorium intybus L.) on boar taint in entire male and female pigs. Animal Science 82, 359–368.CrossRefGoogle Scholar
Jensen, BB, Jørgensen, H 1994. Effect of dietary fiber on microbial activity and microbial gas production in various regions of the gastrointestinal tract of pigs. Applied and Environmental Microbiology 60, 1897–1904.Google Scholar
Jensen, AN, Lodal, J, Baggesen, DL 2004. High diversity of Salmonella serotypes found in an experiment with outdoor pigs. Wageningen Journal of Life Sciences 52, 109–117.Google Scholar
Jensen, AN, Dalsgaard, A, Baggesen, DL, Nielsen, EM 2006. The occurrence and characterization of Campylobacter jejuni and C. coli in organic pigs and their outdoor environment. Veterinary Microbiology 116, 96–105.Google Scholar
Kenworthy, R, Crabb, WE 1963. The intestinal flora of young pigs, with reference to early weaning, Escherichia coli and scours. Journal of Comparative Pathology 73, 215–228.Google Scholar
Kringel, H, Roepstorff, A 2006. Trichuris suis population dynamics following a primary experimental infection. Veterinary Parasitology 139, 132–139.Google Scholar
Kringel, H, Roepstorff, A, Murrell, KD 2002. A method for the recovery of immature Trichuris suis from pig intestine. Acta Veterinaria Scandinavica 43, 185–189.Google Scholar
Leser, TD, Amenuvor, JZ, Jensen, TK, Lindecrona, RH, Boye, M, Moller, K 2002. Culture-independent analysis of gut bacteria: the pig gastrointestinal tract microbiota revisited. Applied and Environmental Microbiology 68, 673–690.Google Scholar
Liang, KY, Zeger, SL 1986. Longitudinal data analysis using generalized linear models. Biometrika 73, 13–22.Google Scholar
Mansfield, LS, Gauthier, DT, Abner, SR, Jones, KM, Wilder, SR, Urban, JF 2003. Enhancement of disease and pathology by synergy of Trichuris suis and Campylobacter jejuni in the colon of immunologically naive swine. The American Journal of Tropical Medicine and Hygiene 68, 70–80.Google Scholar
Mejer, H 2006. Transmission, infection dynamics and alternative control of helminths in organic swine. PhD thesis. The Royal Veterinary and Agricultural University, Copenhagen, Denmark.Google Scholar
Mølbak, L, Thomsen, LE, Jensen, TK, Bach Knudsen, KE, Boye, M 2007. Increased amount of Bifidobacterium thermacidophilum and Megasphaera elsdenii in the colonic microbiota of pigs fed a swine dysentery preventive diet containing chicory roots and sweet lupine. Journal of Applied Microbiology 103, 1853–1867.Google Scholar
Murrell, KD, Eriksen, L, Nansen, P, Slotved, HC, Rasmussen, T 1997. Ascaris suum: a revision of its early migratory path and implications for human ascariasis. The Journal of Parasitology 83, 255–260.Google Scholar
Palmer, C, Bik, EM, DiGiulio, DB, Relman, DA, Brown, PO 2007. Development of the human infant intestinal microbiota. PLoS biology 5, 1556–1573.Google Scholar
Pedersen, S, Saeed, I, Michaelsen, KF, Friis, H, Murrell, KD 2002. Impact of protein energy malnutrition on Trichuris suis infection in pigs concomitantly infected with Ascaris suum. Parasitology 124, 561–568.Google Scholar
Petkevičius, S, Bach Knudsen, KE, Murrell, KD, Wachmann, H 2003. The effect of inulin and sugar beet fibre on Oesophagostomum dentatum infection in pigs. Parasitology 127, 61–68.Google Scholar
Petkevičius, S, Thomsen, LE, Bach Knudsen, KE, Murrell, KD, Roepstorff, A, Boes, J 2007. The effect of inulin on new and on patent infections of Trichuris suis in growing pigs. Parasitology 134, 121–127.Google Scholar
Petkevičius, S, Murrell, KD, Bach Knudsen, KE, Jørgensen, H, Roepstorff, A, Laue, A, Wachmann, H 2004. Effects of short-chain fatty acids and lactic acids on survival of Oesophagostomum dentatum in pigs. Veterinary Parasitology 122, 293–301.Google Scholar
Pluske, JR, Hampson, DJ, Williams, IH 1997. Factors influencing the structure and function of the small intestine in the weaned pig: a review. Livestock Production Science 51, 215–236.CrossRefGoogle Scholar
Roepstorff, A, Nansen, P 1998. Epidemiology, diagnosis and control of helminth parasites of swine. A FAO handbook. FAO, Rome, Italy.Google Scholar
Roepstorff, A, Eriksen, L, Slotved, HC, Nansen, P 1997. Experimental Ascaris suum infection in the pig: worm population kinetics following single inoculations with three doses of infective eggs. Parasitology 115, 443–452.Google Scholar
Santini, C, Baffoni, L, Gaggia, F, Granata, M, Gasbarri, R, Di Gioia, D, Biavati, B 2010. Characterization of probiotic strains: an application as feed additives in poultry against Campylobacter jejuni. International Journal of Food Microbiology 141, S98–S108.Google Scholar
Schoeni, JL, Wong, AC 1994. Inhibition of Campylobacter jejuni colonization in chicks by defined competitive exclusion bacteria. Applied and Environmental Microbiology 60, 1191–1197.Google Scholar
Shyu, C, Soule, T, Bent, SJ, Foster, JA, Forney, LJ 2007. MiCA: a web-based tool for the analysis of microbial communities based on terminal-restriction fragment length polymorphisms of 16S and 18S rRNA Genes. Microbial Ecology 53, 562–570.Google Scholar
Slotved, HC, Barnes, EH, Eriksen, L, Roepstorff, A, Nansen, P, Bjorn, H 1997. Use of an agar-gel technique for large scale application to recover Ascaris suum larvae from intestinal contents of pigs. Acta Veterinaria Scandinavica 38, 207–212.Google Scholar
Thamsborg, SM, Roepstorff, A 2003. Parasite problems in organic livestock production systems and options for control. Journal of Parasitology 89, 277–284.Google Scholar
Thomsen, LE, Petkevičius, S, Bach Knudsen, KE, Roepstorff, A 2005. The influence of dietary carbohydrates on experimental infection with Trichuris suis in pigs. Parasitology 131, 857–865.Google Scholar
Thomsen, LE, Bach Knudsen, KE, Jensen, TK, Christensen, AS, Møller, K, Roepstorff, A 2007. The effect of fermentable carbohydrates on experimental swine dysentery and whip worm infections in pigs. Veterinary Microbiology 119, 152–163.CrossRefGoogle ScholarPubMed
Weijtens, MJ, Bijker, PG, Van der Plas, J, Urlings, HA, Biesheuvel, MH 1993. Prevalence of campylobacter in pigs during fattening; an epidemiological study. The Veterinary Quarterly 15, 138–143.Google Scholar
Young, CR, Harvey, R, Anderson, R, Nisbet, D, Stanker, LH 2000. Enteric colonisation following natural exposure to Campylobacter in pigs. Research in Veterinary Science 68, 75–78.CrossRefGoogle ScholarPubMed