Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-23T01:10:10.119Z Has data issue: false hasContentIssue false
  • English
  • Français

Population dynamics of Trichuris suis in trickle-infected pigs

Published online by Cambridge University Press:  16 April 2009

P. NEJSUM ,
S. M. THAMSBORG ,
H. H. PETERSEN ,
H. KRINGEL ,
M. FREDHOLM  and
A. ROEPSTORFF
P. NEJSUM*
Affiliation:
Danish Centre for Experimental Parasitology, Department of Veterinary Disease Biology, Copenhagen University Genetics and Bioinformatics, Department of Animal and Veterinary Basic Sciences, Faculty of Life Sciences, Copenhagen University
S. M. THAMSBORG
Affiliation:
Danish Centre for Experimental Parasitology, Department of Veterinary Disease Biology, Copenhagen University
H. H. PETERSEN
Affiliation:
Danish Centre for Experimental Parasitology, Department of Veterinary Disease Biology, Copenhagen University
H. KRINGEL
Affiliation:
Danish Centre for Experimental Parasitology, Department of Veterinary Disease Biology, Copenhagen University
M. FREDHOLM
Affiliation:
Genetics and Bioinformatics, Department of Animal and Veterinary Basic Sciences, Faculty of Life Sciences, Copenhagen University
A. ROEPSTORFF
Affiliation:
Danish Centre for Experimental Parasitology, Department of Veterinary Disease Biology, Copenhagen University
*
*Corresponding author: Danish Centre for Experimental Parasitology, Department of Veterinary Disease Biology, Faculty of Life Sciences, University of Copenhagen, Dyrlaegevej 100, DK-1870, Frederiksberg C, Copenhagen, Denmark. Tel: +45 35283783. Fax: +45 35282774. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The population dynamics of Trichuris suis in pigs was studied during long-term experimental infections. Twenty-three 10-week-old pigs were inoculated with 5 T. suis eggs/kg/day. Seven, 8, and 8 pigs were necropsied at weeks 4, 8, and 14 post-start of infection (p.i.), respectively. The median numbers of worms in the colon were 538 (min–max: 277–618), 332 (14–1140) and 0 (0–4) at 4, 8, and 14 weeks p.i. respectively, suggesting an increased aggregation of the worms with time and acquisition of nearly sterile immunity. The serum levels of T. suis specific antibodies (IgG1, IgG2 and IgA) peaked at week 8 p.i. By week 14 p.i. the IgG2 and IgA antibody levels remained significantly elevated above the level of week 0. The population dynamics of T. suis trickle infections in pigs is discussed with focus on interpretation of diagnostic and epidemiological data of pigs, the use of pigs as a model for human Trichuris trichiura infections and the novel approach of using T. suis eggs in the treatment of patients with inflammatory bowel disease.

Keywords

Trichuris suispigpopulation dynamicstrickle infectionaggregationELISA
Type
Research Article
Information
Parasitology , Volume 136 , Issue 6 , May 2009 , pp. 691 - 697
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Beer, R. J. S. (1973). Studies on the biology of the life-cycle of Trichuris suis Schrank, 1788. Parasitology 67, 253–262.CrossRefGoogle ScholarPubMed
Beer, R. J. S. (1976). Relationship between Trichuris trichiura (Linnaeus 1758) of man and Trichuris suis (Schrank 1788) of pig. Research in Veterinary Science 20, 47–54.CrossRefGoogle ScholarPubMed
Blackwell, N. M. and Else, K. J. (2002). A comparison of local and peripheral parasite-specific antibody production in different strains of mice infected with Trichuris muris. Parasite Immunology 24, 203–211.CrossRefGoogle ScholarPubMed
Boes, J. and Helwigh, A. B. (2000). Animal models of intestinal nematode infections of humans. Parasitology 121, S97–S111.CrossRefGoogle ScholarPubMed
Bundy, D. A. P. and Cooper, E. S. (1989). Trichuris and Trichuriasis in humans. Advances in Parasitology 28, 107–173.CrossRefGoogle ScholarPubMed
Carstensen, L., Vaarst, M. and Roepstorff, A. (2002). Helminth infections in Danish organic swine herds. Veterinary Parasitology 106, 253–264.CrossRefGoogle ScholarPubMed
Chan, M. S., Medley, G. F., Jamison, D. and Bundy, D. A. P. (1994). The evaluation of potential global morbidity attributable to intestinal nematode infections. Parasitology 109, 373–387.CrossRefGoogle ScholarPubMed
Crawley, A., Raymond, C. and Wilkie, B. N. (2003). Control of immunoglobulin isotype production by porcine B-cells cultured with cytokines. Veterinary Immunology and Immunopathology 91, 141–154.CrossRefGoogle ScholarPubMed
Eijck, I. A. J. M. and Borgsteede, F. H. M. (2005). A survey of gastrointestinal pig parasites on free-range, organic and conventional pig farms in The Netherlands. Veterinary Research Communications 29, 407–414.CrossRefGoogle ScholarPubMed
Elliott, D. E., Summers, R. W. and Weinstock, J. V. (2007). Helminths as governors of immune-mediated inflammation. International Journal for Parasitology 37, 457–464.CrossRefGoogle ScholarPubMed
Eriksen, L., Nansen, P., Roepstorff, A., Lind, P. and Nilsson, O. (1992). Response to repeated inoculations with Ascaris suum eggs in pigs during the fattening period. I. Studies on worm population kinetics. Parasitology Research 78, 241–246.CrossRefGoogle ScholarPubMed
Helwigh, A. B., Christensen, C. M., Roepstorff, A. and Nansen, P. (1999). Concurrent Ascaris suum and Oesophagostomum dentatum infections in pigs. Veterinary Parasitology 82, 221–234.CrossRefGoogle ScholarPubMed
Hill, D. E., Romanowski, R. D. and Urban, J. F. Jr. (1997). A Trichuris specific diagnostic antigen from culture fluids of Trichuris suis adult worms. Veterinary Parasitology 68, 91–102.CrossRefGoogle ScholarPubMed
Jacobs, D. E. and Dunn, A. M. (1969). Helminths of Scottish pigs: occurrence, age incidences and seasonal variations. Journal of Helminthology 43, 327–340.CrossRefGoogle ScholarPubMed
Jensen, T. K. and Svensmark, B. (1996). Trichuriasis hos udendørs slagtesvin (in Danish). Veterinær Information 2, 3–7.Google Scholar
Joachim, A., Dulmer, N., Daugschies, A. and Roepstorff, A. (2001). Occurrence of helminths in pig fattening units with different management systems in Northern Germany. Veterinary Parasitology 96, 135–146.CrossRefGoogle ScholarPubMed
Kradin, R. L., Badizadegan, K., Auluck, P., Korzenik, J. and Lauwers, G. Y. (2006). Iatrogenic Trichuris suis infection in a patient with Crohn disease. Archives of Pathology and Laboratory Medicine 130, 718–720.CrossRefGoogle Scholar
Kringel, H. and Roepstorff, A. (2006). Trichuris suis population dynamics following a primary experimental infection. Veterinary Parasitology 139, 132–139.CrossRefGoogle ScholarPubMed
Kringel, H., Iburg, T., Dawson, H., Aasted, B. and Roepstorff, A. (2006). A time course study of immunological responses in Trichuris suis infected pigs demonstrates induction of a local type 2 response associated with worm burden. International Journal for Parasitology 36, 915–924.CrossRefGoogle ScholarPubMed
Kringel, H. and Roepstorff, A. (2007). Trichuris suis excretory/secretory antigen-specific antibodies in serum from single-inoculated pigs. Parasite Immunology 29, 327–330.CrossRefGoogle ScholarPubMed
Kringel, H., Roepstorff, A. and Murrell, K. D. (2002). A method for the recovery of immature Trichuris suis from pig intestine. Acta Veterinaria Scandinavica 43, 185–189.Google ScholarPubMed
Lillywhite, J. E., Bundy, D. A., Didier, J. M., Cooper, E. S. and Bianco, A. E. (1991). Humoral immune responses in human infection with the whipworm Trichuris trichiura. Parasite Immunology 13, 491–507.CrossRefGoogle ScholarPubMed
Marufu, M. C., Chanayiwa, P., Chimonyo, M. and Bhebhe, E. (2008). Prevalence of gastrointestinal nematodes in Mukota pigs in a communal area of Zimbabwe. African Journal of Agricultural Research 3, 91–95.Google Scholar
Miller, E. R. and Ullrey, D. E. (1987). The pig as a model for human nutrition. Annual Review of Nutrition 7, 361–382.CrossRefGoogle Scholar
Miquel, N., Roepstorff, A., Bailey, M. and Eriksen, L. (2005). Host immune reactions and worm kinetics during the expulsion of Ascaris suum in pigs. Parasite Immunology 27, 79–88.CrossRefGoogle ScholarPubMed
Nejsum, P., Roepstorff, A., Jørgensen, C. B., Fredholm, M., Göring, H. H. H., Anderson, T. J. C. and Thamsborg, S. M. (2009 a). High heritability for Ascaris and Trichuris infection levels in pigs. Heredity. Advance online publication, January 14, 2009. doi:10.1038/hdy.2008.131CrossRefGoogle ScholarPubMed
Nejsum, P., Thamsborg, S. M., Petersen, H. H., Fredholm, M. and Roepstorff, A. (2009 b). Population dynamics of Ascaris suum in trickle infected pigs. Journal of Parasitology (in the Press).Google ScholarPubMed
Pedersen, S. and Saeed, I. (2000). Experimental infection of pigs with three dose levels of Trichuris suis. Parasite 7, 275–281.CrossRefGoogle ScholarPubMed
Pedersen, S., Saeed, I., Michaelsen, K. F., Friis, H. and Murrell, K. D. (2002). Impact of protein energy malnutrition on Trichuris suis infection in pigs concomitantly infected with Ascaris suum. Parasitology 124, 561–568.CrossRefGoogle ScholarPubMed
Permin, A., Yelifari, L., Bloch, P., Steenhard, N., Hansen, N. P. and Nansen, P. (1999). Parasites in cross-bred pigs in the upper east region of Ghana. Veterinary Parasitology 87, 63–71.CrossRefGoogle ScholarPubMed
Roepstorff, A., Bjørn, H., Nansen, P., Barnes, E. H. and Christensen, C. M. (1996). Experimental Oesophagostomum dentatum infections in the pig: worm populations resulting from trickle infections with three dose levels of larvae. International Journal for Parasitology 26, 399–408.CrossRefGoogle ScholarPubMed
Roepstorff, A., Eriksen, L., Slotved, H. C. and 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.CrossRefGoogle ScholarPubMed
Roepstorff, A., Jørgensen, R. J., Nansen, P., Henriksen, S. A., Skovgaard-Petersen, J. and Andreasen, M. (1992). Parasitter hos økologiske svin (in Danish). Landsudvalget for Svin, Danske Slagterier. Copenhagen1–36.Google Scholar
Roepstorff, A. and Murrell, K. D. (1997). Transmission dynamics of helminth parasites of pigs on continuous pasture: Ascaris suum and Trichuris suis. International Journal for Parasitology 27, 563–572.CrossRefGoogle ScholarPubMed
Roepstorff, A. and Nansen, P. (1994). Epidemiology and control of helminth infections in pigs under intensive and non-intensive production systems. Veterinary Parasitology 54, 69–85.CrossRefGoogle ScholarPubMed
Roepstorff, A. and Nansen, P. (1998). The Epidemiology, Diagnosis and Control of Helminth Parasites in Swine. An FAO Handbook FAO, Rome, Italy.Google Scholar
Roepstorff, A., Nilsson, O., Oksanen, A., Gjerde, B., Richter, S. H., Ortenberg, E., Christensson, D., Martinsson, K. B., Bartlett, P. C., Nansen, P., Eriksen, L., Helle, O., Nikander, S. and Larsen, K. (1998). Intestinal parasites in swine in the Nordic countries: prevalence and geographical distribution. Veterinary Parasitology 76, 305–319.CrossRefGoogle ScholarPubMed
Steenhard, N. R., Kringel, H., Roepstorff, A., Thamsborg, S. M. and Jungersen, G. (2007). Parasite-specific IL-4 responses in Ascaris suum and Trichuris suis-infected pigs evaluated by ELISPOT. Parasite Immunology 29, 535–538.CrossRefGoogle ScholarPubMed
Stephenson, L. S., Holland, C. V. and Cooper, E. S. (2000). The public health significance of Trichuris trichiura. Parasitology 121, S73–S95.CrossRefGoogle ScholarPubMed
Summers, R. W., Elliott, D. E., Urban, J. F., Thompson, R. and Weinstock, J. V. (2005 a). Trichuris suis therapy in Crohn's disease. Gut 54, 87–90.CrossRefGoogle ScholarPubMed
Summers, R. W., Elliott, D. E. and Weinstock, J. V. (2005 b). Trichuris suis therapy for ulcerative colitis: nonresponsive patients may need anti-helminth therapy. Gastroenterology 129, 769.CrossRefGoogle Scholar
Summers, R. W., Elliott, D. E. and Weinstock, J. V. (2006). Therapeutic colonization with Trichuris suis. Archives of Pathology and Laboratory Medicine 130, 1753–1754.CrossRefGoogle ScholarPubMed
Tamboura, H. H., Banga-Mboko, H., Maes, D., Youssao, I., Traore, A., Bayala, B. and Dembele, M. A. (2006). Prevalence of common gastrointestinal nematode parasites in scavenging pigs of different ages and sexes in eastern centre province, Burkina Faso. The Onderstepoort Journal of Veterinary Research 73, 53–60.CrossRefGoogle ScholarPubMed
Urban, J. F., Alizadeh, H. and Romanowski, R. D. (1988). Ascaris suum – development of intestinal immunity to infective 2nd-stage larvae in swine. Experimental Parasitology 66, 66–77.CrossRefGoogle Scholar
Weng, Y. B., Hu, Y. J., Li, Y., Li, B. S., Lin, R. Q., Xie, D. H., Gasser, R. B. and Zhu, X. Q. (2005). Survey of intestinal parasites in pigs from intensive farms in Guangdong Province, People's Republic of China. Veterinary Parasitology 127, 333–336.CrossRefGoogle ScholarPubMed