Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-23T22:59:36.218Z Has data issue: false hasContentIssue false
  • English
  • Français

Anthelmintic activity of chicory (Cichorium intybus): in vitro effects on swine nematodes and relationship to sesquiterpene lactone composition

Published online by Cambridge University Press:  03 March 2016

ANDREW R. WILLIAMS ,
MIGUEL A. PEÑA-ESPINOZA ,
ULRIK BOAS ,
HENRIK T. SIMONSEN Open the ORCID record for HENRIK T. SIMONSEN [Opens in a new window] ,
HEIDI L. ENEMARK  and
STIG M. THAMSBORG
ANDREW R. WILLIAMS*
Affiliation:
Department of Veterinary Disease Biology, University of Copenhagen, Frederiksberg C, Denmark
MIGUEL A. PEÑA-ESPINOZA
Affiliation:
National Veterinary Institute, Technical University of Denmark, Frederiksberg C, Denmark
ULRIK BOAS
Affiliation:
National Veterinary Institute, Technical University of Denmark, Frederiksberg C, Denmark
HENRIK T. SIMONSEN
Affiliation:
Department of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg C, Denmark
HEIDI L. ENEMARK
Affiliation:
National Veterinary Institute, Technical University of Denmark, Frederiksberg C, Denmark
STIG M. THAMSBORG
Affiliation:
Department of Veterinary Disease Biology, University of Copenhagen, Frederiksberg C, Denmark
*
*Corresponding author: Department of Veterinary Disease Biology, University of Copenhagen, Frederiksberg C, Denmark. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Chicory is a perennial crop that has been investigated as a forage source for outdoor-reared ruminants and pigs, and has been reported to have anthelmintic properties. Here, we investigated in vitro anthelmintic effects of forage chicory-extracts against the highly prevalent swine parasites Ascaris suum and Oesophagostomum dentatum. Methanol extracts were prepared and purified from two different cultivars of chicory (Spadona and Puna II). Marked differences were observed between the anthelmintic activity of extracts from the two cultivars. Spadona extracts had potent activity against A. suum third (L3) and fourth (L4) – stage larvae, as well as O. dentatum L4 and adults, whereas Puna II extracts had less activity against A. suum and no activity towards O. dentatum L4. Transmission-electron microscopy of A. suum L4 exposed to Spadona extracts revealed only subtle changes, perhaps indicative of a specific anthelmintic effect rather than generalized toxicity. Ultra-high liquid chromatography-mass spectrometry analysis revealed that the purified extracts were rich in sesquiterpene lactones (SL), and that the SL profile differed significantly between cultivars. This is the first report of anthelmintic activity of forage chicory towards swine nematodes. Our results indicate a significant anthelmintic effect, which may possibly be related to SL composition.

Keywords

ChicoryanthelminticAscaris suumOesophagostomum dentatumsesquiterpene lactones
Type
Research Article
Information
Parasitology , Volume 143 , Issue 6 , May 2016 , pp. 770 - 777
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

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

Bardón, A., Popich, S., Valdés, D. A. and Catalán, C. A. N. (1999). Toxic effects of a lactone-containing fraction of Cyrtocymura cincta (Asteraceae) on Sitotroga cerealella (Lepidoptera: Gelechiidae). Journal of Economic Entomology 92, 1369–1372.CrossRefGoogle Scholar
Cavin, C., Delannoy, M., Malnoe, A., Debefve, E., Touché, A., Courtois, D. and Schilter, B. (2005). Inhibition of the expression and activity of cyclooxygenase-2 by chicory extract. Biochemical and Biophysical Research Communications 327, 742–749.CrossRefGoogle ScholarPubMed
Charlier, J., van der Voort, M., Kenyon, F., Skuce, P. and Vercruysse, J. (2014). Chasing helminths and their economic impact on farmed ruminants. Trends in Parasitology 30, 361–367.CrossRefGoogle ScholarPubMed
Ernst, M., Chatterton, N. J. and Harrison, P. A. (1995). Carbohydrate changes in chicory (Cichorium intybus L. var. foliosum) during growth and storage. Scientia Horticulturae 63, 251–261.CrossRefGoogle Scholar
Ferioli, F. and D'Antuono, L. F. (2012). An update procedure for an effective and simultaneous extraction of sesquiterpene lactones and phenolics from chicory. Food Chemistry 135, 243–250.CrossRefGoogle Scholar
Fitzpatrick, J. L. (2013). Global food security: the impact of veterinary parasites and parasitologists. Veterinary Parasitology 195, 233–248.CrossRefGoogle ScholarPubMed
Foster, J. G., Cassida, K. A. and Turner, K. E. (2011). In vitro analysis of the anthelmintic activity of forage chicory (Cichorium intybus L.) sesquiterpene lactones against a predominantly Haemonchus contortus egg population. Veterinary Parasitology 180, 298–306.CrossRefGoogle ScholarPubMed
Haugegaard, J. (2010). Prevalence of nematodes in Danish industrialized sow farms with loose housed sows in dynamic groups. Veterinary Parasitology 168, 156–159.CrossRefGoogle ScholarPubMed
Hoste, H., Martinez-Ortiz-De-Montellano, C., Manolaraki, F., Brunet, S., Ojeda-Robertos, N., Fourquaux, I., Torres-Acosta, J. F. J. and Sandoval-Castro, C. A. (2012). Direct and indirect effects of bioactive tannin-rich tropical and temperate legumes against nematode infections. Veterinary Parasitology 186, 18–27.CrossRefGoogle ScholarPubMed
Ivarsson, E., Liu, H. Y., Dicksved, J., Roos, S. and Lindberg, J. E. (2012). Impact of chicory inclusion in a cereal-based diet on digestibility, organ size and faecal microbiota in growing pigs. Animal 6, 1077–1085.CrossRefGoogle Scholar
Jensen, A. N., Mejer, H., Mølbak, L., Langkjær, M., Jensen, T. K., Angen, Ø., Martinussen, T., Klitgaard, K., Baggesen, D. L., Thamsborg, S. M. and Roepstorff, A. (2011). 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. Animal 5, 851–860.CrossRefGoogle ScholarPubMed
Kidane, A., Houdijk, J. G. M., Athanasiadou, S., Tolkamp, B. J. and Kyriazakis, I. (2010). Effects of maternal protein nutrition and subsequent grazing on chicory (Cichorium intybus) on parasitism and performance of lambs1. Journal of Animal Science 88, 1513–1521.CrossRefGoogle Scholar
Kumarasingha, R., Palombo, E. A., Bhave, M., Yeo, T. C., Lim, D. S. L., Tu, C. L., Shaw, J. M. and Boag, P. R. (2014). Enhancing a search for traditional medicinal plants with anthelmintic action by using wild type and stress reporter Caenorhabditis elegans strains as screening tools. International Journal for Parasitology 44, 291–298.CrossRefGoogle ScholarPubMed
Liu, H., Ivarsson, E., Lundh, T. and Lindberg, J. (2013). Chicory (Cichorium intybus L.) and cereals differently affect gut development in broiler chickens and young pigs. Journal of Animal Science and Biotechnology 4, 50.CrossRefGoogle ScholarPubMed
Martínez-Ortíz-de-Montellano, C., Arroyo-López, C., Fourquaux, I., Torres-Acosta, J. F. J., Sandoval-Castro, C. A. and Hoste, H. (2013). Scanning electron microscopy of Haemonchus contortus exposed to tannin-rich plants under in vivo and in vitro conditions. Experimental Parasitology 133, 281–286.CrossRefGoogle ScholarPubMed
Masure, D., Vlaminck, J., Wang, T., Chiers, K., Van den Broeck, W., Vercruysse, J. and Geldhof, P. (2013). A role for eosinophils in the intestinal immunity against infective Ascaris suum larvae. PLoS Neglected Tropical Disease 7, e2138.CrossRefGoogle ScholarPubMed
Mejer, H. (2006). Transmission, Infection Dynamics and Alternative Control of Helminths in Organic Swine. Vol. Ph.D. The Royal Agricultural and Veterinary University, Copenhagen, Denmark.Google Scholar
Milala, J., Grzelak, K., Król, B., Juśkiewicz, J. and Zduńczyk, Z. (2009). Composition and properties of chicory extracts rich in fructans and polyphenols. Polish Journal of Food and Nutrition Sciences 59, 35–43.Google Scholar
Murrell, K. D., Eriksen, L., Nansen, P., Slotved, H. C. and Rasmussen, T. (1997). Ascaris suum: a revision of its early migratory path and implications for human ascariasis. The Journal of Parasitology 83, 255–260.CrossRefGoogle ScholarPubMed
Novobilský, A., Stringano, E., Hayot Carbonero, C., Smith, L. M. J., Enemark, H. L., Mueller-Harvey, I. and Thamsborg, S. M. (2013). In vitro effects of extracts and purified tannins of sainfoin (Onobrychis viciifolia) against two cattle nematodes. Veterinary Parasitology 196, 532–537.CrossRefGoogle ScholarPubMed
Oksanen, A., Eriksen, L., Roepstorff, A., Ilsøe, B., Nansen, P. and Lind, P. (1990). Embryonation and infectivity of Ascaris suum eggs. A comparison of eggs collected from worm uteri with eggs isolated from pig faeces. Acta Veterinaria Scandinavica 31, 393–398.CrossRefGoogle ScholarPubMed
Peña-Espinoza, M., Boas, U., Williams, A. R., Thamsborg, S. M., Simonsen, H. T. and Enemark, H. L. (2015). Sesquiterpene lactone containing extracts from two cultivars of forage chicory (Cichorium intybus) show distinctive chemical profiles and in vitro activity against Ostertagia ostertagi . International Journal for Parasitology: Drugs and Drug Resistance 5, 191–200.Google ScholarPubMed
Petkevičius, S., Murrell, K. D., Bach Knudsen, K. E., Jørgensen, H., Roepstorff, A., Laue, A. and Wachmann, H. (2004). Effects of short-chain fatty acids and lactic acids on survival of Oesophagostomum dentatum in pigs. Veterinary Parasitology 122, 293–301.CrossRefGoogle ScholarPubMed
Roepstorff, A., Mejer, H., Nejsum, P. and Thamsborg, S. M. (2011). Helminth parasites in pigs: new challenges in pig production and current research highlights. Veterinary Parasitology 180, 72–81.CrossRefGoogle ScholarPubMed
Sargison, N. D. (2012). Pharmaceutical treatments of gastrointestinal nematode infections of sheep – future of anthelmintic drugs. Veterinary Parasitology 189, 79–84.CrossRefGoogle ScholarPubMed
Simonsen, H., Weitzel, C. and Christensen, S. (2013). Guaianolide Sesquiterpenoids: Pharmacology and Biosynthesis. In Natural Products (ed. Ramawat, K. and Merillon, J.), pp. 3069–3098. Springer-Verlag, Berlin.CrossRefGoogle Scholar
Stewart, T. B. and Hale, O. M. (1988). Losses to internal parasites in swine production. Journal of Animal Science 66, 1548–1554.CrossRefGoogle ScholarPubMed
Thamsborg, S., Roepstorff, A., Nejsum, P. and Mejer, H. (2010). Alternative approaches to control of parasites in livestock: Nordic and Baltic perspectives. Acta Veterinaria Scandinavica 52, S27.CrossRefGoogle Scholar
Thamsborg, S. M., Nejsum, P. and Mejer, H. (2013). Chapter 14 – impact of Ascaris suum in livestock. In Ascaris: the Neglected Parasite (ed. Holland, C.), pp. 363–381. Elsevier, Amsterdam.CrossRefGoogle Scholar
Tzamaloukas, O., Athanasiadou, S., Kyriazakis, I., Huntley, J. F. and Jackson, F. (2006). The effect of chicory (Cichorium intybus) and sulla (Hedysarum coronarium) on larval development and mucosal cell responses of growing lambs challenged with Teladorsagia circumcincta . Parasitology 132, 419–426.CrossRefGoogle ScholarPubMed
Williams, A. R., Fryganas, C., Ramsay, A., Mueller-Harvey, I. and Thamsborg, S. M. (2014 a). Direct anthelmintic effects of condensed tannins from diverse plant sources against Ascaris suum . PLoS ONE 9, e97053.CrossRefGoogle ScholarPubMed
Williams, A. R., Ropiak, H. M., Fryganas, C., Desrues, O., Mueller-Harvey, I. and Thamsborg, S. M. (2014 b). Assessment of the anthelmintic activity of medicinal plant extracts and purified condensed tannins against free-living and parasitic stages of Oesophagostomum dentatum . Parasites & Vectors 7, 518.CrossRefGoogle ScholarPubMed