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Anthelmintic activity of some Mediterranean browse plants against parasitic nematodes

Published online by Cambridge University Press:  07 December 2009

F. MANOLARAKI ,
S. SOTIRAKI ,
A. STEFANAKIS ,
V. SKAMPARDONIS ,
M. VOLANIS  and
H. HOSTE
F. MANOLARAKI
Affiliation:
NAGREF-VRI NAGREF Campus, Thermi57001PO Box 60272Thessaloniki, Greece UMR 1225 INRA/ENVT. Ecole Nationale Vétérinaire de Toulouse – 23 Chemin des Capelles, 31076ToulouseCedex, France
S. SOTIRAKI
Affiliation:
NAGREF-VRI NAGREF Campus, Thermi57001PO Box 60272Thessaloniki, Greece
A. STEFANAKIS
Affiliation:
NAGREF-Subtropical Plant and Olive Tree Institute of Chania, Argokepion73100, ChaniaCreta, Greece
V. SKAMPARDONIS
Affiliation:
NAGREF-VRI NAGREF Campus, Thermi57001PO Box 60272Thessaloniki, Greece
M. VOLANIS
Affiliation:
NAGREF-Subtropical Plant and Olive Tree Institute of Chania, Argokepion73100, ChaniaCreta, Greece
H. HOSTE*
Affiliation:
UMR 1225 INRA/ENVT. Ecole Nationale Vétérinaire de Toulouse – 23 Chemin des Capelles, 31076ToulouseCedex, France
*
*Corresponding author: UMR 1225 INRA/ENVT. Ecole Nationale Vétérinaire de Toulouse – 23 Chemin des Capelles, 31076ToulouseCedex,France. Tel: +33 5 61 19 38 75. Fax: +33 5 61 19 32 43. E-mail: h.hoste@envt.fr
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Summary

The anthelmintic properties of tannin-rich plants are being explored as an alternative to chemical drugs. Most data have been acquired on legume forages, but only few on browse plants. The present study aimed to (i) screen the in vitro effects of extracts from 7 Mediterranean plants on Haemonchus contortus, (ii) verify the role of tannins using an inhibitor, polyvinyl polypyrrolidone (PVPP) and (iii) verify the in vivo effects of extracts from 4 plants. Significant inhibition was shown in vitro using a larval migration inhibition (LMI) assay for all extracts except that from Olea europaea var. koroneiki. After adding PVPP, the LMI values were restored to control levels for all plants except Pistacia lentiscus and Ceratonia siliqua, confirming a role for tannins in the activity. In the in vivo experiment, 48 lambs composed 6 groups, depending on diet. On Day 0, groups G1–G5 received H. contortus and Trichostrongylus colubriformis larvae and G6 remained uninfected. The various diets were distributed from Days 14 to 45: P. lentiscus (G1), Quercus coccifera (G2), C. siliqua (G3), Onobrychis viciifolia (G4), or Medicago sativa for the 2 control groups (G5, G6). Egg excretion, packed cell volumes (PCVs) and inorganic phosphate were measured weekly throughout the entire experimental period. At slaughter, the worms were enumerated and their fecundity assessed. Consumption of the 4 browser plants did not provoke differences in pathophysiological measurements but there were significant decreases in egg excretion, mainly explained by significant decreases in worm fecundity for both species, without any statistical difference in worm numbers.

Keywords

nematodestanninsbrowse plantsnatural anthelminticsheep
Type
Research Article
Information
Parasitology , Volume 137 , Issue 4 , April 2010 , pp. 685 - 696
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Ahmamdi, H., Aouinti, F., Wathelet, J. P. and Elbachiri, A. (2009). Chemical composition of the essential oil of Pistacia lentiscus L. from Eastern Morocco. Records of Natural Products 3, 90–95.Google Scholar
Akkari, H., Ben Salem, H., Gharbi, M., Abidi, S. and Darghouth, M. A. (2008). Feeding Acacia cyanophylla Lindl. foliage to Barbarine lambs with or without PEG: Effect on the excretion of gastro-intestinal nematode eggs. Animal Feed Science and Technology 147, 182–192. doi:10.1016/j.anifeedsci.2007.09.017.CrossRefGoogle Scholar
Athanasiadou, S., Kyriazakis, I., Jackson, F. and Coop, R. L. (2001). Direct anthelmintic effects of condensed tannins towards different gastrointestinal nematodes of sheep: in vitro and in vivo studies. Veterinary Parasitology 99, 205–219. doi: 10.1016/S0304-4017(01)00467-8.CrossRefGoogle ScholarPubMed
Bahuaud, D., Martinez-Ortiz de Montellano, C., Chauveau, S., Prevot, F., Torres-Acosta, F., Fouraste, I. and Hoste, H. (2006). Effects of four tanniferous plant extracts on the in vitro exsheathment of third-stage larvae of parasitic nematodes. Parasitology 132, 545–554. doi: 10.1017/S0031182005009509.CrossRefGoogle ScholarPubMed
Barazani, O., Dudai, N. and Golan-Goldhirsh, A. (2003). Comparison of Mediterranean Pistacia lentiscus genotypes by random amplified polymorphic DNA, chemical, and morphological analyses. Journal of Chemical Ecology 29, 1939–1952. doi: 10.1023/A:1024862614345.CrossRefGoogle ScholarPubMed
Barrau, E., Fabre, N., Fouraste, I. and Hoste, H. (2005). Effect of bioactive compounds from sainfoin (Onobrychis viciifolia Scop.) on the in vitro larval migration of Haemonchus contortus: role of tannins and flavonol glycosides. Parasitology 131, 531–538. doi: 10.1017/S0031182005008024.CrossRefGoogle ScholarPubMed
Ben Salem, H., Ben Salem, I., Nefzaoui, A. and Ben Said, M. S. (2003). Effect of PEG and olive cake feed blocks supply on feed intake, digestion, and health of goats given kermes oak (Quercus coccifera L.) foliage. Animal Feed Science and Technology 110, 45–59. doi: 10.1016/S0377-8401(03)00215-3.CrossRefGoogle Scholar
Ben Salem, H., Nefzaoui, A. and Makkar, H. P. S. (2007). Feed supplementation blocks for increased utilization of tanniniferous foliages by ruminants. In Feed Supplementation Blocks. Urea Molasses Multinutrient Blocks: Simple and Effective Feed Supplement Technology for Ruminant Agriculture. FAO Animal Production and Health Paper (FAO) 164, 185–105.Google Scholar
Ben Salem, H., Priolo, A. and Morand-Fehr, P. (2008). Shrubby vegetation and agro-industrial by-products as alternative feed resources for sheep and goats: Effects on digestion, performance and product quality. Animal Feed Science and Technology 147, 1–2. doi: 10.1016/j.anifeedsci.2007.10.001.CrossRefGoogle Scholar
Brunet, S. and Hoste, H. (2006). Monomers of condensed tannins affect the larval exsheathment of parasitic nematodes of ruminants. Journal of Agricultural and Food Chemistry 54, 7481–7487. doi: 10.1021/jf0610007.CrossRefGoogle ScholarPubMed
Brunet, S., Jackson, F. and Hoste, H. (2008). Effects of sainfoin (Onobrychis viciifolia) extract and monomers of condensed tannins on the association of abomasal nematode larvae with fundic explants. International Journal for Parasitology 38, 783–790. doi:10.1016/j.ijpara.2007.10.018.CrossRefGoogle ScholarPubMed
Camurca-Vasconcelos, A. L., Bevilaqua, C. M., Morais, S. M., Maciel, M. V., Costa, C. T., Macedo, I. T., Oliveira, L. M., Braga, R. R., Silva, R. A. and Vieira, L. S. (2007). Anthelmintic activity of Croton zehntneri and Lippia sidoides essential oils. Veterinary Parasitology 148, 288–294. doi: 10.1016/j.vetpar.2007.06.012.CrossRefGoogle ScholarPubMed
Coop, R. L. and Kyriazakis, I. (1999). Nutrition-parasite interaction. Veterinary Parasitology 84, 187–204. doi: 10.1016/S0304-4017(99)00070-9.CrossRefGoogle ScholarPubMed
Doner, W. L., Becard, G. and Irwin, L. P. (1993). Binding of flavonoids by polyvinylpolypyrrolidone. Journal of Agricultural and Food Chemistry 41, 753–757. doi: 10.1021/jf00029a014.CrossRefGoogle Scholar
Frutos, P., Hervas, G., Ramos, G., Giraldez, F. J. and Mantecon, A. R. (2002). Condensed tannin content of several shrub species from a mountain area in northern Spain, and its relationship to various indicators of nutritive value. Animal Feed Science and Technology 95, 215–226. doi: 10.1016/S0377-8401(01)00323-6.CrossRefGoogle Scholar
Frutos, P., Moreno-Gonzalo, J., Hervás, G., García, U., Ferreira, M. M. L., Celaya, R., Toral, G. P., Ortega-Mora, M. L., Ferre, I. and Osoro, K. (2008). Is the anthelmintic effect of heather supplementation to grazing goats always accompanied by anti-nutritional effects? Animal 2, 1449–1456. doi:10.1017/S1751731108002681.CrossRefGoogle ScholarPubMed
Githiori, B. J., Hoglund, J., Waller, J. P. and Baker, L. R. (2004). Evaluation of anthelmintic properties of some plants used as livestock dewormers against Haemonchus contortus infections in sheep. Parasitology 129, 245–253. doi: 10.1017/S0031182004005566.CrossRefGoogle ScholarPubMed
Hagerman, E. A. and Butler, G. L. (1978). Protein precipitation method for the quantitative determination of tannins. Journal of Agricultural and Food Chemistry 26, 809–812. doi: 10.1021/jf60218a027.CrossRefGoogle Scholar
Heckendorn, F., Haring, D. A., Maurer, V., Senn, M. and Hertzberg, H. (2007). Individual administration of three tanniferous forage plants to lambs artificially infected with Haemonchus contortus and Cooperia curticei. Veterinary Parasitology 146, 123–134. doi: 10.1016/j.vetpar.2007.01.009.CrossRefGoogle ScholarPubMed
Heckendorn, F., Häring, D. A., Maurer, V., Zinsstag, J., Langhans, W. and Hertzberg, H. (2006). Effect of sainfoin (Onobrychis viciifolia) silage and hay on established populations of Haemonchus contortus and Cooperia curticei in lambs. Veterinary Parasitology 142, 293–300. doi: org/10.1016/j.vetpar.2006.07.014.CrossRefGoogle ScholarPubMed
Hoste, H., Jackson, F., Athanasiadou, S., Thamsborg, S. M. and Hoskin, S. O. (2006). The effects of tannin-rich plants on parasitic nematodes in ruminants. Trends in Parasitology 22, 253–261. doi: 10.1016/j.pt.2006.04.004.CrossRefGoogle ScholarPubMed
Hoste, H., Torres-Acosta, J. F., Paolini, V., Aguilar-Caballero, A., Etter, E., Lefrileux, Y., Chartier, C. and Broqua, C. (2005). Interactions between nutrition and gastrointestinal infections with parasitic nematodes in goats. Small Ruminant Research 60, 141–151. doi: 10.1016/j.smallrumres.2005.06.008.CrossRefGoogle Scholar
Jackson, F. and Coop, R. L. (2000). The development of anthelmintic resistance in sheep nematodes. Parasitology 120, 95–107. doi: 10.1017/S0031182099005740.CrossRefGoogle ScholarPubMed
Kaplan, R. M. (2004). Drug resistance in nematodes of veterinary importance: a status report. Trends in Parasitology 20, 477–481. doi: 10.1016/j.pt.2004.08.001.CrossRefGoogle ScholarPubMed
Kloosterman, A., Albers, G. A. A. and Van Den Brink, R. (1978). Genetic variation among calves in resistance to nematode parasites. Veterinary Parasitology 4, 353–368.CrossRefGoogle Scholar
Lange, K. C., Olcott, D. D., Miller, J. E., Mosjidis, J. A., Terrill, T. H., Burke, J. M. and Kearney, M. T. (2006). Effect of sericea lespedeza (Lespedeza cuneata) fed as hay, on natural and experimental Haemonchus contortus infections in lambs. Veterinary Parasitology 141, 273–278. doi: 10.1016/j.vetpar.2006.06.001.CrossRefGoogle ScholarPubMed
LIusia, J. and Penuelas, J. (1998). Changes in terpene content and emission in potted Mediterranean woody plants under severe drought. Canadian Journal of Botany 76, 1366–1373. doi: 10.1139/cjb-76-8-1366.Google Scholar
Lorimer, S. D., Perry, N. B., Foster, L. M., Burgess, E. J. B., Douch, P. G. C., Hamilton, M. C., Donaghy, M. J. and McGregor, R. A. (1996). A nematode larval motility inhibition assay for screening plant extracts and natural products. Journal of Agricultural and Food Chemistry 44, 2842–2845. doi: 10.1021/jf9602176.CrossRefGoogle Scholar
MAFF. (1986). Ministry of Agriculture, Fisheries and Food. Manual of Veterinary Parasitological Laboratory Techniques. Her Majesty's Stationery Office, London, UK.Google Scholar
Makkar, H. P. (2003). Quantification of tannins in tree and shrub foliage, In A Laboratory Manual Food and Agriculture Organization of the United Nations/International Atomic Energy (FAO/IAEA), pp. 49–53.Google Scholar
Min, B. R. and Hart, S. P. (2003). Tannins for suppression of internal parasites. Journal of Animal Science 81, 102–109.Google Scholar
Molan, A. L., Hoskin, S. O., Barry, T. N. and McNabb, W. C. (2000). Effect of condensed tannins extracted from four forages on the viability of the larvae of deer lungworms and gastrointestinal nematodes. Veterinary Record 147, 44–48.CrossRefGoogle ScholarPubMed
Molan, A. L., Meagher, L. P., Spencer, P. A. and Sivakumaran, S. (2003). Effect of flavan-3-ols on in vitro egg hatching, larval development and viability of infective larvae of Trichostrongylus colubriformis. International Journal for Parasitology 33, 1691–1698. doi: 10.1016/S0020-7519(03)00207-8.CrossRefGoogle ScholarPubMed
Morand-Fehr, P., Bourbouze, A., Le Houérou, H. N., Gall, C. and Boyazoglu, G. J. (1983). The role of goats in the Mediterranean area. Livestock Production Science 10, 569–587. doi: 10.1016/0301-6226(83)90050-7.CrossRefGoogle Scholar
Osoro, K., Benito-Peña, A., Frutos, P., Garcia, P. M., Ortega-Mora, L. M., Celaya, R. and Ferre, I. (2007 a). The effect of heather supplementation on gastrointestinal nematode infections and performance in Cashmere and local Celtiberic goats on pasture. Small Ruminant Research 67, 184–191. doi: 10.1016/j.smallrumres.2005.09.032.CrossRefGoogle Scholar
Osoro, K., Mateos-Sanz, A., Frutos, P., Garcia, U., Ortega-Mora, L. M., Ferreira, L. M., Celaya, R. and Ferre, I. (2007 b). Anthelmintic and nutritional effects of heather supplementation on Cashmere goats grazing perennial ryegrass-white clover pastures. Journal of Animal Science 85, 861–870. doi:10.2527/jas.2006-388.CrossRefGoogle ScholarPubMed
Paolini, V., De La Farge, F., Prevot, F., Dorchies, P. and Hoste, H. (2005). Effects of the repeated distribution of sainfoin hay on the resistance and the resilience of goats naturally infected with gastrointestinal nematodes. Veterinary Parasitology 127, 277–283. doi: 10.1016/j.vetpar.2004.10.015.CrossRefGoogle ScholarPubMed
Paolini, V., Dorchies, P. and Hoste, H. (2003). Effects of sainfoin hay on gastrointestinal nematode infections in goats. Veterinary Record 152, 600–601.CrossRefGoogle ScholarPubMed
Paolini, V., Fouraste, I. and Hoste, H. (2004). In vitro effects of three woody plant and sainfoin extracts on 3rd-stage larvae and adult worms of three gastrointestinal nematodes. Parasitology 129, 69–77. doi: 10.1017/S0031182004005268.CrossRefGoogle ScholarPubMed
Papachristou, T. G., Platis, P. D. and Nastis, A. S. (2005). Foraging behaviour of cattle and goats in oak forest stands of varying coppicing age in Northern Greece. Small Ruminant Research 59, 181–189. doi: 10.1016/j.smallrumres.2005.05.006.CrossRefGoogle Scholar
Pessoa, L. M., Morais, S. M., Bevilaqua, C. M. L. and Luciano, J. H. S. (2002). Anthelmintic activity of essential oil of Ocimum gratissimum Linn. and eugenol against Haemonchus contortus. Veterinary Parasitology 109, 59–63. doi: 10.1016/S0304-4017(02)00253-4.CrossRefGoogle ScholarPubMed
Rabel, B., McGregor, R. and Douch, P. G. C. (1994). Improved bioassay for estimation of inhibitory effects of ovine gastrointestinal mucus and anthelmintics on nematode larval migration. International Journal for Parasitology 24, 671–676. doi: 10.1016/0020-7519(94)90119-8.CrossRefGoogle ScholarPubMed
Raynaud, J. P. (1970). Etude de l'efficacité d'une technique de coproscopie quantitative pour le diagnostic de routine et le contrôle des infestations parasitaires des bovins, ovins, équins et porcins. Annales de Parasitologie 45, 321–342.Google Scholar
Robinson, R., Roughan, M. and Wagstaff, D. F. (1971). Measuring inorganic phosphate without using a reducing agent. Annals of Clinical Biochemistry 8, 168–170.CrossRefGoogle Scholar
Rochfort, S., Parker, A. J. and Dunshea, F. R. (2008). Plant bioactives for ruminant health and productivity. Phytochemistry 69, 299–322. doi: 10.1016/j.phytochem.2007.08.017.CrossRefGoogle ScholarPubMed
Shaik, S. A., Terrill, T. H., Miller, J. E., Kouakou, B., Kannan, G., Kaplan, R. M., Burke, J. M. and Mosjidis, J. A. (2006). Sericea lespedeza hay as a natural deworming agent against gastrointestinal nematode infection in goats. Veterinary Parasitology 139, 150–157. doi: 10.1016/j.vetpar.2006.02.020.CrossRefGoogle Scholar
Stepek, G., Behnke, J. M., Buttle, D. J. and Duce, I. R. (2004). Natural plant cysteine proteinases as anthelmintics? Trends in Parasitology 20, 322–327. doi: 10.1016/j.pt.2004.05.003.CrossRefGoogle ScholarPubMed
Sykes, A. R. (1994). Parasitism and production in farm animals. Animal Production 59, 155–172.Google Scholar
Waller, P. J. (1999). International approaches to the concept of integrated control of nematode parasites of livestock. International Journal for Parasitology 29, 155–164. doi: 10.1016/S0020-7519(98)00178-7.CrossRefGoogle Scholar