In vitro effect of heather (Ericaceae) extracts on different development stages of Teladorsagia circumcincta and Haemonchus contortus

Veterinary Parasitology

Volumn 197, Issue 1-2, 2013, Pages 235-243

  Moreno Gonzalo, J ^a   Manolaraki, F ^b,c   Frutos, P ^d   Hervas G ^d   Celaya, R ^e   Osoro, K ^e   Ortega Mora, L M ^a   Hoste, H ^b,c   Ferre, I ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b CNRS   (France)

^c UNIVERSITÉ DE TOULOUSE   (France)

^d Instituto de Ganadería de Montana   (Spain)

^e Servicio Regional de Investigación y Desarrollo Agroalimentario de Asturias   (Spain)

Author keywords

Adult motility inhibition assay; Calluna vulgaris; Egg hatching assay; Erica spp.; Haemonchus contortus; Heather; Larval exsheathment inhibition assay; Phenolics; Teladorsagia circumcincta

Indexed keywords

CALLUNA VULGARIS EXTRACT; ERICA CINEREA EXTRACT; ERICA UMBELLATA EXTRACT; PLANT EXTRACT; UNCLASSIFIED DRUG;

ARTICLE; CALLUNA VULGARIS; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DEVELOPMENTAL STAGE; DRUG EFFECT; ERICA CINEREA; ERICA UMBELLATA; ERICACEAE; HAEMONCHUS CONTORTUS; HATCHING; IN VITRO STUDY; LARVA; NONHUMAN; TELADORSAGIA CIRCUMCINCTA; WORM EGG;

CALLUNA; CALLUNA VULGARIS; CAPRA HIRCUS; ERICA; ERICA CINEREA; ERICA UMBELLATA; ERICACEAE; HAEMONCHUS CONTORTUS; NEMATODA; TELADORSAGIA CIRCUMCINCTA;

ADULT MOTILITY INHIBITION ASSAY; CALLUNA VULGARIS; EGG HATCHING ASSAY; ERICA SPP.; HAEMONCHUS CONTORTUS; HEATHER; LARVAL EXSHEATHMENT INHIBITION ASSAY; PHENOLICS; TELADORSAGIA CIRCUMCINCTA;

ANIMALS; ERICACEAE; HAEMONCHUS; NEMATODA; PLANT EXTRACTS;

EID: 84883257440     PISSN: 03044017     EISSN: 18732550     Source Type: Journal    
DOI: 10.1016/j.vetpar.2013.05.010     Document Type: Article

References (47)

1. Ademola I.O., Akanbi A.I., Idowu S.O. Comparative nematocidal activity of chromatographic fractions of Leucaena leucocephala seed against gastrointestinal sheep nematodes. Pharm. Biol. 2005, 43:599-604.
2. Akkari H., Ben Salem H., Gharbi M., Abidi S., Darghouth M.A. Feeding Acacia cyanophylla Lindl. foliage to barbarine lambs with or without PEG effect on the excretion of gastro-intestinal nematode eggs. Anim. Feed Sci. Technol. 2008, 147:182-192.
3. Alawa C.B.I., Adamu A.M., Gefu J.O., Ajanusi O.J., Abdu P.A., Chiezey N.P., Alawa J.N., Bowman D.D. In vitro screening of two Nigerian medicinal plants (Vernonia amygdalina and Annona senegalensis) for anthelmintic activity. Vet. Parasitol. 2003, 113:73-81.
4. Al-Rofaai A., Rahman W.A., Sulaiman S.F., Yahaya Z.S. In vitro activity of neem (Azadirachta indica) and cassava (Manihot esculenta) on three pre-parasitic stages of susceptible and resistant strains of Teladorsagia (Ostertagia) circumcincta. Vet. Parasitol. 2012, 188:85-92.
5. Assis L.M., Bevilaqua C.M.L., Morais S.M., Vieira L.S., Costa C.T.C., Souza J.A.L. Ovicidal and larvicidal activity in vitro of Spigelia anthelmia Linn. extracts on Haemonchus contortus. Vet. Parasitol. 2003, 117:43-49.
6. Azando E.V.B., Hounzangbe-Adote M.S., Olounlade P.A., Brunet S., Fabre N., Valentin A., Hoste H. Involvement of tannins and flavonoids in the in vitro effects of Newbouldia laevis and Zanthoxylum zanthoxyloides extracts on the exsheathment of third-stage infective larvae of gastrointestinal nematodes. Vet. Parasitol. 2011, 180:292-297.
7. Bachaya H.A., Iqbal Z., Khan M.N., Sindhu Z.U.D., Jabbar A. Anthelmintic activity of Ziziphus nummularia (bark) and Acacia nilotica (fruit) against Trichostrongylid nematodes of sheep. J. Ethnopharmacol. 2009, 123:325-329.
8. Bahuaud D., De Montellano C.M.O., Chauveau S., Prevot F., Torres-Acosta F., Fouraste I., Hoste H. Effects of four tanniferous plant extracts on the in vitro exsheathment of third-stage larvae of parasitic nematodes. Parasitology 2006, 132:545-554.
9. Barrau E., Fabre N., Fouraste I., Hoste H. 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 2005, 131:531-538.
10. Brunet S., Hoste H. Monomers of condensed tannins affect the larval exsheathment of parasitic nematodes of ruminants. J. Agric. Food Chem. 2006, 54:7481-7487.
11. Brunet S., Jackson F., Hoste H. Effects of sainfoin (Onobrychis viciifolia) extract and monomers of condensed tannins on the association of abomasal nematode larvae with fundic explants. Int. J. Parasitol. 2008, 38:783-790.
12. Cala A.C., Chagas A.C.S., Oliveira M.C.S., Matos A.P., Borges L.M.F., Sousa L.A.D., Souza F.A., Oliveira G.P. In vitro anthelmintic effect of Melia azedarach L. and Trichilia classenii C. against sheep gastrointestinal nematodes. Exp. Parasitol. 2012, 130:98-102.
13. Coles G.C., Bauer C., Borgsteede F., Geerts S., Klei T.R., Taylor M.A., Waller P.J. World association for advancement in veterinary parasitology (WAAVP) methods for the detection of anthelmintic resistance in nematodes of veterinary importance. Vet. Parasitol. 1992, 44:35-43.
14. Copani G., Hall J.O., Miller J., Priolo A., Villalba J.J. Plant secondary compounds as complementary resources: are they always complementary?. Oecologia 2012, (Epub ahead of print). 10.1007/s00442-012-2551-1.
15. Costa C.T.C., Bevilaqua C.M.L., Camurca-Vasconcelos A.L.F., Maciel M.V., Morais S.M., Castro C.M.S., Braga R.R., Oliveira L.M.B. In vitro ovicidal and larvicidal activity of Azadirachta indica extracts on Haemonchus contortus. Small Rumin. Res. 2008, 74:284-287.
16. Eguale T., Tilahun G., Debella A., Feleke A., Makonnen E. Haemonchus contortus: in vitro and in vivo anthelmintic activity of aqueous and hydro-alcoholic extracts of Hedera helix. Exp. Parasitol. 2007, 116:340-345.
17. Frutos P., Hervás G., Celaya R., Moreno-Gonzalo J., Rodríguez A.B., García U., Ferre I., Ortega-Mora L.M., Osoro K. Effects of the use of heather as anthelmintic in goats infected with Trichostrongylus colubriformis on ruminal fermentation and digestibility. Opt. Med. 2011, 99:321-327.
18. Hertzberg H., Huwyler U., Kohler L., Rehbein S., Wanner M. Kinetics of exsheathment of infective ovine and bovine strongylid larvae in vivo and in vitro. Parasitology 2002, 125:65-70.
19. Hoste H., Jackson F., Athanasiadou S., Thamsborg S.M., Hoskin S.O. The effects of tannin-rich plants on parasitic nematodes in ruminants. Trends Parasitol. 2006, 22:253-261.
20. Hoste H., Torres-Acosta J.F.J. Non chemical control of helminths in ruminants adapting solutions for changing worms in a changing world. Vet. Parasitol. 2011, 180:144-154.
21. Hoste H., Martinez-Ortiz-De-Montellano C., Manolaraki F., Brunet S., Ojeda-Robertos N., Fourquaux I., Torres-Acosta J.F.J., Sandoval-Castro C.A. Direct and indirect effects of bioactive tannin-rich tropical and temperate legumes against nematode infections. Vet. Parasitol. 2012, 186:18-27.
22. Hounzangbe-Adote M.S., Paolini V., Fouraste I., Moutairou K., Hoste H. In vitro effects of four tropical plants on three life-cycle stages of the parasitic nematode Haemonchus contortus. Res. Vet. Sci. 2005, 78:155-160.
23. Hussain A., Khan M.N., Iqbal Z., Sajid M.S., Khan M.K. Anthelmintic activity of Trianthema portulacastrum L. and Musa paradisiaca L. against gastrointestinal nematodes of sheep. Vet. Parasitol. 2011, 179:92-99.
24. Kamaraj C., Rahuman A.A. Efficacy of anthelmintic properties of medicinal plant extracts against Haemonchus contortus. Res. Vet. Sci. 2010, 10:1-5.
25. Kaplan R.M. Drug resistance in nematodes of veterinary importance: a status report. Trends Parasitol. 2004, 20:477-481.
26. Katiki L.M., Chagas A.C.S., Bizzo H.R., Ferreira J.F.S., Amarante A.F.T. Anthelmintic activity of Cymbopogon martinii Cymbopogon schoenanthus and Mentha piperita essential oils evaluated in four different in vitro tests. Vet. Parasitol. 2011, 183:103-108.
27. Kotze A.C., O'Grady J.O., Emms J., Toovey A.F., Hughes S., Jessop P., Bennell M.R., Vercoe P.E., Revell D.K. Exploiting the anthelmintic properties of Australian native shrubs with respect to their potential role in livestock grazing systems. Parasitology 2009, 136:1065-1080.
28. Landau S., Azaizeh H., Muklada H., Glasser T., Ungar E.D., Baram H., Abbas N., Markovics A. Anthelmintic activity of Pistacia lentiscus foliage in two middle eastern breeds of goats differing in their propensity to consume tannin-rich browse. Vet. Parasitol. 2010, 173:280-286.
29. Maciel M.V., Morais S.M., Bevilaqua C.M.L., Camurça-Vasconcelos A.L.F., Costa C.T.C., Castro C.M.S. Ovicidal and larvicidal activity of Melia azedarach extracts on Haemonchus contortus. Vet. Parasitol. 2006, 140:98-104.
30. Makkar H.P.S., Blümmel M., Borowy N.K., Becker K. Gravimetric determination of tannins and their correlations with chemical and protein precipitation methods. J. Sci. Food Agric. 1993, 61:161-165.
31. Manolaraki F., Sotiraki S., Stefanakis A., Skampardonis V., Volanis M., Hoste H. Anthelmintic activity of some mediterranean browse plants against parasitic nematodes. Parasitology 2010, 137:685-696.
32. Marie-Magdeleine C., Hoste H., Mahieu M., Varo H., Archimede H. In vitro effects of Cucurbita moshata seed extracts on Haemonchus contortus. Vet. Parasitol. 2009, 161:99-105.
33. Marie-Magdeleine C., Udino L., Philibert L., Bocagea B., Archimede H. In vitro effects of Cassava (Manihot esculenta) leaf extracts on four development stages of Haemonchus contortus. Vet. Parasitol. 2010, 173:85-92.
34. Molan A.L., Sivakumaran S., Spencer P.A., Meagher L.P. Green tea flavan-3-ols and oligomeric proanthocyanidins inhibit the motility of infective larvae of Teladorsagia circumcincta and Trichostrongylus colubriformis in vitro. Res. Vet. Sci. 2004, 77:239-243.
35. Molan A.L., Faraj A.M. The effects of condensed tannins extracted from different plant species on egg hatching and larval development of Teladorsagia circumcincta (Nematoda: Trichostrongylidae). Folia Parasitol. (Praha) 2010, 57:62-68.
36. Monteiro M.V.B., Bevilaqua C.M.L., Morais S.M., Machado L.K.A., Camurça-Vasconcelos A.L.F., Campello C.C., Ribeiro W.L.C., Mesquita M.D.A. Anthelmintic activity of Jatropha curcas L. seeds on Haemonchus contortus. Vet. Parasitol. 2011, 182:259-263.
37. Moreno-Gonzalo J., Ferre I., Celaya R., Frutos P., Ferreira L.M.M., Hervás G., García U., Ortega-Mora L.M., Osoro K. Potential use of heather to control gastrointestinal nematodes in goats. Small Rumin. Res. 2012, 103:60-68.
38. Moreno-Gonzalo J., Osoro K., García U., Frutos P., Celaya R., Ferreira L.M.M., Ortega-Mora L.M., Ferre I. Effect of the consumption of heather on incoming larvae and established population of Teladorsagia circumcincta in experimentally infected Cashmere goats. Vet. Parasitol. 2013, 10.1016/j.vetpar.2013.02.005.
39. Oliveira L.M.B., Bevilaqua C.M.L., Costa C.T.C., Macedo I.T.F., Barros R.S., Rodrigues A.C.M., Camurça-Vasconcelos A.L.F., Morais S.M., Lima Y.C., Vieira L.S., Navarro A.M.C. Anthelmintic activity of Cocos nucifiera L. Vet. Parasitol. 2009, 159:55-59.
40. Oliveira L.M.B., Bevilaqua C.M.L., Macedo I.T.F., Morais S.M., Machado L.K.A., Campello C.C., Mesquita M.D. Effects of Myracrodruon urundeuva extracts on egg hatching and larval exsheathment of Haemonchus contortus. Parasitol. Res. 2011, 109:893-898.
41. Osoro K., Mateos-Sanz A., Frutos P., García U., Ortega-Mora L.M., Ferreira L.M.M., Celaya R., Ferre I. Anthelmintic and nutritional effects of heather supplementation on Cashmere goats grazing perennial ryegrass-white clover pastures. J. Anim. Sci. 2007, 85:861-870.
42. Osoro K., Celaya R., Moreno-Gonzalo J., Ferreira L.M.M., García U., Frutos P., Ortega-Mora L.M., Ferre I. Effects of stocking rate and heather supplementation on gastrointestinal nematode infections and host performance in naturally-infected Cashmere goats. Rangel. Ecol. Manage. 2009, 62:127-135.
43. Paolini V., Fouraste I., Hoste H. In vitro effects of three woody plant and sainfoin extracts on 3rd-stage larvae and adult worms of three gastrointestinal nematodes. Parasitology 2004, 129:69-77.
44. Papachristou T.G., Dziba L.E., Provenza F.D. Foraging ecology of goats and sheep on wooded rangelands. Small Rumin. Res. 2005, 59:141-156.
45. Perry B.D., Randolph T.F. Improving the assessment of the economic impact of parasitic diseases and of their control in production animals. Vet. Parasitol. 1999, 84:145-168.
46. SAS SAS/STAT User's Guide. V8 1999, SAS Institute Inc., Cary, NC, USA.
47. Valcárcel F., Romero C.G. Prevalence and seasonal pattern of caprine trichostrongyles in a dry area of central Spain. J. Vet. Med. Ser. B - Infect. Dis. Vet. Public Health 1999, 46:673-681.