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

Veterinary Parasitology

Volumn 188, Issue 1-2, 2012, Pages 85-92

  Al Rofaai, A ^a   Rahman, W A ^a   Sulaiman, S F ^a   Yahaya, Z S ^a  

^a SCHOOL OF PHYSICS   (Malaysia)

Author keywords

Anthelmintic; Cassava; Cytotoxicity; Neem; Plant extract; Teladorsagia circumcincta

Indexed keywords

ACETIC ACID ETHYL ESTER; ALBENDAZOLE; ALKALOID; ANTHELMINTIC AGENT; AZADIRACHTA INDICA EXTRACT; CHLOROFORM; FLAVONOID; HEXANE; MANIHOT ESCULENTA EXTRACT; METHANOL; PHYTOSTEROL; PLANT EXTRACT; SAPONIN; TANNIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTHELMINTIC ACTIVITY; ANTHELMINTIC DRUG RESISTANCE; ANTHELMINTIC DRUG SUSCEPTIBILITY; ARTICLE; AZADIRACHTA INDICA; CASSAVA; CELL DEATH; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY TEST; DRUG ACTIVITY; DRUG CYTOTOXICITY; DRUG DETERMINATION; DRUG EFFICACY; DRUG RESISTANCE; DRUG SENSITIVITY; EGG HATCH TEST; FIRST STAGE LARVA; GOAT; IN VITRO STUDY; INFECTIVE STAGE LARVA; LARVAL DEVELOPMENT ASSAY; LARVAL PARALYSIS ASSAY; LARVICIDAL ACTIVITY; LC 50; NEMATODE EGG; NEMATODE LIFE CYCLE STAGE; NONHUMAN; OSTERTAGIA; OVICIDAL ACTIVITY; PARASITE EXAMINATION; PERIPHERAL BLOOD MONONUCLEAR CELL; PHYTOCHEMISTRY; PLANT LEAF; TELADORSAGIA CIRCUMCINCTA;

ALBENDAZOLE; ANIMALS; ANTHELMINTICS; AZADIRACHTA; DRUG RESISTANCE; LARVA; MANIHOT; OSTERTAGIA; PLANT EXTRACTS;

AZADIRACHTA INDICA; CAPRA HIRCUS; MANIHOT ESCULENTA; NEMATODA; TELADORSAGIA CIRCUMCINCTA;

EID: 84863205850     PISSN: 03044017     EISSN: 18732550     Source Type: Journal    
DOI: 10.1016/j.vetpar.2012.03.002     Document Type: Article

References (71)

1. Adam Shama I.Y., Ahmed Wasma A.A. Evaluation of the toxicity of Manihot esculenta on Wistar rats after traditional Sudanese processing. J. Pharmacol. Toxicol. 2011, 6:418-426.
2. Ademola I.O., Eloff J.N. In vitro anthelmintic activity of Combretum molle (R. Br. ex G. Don) (Combretaceae) against Haemonchus contortus ova and larvae. Vet. Parasitol. 2010, 169:198-203.
3. Akhter N., Arijo A.G., Phulan M.S., Iqbal Z., Mirbahar K.B. Prevalence of gastrointestinal nematodes in goats in Hyderabad and adjoining areas. Pakistan Vet. J. 2011, 31:287-290.
4. Ali B.H. The toxicity of Azadirachta indica leaves in goats and guinea pigs. Vet. Hum. Toxicol. 1987, 29:16-19.
5. Al-Saqur I.M., Altaif K.I., Al-Zubaidy A.J. Study on the pathogenicity of ostertagiosis due to Ostertagia circumcincta in sheep. Iraq Vet. Parasitol. 1981, 9:133-143.
6. Al-Shaibani I.R.M., Phulan M.S., Arijo A., Qureshi T.A. Ovicidal and larvicidal properties of Adhatoda vasica (L.) extracts against gastrointestinal nematodes of sheep in vitro. Pakistan Vet. J. 2008, 28:79-83.
7. Al-Shaibani I.R.M., Phulan M.S., Shiekh M. Anthelmintic activity of Fumaria parviflora (Fumariaceae) against gastrointestinal nematodes of sheep. Int. J. Agric. Biol. 2009, 11:431-436.
8. Athanasiadou S., Kyriazakis I., Jackson F., Coop R.L. Direct anthelmintic effects of condensed tannins towards different gastrointestinal nematodes of sheep: in vitro and in vivo studies. Vet. Parasitol. 2001, 99:205-219.
9. Bellaver C., Bellaver I.H. Livestock production and quality of societies' life in transition economies. Livest. Prod. Sci. 1999, 59:125-135.
10. Bishop S.C., Bairden K., McKellar Q.A., Park M., Stear M.J. Genetic parameters for faecal egg count following mixed natural, predominantly Ostertagia circumcincta infection and relationships with live weight in young lambs. J. Anim. Sci. 1996, 63:423-428.
11. Biu A.A., Yusufu S.D., Rabo J.S. Acute toxicity study on neem (Azadirachta indica, juss) leaf aqueous extract in chicken (Gallus gallus domesticus). Afr. Sci. 2010, 11:241-244.
12. Bjørn H., Monrad J., Nansen P. Anthelmintic resistance in nematode parasites of sheep in Denmark with special emphasis on levamisole resistance in Ostertagia circumcincta. Acta Vet. Scand. 1991, 32:145-154.
13. Boeke S.J., Boersma M.G., Alink G.M., van Loon J.J., van Huis A., Dicke M., Rietjens I.M. Safety evaluation of neem (Azadirachta indica) derived pesticides. J. Ethnopharmacol. 2004, 94:25-41.
14. Cawthorne R.J., Whitehead J.D. Isolation of benzimidazole resistant strains of Ostertagia circumcincta from British sheep. Vet. Rec. 1983, 19:274-277.
15. Cereda M.P., Mattos M.C.Y. Linamarin - the toxic compound of cassava. J. Venom Anim. Toxins 1996, 2:6-12.
16. Chandrawathani P., Chang K.W., Nurulaini R., Waller P.J., Adnan M., Zaini C.M., Jamnah O., Khadijah S., Vincent N. Daily feeding of fresh neem leaves (Azadirachta indica) for worm control in sheep. Trop. Biomed. 2006, 23:23-30.
17. Chartier C., Reche B. Gastrointestinal helminths and lungworms of French dairy goats: prevalence and geographical distribution in Poitou-Charentes. Vet. Res. Commun. 1992, 16:327-335.
18. Cohen E., Quistad G.B., Casida J.E. Cytotoxicity of nimbolide, epoxyazadiradione and other limonoids from neem insecticide. Life Sci. 1996, 58:1075-1081.
19. Coles G.C., Bauer C., Borgsteede F.H.M., Geerts S., Klei T.R., Taylor M.A., Waller P.J. World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P.) methods for the detection of anthelmintic resistance in nematodes of veterinary importance. Vet. Parasitol. 1992, 44:35-44.
20. Coles G.C., Jackson F., Pomroy W.E., Prichard R.K., von Samson-Himmelstjerna G., Silvestre A. The detection of anthelmintic resistance in nematodes of veterinary importance. Vet. Parasitol. 2006, 136:167-185.
21. Costa C.T.C., Bevilaqua C.M.L., Maciel M.V., Camurça-Vasconcelos A.L.F., Morais S.M., Monteiro M.V.B., Farias V.M., Silva M.V., Souza M.M.C. Anthelmintic activity of Azadirachta indica A. Juss against sheep gastrointestinal nematodes. Vet. Parasitol. 2006, 137:306-310.
22. Costa C.T.C., Bevilaqua C.M.L., Camurcça-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 Ruminant Res. 2008, 74:284-287.
23. Doligalskaa M., Joózwickaa K., Kiersnowskaa M., Mroczekb A., aczkowskib C.P., Janiszowska W. Triterpenoid saponins affect the function of P-glycoprotein and reduce the survival of the free-living stages of Heligmosomoides bakeri. Vet. Parasitol. 2011, 179:144-151.
24. Eckert J., Hertzberg H. Parasite control in transhuman situations. Vet. Parasitol. 1994, 54:103-125.
25. 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.
26. Eguale T., Tilahun G., Debella A., Feleke A., Makonnen E. In vitro and in vivo anthelmintic activity of crude extracts of Coriandrum sativum against Haemonchus contortus. J. Ethnopharmacol. 2007, 110:428-433.
27. Eysker M., van Graafeiland A.E., Ploeger H.W. Resistance of Teladorsagia circumcincta in goats to ivermectin in the Netherlands. Tijd. Diergeneeskd 2006, 15:358-361.
28. Fox M.T. Pathophysiology of infection with gastrointestinal nematodes in domestic ruminants: recent developments. Vet. Parasitol. 1997, 72:285-308.
29. Gopal R.M., Pomroy W.E., West D.M. Resistance of field isolates of Trichostrongylus colubriformis and Ostertagia circumcincta to ivermectin. Int. J. Parasitol. 1999, 29:781-786.
30. Gura, S. (Ed.), 2008. Industrial livestock Production and its Impact on Smallholders in Developing Countries. Consultancy Report to the League for Pastoral Peoples and Endogenous Livestock Development, Germany. http://www.pastoralpeoples.org/.
31. 50s without a computer. Parasitol. Today 1988, 4:25-27.
32. 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.
33. Hubert J., Kerbouef D. A microlarval development assay for the detection of anthelmintic resistance in sheep nematodes. Vet. Rec. 1992, 130:442-446.
34. Iqbal Z., Sarwar M., Jabbar A., Ahmed S., Nisa M., Sajid M.S., Khan M.N., Mufti K.A., Yaseen M. Direct and indirect anthelmintic effects of condensed tannins in sheep. Vet. Parasitol. 2007, 144:125-131.
35. Iqbal Z., Lateef M., Jabbar A., Gilani A.H. In vivo anthelmintic activity of Azadirachta indica A. Juss seeds against gastrointestinal nematodes of sheep. Vet. Parasitol. 2010, 168:342-345.
36. Islam MdM., Shams MdI., Ilias G.N.M., Hannan MdO. Protective antifungal effect of neem (Azadirachta indica) extracts on mango (Mangifera indica) and rain tree (Albizia saman) wood. Int. Biodeter. Biodegr. 2009, 63:241-243.
37. Jabbar A., Iqbal Z., Kerboeuf D., Muhammad G., Khan M.N., Afaq M. Anthelmintic resistance: the state of play revisited. Life Sci. 2006, 79:2413-2431.
38. Jackson F., Jackson E., Coop R.L. Evidence of multiple anthelmintic resistance in a strain of Teladorsagia circumcincta (Ostertagia circumcincta) isolated from goats in Scotland. Res. Vet. Sci. 1992, 53:371-374.
39. Kamaraj C., Rahuman A.A. Efficacy of anthelmintic properties of medicinal plant extracts against Haemonchus contortus. Res. Vet. Sci. 2011, 91:400-404.
40. 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.
41. Khan P.K., Awasthy K.S. Cytogenetic toxicity of neem. Food Chem. Toxicol. 2003, 41:1325-1328.
42. Kusiluka L., Kambarage D. Diseases of Small Ruminants A Handbook. Common Diseases of Sheep and Goats in Sub-Saharan Africa 1996, VETAID, ISBN: 09522299 5, 116 pp.
43. López J., Machín E., Zentella A., Vázquez V., Tejada I., Shimada A., Sánchez D. Effect of cassava (Manihot esculenta) foliage supplementation to calves on the viability and egg count of Haemonchus contortus nematodes. Am. J. Anim. Vet. Sci. 2007, 2:93-98.
44. Macedo F.R., Louvandini H., Paludo G.R., McManus C.M., Porto A.D., Martins R.F.S., Viana P.G., Neves B.P. Effects of Azadirachta indica on sheep infected naturally with helminths. Am. J. Anim. Vet. Sci. 2007, 2:121-126.
45. Macedo I.T., Bevilaqua C.M., Oliveira L.M., Camurcça-Vasconcelos A.L., Vieira L.S., Oliveira F.R., Queiroz-Junior E.M., Tomé A.R., Nascimento N.R. Anthelmintic effect of Eucalyptus staigeriana essential oil against goat gastrointestinal nematodes. Vet. Parasitol. 2010, 173:93-98.
46. Marie-Magdeleine C., Hoste H., Mahieu M., Varo H., Archimede H. In vitro effects of Cucurbita moschata seed extracts on Haemonchus contortus. Vet. Parasitol. 2009, 161:99-105.
47. Marie-Magdeleine C., Udino L., Philibert L., Bocage 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.
48. Melo F.M.P., Fiore M.F., Moraes L.A.B., Silva- tenico M.E., Scramin S., Teixeira M.A., Melo I.S. Antifungal compound produced by the cassava endophyte Bacillus pumilus MAIIIM4A. Scientia Agricola (Piracicaba, Braz.) 2009, 66:583-592.
49. Minho A.P., Bueno I.C., Gennari S.M., Jackson F., Abdalla A.L. In vitro effect of condensed tannin extract from acacia (Acacia mearnsii) on gastrointestinal nematodes of sheep. Braz. J. Vet. Parasitol. 2008, 17:144-148.
50. Mishra V., Parveen N., Singhal K.C., Khan N.U. Antifilarial activity of Azadirachta indica on cattle filarial parasite Setaria cervi. Fitoterapia 2005, 76:54-61.
51. Molan A.C., Waghorn W.C., McNabb W.C. Effect of condensed tannins on egg hatching and larval development of Trichostrongylus colubriformis in vitro. Vet. Rec. 2002, 150:65-69.
52. Nabavi R., Eslami A., Shokrani H.R., Bokaie S., Shayan P., Saadati D. Study on the prevalence, intensity, seasonal dynamics of abomasal helminths in sheep from different climatic zones of Iran. World Appl. Sci. J. 2011, 12:441-445.
53. Oliveira L.M.B., Bevilaqua C.M.L., Costa C.T.C., Macedo I.T.F., Barros R.S., Rodrigues A.C.M., Camurcça-Vasconcelos A.L.F., Morais S.M., Lima Y.C., Vieira L.S., Navarro A.M.C. Anthelmintic activity of Cocos nucifera L. against sheep gastrointestinal nematodes. Vet. Parasitol. 2009, 159:55-59.
54. Patel S., Gheewala N., Suthar A., Shah A. In vitro cytotoxicity activity of Solanum nigrum extract against Hela cell line and Vero cell line. Int. J. Pharm. Pharm. Sci. 2009, 1:38-46.
55. ® AQueous Non-Radioactive Cell Proliferation Assay, Technical Bulletin #TB169, Revised 4/05 2005, Promega Corporation, Madison, USA.
56. Manual for Field trials in Plant Protection 1981, Agricultural Division, Ciba-Geigy Limited. second edition. W. Püntener (Ed.).
57. Punthanara S., Chairatanayuth P., Vijchulata P., Surapat S., Kuntho U., Narongwanichakarn W. Effects of cassava hay supplementation on antibacterial activity of the lactoperoxidase system in raw milk of dairy cows. Kasetsart J. (Nat. Sci.) 2009, 43:486-496.
58. Rahman W.A., Lee R., Sulaiman S.F. In vitro anthelmintic activity of neem plant (Azadirachta indica) extract against third-stage Haemonchus contortus larvae from goats. Global Vet. 2011, 7:22-26.
59. Rosenkranz H.S., Klopman G. An examination of the potential genotoxic carcinogenicity of a biopesticide derived from neem tree. Environ. Mol. Mutagen. 1995, 26:255-260.
60. Sarwar A., Enbergs H. Effects of Saussurea lappa roots extract in ethanol on leukocyte phagocytic activity, lymphocyte proliferation and interferon-gamma (IFN-gamma). Pakistan J. Pharm. Sci. 2007, 20:175-179.
61. Schürmann S., Harder A., Schnieder T., von Samson-Himmelstjerna G. Effects of emodepside on egg hatching, larval development and larval motility in parasitic nematodes. Parasitol. Res. 2007, S45-S56.
62. Simpson H.V., Przemeck S.M.C., Scott I., Thomas D.G., Green R.S., Reynolds G.W. Pathophysiology in Teladorsagia (Ostertagia) circumcincta-infected sheep selected for high fleece weight. Vet. Parasitol. 2009, 163:73-80.
63. Sokerya S., Waller P.J., Ledin I., Höglund J. The effects of short-term feeding of fresh cassava (Manihot esculenta) foliage on gastrointestinal nematode parasite infections in goats in Cambodia. Trop. Biomed. 2007, 24:47-54.
64. Suter R.J., Besier R.B., Perkins N.R., Robertson I.D., Chapman H.M. Sheep-farm risk factors for ivermectin resistance in Ostertagia circumcincta in Western Australia. Prev. Vet. Med. 2004, 14:257-269.
65. Taylor M.A., Hunt K.R., Goodyear K.L. Anthelmintic resistance detection methods. Vet. Parasitol. 2002, 103:183-194.
66. Timon V.M., Hanrahan J.P., 1985. Small ruminant production in the developing countries. FAO Animal Production and Health Paper No. 58.
67. Udeinya I.J., Mbah A.U., Chijioke C.P., Shu E.N. An antimalarial extract from neem leaves is antiretroviral. Trans. Roy. Soc. Trop. Med. Hyg. 2004, 98:435-437.
68. Várady M., Čorba J. Comparison of six in vitro tests in determining benzimidazole and levamisole resistance in Haemonchus contortus and Ostertagia circumcincta of sheep. Vet. Parasitol. 1999, 80:239-249.
69. Várady M., Corba J., Letkova V., Kovac G. Comparison of two versions of larval development test to detect anthelmintic resistance in Haemonchus contortus. Vet. Parasitol. 2009, 160:267-271.
70. Vercruysse J., Holdsworth P., Letonja T., Barth D., Conder G., Hamamotof K., Okano K. International harmonisation of anthelmintic efficacy guidelines. Vet. Parasitol. 2001, 96:171-193.
71. Zakaria Z.A., Khairi H.M., Somchit M.N., Sulaiman M.R., Mat Jais A.M., Reezal I., Mat Zaid N.N., Abdul Wahab S.N.Z., Fadzil N.S., Abdullah M., Fatimah C.A. The in vitro antibacterial activity and brine shrimp toxicity of Manihot esculenta var. Sri Pontian (Euphorbiacea) extracts. Int. J. Pharmacol. 2006, 2:216-220.