Advertisement

Journal of Parasitic Diseases

, Volume 41, Issue 2, pp 467–472 | Cite as

In vitro ovicidal activity of Peganum harmala seeds extract on the eggs of Fasciola hepatica

  • Mohammad MoazeniEmail author
  • Zahra Sadat Saadaty Ardakani
  • Mohammad Jamal Saharkhiz
  • Jafar Jalaei
  • Ali Asghar Khademolhoseini
  • Shahab Shams Esfand Abad
  • Amir Mootabi Alavi
Original Article

Abstract

Peganum harmala seeds extract has been previously reported to have antimicrobial and other medicinal properties. The aim of this study was to evaluate the ovicidal activity of the methanolic extract of P. harmala seeds against the eggs of F. hepatica. The phenolic compounds of the methanolic extract of P. harmala seeds were identified by HPLC analysis. Catechin, rutin, p-Coumaric acid, chloregenic acid and hesperetin were found to be the major phenolic compounds. F. hepatica eggs were collected from the gall bladder of naturally infected sheep. The eggs were exposed to two concentrations of P. harmala seeds extract (1 and 3 mg/mL) for 24 and 48 h. To investigate the effect of the P. harmala seeds extract on the miracidial formation, the treated eggs were incubated at 28 °C for 14 days. The results indicated that F. hepatica eggs were susceptible to the methanolic extract of P. harmala seeds. Following 24 h exposure of the eggs to P. harmala seeds extract with concentrations of 1 and 3 mg/mL, the miracidial formation reduced to 5 and 2.2 % respectively (compared with 60 % for the control group). Following 48 h of exposure of the eggs to P. harmala seeds extract with 1 mg/mL concentration, the miracidial formation reduced to 0.5 %. In this exposure time, no miracidial formation was observed in the eggs exposed to P. harmala seeds extract with concentration of 3 mg/mL. Therefore, the results of this study indicated that P. harmala seeds extract has high ovicidal activity against the eggs of F. hepatica. Accordingly, this extract may have the potential flukicidal activity against the immature and mature F. hepatica.

Keywords

Fasciola hepatica Miracidial formation Ovicidal Methanolic extract Peganum harmala Phenolic compounds 

References

  1. Alvarez L, Moreno G, Moreno L, Ceballos L, Shaw L, Fairweather I, Lanusse C (2009) Comparative assessment of albendazole and triclabendazole ovicidal activity on Fasciola hepatica eggs. Vet Parasitol 164:211–216CrossRefPubMedGoogle Scholar
  2. Astulla A, Zaima K, Matsuno Y, Hirasawa Y, Ekasari W, Widyawaruyanti A, Zaini NC, Morita H (2008) Alkaloids from the seeds of P. harmala showing antiplasmodial and vasorelaxant activities. J Nat Med 62:470–472CrossRefPubMedGoogle Scholar
  3. Berrougui H, Isabelle M, Cloutier M, Hmamouchi M, Khalil A (2006) Protective effects of Peganum harmala extract harmine and harmaline against human low-density lipoprotein oxidation. J Pharm Pharmacol 58:967–974CrossRefPubMedGoogle Scholar
  4. Brennan GP, Fairweather IF, Trudgett A, Hoey E, Coy M, McConville M, Meaney M, Robinson M, McFerran N, Ryan L, Lanusse C, Mottier L, Alvarez L, Solana H, Virkel G, Brophy PM (2007) Understanding triclabendazole resistance. Exp Mol Pathol 82:104–109CrossRefPubMedGoogle Scholar
  5. Brockwell YM, Elliott TP, Anderson GR, Stanton R, Spithill TW, Sangster NC (2014) Confirmation of Fasciola hepatica resistant to triclabendazole in naturally infected Australian beef and dairy cattle. Int J Parasitol Drugs Drug Resist 4:48–54CrossRefPubMedGoogle Scholar
  6. Chunmei D, Jiabo W, Weijun K, Cheng P, Xiaohe X (2010) Investigation of anti-microbial activity of catechin on Escherichia coli growth by microcalorimetry. Environ Toxicol Pharmacol 30:284–288CrossRefPubMedGoogle Scholar
  7. Costa CTC, Morais SM, Bevilaqua CML, Souza MMC, Leite FKA (2002) Ovicidal effect of Mangifera indica L. seed extracts on Haemonchus contortus. Braz J Vet Parasitol 11(57):60Google Scholar
  8. Daikoku T, Horiba K, Miyata K, Takemoto M, Okuda T, Yoshida Y et al (2011) Polyphenols including catechin from green tea with in vitro antiviral activity exhibited anti-herpes simplex virus activity but not anti-influenza virus activity in mice. J Trad Med 28:63–72Google Scholar
  9. Derakhshanfar A, Mirzaei M (2008) Effect of Peganum harmala (wild rue) extract on experimental ovine malignant theileriosis: pathological and parasitological findings. Onderstepoort J Vet Res 75:67–72CrossRefPubMedGoogle Scholar
  10. Diab TM, Mansour HH, Mahmoud SS (2009) Fasciola gigantica: parasitological and scanning electron microscopy study of the in vitro effects of ivermectin and/or artemether. Exp Parasitol 124:279–284CrossRefPubMedGoogle Scholar
  11. Diba K, Gerami Shoar M, Sharbatkhori M, Khorshivand Z (2011) Anti-fungal activity of alcoholic extract of Peganum harmala seed. J Med Plants Res 5:5550–5554Google Scholar
  12. Fairweather I (2009) Triclabendazole progress report 2005–2009: an advancement of learning? J Helminthol 83:139–150CrossRefPubMedGoogle Scholar
  13. Fairweather I, Boray JC (1999) Fasciolicides: efficacy actions resistance and its management. Vet J 158:81–112CrossRefPubMedGoogle Scholar
  14. Fan B, Liang J, Men J, Gao F, Li G, Zhao S (1997) Effect of total alkaloid of Peganum harmala in the treatment of experimental haemosporidian infections in cattle. Trop Anim Health Prod 29:77S–83SCrossRefPubMedGoogle Scholar
  15. Farouk L, Laroubi A, Aboufatima R, Benharref A, Chait A (2008) Evaluation of the analgesic effect of alkaloid extract of Peganum harmala L.: possible mechanisms involved. J Ethnopharmacol 115:449–454CrossRefPubMedGoogle Scholar
  16. Han Y, Ding Y, Xie D, Hu D, Li P, Li X, Xue W, Jin L, Song B (2015) Design, synthesis, and antiviral activity of novel rutin derivatives containing 1, 4-pentadien-3-one moiety. Eur J Med Chem 92:732–737CrossRefPubMedGoogle Scholar
  17. Harris JC, Plummer S, Turner MP, Lloyd D (2000) The microaerophilic flagellate Giardia intestinalis: Allium sativum (garlic) is an effective antigiardial. Microbiology 146:3119–3127CrossRefPubMedGoogle Scholar
  18. Hounzangbe-Adote MS, Zinsou FE, Affognon KJ, Koutinhouin B, Adamou-N’Diaye M, Moutaeirou K (2001) Efficacite antiparasitaire de la poudre des graines de papaye (Carica papaya) surles strongles gastro intestinaux des moutons Djallonke au sud du Benin. Rev Elev Med Vet Pays Trop 54:225–229CrossRefGoogle Scholar
  19. Iacopini P, Baldi M, Storchi P, Sebastiani L (2008) Catechin, epicatechin, quercetin, rutin and resveratrol in red grape: content, in vitro antioxidant activity and interactions. J Food Compos Anal 21:589–598CrossRefGoogle Scholar
  20. Kadoma Y, Fujisawa S (2008) A comparative study of the radical-scavenging activity of the phenolcarboxylic acids caffeic acid, p-coumaric acid, chlorogenic acid and ferulic acid, with or without 2-mercaptoethanol, a thiol, using the induction period method. Molecules 13:2488–2499CrossRefPubMedGoogle Scholar
  21. Kamaraj C, Rahuman AA (2011) Efficacy of anthelmintic properties of medicinal plant extracts against Haemonchus contortus. Res Vet Sci 91:400–404CrossRefPubMedGoogle Scholar
  22. Keiser J, Rinaldi L, Veneziano V, Mezzino L, Tanner M, Utzinger J, Cringoli G (2008) Efficacy and safety of artemether against a natural Fasciola hepatica infection in sheep. Parasitol Res 103:517–522CrossRefPubMedGoogle Scholar
  23. Kirchhofer C, Vargas M, Braissant O, Dong Y, Wang X, Vennerstrom JL, Keiser J (2011) Activity of OZ78 analogues against Fasciola hepatica and Echinostoma caproni. Acta Trop 118:56–62CrossRefPubMedPubMedCentralGoogle Scholar
  24. Lamchouri F, Settaf A, Cherrah Y, Zemzami M, Lyoussi B, Zaid A, Atif N, Hassar M (1999) Antitumour principles from Peganum harmala seed. Therapie 54:753–758PubMedGoogle Scholar
  25. Lane G (1998) Anthelmintic resistance. Vet Rec 143:232Google Scholar
  26. Liu L, Zhao T, Cheng XM, Wang CH, Wang ZT (2013) Characterization and determination of trace alkaloids in seed extracts from Peganum harmala linn. Using LC-ESI-MS and HPLC. Acta Chromatogr 25:221–240CrossRefGoogle Scholar
  27. Ma X, Liu D, Tang H, Wang Y, Wu T, Li Y, Yang J, Yang J, Sun S, Zhang F (2013) Purification and characterization of a novel antifungal protein with antiproliferation and anti-HIV-1 reverse transcriptase activities from Peganum harmala seed. Acta Biochim Biophys Sin 45:87–94CrossRefPubMedGoogle Scholar
  28. Martínez-Valladares M, Famularo MR, Fernández-Pato N, Castanón- Ordónez L, Cordero-Pérez C, Rojo-Vázquez FA (2010) Activity of nytroxinil against Fasciola hepatica resistant to triclabendazole in a naturally infected sheep flock. Parasitol Res 107:1205–1211CrossRefPubMedGoogle Scholar
  29. Mirzaei M (2007) Treatment of natural tropical theileriosis with the extract of the plant Peganum harmala. Korean J Parasitol 45:267–271CrossRefPubMedPubMedCentralGoogle Scholar
  30. Mirzaie M, Nosratabadi SJ, Derakhshanfar A, Sharifi I (2007) Antileishmanial activity of Peganum harmala extract on the in vitro growth of Leishmania major promastigotes in comparison to a trivalent antimony drug. Veterinarski Arhiv 77:365–375Google Scholar
  31. Mitchell GBB, Maris L, Bonniwell MA (1998) Triclabendazole-resistant liver fluke in Scottish sheep. Vet Rec 143:399PubMedGoogle Scholar
  32. Moazeni M, Khademolhoseini AA (2016) Ovicidal effect of the methanolic extract of ginger (Zingiber officinale) on Fasciola hepatica eggs: an in vitro study. J Parasit Dis 40:662–666CrossRefPubMedGoogle Scholar
  33. Moazeni M, Nazer A (2010) In vitro effectiveness of garlic (Allium sativum) extract on scolices of hydatid cyst. World J Surg 34:2677–2681CrossRefPubMedGoogle Scholar
  34. Moazeni M, Ansari-Lari M, Masoodfar M, Hosseinzadeh S, Mootabi Alavi A (2010) Lethal effect of high temperatures on the eggs of Fasciola hepatica. Iran J Vet Res 11:168–173Google Scholar
  35. Moazeni M, Larki S, Oryan A, Saharkhiz MJ (2014a) Preventive and therapeutic effects of Zataria multiflora methanolic extract on hydatid cyst: an in vivo study. Vet Parasitol 205:107–112CrossRefPubMedGoogle Scholar
  36. Moazeni M, Larki S, Saharkhiz MJ, Oryan A, Ansary Lari M, Motabi Alavi A (2014b) In vivo study of the efficacy of the aromatic water of Zataria multiflora on hydatid cysts. Antimicrob Agents Chemother 58:6003–6008CrossRefPubMedPubMedCentralGoogle Scholar
  37. Nenaah G (2010) Antibacterial and antifungal activities of (beta)-carboline alkaloids of Peganum harmala (L) seed and their combination effects. Fitoterapia 81:779–782CrossRefPubMedGoogle Scholar
  38. Nery PS, Duarte ER, Martins ER (2009) Eficácia de plantas para o controle de nematoides gastrintestinais de pequenos ruminantes. Rev Bras Plantas Med 11:330–338CrossRefGoogle Scholar
  39. O’Brien DJ (1998) Fasciolosis: a threat to livestock. Irish Vet J 51:539–541Google Scholar
  40. Obeng-Ofori D, Reichmuth CH (1997) Bioactivity of eugenol a major component of Ocimum suave (Wild) against four species of stored product Coleoptera. Int J Pest Manag 43:89–94CrossRefGoogle Scholar
  41. Obeng-Ofori D, Reichmuth CH, Bekele J, Hassanali A (1997) Biological activity of 1, 8 cineole a major component of essential oil of Ocimum kenyense (Ayobaugira) against stored product beetles. J Appl Entomol 121:237–243CrossRefGoogle Scholar
  42. Overend DJ, Bowen FL (1995) Resistance of Fasciola hepatica to triclabendazole. Aust Vet J 72:275–276CrossRefPubMedGoogle Scholar
  43. Panarella M (2002) Fenbendazole used as a benzimidazole anthelmintic and antiprotozoal agent. Compendium 24:40–44Google Scholar
  44. Rashan LJ, Adaay MH, Al-Khazraji ALT (1989) In vitro antiviral activity of the aqueous extract from the seed of Peganum harmala. Fitoterapia 60:365–367Google Scholar
  45. Sangster NC (1999) Anthelmintic resistance: past present and future. Int J Parasitol 29:115–124CrossRefPubMedGoogle Scholar
  46. Shahverdi AR, Monsef-Esfahani HR, Nickavar B, Bitarafan L, Khodaee S, Khoshakhlagh N (2005) Antimicrobial activity and main chemical composition of two smoke condensates from Peganum harmala seed. Z Naturforsch C 60:707–710CrossRefPubMedGoogle Scholar
  47. Shimizu N, Naoe T, Kawazoe Y, Sakagami H, Nakashima H, Murakam T, Yamamoto N (1993) Lignified materials as medicinal resources. VI. Anti-HIV activity of dehydrogenation polymer of p-coumaric acid, a synthetic lignin, in a quasi-in vivo assay system as an intermediary step to clinical trials. Biol Pharm Bull 16:434–436CrossRefPubMedGoogle Scholar
  48. Singh AB, Chaturvedi JP, Narender T, Srivastava AS (2008) Preliminary studies on the hypoglycemic effect of Peganum harmala L. seed ethanol extract on normal and streptozotocin induced diabetic rats. Indian J Clin Biochem 23:391–393CrossRefPubMedPubMedCentralGoogle Scholar
  49. Soliman AM, Fahmy SR (2011) Protective and curative effects of the 15 KD isolated protein from the Peganum harmala L. seed against carbon tetrachloride induced oxidative stress in brain, tests and erythrocytes of rats. Eur Rev Med Pharmacol Sci 15:888–899PubMedGoogle Scholar
  50. Tunc IB, Berger BM, Erler F, Dagli F (2000) Ovicidal activity of essential oils from five plants against two stored-product insects. J Stored Prod Res 36:161–168CrossRefGoogle Scholar
  51. Ultee A, Bennik MHJ, Moezelaar R (2002) The phenolic hydroxyl groupof carvacrol is essential for action against the food borne pathogen Bacillus cereus. Appl Environ Microbiol 68:1561–1568CrossRefPubMedPubMedCentralGoogle Scholar
  52. Wolstenholme AJ, Fairweather I, Pricard R, Von Samson-Himmelstjerna G, Sangster NC (2004) Drug resistance in veterinary helminths. Trends Parasitol 20:469–476CrossRefPubMedGoogle Scholar
  53. Zhu W, Zhang Z (2014) Preparation and characterization of catechin-grafted chitosan with antioxidant and antidiabetic potential. Int J Biol Macromol 70:150–155CrossRefPubMedGoogle Scholar

Copyright information

© Indian Society for Parasitology 2016

Authors and Affiliations

  • Mohammad Moazeni
    • 1
    Email author
  • Zahra Sadat Saadaty Ardakani
    • 1
  • Mohammad Jamal Saharkhiz
    • 2
  • Jafar Jalaei
    • 3
  • Ali Asghar Khademolhoseini
    • 1
  • Shahab Shams Esfand Abad
    • 1
  • Amir Mootabi Alavi
    • 1
  1. 1.Department of Pathobiology, School of Veterinary MedicineShiraz UniversityShirazIran
  2. 2.Department of Horticulture, College of AgricultureShiraz UniversityShirazIran
  3. 3.Department of Pharmacology and Toxicology, School of Veterinary MedicineShiraz UniversityShirazIran

Personalised recommendations