Skip to main content
SpringerLink
Log in

In vitro acaricidal effect of Melia azedarach and Artemisia herba-alba extracts on Hyalomma dromedarii (Acari: Ixodidae): embryonated eggs and engorged nymphs

  • Original Article
  • Published:
Journal of Parasitic Diseases Aims and scope Submit manuscript

Abstract

The present study aimed to evaluate the in vitro efficacy of four medicinal plant extracts: petroleum ether and ethyl alcohol extracts of the ripen fruits of Melia azedarach and whole aerial parts of Artemisia herba-alba against the two inactive stages of the camel tick Hyalomma dromedarii, embryonated eggs and engorged nymphs in comparison to reference acaricide Butox®5.0 (Deltamethrin). Egg and nymphal immersion tests at four concentrations with three replicates were used. The deformity in larvae hatched from treated eggs and adults moulted from treated nymphs were observed and photographed by light microscope (LM) and scanning electron microscope (SEM). The results showed that M. azedarach and A. herba-alba extracts revealed higher significant toxic effects on embryonated eggs and engorged nymphs comparing with the reference acaricide (Butox®5.0) and control. In egg emmersion test, the LC50 of petroleum ether extracts of M. azedarach and A. herba-alba was 3.14 and 3.91%, respectively and LC50 of the respective ethyl alcohol extracts was 1.77 and 2.45%. In nymphal immersion test, LC50 of petroleum ether extracts of M. azedarach and A. herba-alba was 0.26 and 1%, respectively, and LC50 of the respective ethyl alcohol extracts was 4.17 and 8.7%. Abnormalities were observed by LM and SEM in the larvae hatched from the treated eggs as incomplete development of legs and mouth parts as well as shrinkage mainly in legs and mouthparts of adults emerged from treated nymphs. In conclusion, all extracts and petroleum ether extracts of the two plants have great potential to be developed as a novel acaricidal for controlling eggs and nymphs of H. dromedarii, respectively.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abbas A, Abbas RZ, Khan JA, Iqbal Z, Bhatt MMH, Sindhu ZD, Zia MA (2014) Integrated strategies for the control and prevention of dengue vectors with particular reference to Aedes aegypti. Pak Vet J 34:1–10

    Google Scholar 

  • Abbas A, Iqbal Z, Abbas RZ, Khan MK, Khan JA, Sindhu ZD, Mahmood MS, Saleemi MK (2017) In vivo anticoccidial effects of Beta vulgaris (sugar beet) in broiler chickens. Microb Path 111:139–144

    CAS  Google Scholar 

  • Abdel-Shafy S, Soliman MM, Habeeb SM (2007) In vitro acaricidal effect of some crude extracts and essential oils of wild plants against certain tick species. Acarologia 47:33–42

    Google Scholar 

  • Abdel-Shafy S, Allam NA, Mediannikov O, Parola P, Raoult D (2012) Molecular detection of spotted fever group rickettsiae associated with ixodid ticks in Egypt. Vector Borne Zoonotic Dis 12:346–359

    PubMed  Google Scholar 

  • Abdullah HH, El-Molla A, Salib FA, Allam NA, Ghazy AA, Abdel-Shafy S (2016) Morphological and molecular identification of the brown dog tick Rhipicephalus sanguineus and the camel tick Hyalomma dromedarii (Acari: Ixodidae) vectors of Rickettsioses in Egypt. Vet World 9:1087–1101

    PubMed  PubMed Central  CAS  Google Scholar 

  • Aboelhadid SM, Arafa WM, Mahrous LN, Fahmy MM, Kamel AA (2018) Molecular detection of Rhipicephalus (Boophilus) annulatus resistance against deltamethrin in middle Egypt. Vet Parasitol Reg Stud Rep 13:198–204

    CAS  Google Scholar 

  • Al-Rajhy DH, Alahmed AM, Hussein HI, Kheir SM (2003) Acaricidal effects of cardiac glycosides, azadirachtin and neem oil against the camel tick, Hyalomma dromedarii (Acari: Ixodidae). Pest Manag Sci 59:1250–1254

    PubMed  CAS  Google Scholar 

  • Bansal GC (2005) Bovine theileriosis in India: an overview. Proc Nat Acad Sci India 75:134–143

    Google Scholar 

  • Borges LMF, Ferri PH, Silva WJ, Silva WC, Silva JG (2003) In vitro efficacy of extracts of Melia azedarach against the tick Boophilus microplus. Med Vet Entomol 17:228–231

    PubMed  CAS  Google Scholar 

  • Brody AR, Wharton GW (1971) The use of glycerol-kcl in scanning electron microscopy of Acari. Ann Entomol Soc Am 64:528–530

    Google Scholar 

  • Chagas ACDS, Georgetti CS, Carvalho COD, Oliveira MCDS, Rodrigues RA, Foglio MA, Magalhaes PMD (2011) In vitro activity of Artemisia annua L (Asteraceae) extracts against Rhipicephalus (Boophilus) microplus. Rev Bras Parasitol Vet 20:31–35

    PubMed  Google Scholar 

  • Chagas ACS, Barros LD, Cotinguiba F, Furlan M, Giglioti R, Oliveira MCS, Bizzo HR (2012) In vitro efficacy of plant extracts and synthesized substances on Rhipicephalus (Boophilus) microplus (Acari: Ixodidae). Parasitol Res 110:295–303

    Google Scholar 

  • De Sousa LA, Da Costa DP, Ferri PH, Showler AT, Borges LM (2014) Soil quality influences efficacy of Melia azedarach (Sapindales: Meliaceae), fruit extracts against Rhipicephalus (Boophilus) microplus (Acari: Ixodidae). Ann Entomol Soc Am 107:484–489

    Google Scholar 

  • Ehabsoft. http://www.ehabsoft.com/Ldpline

  • Elghali A, Hassan SM (2009) Ticks (Acari: Ixodidae) infesting camels (Camelus dromedarius) in Northern Sudan. Onderstepoort J Vet Res 76:177–185

    PubMed  CAS  Google Scholar 

  • El-Kammah KM (1969) Definition of the characters of Hyalomma anatolicum (Koch) subspecies anatolicum and excavatum and their hybrids. Ph.D. Thesis. Faculty of Agri, Cairo University, p 103

  • El-Seedi HR, Azeem M, Khalil NS, Sakr HH, Khalifa SA, Awang K, Borg-Karlson AK (2017) Essential oils of aromatic Egyptian plants repel nymphs of the tick Ixodes ricinus (Acari: Ixodidae). Exp Appl Acarol 73:139–157

    PubMed  PubMed Central  CAS  Google Scholar 

  • Estrada-Pena A, Bouattour A, Camicas JL, Walker AR (2004) Ticks of domestic animals in the Mediterranean region. University of Zaragoza, Spain, p 131

    Google Scholar 

  • Fahmy MM (1980) Studies on the cattle ticks and parasitic tick born disease in Giza Governorate. M.V.Sc. Vet. Thesis Fac Vet Med Cairo Univ Egypt

  • Fahmy MM (1982) Parasitological and Ecological studies on the ticks Hyalomma anatolicum subspecies (H. a. anatolicum and H. a. excavatum), the main vectors of theileriosis in cattle in Egypt. Cairo Univ PhD. Thesis

  • Ferreira JF, Gonzalez JM (2008) Chemical and biological stability of artemisinin in bovine rumen fluid and its kinetic in goats (Capra hircus). Rev Bras Parasitol Vet 17:103–109

    PubMed  Google Scholar 

  • Finney DJ (1962) Probit analysis a statistical treatment of the response curve. Cambridge University Press, Cambridge

    Google Scholar 

  • Ghosh S, Azhahianambi P, Yadav MP (2007) Upcoming and future strategies of tick control: a review. J Vect Borne Dis 44:79–89

    CAS  Google Scholar 

  • Godara R, Parveen S, Katoch R, Yadav A, Verma PK, Katoch M, Kaur D, Ganai A, Raghuvanshi P, Singh NK (2014) Acaricidal activity of extract of Artemisia absinthium against Rhipicephalus sanguineus of dogs. Parasitol Res 113:747–754

    PubMed  CAS  Google Scholar 

  • Godara R, Parveen S, Katoch R, Yadav A, Katoch M, Khajuria JK, Singh NK (2015) Acaricidal activity of ethanolic extract of Artemisia absinthium against Hyalomma anatolicum ticks. Exp Appl Acarol 65:141–148

    PubMed  CAS  Google Scholar 

  • Guglielmone AA, Robbins RG, Apanaskevich DA, Petney TN, Estrada-Pena A, Horak IG (2014) Hard ticks (Acari: Ixodida: Ixodidae) of the world. Springer, Heidelberg

    Google Scholar 

  • Habeeb SM, Abdel-Shafy S, Youssef AA (2007) Light, scanning electron microscopy and SDS-PAGE studies on the effect of the essential oil Citrus sinensis var. balady on the embryonic development of camel tick Hyalomma dromedarii (Koch 1818) (Acari-Ixodidae). Pak J Biol Sci 10:1151–1160

    CAS  Google Scholar 

  • Homsher PJ, Sonenshine DE (1977) Scanning electron microscopy of ticks for systematic studies. 2. Structure of Haller’s organ in Ixodes brunneus and Ixodes frontalis. J Med Entomol 14:93–97

    PubMed  CAS  Google Scholar 

  • Idris M, Abbas RZ, Masood S, Rehman T, Farooq U, Babar W, Hussain R, Raza A, Riaz U (2017) The potential of antioxidant rich essential oils against avian coccidiosis. World Poult Sci J 73:89–104

    Google Scholar 

  • Keirans JE, Clifford CM, Corwin D (1976) Ixodes sigelos, n. sp. (Acarina: Ixodidae), parasite of rodents in Chile, with a method for preparing ticks for examination by scanning electron microscopy. Acarologia 18:217–225

    PubMed  CAS  Google Scholar 

  • Khan MN, Sajid MS, Rizwan HM, Qudoos A, Abbas RZ, Riaz M, Khan MK (2017) Comparative efficacy of six anthelmintic treatments against natural infection of fasciola species in sheep. Pak Vet J 37:65–68

    CAS  Google Scholar 

  • Laghzaoui EM, Kasrati A, Abbad A, Leach D, Spooner-Hart R, El Mouden EH (2018) Acaricidal properties of essential oils from Moroccan plants against immature ticks of Hyalomma aegyptium (Linnaeus, 1758); an external parasite of the spur-thighed tortoise (Testudograeca). Int J Acarol 44:315–321

    Google Scholar 

  • Liebisch A, Abel-Rahman MS, Hoogstraal HC (1984) Studies on the occurrence and veterinary significance of ticks domestic animals in Egypt. A Project report in: Recent German research on problems of parasitology, Animal Health and Animal Breeding in the Tropics and Sub Tropics 74–84

  • Madbouly MH (1965) Comparative studies on the biology, behavior and sensory physiology of two Hyalomma ticks in Egypt. Ph.D. Thesis. Dep Entomol Fac Sci Cairo University, pp 301–308

  • Masood S, Abbas RZ, Iqbal Z, Mansoor MK, Sindhu ZD, Zia MA, Khan JA (2013) Role of natural antioxidants for the control of coccidiosis in poultry. Pak Vet J 33:401–407

    CAS  Google Scholar 

  • Maxwell CA, Msuya E, Sudi M, Njunwa KJ, Carneiro IA, Curtis CF (2002) Effect of community-wide use of insecticide-treated nets for 3-4 years on malarial morbidity in Tanzania. Trop Med Int Health 7:1003–1008

    PubMed  CAS  Google Scholar 

  • Mohamed AEHH, El-Sayed M, Hegazy ME, Helaly SE, Esmail AM, Mohamed NS (2010) Chemical constituents and biological activities of Artemisia herba-alba. Rec Nat Prod 4:1–25

    CAS  Google Scholar 

  • Mulla MS, Su T (1999) Activity of biological effects of neem products against arthropods of medical and veterinary importance. J Am Mosq Cont Assoc 15:133–152

    CAS  Google Scholar 

  • Osman IM, Mohammed AS, Abdalla AB (2014) Acaricidal properties of two extracts from Guiera senegalensis JF Gmel. (Combrataceae) against Hyalomma anatolicum (Acari: Ixodidae). Vet Parasitol 199:201–205

    PubMed  Google Scholar 

  • Pillay P, Maharaj VJ, Smith PJ (2008) Investigating South African plants as a source of new antimalarial drugs. J Ethnopharmacol 119:438–454

    PubMed  CAS  Google Scholar 

  • Ramadan MY (1997) Studies on some ectoparasites of camels. MSc thesis, Zagazig University (Benha Branch), Egypt

  • Roberts LS, Janovy J (2005) Foundations of parasitology, 7th edn. McGraw Hill, New York, pp 644–646

    Google Scholar 

  • Rubae AAY (2009) The potential uses of Melia azedarach L. as pesticidal and medicinal plant, review. Am Eurasian J Sustain Agric 3:185–195

    Google Scholar 

  • Sariosseiri A, Moshaverinia A, Khodaparast MHH, Kalidari GA (2018) In vitro acaricidal effect of Melia azedarach ripe fruit extract against Dermanyssus gallinae (Acari: Dermanyssidae). Persian J Acarol 7:203–208

    Google Scholar 

  • Showler AT (2017) Botanically based repellent and insecticidal effects against horn flies and stable flies (Diptera: Muscidae). J Integr Pest Manag 8:1–11

    Google Scholar 

  • Soares SF, Borges LMF, de Sousa Braga R, Ferreira LL, Louly CCB, Tresvenzol LMF, Ferri PH (2010) Repellent activity of plant-derived compounds against Amblyomma cajennense (Acari: Ixodidae) nymphs. Vet Parasitol 167:67–73

    PubMed  CAS  Google Scholar 

  • Tunon H, Thorsell W, Mikiver A, Malander I (2006) Arthropod repellency, especially tick (Ixodes ricinus), exerted by extract from Artemisia abrotanum and essential oil from flowers of Dianthus caryophyllum. Fitoterapia 77:257–261

    PubMed  CAS  Google Scholar 

  • Van Straten M, Jongejan F (1993) Ticks (Acari: Ixodidae) infesting the Arabian camel (Camelus dromedarius) in the Sinai, Egypt with a note on the acaricidal efficacy of Ivermectin. Exp Appl Acarol 17:605–616

    PubMed  Google Scholar 

  • Walker AR (2003) Ticks of domestic animals in Africa: a guide to identification of species. Bioscience Reports, Edinburgh, pp 3–210

    Google Scholar 

  • Yadav PK, Rafiqi SM, Panigrahi PN, Kumar D, Kumar R, Kumar S (2017) Recent trends in control of ectoparasites: a review. J Entomol Zool Stud 5:808–813

    Google Scholar 

Download references

Acknowledgements

This study is a part of a Ph.D. Thesis to be submitted to The Department of Parasitology, Faculty of Veterinary Medicine, Cairo University. The study was carried out by financial support of National Research Centre as a part of Ph.D. Thesis No. 12/2/19.

Author information

Authors and Affiliations

  1. Department of Parasitology and Animal Diseases, Veterinary Research Division, National Research Centre, Dokki, Giza, Egypt

    Hoda S. M. Abdel-Ghany, Sobhy Abdel-Shafy & Rabab M. El-Khateeb

  2. Department of Parasitology, Faculty of Veterinary Medicine, Cairo University, Giza, Egypt

    Magdy M. Fahmy & Mai M. Abuowarda

  3. Department of Agriculture Microbiology, Agriculture and Biology Research Division, National Research Centre, Dokki, Giza, Egypt

    Essam M. Hoballah

Authors
  1. Hoda S. M. Abdel-Ghany
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Magdy M. Fahmy
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mai M. Abuowarda
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sobhy Abdel-Shafy
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rabab M. El-Khateeb
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Essam M. Hoballah
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MMF, SA, MMA, RME, and HSMA designed the experiments. EMH and HSMA participated in the preparation of the plant extracts. MMF, SA, MMA, RME, and HSMA shared in the following protocols: bioassay of plant extracts against both embryonated eggs and engorged nymphs, detection of abnormalities in treated tick specimens by light microscope and scanning electron microscopy. SA and HSMA analysed and tabulated the data. MMF, SA, MMA, and HSMA wrote the draft of the manuscript. All authors revised and approved the final version of the manuscript.

Corresponding author

Correspondence to Sobhy Abdel-Shafy.

Ethics declarations

Conflict of interest

The authors declare that there is no conflict of interest.

Ethical standard

This study was approved by Ethical Committee for Medical Research (MREC) at the National Research Centre (NRC), Egypt in accordance with local laws and regulations (Approval Protocol No. 19085).

Informed consent

Consent was obtained from the owners of camels included in this study.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Abdel-Ghany, H.S.M., Fahmy, M.M., Abuowarda, M.M. et al. In vitro acaricidal effect of Melia azedarach and Artemisia herba-alba extracts on Hyalomma dromedarii (Acari: Ixodidae): embryonated eggs and engorged nymphs. J Parasit Dis 43, 696–710 (2019). https://doi.org/10.1007/s12639-019-01149-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12639-019-01149-9

Keywords

Search

Navigation