Abstract
Haemonchosis is a worldwide helminthic disease affecting ruminants. The anthelminthic resistance has become raised. Medicinal plants are safely used as synthetic anthelmintics. Currently, the efficacy of black pepper essential oil (BPO) and tea tree oil (TTO) were in vitro evaluated against Haemonchus contortus adults, eggs and larvae at concentrations of 1.25, 2.5 and 5 mg/ml in addition to the commercially used albendazole at a concentration of 10 μg/ml. Oils were used in both normal and nanoparticles-loaded forms. Oxidative stress enzymes of worms were estimated. Scanning electron microscopy (SEM) for treated worms was done. Both normal and nanoemulsion forms of both BPO and TTO stopped the adult motility [BPO 2.5 h (hrs), NBPO 1.5 h, TTO 3 h, NTTO 1.5 h] and induced a marked decrease in the oviposition. Post treatment, the egg development and hatching were significantly (P ≤ 0.05) reduced. The damage of the egg shell, embryonal cessation and destruction of larvae occurred. Noticeable elevated antioxidant enzymes (catalase CAT, glutathione transferase GST and glutathione GSH) were found, while oxidative enzymes (lipid peroxidation LPO and nitric oxide synthase NOS) decreased. Scanning electron microscopy (SEM) for both oil-treated worms revealed anterior ends damage and several cuts associated with cuticular pores. The use of albendazole induced more or less anthelmintic and enzymatic activities with less morphological alterations of adults revealed by SEM. This study proved the marked anthelmintic potency of the BPO and TTO and their nanoemulsion forms against H. contortus rather than the widely used anthelmintic drugs.
Similar content being viewed by others
Data availability
The datasets uses and/or analyzed in the manuscript are available from the corresponding author upon reasonable request.
Code availability
Not applicable.
References
Adams RP (2007) Identification of essential oil components by gas chromatography/mass spectrometry, 4th edn. Allured Publishing, Carol Stream, IL, USA
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126. https://doi.org/10.1016/s0076-6879(84)05016-3
Albadawi ROE (2010) In vivo and in vitro anthelmintic activity of Balanites aegyptiaca and Artemisia herba Alba on Haemonchus contortus of sheep. PhD thesis Fac Vet Med Khartoum
Anthony JP, Fyfe L, Smith H (2005) Plant active components—a resource for antiparasitic agent. Trends Parasitol 21(10):462–468. https://doi.org/10.1016/j.pt.2005.08.004
Ashokkumar K, Murugan M, Dhanya MK, Pandian A, Warkentin TD (2021) Phytochemistry and therapeutic potential of black pepper [Piper nigrum (L.)] essential oil and piperine: a review. Clin Phytosci 7(52):1–11. https://doi.org/10.1186/s40816-021-00292
Baihaqi ZA, Widiyono I, Nurcahyo W (2019) Prevalence of gastrointestinal worms in Wonosobo andthin-tailed sheep on the slope of mount sumbing, central java Indonesia. Vet World 12(11):1866–1871. https://doi.org/10.14202/vetworld.2019.1866-1871
Baihaqi ZA, Widiyono I, Nurcahyo W (2020) In vitro anthelmintic activity of aqueous and ethanol extracts of Paraserianthes falcataria bark waste against Haemonchus contortus obtained from a local slaughterhouse in Indonesia. Vet World 13(8):1549–1554. https://doi.org/10.14202/vetworld.2020.1549-1554
Baldissera MD, Da Silva AS, Oliveira CB, Santos RC, Vaucher RA, Raffin RP, Gomes P, Dambros MG, Miletti LC, Boligon AA, Athayde ML, Monteiro SG (2014) Trypanocidal action of tea tree oil (Melaleuca alternifolia) against Trypanosoma evansiin vitro and in vivo using mice as experimental model. Exp Parasitol 141:21–27. https://doi.org/10.1016/j.exppara.2014.03.007
Benchaar C, McAllister TA, Chouinard PY (2008) Digestion, ruminal fermentation, ciliate protozoal populations, and milk production from dairy cows fed cinnamaldehyde, quebracho con densed tannin, or Yucca schidigera saponinextracts. J Dairy Sci 91(12):4765–4777. https://doi.org/10.3168/jds.2008-1338
Betts TJ (1994) Evaluation of a “Chirasil-Val” capillary for the gas chromatography of volatile oil constitu- ents, including sesquiterpenes in patchouli oil. J ChromatogrA 664:295–300. https://doi.org/10.1016/0021-9673(94)87020-9
Brophy JJ, Davies NW, Southwell IA, Stiff IA, Williams LR (1989) Gas chromatographic quality control for oil of Melaleuca terpinen-4-ol type (Australian tea tree). J Agric Food Chem 37(5):1330–1335. https://doi.org/10.1021/jf00089a027
Carvalho CO, Chagas ACS, Cotinguiba F, Furlan M, Brito LG, Chaves FC, Amarante AF (2012) The anthelmintic effect of plant extracts on Haemonchus contortus and Strongyloides venezuelensis. Vet Parasitol 183(3–4):260–268. https://doi.org/10.1016/j.vetpar.2011.07.051
Cawthorne R, Whitehead J (1983) Isolation of benzimidazole resistant strains of Ostertagia circumcincta from British sheep. Vet Rec 112(12):274–277. https://doi.org/10.1136/vr.112.12.274
Chagas ACS, Katiki LM, Silva IC, Giglioti R, Esteves SN, Oliveira MCS (2013) Haemonchus contortus: a multiple-resistant Brazilian isolate and the costs for its characterization and maintenance for research use. Parasitol Int 62(1):1–6. https://doi.org/10.1016/j.parint.2012.07.001
Coles GC (2005) Anthelmintic resistance looking to the future: a UK perspective. Res Vet Sci 78(2):99–108. https://doi.org/10.1016/j.rvsc.2004.09.001
DeVaney JA, Craig TM, Rowe LD (1992) Resistance to ivermectin by Haemonchus contortus in goats and calves. Int J Parasitol 22(3):369–376. https://doi.org/10.1016/s0020-519(05)80015-3
Draper HH, Hadley M (1990) Malondialdehyde determination as index of lipid Peroxidation. Methods Enzymol 186:421–431. https://doi.org/10.1016/0076-6879(90)86135-i
Drudge J, Szanto J, Wyant Z, Elam G (1964) Field studies on parasite control in sheep:comparison of thiabendazole, ruelene, and phenothiazine. Am J Vet Res 25:1512–1518
Entrocasso C, Alvarez L, Manazza J, Lifschitz A, Borda B, Virkel G, Mottier L, nusse C (2008) Clinical efficacy assessment of the albendazole–ivermectin combination in lambs parasitized with resistant nematodes. Vet Parasitol 155(3–4):249–256. https://doi.org/10.1016/j.vetpar.2008.04.015
Ferreira LE, Benincasa BI, Fachin AL, Taleb SH, França SC, Souza AC, Beleboni RO (2018) Essential oils of Citrus aurantifolia, Anthemisnobile and Lavandula officinalis: in vitro anthelmintic activities against Haemonchus contortus. Parasit Vectors 11:269. https://doi.org/10.1186/s13071-
Fetterer RH, Rhoads ML (1993) Biochemistry of the nematode cuticle: relevance to parasitic nematodes of livestock. Vet Parasitol 46(1–4):103–111. https://doi.org/10.1016/0304-4017(93)90051-n
Gaínza YA, Domingues LF, Perez OP, Rabelo MD, López ER, de Chagas AC, S, (2015) Anthelmintic activity in vitro of Citrus sinensis and Melaleuca quinquenervia essential oil from Cuba on Haemonchus contortus. Ind Crops Prod 76:647–652. https://doi.org/10.1016/j.indcrop.2015.07.056
Gaínza YA, Fantatto RR, Chaves FCM, Bizzo HR, Esteves SN, de Chagas AC (2016) Piper aduncum against Haemonchus contortus isolates: crossresistance and the research of natural bioactive compounds. Braz J Vet Parasitol 25(4):383–393. https://doi.org/10.1590/S1984-29612016073
Getachew T, Dorchies P, Jacquiet P (2007) Trends and challenges in the effective and sustainable control of Haemonchuscontortus infection in sheep. Rev Parasite 14(1):3–14. https://doi.org/10.1051/parasite/2007141003
Gilleard JS (2013) Haemonchus contortus as a paradigm and model to study anthelmintic drug resistance. Parasitology 140:1506–1522. https://doi.org/10.1017/S0031182013001145
Goel V, Singla LD, Choudhury D (2020) Cuminaldehyde induces oxidative stress-mediated physical damage and death of Haemonchus contortus. Biomed Pharmacother 130:110411. https://doi.org/10.1016/j.biopha.2020.110411
Grando TH, de Sá MF, Baldissera MD, Oliveira CB, de Souza ME, Raffin RP, Santos RCV, Domingues R, Minho AP, Leal MLR, Monteiro SG (2016) In vitro activity of essential oils of free and nanostructured Melaleuca alternifolia and of terpinen-4-ol on eggs and larvae of Haemonchus contortus. J Helminthol 90(3):377–382. https://doi.org/10.1017/S0022149X15000401. (Epub 2015 Jun 22)
Habig WH, Jakoby WB (1981) Assays for differentiation of glutathione S-Transferases. Methods Enzymol 77:398–405. https://doi.org/10.1016/s0076-6879(81)77053-8
Hassan NMF, Zaghawa AA, Abu-Elezz NMT, Nayel MA, Salama AA (2021) Efficacy of some Egyptian native plant extracts against Haemonchus contortusin vitro and in experimentally infected sheep along with the associated haematological and biochemical alterations. Bull Natl Res Cent 45(180):1–10. https://doi.org/10.1186/s42269-021-00636-5
Hoste H, Martinez-Ortiz-De-Montellano C, Manolaraki F, Brunet S, Ojeda-Robertos N, Fourquaux I, Torres-Acosta JFJ, Sandoval-Castro CA (2015) Direct and indirect effects of bioactive tannin-rich tropical and temperate legumes against nematode infections. Vet Parasitol 186(1–2):18–27. https://doi.org/10.1016/j.exppara.2012.11.024
Huynh Q, Phan TD, Thieu VQQ, Tran ST, Do HS (2012) Extraction and refining of essential oil from Australian tea tree, Melaleuca alterfornia, and the antimicrobial activity in cosmetic products. J Phys Conf Ser 352(1):129–133. https://doi.org/10.1088/1742-6596/352/1/012053
Ibrahium SM, Wahba AA, Farghali AA, Abdel-Baki AAS, Mohamed S, Al-Quraishy SAA, Hassan AO, Aboelhadid SM (2022) Acaricidal activity of tea tree and lemon oil nanoemulsions against Rhipicephalus annulatus. Pathogens 11:1506. https://doi.org/10.3390/pathogens11121506
Idris UE, Adam SE, Tartour G (1982) The anthelmintic efficacy of Artemisia herba-albaagainst Haemonchus contortus infection in goats. Natl Inst Anim Health Q 22(3):138–143
Jaramillo MA, Manos PS (2001) Phylogeny and patterns of floral diversity in the genus Piper (Piperaceae). Am J Bot 88(4):706–716. https://doi.org/10.2307/2657072
Jollow DJ, Mitchell JR, Nal Z, Gillette JR (1974) Bromobenzene-induced liver necrosis. Protective role of glutathione and evidence for 3, 4-bromobenzene oxide as the hepatotoxic metabolite. Pharmacology 11(3):151–169. https://doi.org/10.1159/000136485
Kaplan RM (2004) Drug resistance in nematodes of veterinary importance: a status report. Trends Parasitol 20:477–481. https://doi.org/10.1016/j.pt.2004.08.001
Kaplan RM, Vidyashankar AN (2012) An inconvenient truth: Global warming and anthelmintic resistance. Vet Parasitol 186:70–80. https://doi.org/10.1016/j.vetpar.2011.11.048
Katiki LM, Chagas ACS, Bizzo HR, Ferreira JFS, Amarante AFT (2011) Anthelmintic activity of Cymbopogon martinii, Cymbopogon schoenanthus and Mentha piperita essential oils evaluated in four different in vitro tests. Vet Parasitol 183(1–2):103–108. https://doi.org/10.1016/j.vetpar.2011.07.001
Kebede A (2019) Review on anthelmintic drug resistance nematodes and its methods of detection in Ethiopia. J Vet Med Animal Sci 2(2640–1223):10–13
Lespine A, Ménez C, Bourguinat C, Prichard RK (2012) P-glycoproteins and other multidrug resistance transporters in the pharmacology of anthelmintics: prospects for reversing transport-dependent anthelmintic resistance. Int J Parasitol Drugs Resist 2:58–75. https://doi.org/10.1016/j.ijpddr.2011.10.001
Macedo IT, Bevilaqua CM, de Oliveira LM, Camurça-Vasconcelos AL, Vieira Lda S, Oliveira FR, Queiroz-Junior EM, Portela BG, Barros RS, Chagas AC (2009) Atividade ovicida e larvicida in vitro do óleo essencial de Eucalyptus globulus sobre Haemonchus contortus [Ovicidal and larvicidal activity in vitro of Eucalyptus globulus essential oils on Haemonchus contortus]. Rev Bras Parasitol Vet 18(3):62–66. https://doi.org/10.4322/rbpv.01803011
Macedo IT, Bevilaqua CM, de Oliveira LM, Camurça-Vasconcelos AL, Vieira Lda S, Oliveira FR, Queiroz-Junior EM, Tomé Ada R, Nascimento NR (2010) Anthelmintic effect of Eucalyptus taigeriana essential oil against goat gastrointestinal nematodes. Vet Parasitol 173:93–98. https://doi.org/10.1016/j.vetpar.2010.06.004
Macedo IT, Bevilaqua CM, Oliveira LM, Camurc ̧a- Vasconcelos AL, Vieira LS, Amo ́ ra Sdos S (2011) Evaluation of Eucalyptus citriodora essential oil on goat gastrointestinal nematodes. Rev Bras Parasitol Vet 20(3):223–227. https://doi.org/10.1590/s1984-29612011000300009
Manoharan S, Balakrishnan S, Menon V, Alias L, Reena A (2009) Chemopreventive efficacy of curcumin and piperine during 7,12-dimethylbenz anthracene-induced hamster buccal pouch carcinogenesis. Singapore Med J 50(2):139–146
Martínez-Ortíz-De-Montellano C, Arroyo-López C, FourquauxI T-A, Sandoval-Castro CA, Hoste H (2013) Scanning electron microscopy of Haemonchus contortus exposed to tannin-rich plants under in vivo and in vitro conditions. Exp Parasitol 133(3):281–286. https://doi.org/10.1016/j.exppara.2012.11.024
Masood S, Abbas RZ, Iqbal Z, Mansoor MK, Sindhu ZUD, Zia MA (2013) Role of natural antioxidants for the control of coccidiosis in poultry. Pak Vet J 33(4):401–407
Mills C, Cleary BJ, Gilmer JF, Walsh JJ (2004) Inhibition of acetylcholinesterase by teatree oil. J Pharm Pharmacol 56:375–379. https://doi.org/10.1211/0022357022773
Montgomery HACDJ, Dymock JF (1961) Determination of nitrite in water. In: Royal soc chemistry thomas graham house, science park, milton rd, Cambridge, (vol 86, pp 414-&)
Oliveira GL, Vieira TM, Nunes VF, Ruas MO, Duarte ER, Moreira DL (2014) Chemical composition and efficacy in the egg-hatching inhibition of essential oil of Pipera duncum against Haemonchus contortus from sheep. Rev Bras Farmacogn 24(3):288–292. https://doi.org/10.1016/j.bjp.2014.07.004
Page AP (2001) The nematode cuticle: synthesis, modification and mutants. In: Kennedy MW, Harnett W (eds) Parasitic nematodes: molecular biology, biochemistry and immunology. CABI Publishing, London, pp 167–193
Page AP, Winter AD (2003) Enzymes involved in the biogenesis of the nematode cuticle. Adv Parasitol 53:85–148. https://doi.org/10.1016/s0065-308x(03)53003-2
Payne SE, Kotze AC, Durmic Z, Vercoe PE (2013) Australian plants show anthelmintic activity toward equine cyathostomins in vitro. Vet Parasitol 196:153–160. https://doi.org/10.1016/j.vetpar.2013.01.012
Pazinato R, Klauck V, Volpato A, Tonin AA, Santos RC, de Souza ME, Vaucher RA, Raffin R, Gomes P, Felippi CC, Stefani LM, Da Silva AS (2014) Influence of tea tree oil (Melaleuca alternifolia) on the cattle tick Rhipicephalus microplus. Exp Appl Acarol 63:77–83. https://doi.org/10.1007/s10493-013-9765-8
Ribeiro JC, Ribeiro WLC, Camurca-Vasconcelos ALF, Macedo ITF, Santos JML, Paula HCB, Ara´ujoFilho JV, Magalh˜aes RD, Bevilaqua CML, (2014) Efficacy of free and nanoencapsulated Eucalyptus citriodora essential oils on sheep gastrointestinal nematodes and toxicity for mice. Vet Parasitol 204(3–4):243–248. https://doi.org/10.1016/j.vetpar.2014.05.026
Roeber F, Jex AR, Gasser RB (2013) Impact of gastrointestinal parasitic nematodes of sheep, and the role of advanced molecular tools for exploring epidemiology and drug resistance—an Australian perspective. Parasit Vectors 6:153. https://doi.org/10.1186/1756-3305-6-153
Sambodo P, Prastowo J, Kurniasih K, Indarjulianto S (2018) In vitro potential anthelmintic activity of Biophytum petersianum on Haemonchus contortus. Vet World 11(1):1–4. https://doi.org/10.14202/vetworld.2018.1-4
Sanders J, Xie Y, Gazzola D, Li H, Abraham A, Flanagan K, Rus F, Miller M, Hu Y, Guynn S, Draper A, Vakalapudi S, Petersson KH, Zarlenga D, Li RW, Urban JF, Ostroff GR, Zajac A, Aroian RV (2020) A new paraprobiotic-based treatment for control of Haemonchus contortus in sheep. Int J Parasitol Drugs Drug Resist 14:230–236. https://doi.org/10.1016/j.ijpddr.2020.11.004
Sangster N, Whitlock H, Russ I, Gunawan I, Griffin D, Kelly J (1979) Trichostrongylus colubriformis and Ostertagia circumcincta resistant to levamisole, morantel tartrate and thiabendazole: occurrence of field strains. Res Vet Sci 27(1):106–110
Schwab AE, BoakyeDK PRK (2005) Detection of benzimidazoleresistance–associated mutations in the filarial nematode Wuchereria bancrofti and evidence for selection by albendazole and ivermectin combination treatment. Am J Trop Med Hyg 73(2):234–238
Shahardarn RA, Itoo SA, Allaie IM, Wani ZA (2014) Anthelmintic resistance in GI nematodes of sheep at farms of Kashmir Valley. J Vet Parasitol 28(2):151–153. https://doi.org/10.1016/j.parepi.2020.e00163
Sissay MM, Asefa A, Uggla A, Waller PJ (2006) Assessment of anthelmintic resistance in nematode parasites of sheep and goats owned by smallholder farmers in eastern Ethiopia. Trop Anim Health Prod 38:215–222. https://doi.org/10.1007/s11250-006-4346
Soulsby EJL (1986) Helminths, arthropods & protozoa of domesticated animals, 7th edn. Bailliere Tindall, London
Torres-Acosta JFJ, Molento M, Gives PM (2012) Research and implementation of novel approaches for the control of nematode parasites in Latin America and the Caribbean: is there sufficient incentive for a greater extension effort? Vet Parasitol 186(1–2):132–142. https://doi.org/10.1016/j.vetpar.2011.11.053
Tresia GE, Evvyernie D, Tiuria R (2016) Phytochemical screening and in vitro ovicidal, larvacidal, and nematicidal effects of Murraya paniculata (L.) jack extract on gastrointestinal parasites of goats. Med Peternakan 39(3):173–179. https://doi.org/10.5398/medpet.2016.39.3.173
Vidal F, Vidal JC, Gadelha APR, Lopes CS, Coelho MGP, Monteiro-Leal LH (2007) Giardia lamblia: the effects of extracts and fractions from Mentha £ piperita Lin. (Lamiaceae) on trophozoites. Exp Parasitol 115(1):25–31. https://doi.org/10.1016/j.exppara.2006.05.001
Vieira LS (2008) Métodos alternativos de controle de nematóides gastrintestinais em caprinos e ovinos. Tecnologia e Ciência Agropecuária 22:49–56
Waruiru R (1997) Efficacy of closantel, albendazole and levamisole on an ivermectin resistant strain of Haemonchus contortus in sheep. Vet Parasitol 73:65–71. https://doi.org/10.1016/s0304-4017(97)00065-4
Wattanathorn J, Chonpathompikunlert P, Muchimapura S, Priprem A, Tankamnerdthai O (2008) Piperine, the potential functional food for mood and cognitive disorders. Food Chem Toxicol 46(9):3106–3110. https://doi.org/10.1016/j.fct.2008.06.014
Westers T, Jones-Bitton A, Menzies P, Van Leeuwen J, Poljak Z, Peregrine AS (2016) Efficacy of closantel against ivermectin—and fenbendazole-resistant haemonchus sp. in sheep in ontario. Can Vet Parasitol 15(228):30–41. https://doi.org/10.1016/j.vetpar.2016.08.009
Wolstenholme AJ (2011) Ion channels and receptor as targets for the control of parasitic nematodes. Int J Parasitol Drugs Drug Resist 1(1):2–13. https://doi.org/10.1016/j.ijpddr.2011.09.003
Wong and Ling (2014) In vitro study of wound healing potential inblack pepper (Piper nigrum L.). Pharm Biosci J 2:5–9. https://doi.org/10.20510/ukjpb/2/i4/91104
Wood IB, Amaral NK, Bairden K, Duncan JL, Kassai T, Malone JB Jr, Vercruysse J (1995) World association for the advancement of veterinary parasitology (WAAVP) of guidelines for evaluating the efficacy of anthelmintics in ruminants (bovine, ovine, caprine). Vet Parasitol 58(3):181–213. https://doi.org/10.1016/0304-4017(95)00806-2
Zajac AM, ConboyGA GA (2006) Veterinary clinical parasitoloy. Blackwell publishing, New York, USA, pp 3–4
Zhu L, Dai JL, Yang L, Qiu J (2013) In vitro ovicidal and larvicidal activity of the essential oil of Artemisia lancea against Haemonchus contortus (Strongylida). Vet Parasitol 195(1–2):112–117. https://doi.org/10.1016/j.vetpar.2012.12.050
Acknowledgements
Authors all veterinarians and farmers who facilitated collecting fecal specimens. Special thanks are expressed to Prof. Dr. Shawky M. Aboelhadid Professor of Parasitology, Faculty of Veterinary Medicine, Beni-Suef University, for his assistance and giving me much of his valuable time, experience, scientific knowledge and great help throughout this work.
Funding
No funding sources.
Author information
Authors and Affiliations
Contributions
HIM; samples collection, lab work. WMA; designing, executing and drafting the manuscript, OMA; data analysis and statistical analysis. KhME; revising, photo editing. All the authors have given their consent to submit the manuscript in the Journal.
Corresponding author
Ethics declarations
Conflict of interest
No conflict of interest in the submission of this manuscript, and manuscript is approved by all authors for publication.
Ethics approval
The authors assert that all procedures contributing to this work comply with the ethical standards of the institutional Animal Care and Use Committee Beni-Suef University (BSU-IACUC 022-419).
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Mohamed, H.I., Arafa, W.M., Ahmed, O.M. et al. Ovicidal, larvicidal and adulticidal activity of black pepper (Piper nigrum L.) essential oil and tea tree oil (Melaleuca alternifolia) against Haemonchus contortus. J Parasit Dis 48, 117–133 (2024). https://doi.org/10.1007/s12639-024-01650-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12639-024-01650-w