Pig Breeding 2023 №2(80)

POSSIBILITIES AND PROSPECTS OF USING PLANTS FOR THE TREATMENT OF HELMINTOSES IN DOMESTIC RUMINANTS

UDC: 636.3: 615.322: 616-093/-098: 615.246.9

DOI: 10.37143/2786-7730-2023-2(80)05

REFERENCIS АРА style: Lukash, O. V., Tkachenko, H. M., & Kurhaliuk, N. M. (2023). Mozhlyvosti ta perspektyvy zastosuvannia roslyn dlia likuvannia helmintoziv u sviiskykh zhuinykh [Possibilities and prospects of using plants for the treatment of helminthoses in domestic ruminants]. Svynarstvo i ahropromyslove vyrobnytstvo [Pig Breeding and Agroindustrial Production]. Poltava, 2(80), 67-86 [in Ukrainain]. doi: 10.37143/2786-7730-2023-2(80)05

O. V. Lukash Doc. o f Biology Sci., Professor, Professor o f Department o f Ecology, Geography and Nature Management
ORCID:https://orcid.org/0000-0003-2702-6430
E-mail:: lukash1120@gmail.com
T. H. Shevchenko National University “Chernihiv Collegium ” 53, Hetmana Polubotka St., Chernihiv, Ukraine 14013
H. M. Tkaczenko Doc. o f Biology Sci., Professor o f Department o f Zoology
ORCID:https//orcid.org/0000-0003-3951-9005
E-mail:: halina.tkaczenko@upsl.edu.pl
Institute o f Biology, Pomeranian University in Slupsk 22B Arciszewskiego St., Slupsk, Poland 76-200
N. M. Kurhaluk Doc. o f Biology Sci., Professor o f Department o f Animal Physiology,
ORCID:https//orcid.org/0000-0002-4669-1092
E-mail:natalia.kurhaluk@upsl.edu.pl
2Institute o f Biology, Pomeranian University in Slupsk 22B Arciszewskiego St., Slupsk, Poland 76-200

Abstract

Goal. To review the results o f modern research on antihelminthic properties o f plants and to outline the prospects fo r the use o f plants with antiparasitic properties in the practice o f animal husbandry in Europe. Methods. The analysis and generalization o f research results o f anthelmintic properties o f the natural and cultivated plant species o f introduced flora. The results. It has long been known that gastrointestinal helminths are a serious problem fo r animal health and are the most significant limitation in the grazing o f domestic ruminants. A combination o f optimized anthelmintic use and alternative approaches has been found to be a reasonable approach in sustainable parasite control programs. Various in vivo and in vitro methods are used to confirm the anthelmintic properties o f herbal preparations in world practice. In vitro studies are useful as a preliminary screening fo r activity, and are mainly performed on free-living, rather than parasitic, stages o f nematodes. Concentrations o f potentially active compounds used in in vitro studies do not always correspond to in vivo bioavailability. Therefore, in vitro analyzes should always be accompanied by in vivo studies. Controlled in vivo studies show that, in most cases, herbal preparations resulted in significantly lower parasite clearance than synthetic anthelmintics. The results o f modern research on anthelmintic properties ofplants and the prospects fo r the use ofplants with antiparasitic properties in the practice o f animal husbandry in Europe are analyzed. Conclusions. In the context o f the implementation o f organic farm ing and animal husbandry systems, one cannot rely only on chemotherapeutic treatment o f infectious parasitic diseases o f ruminants caused by helminths. Considering the fa ct that phytotherapy shows a more diverse effectiveness compared to the known effectiveness o f anthelmintics, it deserves a wider introduction into the practice o f animal husbandry. The treatment o f domestic ruminants with phytopreparations, like chemotherapy, will be effective i f it is combined with grazing on ecologically and sanitary balanced pastures. For the treatment and prevention o f helminthiasis in domestic ruminants, it is advisable to use ethnobotanically traditional types o f plants in veterinary medicine more widely than the existing scope, the anthelmintic effectiveness o f which has been reliably confirmed experimentally. Promising fo r further research is the search fo r anti-parasitic species o f plants o f the natural and cultivated flora o f Europe, and the study o f the effectiveness o f their toxic action fo r the purpose o f use in the veterinary practice o f cattle breeding, pig breeding, sheep breeding and poultry farming are promising.

Key words: phytomedicine, phytopreparations, plant metabolites, helminths, small domestic ruminants, parasite control, prevention.

REFERENCES

1. Hofmann, R. R. (1989). Evolutionary steps of ecophysiological adaptation and diversification of ruminants: a comparative view of their digestive system. Oecologia, 78(4), 443–457. doi: 10.1007/BF00378733
2. Gordon, I. J. (2003). Browsing and grazing ruminants: are they different beasts? Forest Ecology and Management, 181(1–2), 13–21. doi: 10.1016/S0378-1127(03)00124-5
3. Duncan, A. J., & Poppi, D. P. (2008). Nutritional Ecology of Grazing and Browsing Ruminants. In: Gordon, I. J., Prins, H .H. T. (eds) The Ecology of Browsing and Grazing. Ecological Studies, 195. Springer, Berlin, Heidelberg. doi: 10.1007/978-3-540-72422-3_4
4. Underwood, W. J., Blauwiekel, R., Delano, M. L., Gillesby, R., Mischler, S. A., & Schoell, A. (2015). Biology and Diseases of Ruminants (Sheep, Goats, and Cattle). Laboratory Animal Medicine, 623–694. doi: 10.1016/B978-0-12-409527-4.00015-8
5. Blancou, J. (2001). A history of the traceability of animals and animal products. Revue scientifique et technique (International Office of Epizootics), 20(2), 413–425. 6. Pereira, F. C., & Berry, D. (2017). Microbial nutrient niches in the gut. Environmental Microbiology, 19(4), 1366–1378. doi: 10.1111/1462-2920.13659
7. Tong, F., Wang, T., Gao, N. L., Liu, Z., Cui, K., Duan, Y., Wu, S., Luo, Y., Li, Z., Yang, C., Xu, Y., Lin, B., Yang, L., Pauciullo, A., Shi, D., Hua, G., Chen, W. H., & Liu, Q. (2022). The microbiome of the buffalo digestive tract. Nature Communications, 13(1), 823. doi: 10.1038/s41467-022-28402-9
8. Kingston-Smith, A. H., Edwards, J. E., Huws, S. A., Kim, E. J., & Abberton, M. (2010). Plant-based strategies towards minimising 'livestock's long shadow'. The Proceedings of the Nutrition Society, 69(4), 613–620. doi: 10.1017/S0029665110001953
9. Shaani, Y., Zehavi, T., Eyal, S., Miron, J., & Mizrahi, I. (2018). Microbiome niche modification drives diurnal rumen community assembly, overpowering individual variability and diet effects. The ISME journal, 12(10), 2446–2457. doi: 10.1038/s41396-018-0203-0
10. Strydom, T., Lavan, R. P., Torres, S., & Heaney, K. (2023). The Economic Impact of Parasitism from Nematodes, Trematodes and Ticks on Beef Cattle Production. Animals, 13(10). 1599. doi: 10.3390/ani13101599
11. Roeber, F., Jex, A. R., & Gasser, R. B. (2013). Impact of gastrointestinal parasitic nematodes of sheep, and the role of advanced molecular tools for exploring epidemiology and drug resistance – an Australian perspective. Parasites & Vectors, 6, 153. doi: 10.1186/1756-3305-6-153
12. Fissiha, W., & Kinde, M. Z. (2021). Anthelmintic Resistance and Its Mechanism: A Review. Infection and Drug Resistance, 14, 5403–5410. doi: 10.2147/IDR.S332378
13. Shalaby, H. A., & El-Moghazy, F. M. (2013). In vitro effect of Nigella sativa oil on adult Toxocara vitulorum. Pakistan Journal of Biological Sciences: PJBS, 16(22), 1557–1562. doi: 10.3923/pjbs.2013.1557.1562
15. Bricarello, P. A., Longo, C., da Rocha, R. A., & Hötzel, M. J. (2023). Understanding Animal-Plant- Parasite Interactions to Improve the Management of Gastrointestinal Nematodes in Grazing Ruminants. Pathogens (Basel, Switzerland), 12(4), 531. doi: 10.3390/pathogens12040531
16. Zvinorova, P. I., Halimani, T. E., Muchadeyi, F. C., Matika, O., Riggio, V., & Dzama, K. (2016). Breeding for resistance to gastrointestinal nematodes – the potential in low-input/output small ruminant production systems. Veterinary Parasitology, 225, 19–28. doi: 10.1016/j.vetpar.2016.05.015
18. Isah, T. (2019). Stress and defense responses in plant secondary metabolites production. Biological Research, 52(1), 39. doi: 10.1186/s40659-019-0246-3
19. Mutha, R. E., Tatiya, A. U., & Surana, S. J. (2021). Flavonoids as natural phenolic compounds and their role in therapeutics: an overview. Future Journal of Pharmaceutical Sciences, 7(1), 25. doi: 10.1186/s43094-020-00161-8
20. Ku-Vera, J. C., Jiménez-Ocampo, R., Valencia-Salazar, S. S., Montoya-Flores, M. D., Molina- Botero, I. C., Arango, J., Gómez-Bravo, C. A., Aguilar-Pérez, C. F., & Solorio-Sánchez, F. J. (2020). Role of Secondary Plant Metabolites on Enteric Methane Mitigation in Ruminants. Frontiers in Veterinary Science, 7, 584. doi: 10.3389/fvets.2020.00584
21. McIntos, F. M., Williams, P., Losa, R., Wallace, R. J., Beever, D. A., & Newbold, C. J. (2003). Effects of essential oils on ruminal microorganisms and their protein metabolism. Applied and Environmental Microbiology, 69(8), 5011–5014. doi: 10.1128/AEM.69.8.5011-5014.2003
22. Andri, F., Huda, A. N., & Marjuki, M. (2020). The use of essential oils as a growth promoter for small ruminants: a systematic review and meta-analysis. F1000Research, 9, 486. doi: 10.12688/f1000research.24123.2
23. Besharati, M., Maggiolino, A., Palangi, V., Kaya, A., Jabbar, M., Eseceli, H., De Palo, P., Lorenzo, J. M. (2022). Tannin in Ruminant Nutrition: Review. Molecules (Basel, Switzerland), 27(23), 8273. doi: 10.3390/molecules27238273
24. Cobellis, G., & Trabalza-Marinucci, M. Yu Z. (2016). Critical evaluation of essential oils as rumen modifiers in ruminant nutrition: A review. The Science of the Total Environment, 545–546, 556–568. doi: 10.1016/j.scitotenv.2015.12.103
25. Hoste, H., Meza-Ocampos, G., Marchand, S., Sotiraki, S., Sarasti, K., Blomstrand, B. M., Williams, A. R., … Morgan E. R. (2022). Use of agro-industrial by-products containing tannins for the integrated control of gastrointestinal nematodes in ruminants. Utilisation de sous-produits agro-industriels contenant des tanins pour le contrôle intégré des nématodes gastro-intestinaux chez les ruminants. Parasite (Paris, France), 29, 10. doi: 10.1051/parasite/2022010
26. Lopes, T. S., Fontoura, P. S., Oliveira, A., Rizzo, F. A., Silveira, S., & Streck A. F. (2020). Use of plant extracts and essential oils in the control of bovine mastitis. Research in Veterinary Science, 131, 186–193. doi: 10.1016/j.rvsc.2020.04.025
27. Karreman, H. J. (2007). Treating Dairy Cows Naturally: Thoughts & Strategies. 2nd edition, Publisher: Acres USA.
28. Waller, P. J., Bernes, G., Thamsborg, S. M., Sukura, A., Richter, S. H., Ingebrigtsen, K., & Höglun, J. (2001). Plants as de-worming agents of livestock in the Nordic countries: historical perspective, popular beliefs and prospects for the future. Acta Veterinaria Scandinavica, 42(1), 31–44. doi: 10.1186/1751-0147-42-31
29. Thamsborg, S. M., Jørgensen, R. J., Waller, P. J., & Nansen, P. (1996). The influence of stocking rate on gastrointestinal nematode infections of sheep over a 2-year grazing period. Veterinary Parasitology, 67(3–4), 207–224. doi: 10.1016/s0304-4017(96)01045-x
30. Mee, J. F., & Boyle, L. A. (2020). Assessing whether dairy cow welfare is "better" in pasture- based than in confinement-based management systems. New Zealand Veterinary Journal, 68(3), 168–177. doi: 10.1080/00480169.2020.1721034
31. Spigarelli, C., Zuliani, A., Battini, M., Mattiello, S., & Bovolenta, S. (2020). Welfare Assessment on Pasture: A Review on Animal-Based Measures for Ruminants. Animals, 10(4), 609. doi: 10.3390/ani10040609
32. Marley, C. L., Cook, R., Keatinge, R., Barrett, J., & Lampkin, N. H. (2003). The effect of birdsfoot trefoil (Lotus corniculatus) and chicory (Cichorium intybus) on parasite intensities and performance of lambs naturally infected with helminth parasites. Veterinary Parasitology, 112(1–2), 147–155. doi: 10.1016/s0304-4017(02)00412-0
33. Niezen, J. H., Charleston, W. A., Robertson, H. A., Shelton, D., Waghorn, G. C., & Green, R. (2002). The effect of feeding sulla (Hedysarum coronarium) or lucerne (Medicago sativa) on lamb parasite burdens and development of immunity to gastrointestinal nematodes. Veterinary Parasitology, 105(3), 229–245. doi: 10.1016/s0304-4017(02)00014-6
4. Molan, A. L., Waghorn, G. C., Min, B. R., & McNabb, W. C. (2000). The effect of condensed tannins from seven herbages on Trichostrongylus colubriformis larval migration in vitro. Folia Parasitological, 47(1), 39–44. doi: 10.14411/fp.2000.007
35. Paolini, V., Fouraste, I., & Hoste, H. (2004). In vitro effects of three woody plant and sainfoin extracts on 3rd-stage larvae and adult worms of three gastrointestinal nematodes. Parasitology, 129(Pt 1), 69–77. doi: 10.1017/s0031182004005268
36. Rinaldi, L., Krücken, J., Martinez-Valladares, M., Pepe, P., Maurelli, M. P., de Queiroz, C., Castilla Gómez de Agüero, V., … von Samson-Himmelstjerna, G. (2022). Advances in diagnosis of gastrointestinal nematodes in livestock and companion animals. Advances in Parasitology, 118, 85–176. doi: 10.1016/bs.apar.2022.07.002
37. Assis, L. M., Bevilaqua, C. M., Morais, S. M., Vieira, L. S., Costa, C. T., & Souza, J. A. (2003). Ovicidal and larvicidal activity in vitro of Spigelia anthelmia Linn. extracts on Haemonchus contortus. Veterinary Parasitology, 117(1–2), 43–49. doi: 10.1016/j.vetpar.2003.07.021.
38. Githiori, J. B., Athanasiadou, S., & Thamsborg, S. M. (2006). Use of plants in novel approaches for control of gastrointestinal helminths in livestock with emphasis on small ruminants. Veterinary Parasitology, 139(4), 308–320. doi: 10.1016/j.vetpar.2006.04.021
39. Hoste, H., Torres-Acosta, J. F., Sandoval-Castro, C. A., Mueller-Harvey, I., Sotiraki, S., Louvandini, H., Thamsborg, S. M., & Terrill, T. H. (2015). Tannin containing legumes as a model for nutraceuticals against digestive parasites in livestock. Veterinary Parasitology, 212(1–2), 5–17. doi: 10.1016/j.vetpar.2015.06.026
40. Burke, J. M. & Miller, J. E. (2020). Sustainable Approaches to Parasite Control in Ruminant Livestock. The Veterinary clinics of North America. Food Animal Practice, 36(1), 89–107. doi: 10.1016/j.cvfa.2019.11.007
41. Kearney, P. E., Murray, P. J., Hoy, J. M., Hohenhaus, M., & Kotze, A. (2016). The 'Toolbox' of strategies for managing Haemonchus contortus in goats: What's in and what's out. Veterinary Parasitology, 220, 93–107. doi: 10.1016/j.vetpar.2016.02.028
42. Mbaria, J. M., Maitho, T. E., Mitem, E. S., & Muchiri, D. J. (1998). Comparative efficacy of pyrethrum marc with albendazole against sheep gastrointestinal nematodes. Tropical Animal Health and Production, 30(1), 17–22. doi: 10.1023/a:1005005208588
43. Gathuma, J. M., Mbaria, J. M., Wanyama, J., Kaburia, H. F., Mpoke, L., Mwangi, J. N., Samburu, Healers T. (2004). Efficacy of Myrsine africana, Albizia anthelmintica and Hilderbrantia sepalosa herbal remedies against mixed natural sheep helminthosis in Samburu district, Kenya. Journal of Ethnopharmacology, 91(1), 7–12. doi: 10.1016/j.jep.2003.11.007
44. Onyeyili, P. A., Nwosu, C. O., Amin, J. D., & Jibike, J. I. (2001). Anthelmintic activity of crude aqueous extract of Nauclea latifolia stem bark against ovine nematodes. Fitoterapia, 72(1), 12–21. doi: 10.1016/s0367-326x(00)00237-9
45. Githiori, J. B., Höglund, J., Waller, P. J., & Baker, R. L. (2002). Anthelmintic activity of preparations derived from Myrsine africana and Rapanea melanophloeos against the nematode parasite, Haemonchus contortus, of sheep. Journal of Ethnopharmacology, 80(2–3), 187–191. doi: 10.1016/s0378-8741(02)00030-2
46. Githiori, J. B., Höglund, J., Waller, P. J., & Baker, R. L. (2004). Evaluation of anthelmintic properties of some plants used as livestock dewormers against Haemonchus contortus infections in sheep. Parasitology, 129(Pt 2), 245–253. doi: 10.1017/s0031182004005566
47. Fernandez, T. J., Jr, Portugaliza, H. P., Braga, F. B., Vasquez, E. A., Acabal, A. D., Divina, B. P., & Pedere, W. B. (2013). Effective Dose (ED) and quality control studies of the Crude Ethanolic Extract (CEE) mixture of makabuhay, caimito and makahiya (MCM) as dewormer for goats against Haemonchus contortus. Asian Journal of Experimental Biological Sciences, 41, 28–35.
48. Hördegen, P., Hertzberg, H., Heilmann, J., Langhan, W., & Maurer, V. (2003). The anthelmintic efficacy of five plant products against gastrointestinal trichostrongylids in artificially infected lambs. Veterinary Parasitology, 117(1–2), 51–60. doi: 10.1016/j.vetpar.2003.07.027
49. Haridy, F. M., El Garhy, M. F., & Morsy, T. A. (2003). Efficacy of Mirazid (Commiphora molmol) against fascioliasis in Egyptian sheep. Journal of the Egyptian Society of Parasitology, 33(3), 917–924.
50. Massoud, A., Morsy, T. A., & Haridy, F. M. (2003). Treatment of Egyptian dicrocoeliasis in man and animals with Mirazid. Journal of the Egyptian Society of Parasitology, 33(2), 437–442.
51. Pessoa, L. M., Morais, S. M., Bevilaqua, C. M., & Luciano, J. H. (2002). Anthelmintic activity of essential oil of Ocimum gratissimum Linn. and eugenol against Haemonchus contortus. Veterinary Parasitology, 109(1–2), 59–63. doi: 10.1016/s0304-4017(02)00253-4
52. Anonymous (1996). Garlic for cryptosporidiosis? Treatment review,22, 11.
53. Olson, E. J., Epperson, W. B., Zeman, D. H., Fayer, R., & Hildreth, M. B. (1998). Effects of an allicin-based product on cryptosporidiosis in neonatal calves. Journal of the American Veterinary Medical Association, 212(7), 987–990.
54. Bhavare, V., & Pokharka, R. (2010). Comparative in vitro anticestodal activity of some medicinal plants from western India. Pharmacologyonline, 3, 142–145.
55. Aggarwal, R., Kaur, K., Suri, M., & Bagai, U. (2016). Anthelmintic potential of Calotropis procera, Azadirachta indica and Punica granatum against Gastrothylax indicus. Journal of Parasitic Diseases, 40(4), 1230–1238. doi: 10.1007/s12639-015-0658-0
56. Zamilpa, A., García-Alanís, C., López-Arellano, M. E., Hernández-Velázquez, V. M., Valladares- Cisneros, M. G., Salinas-Sánchez, D. O., & Mendoza-de Gives, P. (2019). In vitro nematicidal effect of Chenopodium ambrosioides and Castela tortuosa n-hexane extracts against Haemonchus contortus (Nematoda) and their anthelmintic effect in gerbils. Journal of Helminthology, 93(4), 434–439. doi: 10.1017/S0022149X18000433
57. Badar, S. N., Iqbal, Z., Sajid, M. S., Rizwan, H. M., Shareef, M., Malik, M. A., & Khan, M. N. (2021). Comparative anthelmintic efficacy of Arundo donax, Areca catechu, and Ferula assa- foetida against Haemonchus contortus. Revista brasileira de parasitologia veterinaria = Brazilian journal of veterinary parasitology: Orgao Oficial do Colegio Brasileiro de Parasitologia Veterinaria, 30(2), e001221. doi: 10.1590/S1984-29612021028
58. Romero, N., Areche, C., Cubides-Cárdenas, J., Escobar, N., García-Beltrán, O., Simirgiotis, M. J., & Céspedes, Á. (2020). In Vitro Anthelmintic Evaluation of Gliricidia sepium, Leucaena leucocephala, and Pithecellobium dulce: Fingerprint Analysis of Extracts by UHPLC-Orbitrap Mass Spectrometry. Molecules (Basel, Switzerland), 25(13), 3002. doi: 10.3390/molecules25133002
59. Hernandez, P. M., Salem, A. Z., Elghandour, M. M., Cipriano-Salazar, M., Cruz-Lagunas, B., & Camacho, L. M. (2014). Anthelmintic effects of Salix babylonica L. and Leucaena leucocephala lam. extracts in growing lambs. Tropical Animal Health and Production, 46(1), 173–178. doi: 10.1007/s11250-013-0471-7
60. Szewczuk, V. D., Mongelli, E. R., & Pomilio, A. B. (2006). In vitro anthelmintic activity of Melia azedarach naturalized in Argentina. Phytotherapy Research: PTR, 20(11), 993–996. doi: 10.1002/ptr.1929
61. Cala, A. C., Chagas, A. C., Oliveira, M. C., Matos, A. P., Borges, L. M., Sousa, L. A., Souza, F. A., & Oliveira, G. P. (2012). In vitro anthelmintic effect of Melia azedarach L. and Trichilia claussenii C. against sheep gastrointestinal nematodes. Experimental Parasitology, 130(2), 98–102. doi: 10.1016/j.exppara.2011.12.011
62. Maciel, M. V., Morais, S. M., Bevilaqua, C. M., Camurça-Vasconcelos, A. L., Cost, C. T., & Castro, C. M. (2006). Ovicidal and larvicidal activity of Melia azedarach extracts on Haemonchus contortus. Veterinary Parasitology, 140(1–2), 98–104. doi: 10.1016/j.vetpar.2006.03.007
63. Kamaraj, C., Rahuman, A. A., Bagavan, A., Mohamed, M. J., Elango, G., Rajakumar, G., Zahir, A. A., Santhoshkumar, T., & Marimuthu, S. (2010). Ovicidal and larvicidal activity of crude extracts of Melia azedarach against Haemonchus contortus (Strongylida). Parasitology Research, 106(5), 1071–1077. doi: 10.1007/s00436-010-1750-0
64. Fakae, B. B., Campbell, A. M., Barrett, J., Scott, I. M., Teesdale-Spittle, P. H., Liebau, E., & Brophy, P. M. (2000). Inhibition of glutathione S-transferases (GSTs) from parasitic nematodes by extracts from traditional Nigerian medicinal plants. Phytotherapy Research: PTR, 14(8), 630–634. doi: 10.1002/1099-1573(200012)14:8<630::aid-ptr773>3.0.co;2-5
65. Kaiaty, A. M., Salib, F. A., El-Gameel, S. M., Hussien, A. M. & Kamel, M. S. (2021). Anthelmintic activity of pomegranate peel extract (Punica granatum) and synthetic anthelmintics against gastrointestinal nematodes in cattle, sheep, goats, and buffalos: in vivo study. Parasitology Research, 120(11), 3883–3893. doi: 10.1007/s00436-021-07311-8
66. Castagna, F., Bava, R., Musolino, V., Piras, C., Cardamone, A., Carresi, C., Lupia, C., Bosco, A., Rinaldi, L., Cringoli, G., Palma, E., Musella, V., & Britti, D. (2022). Potential New Therapeutic Approaches Based on Punica granatum Fruits Compared to Synthetic Anthelmintics for the Sustainable Control of Gastrointestinal Nematodes in Sheep. Animals, 12(20), 2883. doi: 10.3390/ani12202883
67. Dhanraj, K. M., & Veerakumari, L. (2014). In vitro effect of Syzygium aromaticum on the motility and acetylcholinesterase of Cotylophoron cotylophorum. Indian Journal of Veterinary and Animal Sciences Research, 43, 187–194.
68. Imani-Baran, A., Abdollahi, J., Akbari, H., Jafarirad, S., & Moharramnejad, S. (2020). Anthelmintic activity of crude powder and crude aqueous extract of Trachyspermum ammi on gastrointestinal nematodes in donkey (Equus asinus): An in vivo study. Journal of Ethnopharmacology, 248, 112249. doi: 10.1016/j.jep.2019.112249
69. Lateef, M., Iqbal, Z., Akhtar, M. S., Jabbar, A., Khan, M. N., & Gilani, A. H. (2006). Preliminary screening of Trachyspermum ammi (L.) seed for anthelmintic activity in sheep. Tropical Animal Health and Production, 38(6), 491–496. doi: :10.1007/s11250-006-4315-6
70. Hördegen, P., Cabaret, J., Hertzberg, H., Langhans, W., & Maurer, V. (2006). In vitro screening of six anthelmintic plant products against larval Haemonchus contortus with a modified methyl- thiazolyl-tetrazolium reduction assay. Journal of Ethnopharmacology, 108(1), 85–89. doi: 10.1016/j.jep.2006.04.013
71. Cala, A. C., Ferreira, J. F., Chagas, A. C., Gonzalez, J. M., Rodrigues, R. A., Foglio, M. A., Oliveira, M. C., Sousa, I. M., Magalhães, & P. M., Barioni Júnior, W. (2014). Anthelmintic activity of Artemisia annua L. extracts in vitro and the effect of an aqueous extract and artemisinin in sheep naturally infected with gastrointestinal nematodes. Parasitology Research, 113(6), P. 2345–2353. doi: 10.1007/s00436-014-3891-z
72. Boyko, O. O., Kabar, A., & Brygadyrenko, V. (2020). Nematicidal activity of aqueous tinctures of medicinal plants against larvae of the nematodes Strongyloides papillosus and Haemonchus contortus. Biosyst. Divers, 28, 119–123.
73. Mahmoudvand, H., Dezaki, E. S., Kheirandish, F., Ezatpour, B., Jahanbakhsh, S., & Harandi, M. F. (2014). Scolicidal effects of black cumin seed (Nigella sativa) essential oil on hydatid cysts. The Korean Journal of Parasitology, 52(6), 653–659. doi: 10.3347/kjp.2014.52.6.653
74. Boubaker Elandalousi, R., Akkari, H., B'chir, F., Gharbi, M., Mhadhbi, M., Awadi, S., & Darghouth, M. A. (2013). Thymus capitatus from Tunisian arid zone: chemical composition and in vitro anthelmintic effects on Haemonchus contortus. Veterinary Parasitology, 197(1–2), 374–378. doi: 10.1016/j.vetpar.2013.05.016
75. Ferreira, L. E., Benincasa, B. I., Fachin, A. L., França, S. C., Contini, S. S. H. T., Chagas, A. C. S., & Beleboni, R. O. (2016). Thymus vulgaris L. essential oil and its main component thymol : Anthelmintic effects against Haemonchus contortus from sheep. Veterinary Parasitology, 228, 70–76. doi: 10.1016/j.vetpar.2016.08.011
76. Pensel, P. E., Maggiore, M. A., Gende, L. B., Eguaras, M. J., Denegri, M. G., & Elissondo, M. C. (2014). Efficacy of Essential Oils of Thymus vulgaris and Origanum vulgare on Echinococcus granulosus. Interdisciplinary Perspectives on Infectious Diseases, 693289. doi: 10.1155/2014/693289
77. Mupeyo, B., Barry, T. N., Pomroy, W. E., Ramírez-Restrepo, C. A., López-Villalobos, N., & Pernthaner, A. (2011). Effects of feeding willow (Salix spp.) upon death of established parasites and parasite fecundity. Animal Feed Science and Technology, 164(1–2), 8–20. doi: 10.1016/j.anifeedsci.2010.11.015
78. Kļaviņa, A., Keidāne, D., Ganola, K., Lūsis, I., Šukele, R., Bandere, D., & Kovalcuka, L. (2023). Anthelmintic Activity of Tanacetum vulgare L. (Leaf and Flower) Extracts against Trichostrongylidae Nematodes in Sheep In Vitro. Animals, 13(13), 2176. doi: 10.3390/ani13132176