Hostname: page-component-848d4c4894-ttngx Total loading time: 0 Render date: 2024-06-13T07:21:21.255Z Has data issue: false hasContentIssue false
  • English
  • Français

In vitro anthelmintic activity of an R-carvone nanoemulsions towards multiresistant Haemonchus contortus

Published online by Cambridge University Press:  02 September 2022

Antônia Aniellen Raianne Moises Aguiar ,
José Vilemar de Araújo Filho ,
Henety Nascimento Pinheiro ,
Matheus da Silva Campelo ,
Wesley Lyeverton Correia Ribeiro ,
Ana Carolina Fonseca Lindoso Melo ,
Letícia Oliveira da Rocha ,
Maria Elenir Nobre Pinho Ribeiro ,
Nágila Maria Pontes Silva Ricardo  and
Flávia Oliveira Monteiro da Silva Abreu
...Show all authors
Antônia Aniellen Raianne Moises Aguiar
Affiliation:
Laboratório de Doenças Parasitárias, Programa de Pós-Graduação em Ciências Veterinárias, Universidade Estadual do Ceará, Fortaleza, Brazil
José Vilemar de Araújo Filho
Affiliation:
Laboratório de Doenças Parasitárias, Programa de Pós-Graduação em Ciências Veterinárias, Universidade Estadual do Ceará, Fortaleza, Brazil
Henety Nascimento Pinheiro
Affiliation:
Laboratório de Química Analítica e Ambiental, Programa de Pós-Graduação em Ciências Naturais, Universidade Estadual do Ceará, Fortaleza, Brazil
Matheus da Silva Campelo
Affiliation:
Laboratório de Polímeros e Inovação de Materiais, Departamento de Química Orgânica e Inorgânica, Universidade Federal do Ceará, Fortaleza, Brazil
Wesley Lyeverton Correia Ribeiro
Affiliation:
Departamento de Fisiologia e Farmacologia, Faculdade de Medicina, Universidade Federal do Ceará, Fortaleza, Brazil
Ana Carolina Fonseca Lindoso Melo
Affiliation:
Departamento de Patologia e Medicina Legal, Faculdade de Medicina, Universidade Federal do Ceará, Fortaleza, Brazil
Letícia Oliveira da Rocha
Affiliation:
Laboratório de Biologia Celular e Tecidual, Centro de Biociências e Biotecnologia, Universidade Estadual do Norte Fluminense, Rio de Janeiro, Brazil Laboratório de Ecotoxicologia, Centro de Ciências Exatas, Naturais e da Saúde, Universidade Federal do Espírito Santo, Vitória, Brazil
Maria Elenir Nobre Pinho Ribeiro
Affiliation:
Laboratório de Polímeros e Inovação de Materiais, Departamento de Química Orgânica e Inorgânica, Universidade Federal do Ceará, Fortaleza, Brazil
Nágila Maria Pontes Silva Ricardo
Affiliation:
Laboratório de Polímeros e Inovação de Materiais, Departamento de Química Orgânica e Inorgânica, Universidade Federal do Ceará, Fortaleza, Brazil
Flávia Oliveira Monteiro da Silva Abreu
Affiliation:
Laboratório de Química Analítica e Ambiental, Programa de Pós-Graduação em Ciências Naturais, Universidade Estadual do Ceará, Fortaleza, Brazil
Lorena Mayana Beserra de Oliveira
Affiliation:
Laboratório de Doenças Parasitárias, Programa de Pós-Graduação em Ciências Veterinárias, Universidade Estadual do Ceará, Fortaleza, Brazil
Weibson Paz Pinheiro André
Affiliation:
Laboratório de Doenças Parasitárias, Programa de Pós-Graduação em Ciências Veterinárias, Universidade Estadual do Ceará, Fortaleza, Brazil
Claudia Maria Leal Bevilaqua*
Affiliation:
Laboratório de Doenças Parasitárias, Programa de Pós-Graduação em Ciências Veterinárias, Universidade Estadual do Ceará, Fortaleza, Brazil
*
Author for correspondence: Claudia Maria Leal Bevilaqua, E-mail: bevilaqua.uece@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

This work aimed to evaluate the in vitro anthelmintic effect of carvone nanoemulsions on Haemonchus contortus. Three R-carvone nanoemulsions were prepared: uncoated R-carvone nanoemulsions homogenized in a sonicator (UNAlg-son) and homogenized in an ultrahomogenizer (UNAlg-ultra) and sodium alginate-coated R-carvone (CNAlg-ultra). The physicochemical characterizations of the nanoemulsions were carried out. The anthelmintic activity was evaluated using egg hatch test (EHT), larval development test (LDT) and adult worm motility test (AWMT). Changes in cuticle induced in adult H. contortus were evaluated by scanning electron microscopy (SEM). The results were subjected to analysis of variance and compared using the Tukey test (P < 0.05). The effective concentration to inhibit 50% (EC50) of egg hatching and larval development was calculated. The particle sizes were 281.1 nm (UNAlg-son), 152.7 nm (UNAlg-ultra) and 557.8 nm (CNAlg-ultra), and the zeta potentials were −15 mV (UNAlg-son), −10.8 mV (UNAlg-ultra) and −24.2 mV (CNAlg-ultra). The encapsulation efficiency was 99.84 ± 0.01%. SEM of the nanoemulsions showed an increase in size. In EHT, the EC50 values of UNAlg-son, UNAlg-ultra and CNAlg-ultra were 0.19, 0.02 and 0.17 mg mL−1, respectively. In LDT, they were 0.29, 0.31 and 0.95 mg mL−1 for UNAlg-son, UNAlg-ultra and CNAlg-ultra, respectively. The adult motility inhibition was 100% after 12 h of exposure to UNAlg-ultra and CNAlg-ultra, while for UNAlg-son, it was 79.16%. SEM showed changes in the buccal capsule and cuticular damage. It was concluded that R-carvone nanoemulsions showed antiparasitic action demonstrating promise for the control of infections caused by gastrointestinal nematodes in small ruminants.

Keywords

Carvonenanoemulsionnematodesphytotherapysodium alginate
Type
Research Article
Information
Parasitology , Volume 149 , Issue 12 , October 2022 , pp. 1631 - 1641
Check for updates
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abismail, B, Canselier, JP, Wilhelm, AM, Delmas, H and Gourdon, C (1999) Emulsification by ultrasound: drop size distribution and stability. Ultrasonics Sonochemistry 6, 75–83.CrossRefGoogle ScholarPubMed
Abreu, FOM, Costa, EF, Cardial, MRL and André, WPP (2020) Polymeric nanoemulsions enriched with Eucalyptus citriodora essential oil. Polímeros 30, e2020024.CrossRefGoogle Scholar
André, WPP, Ribeiro, WLC, Cavalcante, GS, Santos, JML, Macedo, ITF, Paula, HCB, Freitas, RM, Maia, SM, Melo, JV and Bevilaqua, CML (2016) Comparative efficacy and toxic effects of carvacryl acetate and carvacrol on sheep gastrointestinal nematodes and mice. Veterinary Parasitology 218, 52–58.CrossRefGoogle ScholarPubMed
André, WPP, Cavalcante, GS, Ribeiro, WLC, Santos, JML, Macedo, ITF, Paula, HCB, Morais, SM, Melo, JV and Bevilaqua, CML (2017) Anthelmintic effect of thymol and thymol acetate on sheep gastrointestinal nematodes and their toxicity in mice. Revista Brasileira de Parasitologia Veterinária 26, 323–330.CrossRefGoogle ScholarPubMed
André, WPP, Ribeiro, WLC, Oliveira, LMB, Macedo, ITF, Rondon, FCM and Bevilaqua, CML (2018) Essential oils and their bioactive compounds in the control of gastrointestinal nematodes of small ruminants. Acta Scientiae Veterinariae 46, 552.CrossRefGoogle Scholar
André, WPP, Paiva, JR Jr., Cavalcante, GS, Ribeiro, WLC, Araújo-Filho, JV, Cavalcanti, BC, Morais, SM, Oliveira, LMB, Bevilaqua, CML and Abreu, FOMS (2020) Chitosan nanoparticles loaded with carvacrol and carvacryl acetate for improved anthelmintic activity. Journal of the Brazilian Chemical Society 31, 1614–1622.Google Scholar
Araújo-Filho, JV, Ribeiro, WLC, André, WPP, Cavalcante, GS, Guerra, MCM, Muniz, CR, Macedo, ITF, Rondon, FCM, Bevilaqua, CML and Oliveira, LMB (2018) Effects of Eucalyptus citriodora essential oil and its major component, citronellal, on Haemonchus contortus isolates susceptible and resistant to synthetic anthelmintics. Industrial Crops and Products 124, 294–299.CrossRefGoogle Scholar
Araújo-Filho, JV, Ribeiro, WLC, André, WPP, Cavalcante, GS, Rios, TT, Schwinden, GM, Rocha, LO, Macedo, ITF, Morais, SM, Bevilaqua, CML and Oliveira, LMB (2019) Anthelmintic activity of Eucalyptus citriodora essential oil and its major component, citronellal, on sheep gastrointestinal nematodes. Revista Brasileira de Parasitologia Veterinária 28, 644–651.CrossRefGoogle ScholarPubMed
Barrere, V, Beech, RN, Charvet, CL and Prichard, RK (2014) Novel assay for the detection and monitoring of levamisole resistance in Haemonchus contortus. International Journal for Parasitology 44, 235–241.CrossRefGoogle ScholarPubMed
Bartram, DJ, Leathwick, DM, Taylor, MA, Geurden, T and Maeder, SJ (2012) The role of combination anthelmintic formulations in the sustainable control of sheep nematodes. Veterinary Parasitology 186, 151–158.CrossRefGoogle ScholarPubMed
Benavides, S, Cortés, P, Parada, J and Franco, W (2016) Development of alginate microspheres containing thyme essential oil using ionic gelation. Food Chemistry 204, 77–83.CrossRefGoogle ScholarPubMed
Bortoluzzi, BB, Buzatti, A, Chaaban, A, Pritsch, IC, Anjos, AD, Cipriano, RR, Deschamps, C and Molento, MB (2020) Mentha villosa Hubs., M. x piperita and their bioactives against gastrointestinal nematodes of ruminants and the potential as drug enhancers. Veterinary Parasitology 289, 109317.CrossRefGoogle Scholar
Brunet, S, Fourquaux, I and Hoste, H (2011) Ultrastructural changes in the third-stage, infective larvae of ruminant nematodes treated with sainfoin (Onobrychis viciifolia) extract. Parasitology International 60, 419–424.CrossRefGoogle ScholarPubMed
Campelo, MS, Melo, EO, Arrais, SP, Nascimento, FBSA, Gramosa, NV, Soares, SA, Ribeiro, MENP, Silva, CR, Júnior, HVN and Ricardo, NMPS (2021) Clove essential oil encapsulated on nanocarrier based on polysaccharide: a strategy for the treatment of vaginal candidiasis. Colloids and Surfaces A: Physicochemical and Engineering Aspects 610, 125732.CrossRefGoogle Scholar
Camurça-Vasconcelos, AL, Bevilaqua, CM, Morais, SM, Maciel, MV, Costa, CT, Macedo, IT, Oliveira, LMB, Braga, RR, Silva, RA and Vieira, LS (2007) Anthelmintic activity of Croton zehntneri and Lippia sidoides essential oils. Veterinary Parasitology 148, 288–294.CrossRefGoogle ScholarPubMed
Cavalcante, GS, Morais, SM, André, WPP, Araújo-Filho, JV, Muniz, CR, Rocha, LO, Ribeiro, WLC, Rodrigues, ALM, Oliveira, LMB, Bevilaqua, CML and Ramos, MV (2020) Chemical constituents of Calotropis procera latex and ultrastructural effects on Haemonchus contortus. Revista Brasileira de Parasitologia Veterinária 29, 22–25.CrossRefGoogle Scholar
Cheng, D, Jiang, C, Xu, J, Liu, Z and Mao, X (2020) Characteristics and applications of alginate lyases: a review. International Journal of Biological Macromolecules 164, 1304–1320.CrossRefGoogle Scholar
Clogston, JD and Patri, AK (2011) Zeta potential measurement. In McNeil, S (ed.), Characterization of Nanoparticles Intended for Drug Delivery. Methods in Molecular Biology (Methods and Protocols), 697, 63–70, Humana Press, New York.Google Scholar
Coles, GC, Jackson, F, Pomroy, WE, Prichard, RK, Von Samsonhimmelstjerna, G, Silvestre, A, Taylor, MA and Vercruysse, J (2006) The detection of anthelmintic resistance in nematodes of veterinary importance. Veterinary Parasitology 136, 167–185.CrossRefGoogle ScholarPubMed
Daltin, D (2011) Tensoativos: química, propriedades e aplicações. São Paulo: Edgard Blücher Ltda, 330pp.Google Scholar
Dash, M, Chiellini, F, Ottenbrite, RM and Chiellini, E (2011) Chitosan – a versatile semi-synthetic polymer in biomedical applications. Progress in Polymer Science 36, 981–1014.CrossRefGoogle Scholar
De Sousa, DP, Nóbrega, FFF and Almeida, RN (2007) Influence of the chirality of (R)-(−)- and (S)-(+)-carvone in the central nervous system: a comparative study. Chirality 19, 264–268.CrossRefGoogle ScholarPubMed
Fauvin, A, Charvet, C, Issouf, M, Cortet, J and Neveu, C (2010) cDNA-AFLP analysis in levamisole-resistant Haemonchus contortus reveals alternative splicing in a nicotinic acetylcholine receptor subunit. Molecular and Biochemical Parasitology 170, 105–107.CrossRefGoogle Scholar
Fernandes, RVDB, Borges, SV and Botrel, DA (2014) Gum arabic/starch/maltodextrin/inulin as wall materials on the microencapsulation of rosemary essential oil. Carbohydrate Polymers 101, 524–532.CrossRefGoogle ScholarPubMed
Ferreira, LE, Benincasa, BI, Fachin, AL, França, SC, Contini, SS, Chagas, AC and Beleboni, RO (2016) Thymus vulgaris L. essential oil and its main component thymol: anthelmintic effects against Haemonchus contortus from sheep. Veterinary Parasitology 228, 70–76.CrossRefGoogle ScholarPubMed
Gago, CML, Artiga-Artigas, M, Antunes, MDC, Faleiro, ML, Miguel, MG and Martín-Belloso, O (2019) Effectiveness of nanoemulsions of clove and lemongrass essential oils and their major components against Escherichia coli and Botrytis cinerea. Journal of Food Science and Technology 56, 2721–2736.CrossRefGoogle ScholarPubMed
Garbin, VP, Munguía, B, Saldaña, JC, Deschamps, C, Cipriano, RR and Molento, MB (2021) Chemical characterization and in vitro anthelmintic activity of Citrus bergamia Risso and Citrus X paradisii Macfad essential oil against Haemonchus contortus Kirby isolate. Acta Tropica 217, 105869.CrossRefGoogle ScholarPubMed
Grando, TH, De Sá, MF, Baldissera, MD, Oliveira, CB, De Souza, ME, Raffin, RP, Santos, RCV, Domingues, R, Minho, AP, Leal, M and 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. Journal of Helminthology 90, 377–382.CrossRefGoogle ScholarPubMed
Guerra-Rosas, MI, Morales-Castro, J, Ochoa-Martınez, LA, Salvia-Trujillo, L and Olga Martín-Belloso, O (2016) Long-term stability of food-grade nanoemulsions from high methoxyl pectin containing essential oils. Food Hydrocolloids 52, 438–446.CrossRefGoogle Scholar
Hariyadi, D M and Islam, N (2020) Current Status of Alginate in Drug Delivery. Advances in Pharmacological and Pharmaceutical Sciences 16.Google Scholar
Hounzangbe-Adote, MS, Paolini, V, Fouraste, I, Moutairou, K and Hoste, H (2005) In vitro effects of four tropical plants on three life-cycle stages of the parasitic nematode, Haemonchus contortus. Veterinary Science Research 78, 155–160.CrossRefGoogle ScholarPubMed
Hubert, J and Kerboeuf, DA (1992) Microlarval development assay for the detection of anthelmintic resistance in sheep nematodes. Veterinary Record 130, 442–446.CrossRefGoogle ScholarPubMed
Jackson, F and Coop, RL (2000) The development of anthelmintic resistance in sheep nematodes. Parasitology 120, 95–107.CrossRefGoogle ScholarPubMed
Johri, RK (2011) Cuminum cyminum and Carum carvi: an update. Pharmacognosy Review 5, 63–72.CrossRefGoogle ScholarPubMed
Jukic, M, Politeo, O, Maksimovic, M, Milos, M and Milos, M (2007) In vitro acetylcholinesterase inhibitory properties of thymol, carvacrol and their derivatives thymoquinone and thymohydroquinone. Phytotherapy Research 21, 259–261.CrossRefGoogle ScholarPubMed
Kaplan, RM and Vidyashankar, AN (2012) An inconvenient truth: global warming and anthelmintic resistance. Veterinary Parasitology 186, 70–78.CrossRefGoogle ScholarPubMed
Katiki, LM, Barbieri, AME, Araujo, RC, Veríssimo, CJ, Louvandini, H and Ferreira, JFS (2017) Synergistic interaction of ten essential oils against Haemonchus contortus in vitro. Veterinary Parasitology 243, 47–51.CrossRefGoogle ScholarPubMed
Katiki, LM, Araujo, RC, Ziegelmeyer, ACP, Gomes, G, Gutmanis, L, Rodrigues, MS, Bueno, CJ, Veríssimo, H, Louvandini, JFS and Ferreira, AFT (2019) Evaluation of encapsulated anethole and carvone in lambs artificially- and naturally-infected with Haemonchus contortus. Experimental Parasitology 197, 36–42.CrossRefGoogle ScholarPubMed
Kotze, AC and Prichard, RK (2016) Anthelmintic resistance in Haemonchus contortus: history, mechanisms and diagnosis. Advances in Parasitology 93, 397–428.CrossRefGoogle ScholarPubMed
Kurt, BZ, Gazioglu, L, Dag, A, Salmas, RE, Kaylk, G, Durdagi, S and Sonmez, F (2017) Synthesis, anticholinesterase activity and molecular modeling study of novel carbamate-substituted thymol/carvacrol derivatives. Bioorganic & Medicinal Chemistry 25, 1352–1363.CrossRefGoogle ScholarPubMed
Lertsutthiwong, P and Rojsitthisak, P (2011) Chitosan-alginate nanocapsules for encapsulation of turmeric oil. Pharmazie 66, 911–915.Google ScholarPubMed
López, MD and Pascual-Villalobos, MJ (2010) Mode of inhibition of acetylcholinesterase by monoterpenoids and implications for pest control. Industrial Crops and Products 31, 284–288.CrossRefGoogle Scholar
Lovelyn, C and Attama, AA (2011) Current state of nanoemulsions in drug delivery. Journal of Biomaterials and Nanobiotechnology 2, 626–639.CrossRefGoogle Scholar
Machado, AHE, Lundberg, D, Ribeiro, AJ, Veiga, FJ, Lindman, B, Miguel, MG and Olsson, U (2012) Preparation of calcium alginate nanoparticles using water-in-oil (W/O) nanoemulsions. Langmuir 28, 4131–4141.CrossRefGoogle ScholarPubMed
Martins, E, Poncelet, D, Rodrigues, RC and Renard, D (2017) Oil encapsulation techniques using alginate as encapsulating agent: applications and drawbacks. Journal of Microencapsulation 4, 754–771.CrossRefGoogle Scholar
Martínez-Ortíz-de-Montellano, C, Arroyo-López, C, Fourquaux, I, Torres-Costa, CA and Hoste, H (2013) Scanning electron microscopy of Haemonchus contortus exposed to tannin rich plants under in vivo and in vitro conditions. Experimental Parasitology 133, 281–286.CrossRefGoogle ScholarPubMed
McClements, DJ (2005) Food Emulsions: Principles, Practices, and Techniques, Vol. 2. Boca Raton: CRC Press, 714pp.Google Scholar
Mcclements, DJ (2010) Emulsion design to improve the delivery of functional lipophilic components. Annual Review of Food Science and Technology 1, 241–269.CrossRefGoogle ScholarPubMed
Miller, JE, Baker, NF and Farver, TB (1986) Anthelmintic treatment of pastured dairy cattle in California. American Journal of Veterinary Research 47, 2036–2040.Google ScholarPubMed
Morais, ARV, Alencar, EN, Xavier, FH Jr., Oliveira, CM, Marcelino, HR, Barratt, G, Fessi, H, Egito, EST and Elaissari, A (2016) Freeze-drying of emulsified systems: a review. International Journal of Pharmaceutics 503, 102–114.CrossRefGoogle ScholarPubMed
Mwangi, WW, Ho, KW, Tey, BT and Chan, ES (2016) Effects of environmental factors on the physical stability of pickering-emulsions stabilized by chitosan particles. Food Hydrocolloids 60, 543–550.CrossRefGoogle Scholar
Neveu, C, Charvet, C, Fauvin, A, Cortet, J, Castagnone-Sereno, P and Cabaret, J (2007) Identification of levamisole resistance markers in the parasitic nematode Haemonchus contortus using a cDNA-AFLP approach. Parasitology 134, 1105–1110.CrossRefGoogle ScholarPubMed
Neveu, C, Charvet, CL, Fauvin, A, Cortet, J, Beech, RN and Cabaret, J (2010) Genetic diversity of levamisole receptor subunits in parasitic nematode species and abbreviated transcripts associated with resistance. Pharmacogenetics and Genomics 20, 414–425.CrossRefGoogle ScholarPubMed
Prabaharan, M (2015) Chitosan-based nanoparticles for tumor-targeted drug delivery. International Journal of Biological Macromolecules 72, 1313–1322.CrossRefGoogle ScholarPubMed
Ribeiro, WLC, Macedo, ITF, Santos, JML, Oliveira, EF, Camurça-Vasconcelos, ALF, Paula, HCB and Bevilaqua, CML (2013) Activity of chitosan encapsulated Eucalyptus staigeriana essential oil on Haemonchus contortus. Experimental Parasitology 135, 24–29.CrossRefGoogle ScholarPubMed
Ribeiro, JC, Ribeiro, WLC, Camurça-Vasconcelos, ALF, Macedo, ITF, Santos, JML, Paula, HCB, Aráujo-Filho, JV, Magalhães, RD and Bevilaqua, CML (2014) Efficacy of free and nanoencapsulated Eucalyptus citriodora essential oils on sheep gastrointestinal nematodes and toxicity for mice. Veterinary Parasitology 204, 243–248.CrossRefGoogle ScholarPubMed
Ribeiro, WLC, Camurça-Vasconcelos, ALF, Macedo, ITF, Santos, JML, Ribeiro, JC, Pereira, VA, Viana, DA, Paula, HCB and Bevilaqua, CML (2015) In vitro effects of Eucalyptus staigeriana nanoemulsion on Haemonchus contortus and toxicity in rodents. Veterinary Parasitology 212, 444–447.CrossRefGoogle ScholarPubMed
Ribeiro, WLC, Camurça-Vasconcelos, ALF, Santos, JML, Macedo, ITF, Ribeiro, JC, Oliveira, EF, Paula, HCB and Bevilaqua, CML (2017) The use of Eucalyptus staigeriana nanoemulsion for control of sheep haemonchosis. Pesquisa Veterinária Brasileira 37, 221–226.CrossRefGoogle Scholar
Roberts, FHS and O'Sullivan, JP (1950) Methods for egg counts and larval cultures for strongyles infesting the gastrointestinal tract of cattle. Australian Journal of Agricultural Research 1, 99–102.CrossRefGoogle Scholar
Ross, SM, McManus, IC, Harrison, V and Mason, O (2013) Neurobehavioral problems following low-level exposure to organophosphate pesticides: a systematic and meta-analytic review. Critical Reviews in Toxicology 43, 21–44.CrossRefGoogle ScholarPubMed
Ryan, MF and Byrne, O (1988) Plant-insect coevolution and inhibition of acetylcholinesterase. Journal of Chemical Ecology 14, 1965–1975.CrossRefGoogle ScholarPubMed
Salvia-Trujillo, L, Rojas-Grau, MA, Soliva-Fortuny, R and Martın-Belloso, O (2014) Formulation of antimicrobial edible nanoemulsions with pseudo-ternary phase experimental design. Food and Bioprocess Technology 7, 3022–3032.CrossRefGoogle Scholar
Santos, J, Ramírez, P, Llinares, R, Muñoz, J and Trujillo-Cayado, LA (2018) Enhancing rosemary oil-in-water microfluidized nanoemulsion properties through formulation optimization by response surface methodology. LWT 97, 370.Google Scholar
Silva, CR, Lifschitz, AL, Macedo, SRD, Campos, NRCL, Viana-Filho, M, Alcântara, ACS, Araújo, JG, Alencar, LMR and Costa-Junior, LM (2021) Combination of synthetic anthelmintics and monoterpenes: assessment of efficacy, and ultrastructural and biophysical properties of Haemonchus contortus using atomic force microscopy. Veterinary Parasitology 290, 109345.CrossRefGoogle ScholarPubMed
Toscano, JHB, Lopes, LG, Giraldelo, LA and Da Silva, MH (2018) Identification of appropriate reference genes for local immune-related studies in Morada Nova sheep infected with Haemonchus contortus. Molecular Biology Reports 45, 1253–1262.CrossRefGoogle ScholarPubMed
Tuersong, W, He, L, Zhu, T, Yang, X, Zhang, Z, Ahmad, AA, Di, W, Wang, C, Zhou, C, Liu, H, Chen, J and Hu, M (2020) Development and evaluation of a loop-mediated isothermal amplification (LAMP) assay for the detection of the E198A SNP in the isotype-1 β-tubulin gene of Haemonchus contortus populations in China. Veterinary Parasitology 278, 109040.CrossRefGoogle ScholarPubMed
Wang, C, Li, F, Zhang, Z, Yang, X, Ahmad, AA, Li, X, Du, A and Hu, M (2017) Recent research progress in China on Haemonchus contortus. Frontiers in Microbiology 8, 1509.CrossRefGoogle ScholarPubMed
Wong, TY, Preston, LA and Schiller, NL (2000) Alginate lyase: review of major sources and enzyme characteristics, structure-function analysis, biological roles, and applications. Annual Review of Microbiology 54, 289–340.CrossRefGoogle ScholarPubMed
Zhu, L, Dai, J, Li Yang, L and Qiu, J (2013) Anthelmintic activity of Arisaema franchetianum and Arisaema lobatum essential oils against Haemonchus contortus. Journal of Ethnopharmacology 148, 311–316.CrossRefGoogle ScholarPubMed