{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,26]],"date-time":"2026-02-26T19:37:31Z","timestamp":1772134651433,"version":"3.50.1"},"reference-count":35,"publisher":"MDPI AG","issue":"10","license":[{"start":{"date-parts":[[2021,10,17]],"date-time":"2021-10-17T00:00:00Z","timestamp":1634428800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>Parasiticidal fungi have been used in several in vivo experiments in livestock farms worldwide, constituting an effective tool for the biocontrol of gastrointestinal parasites in grazing animals. In the first year of study, two groups of eight first-season pasturing ewe lambs infected by strongyles were dewormed with albendazole, and then, the test group received an oral dose of 106 chlamydospores of Mucor circinelloides and 106\u00a0Duddingtonia flagrans individually and thrice a week from mid-September to May (FS1), while the control group remained without fungi (CT1). In the second year, two new groups of first-season grazing ewe lambs were treated with ivermectin and subjected to the same experimental design (FS2 and CT2, respectively). The anthelmintic efficacy was 96.6% (CT1), 95.6% (FS1), 96.1% (CT2), and 95.1% (FS2). The counts of strongyle egg output increased in the control groups (CT1 and CT2) throughout the study and reached numbers higher than 600 eggs per gram of feces (EPG), while in FS1 and FS2, they were &lt;250 EPG. The values of red blood cell parameters registered for CT1 and CT2 were lower than those of the reference standards, while a significant increment was recorded in FS1 and FS2, and values within the physiological range were attained. It is concluded that integrating efficient anthelminthic deworming with rotational pasturing and the regular intake of chlamydospores of M. circinelloides and D. flagrans provides a helpful strategy for maintaining low levels of strongyle egg output in first-season grazing ewe lambs and improves their health status.<\/jats:p>","DOI":"10.3390\/pathogens10101338","type":"journal-article","created":{"date-parts":[[2021,10,17]],"date-time":"2021-10-17T23:05:47Z","timestamp":1634511947000},"page":"1338","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":17,"title":["Control of Strongyles in First-Season Grazing Ewe Lambs by Integrating Deworming and Thrice-Weekly Administration of Parasiticidal Fungal Spores"],"prefix":"10.3390","volume":"10","author":[{"given":"Mathilde","family":"Voinot","sequence":"first","affiliation":[{"name":"Control of Parasites Research Group (COPAR, GI-2120), Department of Animal Pathology, Faculty of Veterinary, University of Santiago de Compostela, 27142 Lugo, Spain"}]},{"given":"Rodrigo","family":"Bonilla","sequence":"additional","affiliation":[{"name":"CARVAL Pharmaceuticals, Bogot\u00e1 110211, Colombia"}]},{"given":"S\u00e9rgio","family":"Sousa","sequence":"additional","affiliation":[{"name":"Vasco da Gama Research Centre (CIVG), Department of Veterinary Sciences, Vasco da Gama University School, Avenida Jos\u00e9 R. Sousa Fernandes 197 Lordem\u00e3o, 3020-210 Coimbra, Portugal"},{"name":"CIISA\u2014Centro de Investiga\u00e7\u00e3o Interdisciplinar em Sanidade Animal, Faculdade de Medicina Veterin\u00e1ria, Universidade de Lisboa, Avenida da Universidade T\u00e9cnica, 1300-477 Lisbon, Portugal"}]},{"given":"Jaime","family":"Sanch\u00eds","sequence":"additional","affiliation":[{"name":"Parasitic Diseases, Veterinary Faculty, University of \u201cLa Rep\u00fablica (Regional Norte)\u201d, Salto 50000, Uruguay"}]},{"given":"Miguel","family":"Canh\u00e3o-Dias","sequence":"additional","affiliation":[{"name":"CIISA\u2014Centro de Investiga\u00e7\u00e3o Interdisciplinar em Sanidade Animal, Faculdade de Medicina Veterin\u00e1ria, Universidade de Lisboa, Avenida da Universidade T\u00e9cnica, 1300-477 Lisbon, Portugal"},{"name":"Department of Geography, University College London, London WC1E 6BT, UK"}]},{"given":"Jos\u00e9","family":"Romero Delgado","sequence":"additional","affiliation":[{"name":"Veterinary Inspection, San Crist\u00f3bal de La Laguna City Hall, 38201 La Laguna, Spain"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5390-6998","authenticated-orcid":false,"given":"Jo\u00e3o","family":"Lozano","sequence":"additional","affiliation":[{"name":"CIISA\u2014Centro de Investiga\u00e7\u00e3o Interdisciplinar em Sanidade Animal, Faculdade de Medicina Veterin\u00e1ria, Universidade de Lisboa, Avenida da Universidade T\u00e9cnica, 1300-477 Lisbon, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1212-8250","authenticated-orcid":false,"given":"Rita","family":"S\u00e1nchez-Andrade","sequence":"additional","affiliation":[{"name":"Control of Parasites Research Group (COPAR, GI-2120), Department of Animal Pathology, Faculty of Veterinary, University of Santiago de Compostela, 27142 Lugo, Spain"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2682-9015","authenticated-orcid":false,"given":"Mar\u00eda","family":"Sol Arias","sequence":"additional","affiliation":[{"name":"Control of Parasites Research Group (COPAR, GI-2120), Department of Animal Pathology, Faculty of Veterinary, University of Santiago de Compostela, 27142 Lugo, Spain"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7548-667X","authenticated-orcid":false,"given":"Lu\u00eds","family":"Madeira de Carvalho","sequence":"additional","affiliation":[{"name":"CIISA\u2014Centro de Investiga\u00e7\u00e3o Interdisciplinar em Sanidade Animal, Faculdade de Medicina Veterin\u00e1ria, Universidade de Lisboa, Avenida da Universidade T\u00e9cnica, 1300-477 Lisbon, Portugal"}]}],"member":"1968","published-online":{"date-parts":[[2021,10,17]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1016\/j.vetpar.2013.01.010","article-title":"Soil moisture influences the development of Haemonchus contortus and Trichostrongylus colubriformis to third stage larvae","volume":"196","author":"Khadijah","year":"2013","journal-title":"Vet. Parasitol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"250","DOI":"10.1136\/vr.102512","article-title":"Practices to optimise gastrointestinal nematode control on sheep, goat and cattle farms in Europe using targeted (selective) treatments","volume":"175","author":"Charlier","year":"2014","journal-title":"Vet. Rec."},{"key":"ref_3","first-page":"407","article-title":"Review on anthelmintic resistance against gastrointestinal nematodes of small ruminants: Its status and future perspective in Ethiopia","volume":"6","author":"Furgasa","year":"2018","journal-title":"J. Vet. Sci. Ani Husb."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"van den Pol-van Dasselaar, A., Hennessy, D., and Isselstein, J. (2020). Grazing of Dairy Cows in Europe\u2014An in-depth analysis based on the perception of grassland experts. Sustainability, 12.","DOI":"10.3390\/su12031098"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1007\/s12639-012-0215-z","article-title":"Internal parasite management in grazing livestock","volume":"37","author":"Kumar","year":"2012","journal-title":"J. Parasit. Dis."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1016\/j.pt.2006.04.004","article-title":"The effects of tannin-rich plants on parasitic nematodes in ruminants","volume":"22","author":"Hoste","year":"2006","journal-title":"Trends Parasitol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/j.vetpar.2009.10.004","article-title":"Efficacy of copper oxide wire particles against gastrointestinal nematodes in sheep and goats","volume":"168","author":"Soli","year":"2010","journal-title":"Vet. Parasitol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1016\/j.cvfa.2019.11.007","article-title":"Sustainable Approaches to Parasite Control in Ruminant Livestock","volume":"36","author":"Burke","year":"2020","journal-title":"Vet. Clin. N. Am. Food Anim. Pr."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"707","DOI":"10.1007\/s00436-011-2302-y","article-title":"Efficacy of an energy block containing Duddingtonia flagrans in the control of gastrointestinal nematodes of sheep","volume":"109","author":"Iglesias","year":"2011","journal-title":"Parasitol. Res."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1016\/j.exppara.2017.04.008","article-title":"In vitro predatory activity of Arthrobotrys oligospora and after passing through gastrointestinal tract of small ruminants on infective larvae of trichostrongylides","volume":"177","author":"Cai","year":"2017","journal-title":"Exp. Parasitol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1016\/j.vetpar.2018.10.001","article-title":"The nematophagous fungus Duddingtonia flagrans reduces the gastrointestinal parasitic nematode larvae population in faeces of orally treated calves maintained under tropical conditions. Dose\/Response assessment","volume":"263","year":"2018","journal-title":"Vet. Parasitol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"109173","DOI":"10.1016\/j.vetpar.2020.109173","article-title":"The efficacy of predatory fungi on the control of gastrointestinal parasites in domestic and wild animals\u2014A systematic review","volume":"283","year":"2020","journal-title":"Vet. Parasitol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1016\/j.vetpar.2006.05.007","article-title":"Efficiency of Duddingtonia flagrans against Trichostrongyle infections of sheep on mountain pastures","volume":"141","author":"Uriarte","year":"2006","journal-title":"Vet. Parasitol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"665","DOI":"10.1017\/S0022149X1600081X","article-title":"Consumption of nutritional pellets with Duddingtonia flagrans fungal chlamydospores reduces infective nematode larvae of Haemonchus contortus in faeces of Saint Croix lambs","volume":"91","author":"Marcelino","year":"2016","journal-title":"J. Helminthol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1016\/j.vetpar.2018.02.010","article-title":"Field evaluation of Duddingtonia flagrans IAH 1297 for the reduction of worm burden in grazing animals: Tracer studies in sheep","volume":"253","author":"Healey","year":"2018","journal-title":"Vet. Parasitol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s13205-019-2042-8","article-title":"Efficiency of the Bioverm\u00ae (Duddingtonia flagrans) fungal formulation to control in vivo and in vitro of Haemonchus contortus and Strongyloides papillosus in sheep","volume":"10","author":"Braga","year":"2020","journal-title":"3 Biotech"},{"key":"ref_17","first-page":"1","article-title":"A combined effort to avoid strongyle infection in horses in an oceanic climate region: Rotational grazing and parasiticidal fungi","volume":"11","author":"Arroyo","year":"2018","journal-title":"Parasites Vectors"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"109038","DOI":"10.1016\/j.vetpar.2020.109038","article-title":"Integrating the control of helminths in dairy cattle: Deworming, rotational grazing and nutritional pellets with parasiticide fungi","volume":"278","author":"Voinot","year":"2020","journal-title":"Vet. Parasitol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"791","DOI":"10.1017\/S0031182020000414","article-title":"Soil fungi enable the control of gastrointestinal nematodes in wild bovidae captive in a zoological park: A 4-year trial","volume":"147","author":"Palomero","year":"2020","journal-title":"Parasitology"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1455","DOI":"10.1007\/s11250-016-1117-3","article-title":"Influence of sustained deworming pressure on the anthelmintic resistance status in strongyles of sheep under field conditions","volume":"48","author":"Vijayasarathi","year":"2016","journal-title":"Trop. Anim. Health Prod."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s13620-017-0097-6","article-title":"Field evaluation of the efficacy of common anthelmintics used in the control of gastrointestinal nematodes of sheep in Dabat district, Northwest Ethiopia","volume":"70","author":"Seyoum","year":"2017","journal-title":"Ir. Vet. J."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Mondragon, J., Olmedo-Ju\u00e1rez, A., Reyes-Guerrero, D.E., Ram\u00edrez-Vargas, G., Ariza-Rom\u00e1n, A.E., L\u00f3pez-Arellano, M.E., De Gives, P.M., and Napolitano, F. (2019). Detection of gastrointestinal nematode populations resistant to albendazole and ivermectin in sheep. Animals, 9.","DOI":"10.3390\/ani9100775"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1188","DOI":"10.14202\/vetworld.2019.1188-1194","article-title":"Influence of intensive rearing, continuous and rotational grazing systems of management on parasitic load of lambs","volume":"12","author":"Prasad","year":"2019","journal-title":"Vet. World"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1016\/j.vetpar.2009.03.054","article-title":"Impact of rotational grazing on management of gastrointestinal nematodes in weaned lambs","volume":"163","author":"Burke","year":"2009","journal-title":"Vet. Parasitol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.exppara.2015.07.006","article-title":"Duddingtonia flagrans in the control of gastrointestinal nematodes of horses","volume":"159","author":"Buzatti","year":"2015","journal-title":"Exp. Parasitol."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Malag\u00f3n, J.\u00c1.H., Cazapal-Monteiro, C.F., Quintero, R.B., Salinero, A.M.P., Torres, M.I.S., Messnier, M.V., Pena, M.V., and Blanco, \u00c1.R. (2019). Advantageous Fungi against Parasites Transmitted through Soil. Fungal Infection, IntechOpen.","DOI":"10.5772\/intechopen.81027"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1016\/j.vetpar.2003.10.017","article-title":"Efficiency of feeding Duddingtonia flagrans chlamydospores to grazing ewes on reducing availability of parasitic nematode larvae on pasture","volume":"118","author":"Fontenot","year":"2003","journal-title":"Vet. Parasitol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1590\/s1984-296120180011","article-title":"Control of sheep gastrointestinal nematodes using the combination of Duddingtonia flagrans and Levamisole Hydrochloride 5%","volume":"27","author":"Vilela","year":"2018","journal-title":"Rev. Bras. Parasitol. Vet."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"706","DOI":"10.1017\/S0022149X1500098X","article-title":"Lack of negative effects of the biological control agent Duddingtonia flagrans on soil nematodes and other nematophagous fungi","volume":"90","author":"Saumell","year":"2016","journal-title":"J. Helminthol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1016\/j.vetpar.2016.09.014","article-title":"Feeding horses with industrially manufactured pellets with fungal spores to promote nematode integrated control","volume":"229","author":"Arroyo","year":"2016","journal-title":"Vet. Parasitol."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Hern\u00e1ndez, J.A., V\u00e1zquez-Ruiz, R.A., Cazapal-Monteiro, C.F., Valderr\u00e1bano, E., Arroyo, F.L., Francisco, I., Migu\u00e9lez, S., S\u00e1nchez-Andrade, R., Paz-Silva, A., and Arias, M.S. (2017). Isolation of ovicidal fungi from fecal samples of captive animals maintained in a zoological park. J. Fungi, 3.","DOI":"10.3390\/jof3020029"},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Vi\u00f1a, C., Silva, M.I., Palomero, A.M., Voinot, M., Vil\u00e1, M., Hern\u00e1ndez, J.\u00c1., Paz-Silva, A., S\u00e1nchez-Andrade, R., Cazapal-Monteiro, C.F., and Arias, M.S. (2020). The Control of Zoonotic Soil-Transmitted Helminthoses Using Saprophytic Fungi. Pathogens, 9.","DOI":"10.3390\/pathogens9121071"},{"key":"ref_33","unstructured":"MAFF (1986). Manual of Veterinary Parasitological Laboratory Techniques, Ministry of Agriculture, Fisheries and Food. Her Majesty\u2019s Stationary Office (HMSO). [3rd ed.]."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"306","DOI":"10.1016\/j.vetpar.2012.09.004","article-title":"World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P.) Guideline: Anthelmintic combination products targeting nematode infections of ruminants and horses","volume":"190","author":"Geary","year":"2012","journal-title":"Vet. Parasitol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1016\/j.vetpar.2003.11.012","article-title":"Morphological identification of nematode larvae of small ruminants and cattle simplified","volume":"119","author":"VanWyk","year":"2004","journal-title":"Vet. Parasitol."}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/10\/10\/1338\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T07:16:27Z","timestamp":1760166987000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/10\/10\/1338"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,10,17]]},"references-count":35,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2021,10]]}},"alternative-id":["pathogens10101338"],"URL":"https:\/\/doi.org\/10.3390\/pathogens10101338","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,10,17]]}}}