Bestrijden we runderparasieten in de toekomst met onze gewassen?

Laurens
Zwanenburg

Onze veestapel, specifiek de runderen, worden al vanouds geteisterd door parasitaire infecties. Het is echter pas vrij recent, circa 1940, dat men begonnen is om parasitaire infecties in runderen te bestrijden. Men kwam tot de vaststelling dat deze parasieten schadelijk zijn voor de gezondheid van de dieren waardoor - vooral in deze periode belangrijk geachte - productiviteit van de dieren in het gedrang kwam. Daarnaast hebben zulke infecties natuurlijk een grote impact op het dierenwelzijn vermits ze aanleiding kunnen geven tot ongemak, ziekte en zelfs sterfte. Als we kijken naar de maag- en darmparasieten bij runderen die gehouden worden in westerse landen, dan zien we in de meeste gevallen dat ééncellige parasieten en parasitaire rondwormen verantwoordelijk voor verscheidene ziektes. Zo worden de twee ééncelligen, namelijk Giardia duodenalis en Cryptosporidium parvum, dikwijls verantwoordelijk gehouden voor diarree, groeivertraging, zwakte en sterfte bij jonge kalveren die nog op stal gehouden worden. Daarnaast zijn het juist Ostertagia ostertagi en Cooperia oncophora, de twee belangrijkste parasitaire maag- en darmwormen, die zorgen voor zware infecties bij oudere kalveren en jonge volwassen runderen vanaf dat de dieren op de weide gehouden worden. Het valt dus wel op dat runderen eigenlijk altijd in contact komen met maag- en darmparasieten, ongeacht de kwaliteit en het type van huisvesting. 

image

Om zulke parasitaire infecties te counteren worden onze runderen geregeld, namelijk één- of tweemaal per jaar, behandeld met anti-parasitaire middelen. Normaal gezien, indien op de juiste momenten uitgevoerd, zou dit ervoor moeten zorgen dat ernstige infecties voorkomen worden en dat de dieren eigenlijk weinig parasitair ongemak ondervinden. Echter niet lang na het op de markt brengen van de eerste anti-parasitaire producten, werd al beschreven dat de effectiviteit van de behandeling afnam doordat een deel van de parasieten resistentie-eigenschappen begon te vertonen. De ontwikkeling van resistentie tegen ontwormingsproducten, of anthelmintica, werd oorspronkelijk gedocumenteerd bij schapen in Australië en Nieuw-Zeeland die blootgesteld werden aan de rode lebmaagworm. Deze bloedzuigende maagworm gaf bijgevolg dan ook aanleiding tot ernstige uitbraken van bloedarmoede onder grote populaties van schapen doordat de ontwormingsproducten niet meer hun beoogde effect behaalden. In die periode werden dusdanige problemen bij runderen echter nog niet gerapporteerd, maar recent blijkt dat een steeds groter wordende wormpopulatie resistent begint te worden tegen de huidige anthelmintica, terwijl er in de laatste jaren eigenlijk zeer weinig nieuwe producten op de markt zijn gekomen. Bijgevolg kan het schapen-scenario zich ook bij runderen afspelen als we niet meer in staat zijn om geïnfecteerde dieren effectief te behandelen. Met andere woorden wordt de toepassing van deze ontwormingsproducten, zonder of met onderliggende behandelingsstrategie, steeds controversiëler. Hoewel antibioticaresistentie wereldwijd natuurlijk zeer belangrijk is voor mens en dier, is het essentieel dat we ook beseffen hoe groot de impact van een gevorderde anthelmintica-resistentie zal zijn op de huidige veehouderij. 

Wereldwijd zijn veterinaire parasitologen bijgevolg hard opzoek naar een mogelijke oplossing tegen de ontwikkelende resistentie, maar tot dusver heeft dit nog niet geleid tot dé oplossing. Enkele potentiële alternatieven die naar voren worden geschoven door vooruitstrevende parasitologen zijn onder andere vaccin-ontwikkeling en het voederen van biologisch actieve gewassen aan veedieren. Daarnaast helpt een meer algemene aanpak, zoals weidemanagement en de selectieve behandeling van enkel zieke dieren wel om de ontwikkeling van resistentie af te remmen, maar dit zal - zeker vanuit economisch oogpunt - gecomplementeerd moeten worden met een ander alternatief om echt effectief te zijn op langer termijn. Met deze huidige problematiek in gedachten is het mijn ambitie om mee te werken aan het vinden van een oplossing voor dit ontwikkelend probleem. Voor mijn scriptie was het daarom de bedoeling dat ik één van de alternatieven, de biologisch actieve gewassen, verder ging onderzoeken. Zo'n onderzoek komt natuurlijk niet uit de lucht vallen en is gebaseerd op bouwstenen die gelegd zijn door voorafgaand onderzoek. Zo hebben onderzoekers al kunnen aantonen dat sommige planten, of plantenextracten, daadwerkelijk een anti-parasitaire eigenschap bezitten. In de meeste gevallen worden tannine-rijke plantendelen, ook aanwezig in bijvoorbeeld wijn en thee, verantwoordelijk gehouden voor dit gunstige effect. Zo is het zeer waarschijnlijk dat deze tannines het eiwit in de darm, afkomstig van de voeding, kunnen binden waardoor de parasitaire wormen hiervan geen gebruik kunnen maken. Tevens heeft recent onderzoek aangetoond dat het voederen van deze biologisch actieve planten aanleiding kan geven tot een afname van het voortplantingsvermogen van de wormen met bijgevolg een lagere infectiegraad. Het is bijgevolg gekend dat er planten zijn met een anti-parasitair effect, maar vooraleer deze effectief toegepast kunnen worden is het onder andere belangrijk dat we weten welk specifiek onderdeel van die plant verantwoordelijk is. Door verschillende internationale bedrijven worden er, in het kader van dit onderzoek, extracten of moleculaire verbindingen opgezuiverd uit de verschillende onderdelen van de beoogde planten en deze kunnen vervolgens gebruikt worden in een resem van testen om hun anti-parasitair effect te beoordelen. Daarnaast weet men eigenlijk niet goed of deze stoffen ook een effect hebben tegen andere runderparasieten, waaronder bijvoorbeeld de ééncellige parasieten. Om dit verder te onderzoeken heb ik met mijn scriptie acht extracten getest op enerzijds de twee belangrijkste maagdarm-parasieten, O. ostertagi en C. oncophora, en anderzijds op de ééncellige parasiet G. duodenalis

image

Met dit onderzoek, grotendeels uitgevoerd aan de Universiteit van Kopenhagen, heb ik kunnen aantonen dat de de helft van de geteste extracten zorgt voor een mindere levensvatbaarheid van de G. duodenalis parasiet, iets dat nog niet eerder in de literatuur beschreven werd. Bijgevolg geeft dit een sterke indicatie dat deze biologisch actieve gewassen inzetbaar zijn tegen andere parasieten dan enkel parasitaire maag- en darmwormen en dus een groter toepassingsbereik bezitten. Dit is natuurlijk voordelig op grote schaal, vermits hierdoor de algehele parasitaire infectiedruk verlaagd zou kunnen worden, wat tevens zal resulteren in een verminderd gebruik van ontwormingsproducten met finaal een afname van de resistentie-ontwikkeling. Het is echter nog erg vroeg om te zeggen of we daadwerkelijk gewassen kunnen inzetten om het aantal parasitaire infecties in runderen terug te dringen. Zo zal er toekomstig onderzocht moeten worden of deze gewassen goede nutritionele waarden bezitten, smaakvol geconsumeerd worden door runderen en uiteraard economisch rendabel zijn voor de boer. 

Bibliografie

Abongwa, M., Martin, R.J., Robertson, A.P., 2017. A brief review on the mode of action of antinematodal drugs. Acta veterinaria 67, 137-152. 

Addiss, D.G., Mathews, H.M., Stewart, J.M., Wahlquist, S.P., Williams, R.M., Finton, R.J., Spencer, H.C., Juranek, D.D., 1991. Evaluation of a commercially available enzyme-linked immunosorbent assay for Giardia lamblia antigen in stool. Journal of Clinical Microbiology 29, 1137–1142. 

Adeyemo, F.E., Singh, G., Reddy, P., Stenström, T.A., 2018. Methods for the detection of Cryptosporidium and Giardia: From microscopy to nucleic acid based tools in clinical and environmental regimes. Acta Trop, doi:10.1016. 

Agneessens, J., Claerebout, E., Dorny, P., Borgsteede, F.H.M., Vercruysse, J., 2000. Nematode parasitism in adult dairy cows in Belgium. Veterinary Parasitology 90, 83-92. 

Aloisio, F., Filippini, G., Antenucci, P., Lepri, E., Pezzotti, G., Caccio, S.M., Pozio, E., 2006. Severe weight loss in lambs infected with Giardia duodenalis assemblage B. Veterinary Parasitology 142, 154-158. 

Amar, C.F.L., Dear, P.H., Pedraza-Diaz, S., Looker, N., Linnane, E., McLauchlin, J., 2002. Sensitive PCR-restriction fragment length polymorphism assay for detection and genotyping of Giardia duodenalis in human feces. Journal of Clinical Microbiology 40, 446–452. 

Ansell, B.R.E., Baker, L., Emery, S.J., McConville, M.J., Svärd, S.G., Gasser, R.B., Jex, A.R., 2017. Transcriptomics Indicates Active and Passive Metronidazole Resistance Mechanisms in Three Seminal Giardia Lines. Front Microbiology 8, 398. 

Armour, J., Duncan, M., 1987. Arrested Larval Development in Cattle Nematodes. Parasitology Today 3, 171-176. 

Armour, J., 1989. The influence of host immunity on the epidemiology of trichostrongyle infections in cattle. Veterinary Parasitology 32, 5–19. 

Arroyo-Lopez, C., Manolaraki, F., Saratsis, A., Stefanakis, A., Skampardonis, V., Voutzourakis, N., Hoste, H., Sotiraki, S., 2014. Anthelmintic effect of carob pods and sainfoin hay when fed to lambs after experimental trickle infections with Haemonchus contortus and Trichostrongylus colubriformis. Parasite, 21, 71. 

Athanasiadou, S., Kyriazakis, I., Jackson, F., Coop, R.L., 2001. Direct anthelmintic effects of condensed tannins towards different gastrointestinal nematodes of sheep: in vitro and in vivo studies. Veterinary Parasitology 99, 205-219. 

Athanasiadou, S., Tzamaloukas, O., Kyriazakis, I., Jackson, F., Coop, R.L., 2005. Testing for direct anthelmintic effects of bioactive forages against Trichostrongylus colubriformis in grazing sheep. Veterinary Parasitology 127, 233-243. 

Avramenko, R.W., Redman, E.M., Lewis, R., Yazwinski, T.A., Wasmuth, J.D., Gilleard, J.S., 2015. Exploring the gastrointestinal “Nemabiome”: Deep amplicon sequencing to quantify the species composition of parasitic nematode communities. PLoS ONE 10, doi: 10.1371. 

Bahuaud, D., Martinez-Ortiz de Montellano, C., Chauveau, S., Prevot, F., Torres-Acosta, F., Fouraste, I., Hoste, H., 2006. Effects of four tanniferous plant extracts on the in vitro exsheathment of third-stage larvae of parasitic nematodes. Parasitology 132, 545-554. 44 

 

Barbosa, E., Calzada, F., Campos, R., 2007. In vivo antigiardial activity of three flavonoids isolated of some medicinal plants used in Mexican traditional medicine for the treatment of diarrhea. Journal of ethnopharmacology 109, 552-554. 

Becher, K.A., Robertson, I.D., Fraser, D.M., Palmer, D.G., Thompson, R.C.A., 2004. Molecular epidemiology of Giardia and Cryptosporidium infections in dairy calves originating from three sources in Western Australia. Veterinary Parasitology 123, 1–9. 

Bellet, C., Green, M.J., Vickers, M., Forbes, A., Berry, E., Kaler, J., 2016. Ostertagia spp., rumen fluke and liver fluke single- and poly-infections in cattle: An abattoir study of prevalence and production impacts in England and Wales. Preventive Veterinary Medicine 132, 98-106. 

Bénéré, E., Da Luz, R.A.I., Vermeersch, M., Cos, P., Maes, L., 2007. A new quantitative in vitro microculture method for Giardia duodenalis trophozoites. Journal of Microbiological Methods 71, 101-106. 

Bennema, S., Vercruysse, J., Claerebout, E., Schnieder, T., Strube, C., Ducheyne, E., Hendrickx, G., Charlier, J., 2009. The use of bulk-tank milk ELISAs to assess the spatial distribution of Fasciola hepatica, Ostertagia ostertagi and Dictyocaulus viviparus in dairy cattle in Flanders (Belgium). Veterinary Parasitology 165, 51-57. 

Bennema, S.C., Vercruysse, J., Morgan, E., Stafford, K., Höglund, J., Demeler, J., von Samson-Himmelstjerna, G., Charlier, J., 2010. Epidemiology and risk factors for exposure to gastrointestinal nematodes in dairy herds in northwestern Europe. Veterinary Parasitology 173, 247-254. 

Berrilli, F., Di Cave, D., De Liberato, C., Franco, A., Scaramozzino, P., Orecchia, P., 2004. Genotype characterisation of Giardia duodenalis isolates from domestic and farm animals by SSU-rRNA gene sequencing. Veterinary Parasitology 122, 193–199. 

Besier, R.B., Love, S.C.J., 2003. Anthelmintic resistance in sheep nematodes in Australia: the need for new approaches. Australian Journal of Experimental Agriculture 43, 1383-1391. 

Besier, R.B., 2012. Refugia-based strategies for sustainable worm control: Factors affecting the acceptability to sheep and goat owners. Veterinary Parasitology 186, 2-9. 

Besier, R.B., Kahn, L.P., Sargison, N.D., Van Wyk, J.A., 2016. Chapter Six – Diagnosis, Treatment and Management of Haemonchus contortus in Small Ruminants. Advances in Parasitology 93, 181-238. 

Birky, C.W., 2010. Giardia sex? Yes, but how and how much? Trends in Parasitology 26, 70-74. 

Bishop, S.C., Morris, C.A., 2007. Genetic of disease resistance in sheep and goats. Small Ruminant Research 70, 48–59. 

Blanchard, J.L., Gallina, A.M., Wescott, R.B., 1986. Pathological changes in lambs with Ostertagia circumcincta infections associated with decreased infectivity of Haemonchus contortus. American Journal of Veterinary Research 47, 309-314. 

Boone, J.H., Wilkins, T.D., Nash, T.E., Brandon, J.E., Macias, E.A., Jerris, R.C., Lyerly, D.M., 1999. TechLab and Alexon Giardia enzyme-linked immunosorbent assay kits detect cyst wall protein 1. Journal of Clinical Microbiology 37, 611–614. 

Borgsteede, F.H., 1979. The activity of albendazole against adult and larval gastrointestinal nematodes in naturally infected calves in the Netherlands. Tijdschrift voor diergeneeskunde 104, 181-188. 45 

 

Bosco, A., Rinaldi, L., Maurelli, M.P., Musella, V., Coles, G.C., Cringoli, G., 2014. The comparison of FLOTAC, FECPAK and McMaster techniques for nematode egg counts in cattle. Acta Parasitologica 59, 625-628. 

Burke, J.M., Miller, J.E., Olcott, D.D., Olcott, B.M., Terrill, T.H., 2004. Effect of copper oxide wire particles dosage and feed supplement level on Haemonchus contortus infection in lambs. Veterinary Parasitology 123, 235-243. 

Burke, J.M., Miller, J.E., Terrill, T.H., 2007. Use of copper oxide wire particles (COWP) to control barber pole worm in lambs and kids. www.scsprc.org. 

Cacciò, S.M., Thompson, R.C.A., McLauchlin, J., Smith, H.V., 2005. Unravelling Cryptosporidium and Giardia epidemiology. Trends in Parasitology 21, 430-437. 

Calzada, F., Cedillo-Rivera, R., Bye, R., Mata, R., 2001. Geranins C and D, additional new antiprotozoal A-type proanthocyanidins from Geranium niveum. Planta medica 67, 677-680. 

Calzada, F., Cerda-García-Rojas, C.M., Meckes, M., Cedillo-Rivera, R., Bye, R., Mata, R., 1999. Geranins A and B, new antiprotozoal A-type proanthocyanidins from Geranium niveum. Journal of Natural Products 62, 705-709. 

Calzada, F., Cervantes-Martínez, J.A., Yépez-Mulia, L., 2005. In vitro antiprotozoal activity from the roots of Geranium mexicanum and its constituents on Entamoeba histolytica and Giardia lamblia. Journal of ethnopharmacology 98, 191-193. 

Campbell, N.J., Hall, C.A., Kelly, J.D., Martin, I.C., 1978. The anthelmintic efficacy of non-benzimidazole anthelmintics against benzimidazole resistant strains of Haemonchus contortus and Trichostrongylus colubriformis in sheep. Australian Veterinary Journal 54, 23-25. 

Castro-Hermida, J.A., Delafosse, A., Pors, I., Ares-Mazás, E., Chartier, C., 2005. Giardia duodenalis and Cryptosporidium parvum infections in adult goats and their implications for neonatal kids. Veterinary Record 157, 623–627. 

Cedillo-Rivera, R., Chávez, B., González-Robles, A., Tapia, A., Yépez-Mulia, L., 2002. In vitro effect of nitazoxanide against Entamoeba histolytica, Giardia intestinalis and Trichomonas vaginalis trophozoites. The Journal of eukaryotic microbiology 49, 201-208. 

Charlier, J., Camuset, P., Claerebout, E., Courtay, B., Vercruysse, J., 2007a. A longitudinal survey of anti-Ostertagia ostertagi antibody levels in individual and bulk tank milk in two dairy herds in Normandy. Research in Veterinary Science 83, 194-197. 

Charlier, J., Duchateau, L., Claerebout, E., Vercruysse, J., 2007b. Predicting milk-production responses after an autumn treatment of pastured dairy herds with eprinomectin. Veterinary Parasitology 143, 322-328. 

Charlier, J., Vercruysse, J., Smith, J., Vanderstichel, R., Stryhn, H., Claerebout, E., Dohoo, I., 2010a. Evaluation of anti-Ostertagia ostertagi antibodies in individual milk samples as decision parameter for selective anthelmintic treatment in dairy cows. Preventive Veterinary Medicine 93, 147-152. 

Charlier, J., Demeler, J., Höglund, J., von Samson-Himmelstjerna, G., Dorny, P., Vercruysse, J., 2010b. Ostertagia ostertagi in first-season grazing cattle in Belgium, Germany and Sweden: General levels of infection and related management practices. Veterinary Parasitology 171, 91-98. 

Charlier, J., Morgan, E.R., Rinaldi, L., van Dijk, J., Demeler, J., Hoglund, J., Hertzberg, H., Van Ranst, B., Hendrickx, G., Vercruysse, J., Kenyon, F., 2014. Practices to optimise gastrointestinal nematode 46 

 

control on sheep, goat and cattle farms in Europe using targeted (selective) treatments. Veterinary Record 175, 250–255. 

Charlier, J., Velde, F.V., van der Voort, M., Van Meensel, J., Lauwers, L., Cauberghe, V., Vercruysse, J., Claerebout, E., 2015. ECONOHEALTH: Placing helminth infections of livestock in an economic and social context. Veterinary Parasitology 212, 62-67. 

Charlier, J., Ghebretinsae, A.H., Levecke, B., Ducheyne, E., Claerebout, E., Vercruysse, J., 2016. Climate-driven longitudinal trends in pasture-borne helminth infections of dairy cattle. International Journal for Parasitology 46, 881-888. 

Charlier, J., Thamsborg, S.M., Bartley, D.J., Skuce, P.J., Kenyon, F., Geurden, T., Hoste, H., Williams, A.R., Sotiraki, S., Höglund, J., Chartier, C., Geldhof, P., van Dijk, J., Rinaldi, L., Morgan, E.R., von Samson-Himmelstjerna, G., Vercruysse, J., Claerebout, E., 2017. Mind the gaps in research on the control of gastrointestinal nematodes of farmed ruminants and pigs. Transboundary and emerging diseases, doi: 10.1111 

Chartier, C., Etter, E., Hoste, H., Pors, I., Koch, C., Dellac, B., 2000. Efficacy of copper oxide needles for the control of nematode parasites in dairy goats. Veterinary Research Communications 24, 389-399. 

Chartier, C., Pors, I., 2002. Effect of the nematophagous fungus, Duddingtonia flagrans, on the larval development of goat parasitic nematodes: a plot study. Veterinary Research 34, 221-230. 

Claerebout, E., Agneessens, J., Shaw, D.J., Vercruysse, J., 1999. Larval migration inhibition activity in abomasal mucus and serum from calves infected with Ostertagia ostertagi. Research in Veterinary Science 66, 253-257. 

Coles, G.C., Jackson, F., Pomroy, W.E., Prichard, R.K., von Samson-Himmelstjerna, G., Silvestre, A., Taylor, M.A., Vercruysse, J., 2006. The detection of anthelmintic resistance in nematodes of veterinary importance. Veterinary Parasitology 136, 167–185. 

Coop, R.L., Graham, R.B., Jackson, F., Wright, S.E., Angus, K.W., 1985. Effect of experimental Ostertagia circumcincta infection on the performance of grazing lambs. Research in Veterinary Science 38, 282-287. 

Coop, R.L., Kyriazakis, I., 1999. Nutrition-parasite interaction. Veterinary Parasitology 84, 187–204. 

Coop, R.L., Kyriazakis, I., 2001. Influence of host nutrition on the development and consequences of nematode parasitism in ruminants. Trends in Parasitology 17, 325-330. 

Cooper, K.M., Whelan, M., Kennedy, D.G., Trigueros, G., Cannavan, A., Boon, P.E., Wapperom, D., Danaher, M., 2012. Anthelmintic drug residues in beef: UPLC-MS/MS method validation, European retail beef survey, and associated exposure and risk assessments. Food additives & contaminants. Part A, Chemistry, analysis, control, exposure & risk assessment 29, 746-760. 

Corwin, R.M., 1997. Economics of gastrointestinal parasitism of cattle. Veterinary Parasitology 72, 451-460. 

Cotton, J.A., Beatty, J.K., Buret, A.G., 2011. Host parasite interactions and pathophysiology in Giardia infections. International Journal for Parasitology 41, 925–933. 

Cotter, J.L., Van Burgel, A., Besier, R.B., 2015. Anthelmintic resistance in nematodes of beef cattle in south-west Western Australia. Veterinary Parasitology 207, 276-284. 

Cringoli, G., 2004. Coprological diagnosis: what’s new? Parassitologia 46, 137-139. 47 

 

Cringoli, G., Veneziano, V., Rinaldi, L., Sauve, C., Rubino, R., Fedele, V., Cabaret, J., 2007. Resistance of trichostrongyles to benzimidazoles in Italy: a first report in a goat farm with multiple and repeated introductions. Parasitology Research 101, 577-581. 

Cringoli, G., Rinaldi, L., Maurelli, M.P., Utzinger, J., 2010. FLOTAC: New multivalent techniques for qualitative and quantitative copromicroscopic diagnosis of parasites in animals and humans. Nature Protocols 5, 503–515. 

Cringoli, G., Rinaldi, L., Albonico, M., Bergquist, R., Utzinger, J., 2013. Geospatial (s)tools: Integration of advanced epidemiological sampling and novel diagnostics. Geospat Health 7, 399–404. 

Danaher, M., Shanahan, C., Butler, F., Evans, R., O’Sullivan, D., Glynn, D., Camon, T., Lawlor, P., O’Keeffe, M., 2016. Risk-based approach to developing a national residue sampling plan for testing under European Union regulation for veterinary medicinal products and coccidiostat feed additives in domestic animal production. In: Food Additives & Contaminants: Part A, 1155-1165. 

Daniels, C.W., Belosevic, M., 1994. Serum antibody responses by male and female C57/BI/6 mice infected with Giardia muris. Clin Exp Immunol. 97, 424-429. 

de Albuquerque, A.C.A., Bassetto, C.C., de Almeida, F.A., Amarante, A.F.T., 2017. Development of Haemonchus contortus resistance in sheep under suppressive or targeted selective treatment with monepantel. Veterinary Parasitology 246, 112-117. 

De Graef, J., Sarre, C., Milis, B.J., Mahabir, S., Casaert, S., De Wilde, N., Van Weyenberg, M., Geldhof, P., Marchiondo, A., Vercruysse, J., Meeus, P., Claerebout, E., 2012. Assessing resistance against macrocyclic lactones in gastro-intestinal nematodes in cattle using the faecal egg count reduction test and the controlled efficacy test. Veterinary Parasitology 189, 378-382. 

Demeler, J., Van Zeveren, A.M.J., Kleinschmidt, N., Vercruysse, J., Höglund, J., Koopmann, R., Cabaret, J., Claerebout, E., Areskog, M., von Samson-Himmelstjerna, G., 2009. Monitoring the efficacy of ivermectin and albendazole against gastro intestinal nematodes of cattle in Northern Europe. Veterinary Parasitology 160, 109-115. 

Demeler, J., Küttler, U., von Samson-Himmelstjerna, G., 2010a. Adaptation and evaluation of three different in vitro tests for the detection of resistance to anthelmintics in gastro intestinal nematodes of cattle. Veterinary Parasitology 170, 61-70. 

Demeler, J., Küttler, U., El-Abdellati, A., Stafford, K., Rydzik, A., Varady, M., Kenyon, F., Coles, G., Höglund, J., Jackson, F., Vercruysse, J., von Samson-Himmelstjerna, G., 2010b. Standardization of the larval migration inhibition test for the detection of resistance to ivermectin in gastro intestinal nematodes of ruminants. Veterinary Parasitology 174, 58-64. 

Demeler, J., Kleinschmidt, N., Küttler, U., Koopmann, R., von Samson-Himmelstjerna, G., 2012. Evaluation of the Egg Hatch Assay and the Larval Migration Inhibition Assay to detect anthelmintic resistance in cattle parasitic nematodes on farms. Parasitology International 61, 614-618. 

Desrues, O., Peña-Espinoza, M., Hansen, T.V., Enemark, H.L., Thamsborg, S.M., 2016. Anti-parasitic activity of pelleted sainfoin (Onobrychis viciifolia) against Ostertagia ostertagi and Cooperia oncophora in calves. Parasites & Vectors 9, 329. 

Dorny, P., Vercruysse, J., 1998. Evaluation of a micro method for the routine determination of serum pepsinogen in cattle. Research in Veterinary Science 65, 259-262. 48 

 

Dorny, P., Shawa, D.J, Vercruysse, J., 1999. The determination at housing of exposure to gastrointestinal nematode infections in first-grazing season calves. Veterinary Parasitology 80, 325-340. 

Dreesen, L., Rinaldi, M., Chiers, K., Li, R., Geurden, T., Van den Broeck, W., Goddeeris, B., Vercruysse, J., Claerebout, E., Geldhof, P., 2012. Microarray Analysis of the Intestinal Host Response in Giardia duodenalis Assemblage E Infected Calves. PLoS One, doi: 10.1371. 

Edlind, D., 1989. Susceptibility of Giardia lamblia to Aminoglycoside Protein Synthesis Inhibitors: Correlation with rRNA Structure. Antimicrobial Agents and Chemotherapy 33, 484-488. 

Edlind, T.D., Hang, T.L., Chakraborty, P.R., 1990. Activity of the anthelmintic benzimidazoles against Giardia lamblia in vitro. The Journal of Infectious Diseases 162, 1408–1411. 

Edmonds, M.D., Johnson, E.G., Edmonds, J.D., 2010. Anthelmintic resistance of Ostertagia ostertagi and Cooperia oncophora to macrocyclic lactones in cattle from the western United States. Veterinary Parasitology 170, 224-229. 

Emery, D.L., Hunt, P.W., Le Jambre, L.F., 2016. Haemonchus contortus: the then and now, and where to from here? International Journal for Parasitology 46, 755-769. 

Epe, C., Holst, C., Koopmann, R., Schnieder, T., Larsen, M., von Samson-Himmelstjerna, G., 2009. Experiences with Duddingtonia flagrans administration to parasitized small ruminants. Veterinary Parasitology 159, 86-90. 

Uehlinger, F.D., O'Handley, R.M., Greenwood, S.J., Guselle, N.J., Gabor, L.J., Van Velsen, C.M., Steuart, R.F., Barkema, H.W., 2007. Efficacy of vaccination in preventing giardiasis in calves. Veterinary Parasitology 146, 182-188. 

Eysker, M., van der Aar, W.M., Boersema, J.H., Githiori, J.B., Kooyman, F.N., 1998. The effect of repeated moves to clean pasture on the build up of gastrointestinal nematode infections in calves. Veterinary Parasitology 76, 81–94. 

Eysker, M., Ploeger, H.W., 2000. Value of present diagnostic methods for gastrointestinal nematode infections in ruminants. Parasitology 120, 109–119. 

Faedo, M., Larsen, M., Thamsborg, S., 2000. Effect of different times of administration of the nematophagous fungus Duddingtonia flagrans on the transmission of ovine parasitic nematodes on pasture - a plot study. Veterinary Parasitology 94, 55-65. 

Fernández, A.S., Larsen, M., Henningsen, E., Nansen, P., Grønvold, J., Bjørn, H., Wolstrup, J., 1999. Effect of Duddingtonia flagrans against Ostertagia ostertagi in cattle grazing at different stocking rates. Parasitology 199, 105-111. 

Forbes, A.B., Huckle, C.A., Gibb, M.J., 2004. Impact of eprinomectin on grazing behaviour and performance in dairy cattle with sub-clinical gastrointestinal nematode infections under continuous stocking management. Veterinary Parasitology 125, 353–364. 

Forbes, A.B., Vercruysse, J., Charlier, J., 2008. A survey of the exposure to Ostertagia ostertagi in dairy cow herds in Europe through the measurement of antibodies in milk samples from the bulk tank. Veterinary Parasitology 157, 100–107. 

Forbes, A.B., Warren, M., Upjohn, M., Jackson, B., Jones, J., Charlier, J., Fox, M.T., 2009. Associations between blood gastrin, ghrelin, leptin, pepsinogen and Ostertagia ostertagi antibody concentrations and voluntary feed intake in calves exposed to a trickle infection with O. ostertagi. Veterinary Parasitology 162, 295–305. 49 

 

Garcia, L.S., Shimizu, R.Y., Novak, S., Carroll, M., Chan, F., 2003. Commercial assay for detection of Giardia lamblia and Cryptosporidium parvum antigens in human fecal specimens by rapid solid-phase qualitative immunochromatography. Journal of Clinical Microbiology 41, 209–212. 

Geurden, T., Claerebout, E., Vercruysse, J., Berkvens, D., 2004. Estimation of diagnostic test characteristics and prevalence of Giardia duodenalis in dairy calves in Belgium using a Bayesian approach. International Journal for Parasitology 34, 1121–1127. 

Geurden, T., Claerebout, E., Dursin, L., Deflandre, A., Bernay, F., Kaltsatos, V., Vercruysse, J., 2006a. The efficacy of an oral treatment with paromomycin against an experimental infection with Giardia in calves. Veterinary Parasitology 135, 241–247. 

Geurden, T., Vercruysse, J., Claerebout, E., 2006b. Field testing of a fenbendazole treatment combined with hygienic and management measures against a natural Giardia infection in calves. Veterinary Parasitology 142, 367-371. 

Geurden, T., Geldhof, P., Levecke, B., Martens, C., Berkvens, D., Casaerta, S., Vercruysse, J., Claerebout, E., 2008a. Mixed Giardia duodenalis assemblage A and E infections in calves. International Journal for Parasitology 38, 259-264. 

Geurden, T., Thomas P., Casaert, S., Vercruysse, J., Claerebout, E., 2008b. Prevalence and molecular characterisation of Cryptosporidium and Giardia in lambs and goat kids in Belgium. Veterinary Parasitology 155, 142-145. 

Geurden, T., Vercruysse, J., Claerebout, E., 2010a. Is Giardia a significant pathogen in production animals? Experimental Parasitology 124, 98-106. 

Geurden, T., Vandenhoute, E., Pohle, H., Casaert, S., De Wilde, N., Vercruysse, J., Claerebout, E., 2010b. The effect of a fenbendazole treatment on cyst excretion and weight gain in calves experimentally infected with Giardia duodenalis. Veterinary Parasitology 169, 18-23. 

Geurden, T., Levecke, B., Pohle, H., De Wilde, N., Vercruysse, J., Claerebout, E., 2010c. A Bayesian evaluation of two dip-stick assays for the on-site diagnosis of infection in calves suspected of clinical giardiasis. Veterinary Parasitology 172, 337-340. 

Geurden, T., Pohle, H., Sarre, C., Dreesen, L., Vercruysse, J., Claerebout, E., 2011. The efficacy of a treatment with fenbendazole against an experimental Giardia duodenalis infection in lambs. Small Ruminant Research 96, 211-215. 

Geurden, T., Vanderstichel, R., Pohle, H., Ehsan, A., von Samson-Himmelstjerna, G., Morgan, E.R., Camuset, P., Capelli, G., .Vercruysse, J., Claerebout, E., 2012. A multicentre prevalence study in Europe on Giardia duodenalis in calves, with molecular identification and risk factor analysis. Veterinary Parasitology 190, 383-390. 

Geurden, T., Slootmans, N., Glover, M., Bartram, D.J., 2014. Production benefit of treatment with dual active oral formulation of derquantel-abamectin in slaughter lambs. Veterinary Parasitology 205, 405-407. 

Geurden, T., Chartier, C., Fanke, J., Frangipane di Regalbono, A., Traversa, D., von Samson-Himmelstjerna, G. Demeler, J., Bindu Vanimisetti, H., Bartram, D.J., Denwood, M.J., 2015. Anthelmintic resistance to ivermectin and moxidectin in gastrointestinal nematodes of cattle in Europe. International Journal for Parasitology: Drugs and Drug Resistance 5, 163-171. 50 

 

Gilleard, J.S., 2006. Understanding anthelmintic resistance: The need for genomics and genetics. International Journal for Parasitology 36, 1227-1239. 

Gillis, J. C., Wiseman, L.R., 1996. Secnidazole. A review of its anti-microbial activity, pharmacokinetic properties and therapeutic use in the management of protozoal infections and bacterial vaginosis. Drugs 51, 621–638. 

Godber, O.F., Phythian, C.J., Bosco, A., Ianniello, D., Coles, G., Rinaldi, L., Cringoli, G., 2015. A comparison of the FECPAK and Mini-FLOTAC faecal egg counting techniques. Veterinary Parasitology 207, 342-345. 

González-Hernández, A., Borloo, J., Peelaers, I., Casaert, S., Leclercq, G., Claerebout, E., Geldhof, P., 2018. Comparative analysis of the immune responses induced by native versus recombinant versions of the ASP-based vaccine against the bovine intestinal parasite Cooperia oncophora. International Journal for Parasitology 48, 41-49. 

Gordts, B., Hemelhof, W., Asselman, C., Butzler, J., 1985. In Vitro Susceptibilities of 25 Giardia lamblia Isolates of Human Origin to Six Commonly Used Antiprotozoal Agents. Antimicrobial Agents and Chemotherapy 28, 378-380. 

Greer, A.W., 2008a. Trade-offs and benefits: Implications of promoting a strong immunity to gastrointestinal parasites in sheep. Parasite Immunology 30, 123–132. 

Greer, A.W., Huntley, J.F., Mackellar, A., McAnulty, R.W., Jay, N.P., Green, R.S., Stankiewicz, M., Sykes, A.R., 2008b. The effect of corticosteroid treatment on local immune responses, intake and performance in lambs infected with Teladorsagia circumcincta. International Journal for Parasitology 38, 1717–1728. 

Grit, G.H., Bénéré, E., Ehsan, A., De Wilde, N., Claerebout, E., Vercruysse, J., Maes, L., Geurden, T., 2012. Giardia duodenalis cyst survival in cattle slurry. Veterinary Parasitology 184, 330-334. 

Grit, G.H., Van Coppernolle, S., Devriendt, B., Geurden, T., Dreesen, L., Hope, J., Vercruysse, J., Cox, E., Geldhof, P., Claerebout, E., 2014. Evaluation of cellular and humoral systemic immune response against Giardia duodenalis infection in cattle. Veterinary Parasitology 202, 145-155. 

Heckendorn, F., Häring, D.A., Maurer, V., Zinsstag, J., Langhans, W., Hertzberg, H., 2006. Effect of sainfoin (Onobrychis viciifolia) silage and hay on established populations of Haemonchus contortus and Cooperia curticei in lambs. Veterinary Parasitology 142, 293-300. 

Heyworth, M.F., 2016. Giardia duodenalis genetic assemblages and hosts. Parasite 23, 13. 

Höglund, J., Svensson, C., Hessle, A., 2001. A field survey on the status of internal parasites in calves on organic dairy farms in southwestern Sweden. Veterinary Parasitology 99, 113–128. 

Hosking, B.C., Griffiths, T.M., Woodgate, R.G., Besier, R.B., Le Feuvre, A.S., Nilon, P., Trengove, C., Vankoff, K.J., Kaye-Smith, B.G., Seewald, W., 2009. Clinical field study to evaluate the efficacy and safety of the amino-acetonitrile derivative, monepantel, compared with registered anthelmintics against gastrointestinal nematodes of sheep in Australia. Australian Veterinary Journal 87, 455-462. 

Hoste, H., Jackson, F., Athanasiadou,S., Thamsborg, S.M., Hoskin, S.O., 2006. The effects of tannin-rich plants on parasitic nematodes in ruminants. Trends in Parasitology 22, 253–261. 

Hoste, H., Martinez-Ortiz-De-Montellano, C., Manolaraki, F., Brunet, S., Ojeda-Robertos, N., Fourquaux, I, Torres-Acosta, J.F.J., Sandoval-Castro, C.A., 2012. Direct and indirect effects of bioactive 51 

 

tannin-rich tropical and temperate legumes against nematode infections. Veterinary Parasitology 186, 18-27. 

Hoste, H., Torres-Acosta, J.F.J., 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, 5-17. 

Houdijk, J.G., Kyriazakis, I., Coop, R.L., Jackson, F., 2001. The expression of immunity to Teladorsagia circumcincta in ewes and its relationship to protein nutrition depend on body protein reserves. Parasitology 122, 661-672. 

Hounzangbe-Adote, M.S., Paolini, V., Fouraste, I., Moutairou, K., Hoste, H., 2005. In vitro effects of four tropical plants on three life-cycle stages of the parasitic nematode, Haemonchus contortus. Research in Veterinary Science 78, 155-160. 

Jacobs, D., Fox, M., Gibbons, L., Hermosilla, C., 2016. Nematoda. In: Principles of Veterinary Parasitology, First Edn. Wiley Blackwell, West Sussex, UK. 

Jacquiet, P., Barillet, F., Bouix, J., François, D., Moreno, C., Terefe, G., 2009. Genetic resistance of sheep to gastrointestinal strongyles. Bulletin De l'Academie Veterinaire De France 162, 39–46. 

James, C.E., Hudson, A.L., Davey, M.W., 2009. Drug resistance mechanisms in helminths: is it survival of the fittest? Trends in parasitology 25, 328-335. 

Johansen, M.V., 1989. An evaluation of techniques used for the detection of anthelmintic resistance in nematode parasites of domestic livestock. Veterinary Research Communications 13, 455-466. 

Juhnke, J., Miller, J., Hall, J.O., Provenza, F.D., Villalba, J.J., 2012. Preference for condensed tannins by sheep in response to challenge infection with Haemonchus contortus. Veterinary Parasitology 188, 104-114. 

Kaminsky, R., Gaubry, N., Schorderet Weber, S., Skripsky, T., Bouvier, J., Wenger, A., Schroeder, F., Desaules, Y., Hotz, R., Goebel, T., Hosking, B.C., Pautrat, F., Wieland-Berghausen, S., Ducray, P., 2008. Identification of the amino-acetonitrile derivative monepantel (AAD 1566) as a new anthelmintic drug development candidate. Parasitology research 103, 931-939. 

Keane et al., 2014. High level of treatment failure with commonly used anthelmintics on Irish sheep farms. Irish Veterinary Journal 67, 16. 

Keister, D.B., Axenic culture of Giardia lamblia in TYI-S-33 medium supplemented with bile. Transactions of the Royal Society of Tropical Medicine and Hygiene 77, 487-488. 

Kenyon, F., Sargison, N.D., Skuce, P.J., Jackson, F., 2009. Sheep helminth parasitic disease in south eastern Scotland arising as a possible consequence of climate change. Veterinary Parasitology 163, 293-297. 

Kenyon, F., Jackson, F., 2012. Targeted flock/herd and individual ruminant treatment approaches. Veterinary Parasitology 186, 10-17. 

Klesius, P.H., 1988. Immunity to Ostertagia ostertagi. Veterinary Parasitology 27, 159–167. 

Koudela, B., Vitovec, J., 1998. Experimental giardiosis in goat kids. Veterinary Parasitology 74, 9–18. 52 

 

Kidane, A., Houdijk, J.G., Tolkamp, B.J., Athanasiadou, S., Kyriazakis, I., 2009. Consequences of infection pressure and protein nutrition on periparturient resistance to Teladorsagia circumcincta and performance in ewes. Veterinary Parasitology 165, 78-87. 

Kidane, A., Koudijk, J.G., Athanasiadou, S., Tolkamp, B.J., Kyriazakis, I., 2010. Effects of maternal protein nutrition and subsequent grazing on chicory (Cichorium intybus) on parasitism and performance of lambs. Journal of animal science 88, 1513-1521. 

Lalle, M., Pozio, E., Capelli, G., Bruschi, F., Crotti, D., Cacciò, S.M., 2005. Genetic heterogeneity at the β-giardin locus among human and animal isolates of Giardia duodenalis and identification of potentially zoonotic subgenotypes. International Journal for Parasitology 35, 207–213. 

Lamb, J., Elliott, T., Chambers, M., Chick, B., 2017. Broad spectrum anthelmintic resistance of Haemonchus contortus in Northern NSW of Australia. Veterinary Parasitology 241, 48-51. 

Lange, K.C., Olcott, D.D., Miller, J.E., Mosjidis, J.A., Terrill, T.H., Burke, J.M., Kearney, M.T., 2006. Effect of sericea lespedeza (Lespedeza cuneata) fed as hay, on natural and experimental Haemonchus contortus infections in lambs. Veterinary Parasitology 141, 273-278. 

Leathwick, D.M., Ganesh, S., Waghorn, T.S., 2015. Evidence for reversion towards anthelmintic susceptibility in Teladorsagia circumcincta in response to resistance management programmes. International Journal for Parasitology: Drugs and Drug Resistance 5, 9–15. 

Leitsch, D., Burgess, A.G., Dunn, L.A., Krauer, K.G., Tan, K., Duchene, M., Upcroft, P., Eckmann, L., Upcroft, J.A., 2011. Pyruvate:ferredoxin oxidoreductase and thioredoxin reductase are involved in 5-nitroimidazole activation while flavin metabolism is linked to 5-nitroimidazole resistance in Giardia lamblia. Journal of Antimicrobial Chemotherapy 66, 1756 –1765. 

Lespine, A., Alvinerie, M., Vercruysse, J., Prichard, R.K., Geldhof, P., 2008. ABC transporter modulation: a strategy to enhance the activity of macrocyclic lactone anthelmintics. Trends in Parasitology 24, 293-298. 

Levecke, B., De Wilde, N., Vandenhoute, E., Vercruysse, J., 2009. Field validity and feasibility of four techniques for the detection of Trichuris in simians: a model for monitoring drug efficacy in public health? PLoS Neglected Tropical Diseases 3, doi: 10.1371. 

Logsdon, J.M., 2008. Evolutionary genetics: sex happens in Giardia. Current Biology 18, 66-68. 

Martin, R.J., Verma, S., Choudhary, S., Kashyap, S., Abongwa, M., Zheng, F., Robertson, A.P., 2015. Anthelmintics: The best way to predict the future is to create it. Veterinary Parasitology 212, 18–24. 

Martínez-Valladares, M., Geurden, T., Bartram, D.J., Martínez-Pérez, J.M., Robles-Pérez, D., Bohórquez, A., Florez, E., Meana, A., Rojo-Vázquez, F.A., 2015. Resistance of gastrointestinal nematodes to the most commonly used anthelmintics in sheep, cattle and horses in Spain. Veterinary Parasitology 211, 228-233. 

McAllister, T.A., Annett, C.B., Cockwill, C.L., Olson, M.E., Wang, Y., Cheeke, P.R., 2001. Studies on the use of Yucca schidigera to control giardiosis. Veterinary Parasitology 97, 85-99. 

McRae, K.M., McEwan, J.C., Dodds, K.G., Gemmell, N.J., 2014. Signatures of selection in sheep bred for resistance or susceptibility to gastrointestinal nematodes. Genomics 15, 637. 

Meloni, B.P., Lymbery, A.J., Thompson, R.C., 1989. Characterization of Giardia isolates using a non-radiolabeled DNA probe, and correlation with the results of isoenzyme analysis. American Journal of Tropical Medicine and Hygiene 40, 629–637. 53 

 

Meloni, B.P., Thompson, R.C., Reynoldson, J.A., Seville, P., 1990. Albendazole: a more effective antigiardial agent in vitro than metronidazole or tinidazole. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 375–379. 

Mihi, B., Van Meulder, F., Rinaldi, M., Van Coppernolle, S., Chiers, K., Van den Broeck, W., Goddeeris, B., Vercruysse, J., Claerebout, E., Geldhof, P., 2013. Analysis of cell hyperplasia and parietal cell dysfunction induced by Ostertagia ostertagi infection. Veterinary Research 44, 121. 

Milhes, M., Guillerm, M., Robin, M., Eichstadt, M., Roy, C., Grisez, C., Prévot, F., Liénard, E., Bouhsira, E., Franc, M., Jacquiet, P., 2017. A real-time PCR approach to identify anthelmintic-resistant nematodes in sheep farms. Parasitology Research 166, 909-920. 

Molan, A.L., Waghorn, G.C., Min, B.M., McNabb, W.C., 2000. The effect of condensed tannins from seven herbages on Trichostrongylus colubriformis larval migration in vitro. Folia Parasitology 47, 39-44. 

Morgan, U.M., Reynoldson, J.A., Thompson, R.C., 1993. Activities of several benzimidazoles and tubulin inhibitors against Giardia spp. in vitro. Antimicrobial Agents and Chemotherapy 37, 328–331. 

Moron-Soto, M., Gutierrez, L., Sumano, H., Tapia, G., Alcala-Canto, Y., 2017. Efficacy of nitazoxanide to treat Giardia infections in dogs. Parasitology Vectors 10, 52. 

Nansen, P., Steffan, P., Monrad, J., Grønvold, J., Henriksen, S.A., 1990. Effects of separate and mixed grazing on trichostrongylosis in first and second-season grazing calves. Vet. Parasitol. 36, 265–276. 

Niezen, J.H., Charleston, W.A.G., 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, 229-24. 

Nisbet, A.J., McNeilly, T.N., Greer, A.W., Bartley, Y., Oliver, E.M., Smith, S., Palarea-Albaladejo, J., Matthews, J.B., 2016. Protection of ewes against Teladorsagia circumcincta infection in the periparturient period by vaccination with recombinant antigens. Veterinary Parasitology 228, 130-136. 

Novobilský, A., Mueller-Harvey, I., Thamsborg, S.M., 2011. Condensed tannins act against cattle nematodes. Veterinary Parasitology 182, 213-220. 

Nydam, D.V., Wade, S.E., Schaaf, S.L., Mohammed, H.O., 2001. Number of Cryptosporidium parvum oocysts or Giardia spp. cysts shed by dairy calves after natural infection. American Journal of Veterinary Research 62, 1612–1615. 

Oberhuber, G., Kastner, N., Stolte, M., 1997. Giardiasis: a histologic analysis of 567 cases. Scandinavian Journal of Gastroenterology 32, 48–51. 

O’Brien, J., Wilson, I., Orton, T., Pognan, F., 2000. Investigation of the Alamar Blue (resazurin) fluorescent dye for the assessment of mammalian cell cytotoxicity. European Journal of Biochemistry 267, 5421-5426. 

O’Handley, R.M., Olson, M.E., McAllister, T.A., Morck, D.W., Jelinski, M., Royan, G., Cheng, K.J., 1997. Efficacy of fenbendazole for treatment of giardiosis in calves. American Journal of Veterinary Research 58, 384–388. 

O’Handley, R.M., Cockwill, C., McAllister, T.A., Jelinski, M., Morck, D., Olson, M.E., 1999. Duration of naturally acquired giardiasis and cryptosporidiosis in dairy calves and their association with diarrhea. Journal of the American Veterinary Medical Association 214, 391-396. 54 

 

O’Handley, R.M., Cockwill, C., Jelinski, M., McAllister, T.A., Olson, M.E., 2000. Effects of repeat fenbendazole treatment in dairy calves with giardiasis on cyst excretion, clinical signs and production. Veterinary Parasitology 89, 209-218. 

O’Handley, R.M., Buret, A.G., McAllister, T.A., Jelinski, M., Olson, M.E., 2001. Giardiasis in dairy calves: effect of fenbendazole treatment on intestinal structure and function. International Journal for Parasitology 31, 73-79. 

O’Handley, R.M., Ceri, H., Anette, C., Olson, M.E., 2003. Passive immunity and serological immune response in dairy calves associated with natural Giardia duodenalis infections. Veterinary Parasitology 113, 89–98. 

Olson, M.E., McAllister, T.A., Deselliers, L., Morck, D.W., Cheng, K.J., Buret, A.G., Ceri, H., 1995. Effects of giardiasis on production in a domestic ruminant (lamb) model. American Journal for Veterinary Research 56, 1470–1474. 

Olson, M.E., Morck, D.W., Ceri, H., 1996. The efficacy of a Giardia lamblia vaccine in kittens. Canadian Journal of Veterinary Research 60, 249-256. 

Olson, M.E., Morck, D.W., Ceri, H., 1997. Preliminary data on the efficacy of a Giardia vaccine in puppies. Journal of Veterinary Research 38, 777-779. 

Olson, M.E., Goh, J., Phillips, M., Guselle, N., McAllister, T.A., 1999. Giardia cyst and Cryptosporidium oocyst survival in water, soil, and cattle faeces. Journal of Environmental Quality 28, 1991-1996. 

Ortiz, J.J., Ayoub, A., Gargala, G., Chegne, N.L., Favennec, L., 2001. Randomized clinical study of nitazoxanide compared to metronidazole in the treatment of symptomatic giardiasis in children from northern Peru. Alimentary Pharmacology & Therapeutics 15, 1409–1415. 

Paerewijck, O., Maertens, B., Dreesen, L., Van Meulder, F., Peelaers, I., Ratman, D., Li, R.W., De Bosscher, K., Geldhof, P., 2017. Interleukin-17 receptor A (IL-17RA) as a central regulator of the protective immune response against Giardia. Scientific Reports 7, 8520. 

Paolini, V., Frayssines, A., De-La-Farge, F., Dorchies, P., Hoste, H., 2003. Effects of condensed tannins on established populations and on incoming larvae of Trichostrongylus colubriformis and Teladorsagia circumcincta in goats. Veterinary Research 34, 331-339. 

Paolini, V., De-La-Farge, F., Prevot, F., Dorchies, P., Hoste, H., 2005. Effects of the repeated distribution of sainfoin hay on the resistance and the resilience of goats naturally infected with gastrointestinal nematodes. Veterinary Parasitology 127, 277-283. 

Pecková, R., Doležal, K., Sak, B., Květoňová, D., Kváč, M., Nurcahyo, W., Foitová, I., 2018. Effect of Piper betle on Giardia intestinalis infection in vivo. Experimental Parasitology 184, 39-45. 

Peña-Espinoza, M., Thamsborg, S.M., Desrues, O., Hansen, T.V.A., Enemark, H.L., 2016. Anthelmintic effects of forage chicory (Cichorium intybus) against gastrointestinal nematode parasites in experimentally infected cattle. Parasitology 143, 1279-1293. 

Peña-Espinoza, M., Williams, A.R., Thamsborg, S.M., Simonsen, H.T., Enemark, H.L., 2017. Anthelmintic effects of forage chicory (Cichorium intybus) against free-living and parasitic stages of Cooperia oncophora. Veterinary Parasitology 243, 204-207. 

Ploeger, H.J., 1989. Effect of anthelmintic treatment of dairy cattle on milk production related to some parameters estimating nematode infection. Veterinary Parasitology 34, 239–253. 55 

 

Ploeger, H.W., Borgsteede, F.H.M., Sol, J., Mirck, M.H., Huyben, M.W.C., Kooyman, F.N.J., Eysker, M., 2000. Cross-sectional serological survey on gastrointestinal and lung nematode infections in first and second-year replacement stock in The Netherlands: relation with management practices and use of anthelmintics. Veterinary Parasitology 90, 285–304. 

Ralston, B.J., Cockwill, C., Guselle, N., Van Herk, F.H., McAllister, T.A., Olson, M.E., 2003. Prevalence of Giardia and Cryptosporidium andersoni and their effect on performance in feedlot beef calves. Canadian Journal of Animal Science 83, 153–159. 

Ramírez-Restrepo, C.A., Pernthaner, A., Barry, T.N., López-Villalobos, N., Shaw, R. J., Pomroy, W. E., Hein, W.R., 2010. Characterization of immune responses against gastrointestinal nematodes in weaned lambs grazing willow fodder blocks. Animal Feed Science and Technology 155, 99–110. 

Ranjan, S.,, Wang, G.T., Hirschlein, C., Simkins, K.L., 2002. Selection for resistance to macrcyclic lactones by Haemonchus contortus in sheep. Veterinary Parasitology 103, 109-117. 

Read, C.M., Monis, P.T., Thompson, R.C.A., 2004. Discrimination of all genotypes of Giardia duodenalis at the glutamate dehydrogenase locus using PCR-RFLP. Genetics and Evolution 4, 125–130. 

Rehbein, S., Baggott, D.G., Johnson, E.G., Kunkle, B.N., Yazwinski, T.A., Yoon, S., Cramer, L.G., Soll, M.D., 2013. Nematode burdens of pastured cattle treated once at turnout with eprinomectin extended-release injection. Veterinary Parasitology 192, 321-331. 

Requena-Méndez, A., Goñi, P., Rubio, E., Pou, D., Fumadó, V., Lóbez, S., Aldasoro, E., Cabezos, J., Valls, M.E., Treviño, B., Martínez Montseny, A.F., Clavel, A., Gascon, J., Muñoz, J., 2017. The Use of Quinacrine in Nitroimidazole-resistant Giardia duodenalis: An Old Drug for an Emerging Problem. The Journal of Infectious Diseases 215, 946-953. 

Richards, L.S., Zimmerman, G.L., Hoberg, E.P., Schons, D.J., Dawley, S.W., 1987a. The anthelmintic efficacy of netobimin against naturally acquired gastrointestinal nematodes in sheep. Veterinary Parasitology 26, 87-94 

Richards, L.S., Zimmerman, Weber, D.W., Dawley, S.W., Nelson, M.J., Schons, D.J., 1987b. Anthelmintic efficacy of netobimin against naturally acquired gastrointestinal nematodes in yearling heifers. Veterinary Parasitology 26, 79-85. 

Rinaldi, L., Coles, G.C., Maurelli, M.P., Musella, V., Cringoli, G., 2011. Calibration and diagnostic accuracy of simple flotation, McMaster and FLOTAC for parasite egg counts in sheep. Veterinary Parasitology 177, 345-352. 

Rinaldi, M., Geldhof, P., 2012. Immunologically based control strategies for ostertagiosis in cattle: Where do we stand? Parasite Immunology 34, 254–264. 

Rinaldi et al., 2014. The maintenance of anthelmintic efficacy in sheep in a Mediterranean climate. Veterinary Parasitology 203, 139–143 

Roeber, F., Jex, A.R., Gasser, R.B., 2013. Next-Generation Molecular-Diagnostic Tools for Gastrointestinal Nematodes of Livestock, with an Emphasis on Small Ruminants: A Turning Point? Advances in Parasitology 83, 267-333. 

Roeber, F., Hassan, E.B., Skuce, P., Morrison, A., Claerebout, E., Casaert, S., Homer, D.R., Firestone, S., Stevenson, M., Smith, L., Larsen, J., 2017. An automated, multiplex-tandem PCR platform for the diagnosis of gastrointestinal nematode infections in cattle: An Australian-European validation study. Veterinary Parasitology 239, 62-75. 56 

 

Rossignol, J.F., Ayoub, A., Ayers, M.S., 2001. Treatment of diarrhea caused by Giardia intestinalis and Entamoeba histolytica/dispar: a double blind placebo controlled study of nitazoxanide. Journal of Infectious Diseases 184, 381–384. 

Rossignol, J.F., 2010. Cryptosporidium and Giardia: Treatment options and prospects for new drugs. Experimental Parasitology 124, 45-53. 

Ruest, N., Couture, Y., Faubert, G.M., Girard, C., 1997. Morphological changes in the jejunum of calves naturally infected with Giardia spp. and Cryptosporidium spp. Veterinary Parasitology 69, 177–186. 

Ruest, N., Faubert, G.M., Couture, Y., 1998. Prevalence and geographical distribution of Giardia spp. and Cryptosporidium spp. in dairy farms in Quebec. Canadian Veterinary Journal 39, 697–700. 

Sager, H., Bapst, B., Strehlau, G.A., Kaminsky, R., 2012. Efficacy of monepantel, derquantel and abamectin against adult stages of a multi-resistant Haemonchus contortus isolate. Parasitology Research 111, 2205-2207. 

Sakkas, P., Houdijk, J.G.M., Athanasiadou, S., Kyriazakis, I., 2012. Sensitivity of periparturient breakdown of immunity to parasites to dietary protein source. Journal of Animal Science 90, 3954-3962. 

Sales, N., Love, S., 2016. Resistance of Haemonchus sp. to monepantel and reduced efficacy of a derquantel / abamectin combination confirmed in sheep in NSW, Australia. Veterinary Parasitology 228, 193-196. 

Samuelson, J., 1999. Why Metronidazole Is Active against both Bacteria and Parasites. Antimicrobial Agents and Chemotherapy 43, 1533-1541. 

Scott, K.G., Logan, M.R., Klammer, G.M., Teoh, D.A., Buret, A.G., 2000. Jejunal brush border microvillous alterations in Giardia muris-infected mice: role of T lymphocytes and interleukin-6. Infection and Immunity 68, 3412-3418. 

Shaw, D.J., Vercruysse, J., Claerebout, E., Agneessens, J., Dorny, P., 1997. Gastrointestinal nematode infections of first-season grazing calves in Belgium: general patterns and the effect of chemoprophylaxis. Veterinary Parasitology 69, 103-116. 

Shaw, D.J., Vercruysse, J., Claerebout, E., Dorny, P., 1998a. Gastrointestinal nematode infections of first-grazing season calves in Western Europe: general patterns and the effect of chemoprophylaxis. Veterinary Parasitology 75, 115-131. 

Shaw, D.J., Vercruysse, J., Claerebout, E., Dorny, P., 1998b. Gastrointestinal nematode infections of first-grazing season calves in Western Europe: Associations between parasitological, physiological and physical factors. Veterinary Parasitology 75, 133-151. 

Smith, W.D., Zarlenga, D.S., 2006. Developments and hurdles in generating vaccines for controlling helminth parasites of grazing ruminants. Veterinary Parasitology 139, 347-359. 

Southcott, W.H., Barger, I.A., 1975. Control of nematode parasites by grazing management-II. decontamination of sheep and cattle pastures by varying periods of grazing with the alternate host. International Journal for Parasitology 5, 45-48. 

Suarez, V.H., Cristel, S.L., 2007. Anthelmintic resistance in cattle nematode in the western Pampeana Region of Argentina. Veterinary Parasitology 144, 111-117. 

Sutherland, I.A., Leathwick, D.M., 2011. Anthelmintic resistance in nematode parasites of cattle: A global issue? Trends in Parasitology 27, 176–181. 57 

 

Sweeney, T., Hanrahan, J.P., Good, B., 2016. Immunogenomics of gastrointestinal nematode infection in ruminants – breeding for resistance to produce food sustainably and safely. Parasite Immunology 38, 569-586. 

Taylor, L.M., Parkins, J.J., Armour, J., Holmes, P.H., Bairden, K., Ibarra-Silva, A.M., Salman, S.K., McWilliam, P.N., 1989. Pathophysiological and parasitological studies on Ostertagia ostertagi infections in calves. Research in Veterinary Science 46, 218-225 

Taylor, M.A., Hunt, K.R., Goodyear, K.L., 2002. Anthelmintic resistance detection methods. Veterinary Parasitology 103, 183-194. 

Taylor, M.A., Coop, R.L., Wall, R.L., 2016. Antiparasitics. In: Veterinary Parasitology, Fourth Edn. Wiley Blackwell, West Sussex, UK. 

Tejman-Yarden, N., Miyamoto, Y., Leitsch, D., Santini, J., Debnath, A., Gut, J., McKerrow, J.H., Reed, S.L., Eckmann, L., 2013. A reprofiled drug, auranofin, is effective against metronidazole-resistant Giardia lamblia. Antimicrob Agents Chemother 57, 2029-2035. 

Terrill, T.H., Miller, J.E., Burke, J.M., Mosjidis, J.A., Kaplan, R.M., 2012. Experiences with integrated concepts for the control of Haemonchus contortus in sheep and goats in the United States. Veterinary Parasitology 186, 28–37. 

Thamsborg, S.M., Jørgensen, R.J., Nansen, P., 1998. Internal parasitism of steers grazing extensively at different stocking rates. Acta Veterinaria Scandinavica 39, 311-323. 

Thamsborg, S.M., Roepstorff, A., Larsen, M., 1999. Integrated and biological control of parasites in organic and conventional production systems. Veterinary Parasitology 84, 169-186. 

Thomas, H., 1978. The efficacy of febantel on gastrointestinal nematodes in sheep. Research in Veterinary Science 25, 290-293. 

Thompson, R.C., Reynoldson, J.A., Mendis, A.H., 1993. Giardia and giardiosis. Advances in Parasitology 32, 71–160. 

Tripathi, D. M., N. Gupta, V. Lakshmi, K. C. Saxena, and A. K. Agrawal. 1999. Antigiardial and immunostimulatory effect of Piper longum on giardiasis due to Giardia lamblia. Phytother. Res. 13: 561–565. 

Tsiboukis, D., Sazakli, E., Jelastopulu, E., Leotsinidis, M., 2013. Anthelmintics residues in raw milk. Assessing intake by children population. Polish Journal of Veterinary Sciences 16, 85-91. 

Tzamaloukas, O., Athanasiadou, S., Kyriazakis, I., Jackson, F., Coop, R.L., 2004. Effects of short-term grazing on bioactive forages on lambs artificially infected with Teladorsagia circumcincta. Proc. Br. Soc. An. Sci. 6. 

Uehlinger, F.D., O’Handley, R.M., Greenwood, S.J., Guselle, N.J., Gabor, L.J., Van Velsen, C.M., Steuart, R.F.L., Barkema, H.W., 2007. Efficacy of vaccination in preventing giardiasis in calves. Veterinary Parasitology 146, 182-188. 

Upcroft, J.A., Upcroft, P., Boreham, P.F.L., 1990. Drug resistance in Giardia intestinalis. International Journal for Parasitology 20, 489-496. 

Upcroft, J.A., Upcroft, P., 2001. Drug Susceptibility Testing of Anaerobic Protozoa. Antimicrobial Agents and Chemotherapy 45, 1810-1814. 58 

 

Valderrábano, J., Calvete, C., Uriarte, J., 2010. Effect of feeding bioactive forages on infection and subsequent development of Haemonchus contortus in lamb faeces. Veterinary Parasitology 172, 89-94. 

Van den Putte, N., Claerebout, E., Levecke, B., 2013. Evaluatie van de mini-FLOTAC-methode voor de detectie van gastro-intestinale parasieten bij grote huisdieren. Vlaams Diergeneeskundig Tijdschrift 85, 15-22. 

van Dijk, J., Morgan, E.R., 2010. Variation in the hatching behaviour of Nematodirus battus: Polymorphic bet hedging? International Journal for Parasitology 40, 675-681. 

Van Wyk, J.A., Malan, F.S., Gerber, H.M., Alves, R.M., 1987. Two field strains of Haemonchus contortus resistant to rafoxanide. The Onderstepoort Journal of Veterinary Research 54, 143-146. 

Van Wyk, J.A., 2001. Refugia--overlooked as perhaps the most potent factor concerning the development of anthelmintic resistance. Onderstepoort Journal of Veterinary Research 68, 55-67. 

Van Wyk, J.A., Bath, G.F., 2002. The FAMACHA© system for managing haemonchosis in sheep and goats by clinically identifying individual animals for treatment. Veterinary Research 33, 509-529. 

Van Zeveren, A.M.J., Casaert, S., Alvinerie, M., Geldhof, P., Claerebout, E., Vercruysse, J., 2007. Experimental selection for ivermectin resistance in Ostertagia ostertagi in cattle. Veterinary Parasitology, 150, 104-110. 

Velazquez, C., Beltran, M., Ontiveros, N., Rascon, L., Fiqueroa, D.C., Granados, A.J., Hernandez-Martinez, J., Hernandez, J., Astiazaran-Garcia, H., 2005. Giardia lamblia infection induces different secretory and systemic antibody responses in mice. Parasite Immunology 27, 351-356. 

Vercruysse, J., Deprez, P., Everaert, D., Bassissi, F., Alvinerie, M., 2008. Breed differences in the pharmacokinetics of ivermectin administered subcutaneously to Holstein and Belgian Blue calves. Veterinary Parasitology 152, 136–140. 

Vercruysse, J., Charlier, J., Van Dijk, J., Morgan, E.R., Geary, T., von Samson-Himmelstjerna, G., Claerebout, E., 2018. Control of helminth ruminant infections by 2030. Parasitology doi: 10.1017. 

Verschave, S.H., Vercruysse, J., Forbes, A., Opsomer, G., Hostens, M., Duchateau, L., Charlier, J., 2014. Non-invasive indicators associated with the milk yield response after anthelmintic treatment at calving in dairy cows. Veterinary Research 10, 264. 

Wade, S.E., Mohammed, H.O., Schaaf, S.L., 2000a. Epidemiologic study of Giardia sp. infection in dairy cattle in southeastern New York State. Veterinary Parasitology 89, 11-21. 

Wade, S.E., Mohammed, H.O., Schaaf, S.L., 2000b. Prevalence of Giardia sp. Cryptosporidium parvum and Cryptosporidium andersoni (syn. C. muris) in 109 dairy herds in five counties of southeastern New York. Veterinary Parasitology 93, 1–11. 

Wall, R., Beynon, S., 2012. Area-wide impact of macrocyclic lactone parasiticides in cattle dung. Medical and Veterinary Entomology 26, 1-8. 

Waller, P.J., Bernes, G., Rudby-Martin, L., Ljungström, B-L., Rydzik, A., 2004. Evaluation of Copper Supplementation to Control Haemonchus contortus Infections of Sheep in Sweden. Acta Vet Scand 45, 149-160. 

Waller, P.J., Thamsborg, S.M., 2004. Nematode control in ‘green’ ruminant production systems. Trends in Parasitology 20, 493–497 59 

 

Werne, S., Isensee, A., Maurer, V., Perler, E., Drewek, A., Heckendorn, F., 2013. Integrated control of gastrointestinal nematodes in lambs using a bioactive feed x breed approach. Veterinary Parasitology, 198, 298-304. 

Williams, J.C., Sheehan, D., Fuselier, R.H., 1977. Effect of albendazole on gastrointestinal parasites of cattle. American Journal of Veterinary Research 38, 2037-2038. 

Williams, J.C., Marbury, K.S., Eddi, C.S., Willis, E.R., Luther, D.G., 1988. Efficacy of febantel against abomasal nematodes and lungworms in cattle. Am J Vet Res 49, 2085-2089. 

Williams, J.C., Loyacano, A.F., DeRosa, A., Gurie, J., Clymer, B.C., Guerino, F., 1999. A comparison of persistent anthelmintic efficacy of topical formulations of doramectin, ivermectin, eprinomectin and moxidectin against naturally acquired nematode infections of beef calves. Veterinary Parasitology 85, 277-288. 

Williams, A.R., Soelberg, J., Jäger, A.K., 2016. Anthelmintic properties of traditional African and Caribbean medicinal plants: identification of extracts with potent activity against Ascaris suum in vitro. Parasite 23:24, doi: 10.1051. 

Wilson, D.J., Sargison, N.D., Scott, P.R., Penny, C.D., 2008. Epidemiology of gastrointestinal nematode parasitism in a commercial sheep flock and its implications for control programs. The Veterinary Record 162, 546-550. 

Wright, C.W., Melwani, S.I., Phillipson, J.D., Warhurst, D.C., 1992. Determination of anti-giardial activity in vitro by means of soluble formazan production. Transactions of the Royal Society of Tropical Medicine and Hygiene 86, 517-519. 

Xiao, L., Herd, R.P., 1993. Quantitation of Giardia cysts and Cryptosporidium oocysts in fecal samples by direct immunofluorescence assay. Journal of Clinical Microbiology 31, 2944–2946. 

Xiao, L., Herd, R.P., 1994. Infection pattern of Cryptosporidium and Giardia in calves. Veterinary Parasitology 55, 257–262. 

Xiao, L., Saeed, K., Herd, R.P., 1996. Efficacy of albendazole and fenbendazole against Giardia infection in cattle. Veterinary Parasitology 61, 165–170. 

Yanke, S.J., Ceri, H., McAllister, T.A., Morck, D.W., Olson, M.E., 1998. Serum immune response to Giardia duodenalis in experimentally infected lambs. Veterinary Parasitology 75, 9–19. 

Zajac, A., 1992. Giardiosis. Compendium on the Continuing Education of the Practicing Veterinarian 14, 604–609. 

Zajac, A., 2006. Gastrointestinal Nematode of Small Ruminants: Life Cycle, Anthelmintics, and Diagnosis. Veterinary Clinics of North America: Food Animal Practice 22, 529-541. 

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 255, 19-28. 

Download scriptie (1.88 MB)
Universiteit of Hogeschool
Universiteit Gent
Thesis jaar
2018
Promotor(en)
Prof. Dr. Edwin Claerebout
Thema('s)