Worm infections in cattle

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Infectiimpediment ons with gastrointestinal nematodes are worldwide a major to sustainable livestock production. Infection has direct effects on food quality reducing meat and milk quality and impairing growth rates with serious consequences for production. In addition to the impact of these parasites on food production, quality and safety, these infections are also of major animal welfare concern. Gastrointestinal nematode infections cause diarrhoea, emaciation and abdominal pain in affected animals. Control of these parasites relies heavily on treatment with anthelmintics. The global spend on anthelmintics is estimated to be in the region of 3 billion US dollars, a figure which indicates the scale of the perceived problem imposed by parasitism. Anthelmintics are routinely administered to animals on several occasions during the perceived period of parasite threat to livestock.

1. Epidemiology and diagnosis

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Effective control of these infections is hampered by several factors. Climate change and changing animal husbandry methods are thought to significantly alter the epidemiology of helminth infections. In addition, anthelmintic resistance can reduce the efficacy of the commonly used anthelmintic drugs.
In our research, we aim to understand the impact on production of helminths in cattle and to develop/evaluate new diagnostics. This would allow to identify the herds and animals that would benefit most from anthelmintic control measures and to apply anthelmintics selectively. Furthermore, we study the impact of farm management and climatic factors on helminth infection risks through field observations and mathematical modelling techniques and develop new methods for assessing the impact of infections on farming efficiency.


Links:
www.paracalc.com
www.gloworm.eu


Publications (since 2010):

  • Charlier J., Van der Voort M., Hogeveen H., Vercruysse J., 2012. ParaCalc® - a novel tool to estimate the costs of worm infections on the dairy herd. Veterinary Parasitology 184, 204-211 (IF 2.579).
  • Levecke B., Speybroeck N., Dobson R.J., Vercruysse J., Charlier J., 2011. Novel Insights in the Fecal Egg Count Reduction Test for Monitoring Drug Efficacy against Soil-Transmitted Helminths in Large-Scale Treatment Programs. Plos Neglected Tropical Diseases 5 (12), e1427 (doi:10.1371/journal.pntd.0001427) (IF 4.716).
  • Charlier J., Levecke B., Devleesschauwer B., Vercruysse J., Hogeveen H., 2012. The Economic Effects of Whole-herd versus selective anthelmintic treatment strategies in dairy cows. Journal of Dairy Science 95, 2977-2987 (http://dx.doi.org/ 10.3168/jds.2011-4719) (IF 2.564).
  • Levecke B., Rinaldi L., Charlier J., Maurelli M.P., Bosco A., Vercruysse J., Cringoli G., 2012. The bias, accuracy and precision of faecal egg count reduction test results in cattle using McMaster, Cornell-Wisconsin and FLOTAC egg counting methods. Veterinary Parasitology 188, 194-199 (IF 2.579).
  • Levecke B., Speybroeck N., Dobson R.J., Vercruysse J., Charlier J., 2012. Novel insights in the faecal egg count reduction test for monitoring drug efficacy against gastrointestinal nematodes of veterinary importance. Veterinary Parasitology 188, 391-396 (IF 2.579).
  • Charlier J., Hostens M., Jacobs J., Van Ranst B., Duchateau L., Vercruysse J., 2012. Integrating fasciolosis in the dry cow management: the effect of closantel treatment on milk production. Plos One 7, e43216. doi: 10.1371/journalpone.0043216 (http://dx.plos.org/10.1371/journal.pone.0043216) (IF 4.092).
  • van der Voort M., Charlier J., Lauwers L., Vercruysse J., Van Huylenbroeck G., Van Meensel J., 2013. Conceptual framework for analysing farm-specific economic effects of helminth infections in ruminants and control strategies. Preventive Veterinary Medicine 109, 228-235 (IF 2.046).
  • Charlier J., Meyns T., Soenen K., Vercruysse J., 2013. Monitoring gastrointestinal and liver fluke infections in Belgium by bulk tank milk ELISA: are we making progress in parasite control? Vlaams Diergeneeskundig Tijdschrift 82, 17-22 (IF 0.340).
  • Morgan E.R., Charlier J., Hendrickx G., Biggeri A., Catalan D., von Samson-Himmelstjerna G., Demeler J., Müller E., van Dijk J., Kenyon F., Skuce P., Höglund J., O’Kiely P., van Ranst B., de Waal T., Rinaldi L., Cringoli G., Hertzberg H., Torgerson P., Wolstenholme A., Jozef Vercruysse, 2013. Global Change and Helminth Infections in Grazing Ruminants: Impacts, Trends and Sustainable Solutions. Agriculture 3, 484-502.
  • Charlier J., Vercruysse J., Morgan E., Van Dijk J., Williams D.J.L., 2013. Recent advances in the diagnosis, impact on production and prediction of Fasciola hepatica in cattle. Parasitology 141, 326-335 (IF 2.355).
  • Charlier J., Forbes A., Van Gucht S., Duchateau L., Goddeeris B.M., Vercruysse J., 2013. Serological evidence of Ostertagia ostertagi infection in dairy cows does not impact the efficacy of rabies vaccination during the housing period. Research in Veterinary Science 95, 1055-1058 (IF 1.774).
  • Charlier J., Vercruysse J., Smith J., Vanderstichel R., Stryhn H., Claerebout E., Dohoo I., 2010. 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. (doi: 10.1016/j.prevetmed.2009.10.002).
  • El-Abdellati A., Charlier J., Geldhof P., Levecke B., Demeler J., von Samson-Himmelstjerna G., Claerebout E., Vercruysse J., 2010. The use of a simplified faecal egg count reduction test for assessing anthelmintic efficacy on Belgian and German cattle farms. Veterinary Parasitology 169, 352-357.
  • El-Abdellati A., Geldhof P., Claerebout E., Vercruysse J., Charlier J., 2010. Monitoring macrocyclic lactone resistance in Cooperia oncophora on a Belgian cattle farm during four consecutive years. Veterinary Parasitology 171, 167-171. (doi:10.1016/j.vetpar.2010.03.003)
  • Charlier J., Demeler J., Höglund J., von Samson-Himmelstjerna G., Dorny P., Vercruysse J., 2010. 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. (http://dx.doi.org/10.1016/j.vetpar.2010.03.006)
  • 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.
  • Bennema S.C., Ducheyne E., Vercruysse J., Hendrickx G., Claerebout E., Charlier J., 2011. Relative importance of management, meteorological and environmental factors in the spatial distribution of Fasciola hepatica in dairy cattle in a temperate climate zone. International Journal for Parasitology, 41, 225-233.
  • Dorny P., Stoliaroff V., Charlier J., Meas S., Sorn S., Chea B., Holl D., Van Aken D., Vercruysse J., 2011. Infections with gastro-intestinal nematodes, Fasciola and Paramphistomum in cattle in Cambodia and their association with morbidity parameters. Veterinary Parasitology 175, 293-299.
  • Charlier J., Dorny P., Levecke B., Demeler J., von Samson-Himmelstjerna G., Höglund J., Vercruysse J, 2011. Serum pepsinogen levels to monitor gastrointestinal nematode infections in cattle revisited. Research in Veterinary Science 90, 451-456. (doi:10.1016/j.rvsc.2010.06.029)
  • Levecke B., Rinaldi L., Charlier J., Maurelli M.P., Morgoglione M.E., Vercruysse J., Cringoli G., 2011. Monitoring drug efficacy against gastrointestinal nematodes when faecal egg counts are low: do the analytic sensitivity and the formula matter? Parasitology Research 109, 953-957.

  • Levecke B., Rinaldi L., Charlier J., Maurelli M.P., Bosco A., Vercruysse J., Cringoli G, 2012 The precision and accuracy of faecal egg count reduction test results in cattle using McMaster, Cornell-Wisconsin and FLOTAC egg counting methods. Veterinary Parasitology 188, 194-199

  • Charlier J., Bennema S.C., Caron Y., Counotte M., Ducheyne E., Hendrickx G., Vercruysse J., 2011.Towards assessing fine-scale indicators for the spatial transmission risk of Fasciola hepatica in cattle. Geospatial Health 5, 239-245.
  • Charlier J., Van der Voort M., Hogeveen H., Vercruysse J., 2012. ParaCalc® - a novel tool to estimate the costs of worm infections on the dairy herd. Veterinary Parasitology 184, 204-211.
  • Charlier J., Levecke B., Devleesschauwer B., Vercruysse J., Hogeveen H., 2012. The Economic Effects of Whole-herd versus selective anthelmintic treatment strategies in dairy cows. Journal of Dairy Science 95, 2977-2987 (http://dx.doi.org/ 10.3168/jds.2011-4719).


2. Anthelmintic resistance

Control of parasitic worms relies almost completely on the use of anthelmintic drugs. However, the intensive and frequent use of these drugs during the last decades has resulted in the development of resistance in many different nematode species. Cases of multiple drug resistance in nematodes of small ruminants have been reported globally and recent studies show that resistance in cattle and horses is also emerging. At present the lack of simple and reliable tests for the detection of resistant nematodes seriously compromises our ability to monitor the spread of resistance. We are currently dependent on biological methods, which are not sufficiently sensitive to detect low levels of drug resistance. Moreover, the only test that is currently available to detect resistance against all anthelmintic classes (faecal egg count reduction test) is labour-intensive, which may explain why only few large scale surveys have been conducted. The development of more sensitive and user-friendly diagnostic tests would be greatly aided by an understanding of the genetic and/or biochemical basis of resistance. Resistance to drugs is commonly due to one of two mechanisms: changes in the target site that make it insensitive to the drug or a change in the rate at which the drug is inactivated via metabolism or removal from the target site. Both mechanisms are currently being investigated using resistant Cooperia oncophora worms isolated from several farms in Flandres.

Publications

  • El-Abdellati A., Charlier J., Geldhof P., Levecke B., Demeler J., von Samson-Himmelstjerna G., Claerebout E., Vercruysse J., 2010. The use of a simplified faecal egg count reduction test for assessing anthelmintic efficacy on Belgian and German cattle farms. Veterinary Parasitology 169, 352-357

  • El-Abdellati A., Geldhof P., Claerebout E., Vercruysse J., Charlier J., 2010. Monitoring macrocyclic lactone resistance in Cooperia oncophora on a Belgian cattle farm during four consecutive years. Veterinary Parasitology 171, 167-171

  • El-Abdellati A., De Graef J., Donnan A., Skuce P., Wolstenholme A., Vercruysse J., Claerebout E., Geldhof P., 2011. Altered avr-14B transcription patterns in ivermectin resistant isolates of the cattle parasites, Cooperia oncophora and Ostertagia ostertagi. International Journal for Parasitology 41, 951-957

  • Molento MB, Fortes F., Pondelek D., de Almeida Borges F., de Souza Chagas AC., Torres-Acosta JF., Geldhof P. Challenges of nematode control in ruminants: Focus on Latin America. Veterinary Parasitology 2011 180: 126-132 (IF 2,278)

  • Sarre C., Claerebout E., Vercruysse J., Levecke B., Geldhof P., Pardon B., Alvinerie M., Sutra J.F., Geurden T., 2012. Doramectin resistance in Haemonchus contortus on an alpaca farm in Belgium. Veterinary Parasitology 185, 346-351

  • De Graef J., Sarre C., Mills 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

  • Martinez-Valladares M., Geldhof P., Jonsson N., Rojo-Vazquez F.A., Skuce P. Teladorsagia circumcincta: molecular characterization of the avr-14B subunit and its relatively minor role in ivermectin resistance. International Journal for Parasitology: Drugs and Drug Resistance 2012 3:154-161
  • Komuniecki R., Law W.J., Jex A., Geldhof P., Gray J., Bamber B., Gasser R.B. Monoaminergic signaling as a target for anthelmintic drug discovery: receptor conservation among the free-living and parasitic nematodes. Molecular and Biochemical Parasitology 2012 183:1-7 (IF 2,875)
  • Martinez-Valladarez M., Donnan A., Geldhof P., Jackson F., Rojo-Vazquez FA, Skuce PJ. Pyrosequencing analysis of the beta-tubulin gene in Spanish Teladorsagia circumcincta field isolates. Veterinary Parasitology 2012 184:371-376 (IF 2,278)

  • De Graef J., Demeler J., Skuce P., Mitreva M., von Samson-Himmelstjerna G., Vercruysse J., Claerebout E., Geldhof P., 2013. Gene expression analysis of ABC transporters in a resistant Cooperia oncophora isolate following in vivo and in vitro exposure to macrocyclic lactones. Parasitology 140, 499-508

  • Levecke B., Dobson R.J., Speybroeck N., Vercruysse J., Charlier. (2012). Novel insights in the faecal egg count reduction test for monitoring drug efficacy against gastro-intestinal nematodes of veterinary importance. Veterinary Parasitology 188, 391-396

  • Demeler J., Krücken J., AlGusbi S., Ramünke S., De Graef J., Kerboeuf D., Geldhof P., Pomroy W.E., von Samson-Himmelstjerna G. Potential contribution of P-glycoproteins to macrocyclic lactone resistance in the cattle parasitic nematode Cooperia oncophora. Molecular and Biochemical Parasitology 2013 188:10-19 (IF 2,551)
  • Heizer E., Zarlenga D.S., Gasser R.B., De Graef J., Geldhof P., Mitreva M. Transcriptome analyses reveal protein and domain families that delineate stage-related development in the economically important parasitic nematodes Ostertagia ostertagi and Cooperia oncophora. BMC Genomics 2013 14:118 (IF 4,07)


3. Host-parasite interaction and vaccination

To comply with a requirement for prime quality animal products farmed in a way that is minimally harmful to the environment, immunological control of parasite infections is the most rational way forward. Both the WHO, FAO and OECD regard vaccines as among the most cost-effective methods for promoting both human and animal health. The Laboratory of Parasitology at Ghent University has in recent years developed an experimental vaccine against the abomasal cattle parasite Ostertagia ostertagi, based on 2 Activation-associated Secreted Proteins (ASPs) released by the adult parasites. Intramuscular immunisation of cattle with these antigens raises an effective immune response, resulting in a significant reduction in faecal worm egg shedding of 56-74% during 2 months. This is the highest level of protection ever raised by vaccination of cattle against O. ostertagi and sufficient to protect calves against parasitic gastroenteritis during the whole grazing season. Our current research is focussed on the large scale recombinant expression of the antigens and the analysis of the protective immune responses induced by the vaccine. Based on our success with O. ostertagi, a new research project was recently initiated on the development of a vaccine against the intestinal parasite Cooperia oncophora.

Publications:

  • Hoorens P.R., Rinaldi M., Li R.W., Goddeeris B., Claerebout E., Vercruysse J., Geldhof P., 2011. Genome wide analysis of the bovine mucin genes and their gastrointestinal transcription profile. BMC Genomics 12, 140-151

  • Rinaldi M., Dreesen L., Hoorens P.R., Li R.W., Claerebout E., Goddeeris B., Vercruysse J., Van Den Broek W., Geldhof P., 2011. Infection with the gastrointestinal nematode Ostertagia ostertagi affects mucus biosynthesis in the abomasum of cattle. Veterinary Research 42, 61

  • Mihi B., Rinaldi M., Geldhof P. Effect of an Ostertagia ostertagi infection on the transcriptional stability of housekeeping genes in the bovine abomasum. Veterinary Parasitology 2011 181:354-359 (IF 2,278)
  • Rinaldi M., Geldhof P. Ostertagiosis in cattle: where do we stand? Parasite Immunology 2012 34:254-264 (IF 2,014)

  • Borloo J., Geldhof P., Peelaers I., Van Meulder F., Ameloot P., Callewaert N., Vercruysse J., Claerebout E., Strelkov S., Weeks S.D., 2013. Structure of Ostertagia ostertagi ASP-1: insights into disulfide mediated cyclization and dimerization. Acta Cristallographica Section D, D69, 493-503

  • Van Meulder F., Van Coppernolle S., Borloo J., Rinaldi M., Li R.W., Chiers K., Van den Broeck W., Vercruysse J., Claerebout E., Geldhof P., 2013. Granule-exocytosis of granulysin and granzyme B as a potential key mechanism in vaccine-induced immunity in cattle against the nematode Ostertagia ostertagi. Infection and Immunity 81, 1798-1809

  • 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

  • Borloo J., Claerebout E., De Graef J., Peelaers I., Mitreva M., Devreese B., Hokke C.H., Vercruysse J., Geldhof P., 2013. In-depth proteomic and glycomic analysis of the adult-stage Cooperia oncophora excretome/secretome. Journal of Proteome Research 12(9):3900-11

  • Mihi B., Van Meulder F., Van Coppernolle S., Rinaldi M., Chiers K., Van den Broeck W., Goddeeris B., Vercruysse J., Claerebout E., Geldhof P., 2013. Analysis of the mucosal immune responses induced by single and trickle infections with the bovine abomasal nematode Ostertagia ostertagi. Parasite Immunology (accepted) doi: 10.1111/pim.12094.