Global Change and Helminth Infections in Grazing Ruminants in Europe: Impacts, Trends and Sustainable Solutions

Agriculture (Switzerland) - Tập 3 Số 3 - Trang 484-502
Eric R. Morgan1, Johannes Charlier2, Guy Hendrickx3, Annibale Biggeri4, Dolores Catalan4, Georg von Samson‐Himmelstjerna5, Janina Demeler5, E Müller6, Jan van Dijk7, Fiona Kenyon8, Philip Skuce8, Johan Höglund9, P. O’Kiely10, B. Van Ranst11, Theo de Waal12, Laura Rinaldi13, Giuseppe Cringoli13, Hubertus Hertzberg14, Paul R. Torgerson15, Adrian J. Wolstenholme16, Jozef Vercruysse2
1School of Veterinary Sciences, University of Bristol, Langford House, Langford, North Somerset BS40 5DU, UK
2Laboratory of Parasitology, Faculty of Veterinary Medicine, Ghent University, Merelbeke B-9820, Belgium
3Avia-GIS, Zoersel 2980, Belgium
4"Cooperativa Epidemiologia e Prevenzione ""Giulio Alfredo Maccacaro""
5Institute for Parasitology and Tropical Veterinary Medicine, Freie Universität Berlin, Berlin 14195, Germany
6Laboklin, Bad Kissingen D-97668, Germany
7Institute of Infection and Global Health, University of Liverpool, Liverpool L69 3BX, UK
8Moredun Research Institute, Edinburgh EH26 0PZ, Scotland, UK
9Department of Biomedicine and Vet Public Health, Swedish University of Agricultural Sciences, Uppsala 753 12, Sweden
10Animal & Grassland Research and Innovation Centre, Teagasc, Grange, Dunsany, Co. Meath, Ireland
11UNIFORM-AGRI BV, Assen 9401, The Netherlands
12School of Veterinary Medicine, University College Dublin, Dublin 4, Ireland
13"Department of Pathology and Animal Health, Faculty of Veterinary Medicine, University of Naples ""Federico II""
14Institute of Parasitology, Vetsuisse Faculty, University of Zürich, Zürich 8057, Switzerland
15Section of Epidemiology, Vetsuisse Faculty, University of Zürich, Zürich 8057, Switzerland
16Department of Infectious Diseases, University of Georgia College of Veterinary Medicine, Athens, GA 30602, USA

Tóm tắt

Infections with parasitic helminths (nematodes and trematodes) represent a significant economic and welfare burden to the global ruminant livestock industry. The increasing prevalence of anthelmintic resistance means that current control programmes are costly and unsustainable in the long term. Recent changes in the epidemiology, seasonality and geographic distribution of helminth infections have been attributed to climate change. However, other changes in environment (e.g., land use) and in livestock farming, such as intensification and altered management practices, will also have an impact on helminth infections. Sustainable control of helminth infections in a changing world requires detailed knowledge of these interactions. In particular, there is a need to devise new, sustainable strategies for the effective control of ruminant helminthoses in the face of global change. In this paper, we consider the impact of helminth infections in grazing ruminants, taking a European perspective, and identify scientific and applied priorities to mitigate these impacts. These include the development and deployment of efficient, high-throughput diagnostic tests to support targeted intervention, modelling of geographic and seasonal trends in infection, more thorough economic data and analysis of the impact of helminth infections and greater translation and involvement of end-users in devising and disseminating best practices. Complex changes in helminth epidemiology will require innovative solutions. By developing and using new technologies and models, the use of anthelmintics can be optimised to limit the development and spread of drug resistance and to reduce the overall economic impact of helminth infections. This will be essential to the continued productivity and profitability of livestock farming in Europe and its contribution to regional and global food security.

Từ khóa


Tài liệu tham khảo

FAOSTAT (2009). Available online:http://faostat.fao.org/.

Baulcombe, D., Crute, I., Dunwell, J., Gale, M., Jones, J., Pretty, J., Sutherland, W., and Toulmin, C. (2009). Reaping the Benefits—Science and the Sustainable Intensification of Global Agriculture, Royal Society Policy Document.

Chiotti, 1995, Extending the boundaries of climate change research—A discussion on agriculture, J. Rural Stud., 11, 335, 10.1016/0743-0167(95)00023-G

Nieuwhof, 2005, Costs of the major endemic diseases in Great Britain and the potential benefits of reduction in disease impact, Anim. Sci., 81, 23, 10.1079/ASC41010023

Schweizer, 2005, The economic effects of bovine fasciolosis in Switzerland, Vet. Rec., 157, 188, 10.1136/vr.157.7.188

Selzer, P.M. (2009). Antiparasitic and Antibacterial Drug Discovery. From Molecular Targets to Drug Candidates, Wiley-Blackwell.

Charlier, 2009, Gastrointestinal nematode infections in adult dairy cattle: Impact on production, diagnosis and control, Vet. Parasitol., 164, 70, 10.1016/j.vetpar.2009.04.012

Rehbein, 2013, Nematode burdens of pastured cattle treated once at turnout with eprinomectin extended-release injection, Vet. Parasitol., 192, 321, 10.1016/j.vetpar.2012.11.038

Morgan, 2008, The influence of temperature on the development, hatching and survival of Nematodirus battus larvae, Parasitology, 135, 269, 10.1017/S0031182007003812

Mejia, 2011, Comparison of three methods for gastrointestinal nematode diagnosis determination in grazing dairy cattle in relation to milk production, Vet. Parasitol., 183, 174, 10.1016/j.vetpar.2011.06.027

Charlier, 2012, ParaCalc®—A novel tool to evaluate the economic importance of worm infections on the dairy farm, Vet. Parasitol., 184, 204, 10.1016/j.vetpar.2011.09.008

Charlier, 2012, The economic effects of whole-herd versus selective anthelmintic treatment strategies in dairy cows, J. Dairy Sci., 95, 2977, 10.3168/jds.2011-4719

Mason, 2012, The effect of repeated, four-weekly eprinomectin treatment on milk production in pasture-based, seasonally-calving dairy cattle, Vet. Parasitol., 189, 250, 10.1016/j.vetpar.2012.05.003

Sargison, 2010, Climate change and infectious disease: Helminthological challenge to farmed ruminants in temperate regions, Animal, 4, 377, 10.1017/S1751731109990991

Sargison, 2007, Haemonchosis and teladorsagiosis in a Scottish sheep flock putatively associated with the over-wintering of hypobiotic fourth stage larvae, Vet. Parasitol., 147, 326, 10.1016/j.vetpar.2007.04.011

Kenyon, 2009, Sheep helminth parasitic disease in South-Eastern Scotland arising as a possible consequence of climate change, Vet. Parasitol., 163, 293, 10.1016/j.vetpar.2009.03.027

Lindqvist, 2001, The dynamics, prevalence and impact of nematode infections in organically raised sheep in Sweden, Acta Vet. Scand., 42, 377, 10.1186/1751-0147-42-377

Rioux, 2008, Climate change: Effects on animal disease systems and implications for surveillance and control, Rev. Sci. Tech. Int. Off. of Epizoot., 27, 339

Morgan, 2009, Climate change and parasitic disease: Farmer mitigation?, Trends Parasitol., 7, 308, 10.1016/j.pt.2009.03.012

Leathwick, 1992, A model for nematodiasis in New Zealand lambs, Int. J. Parasitol., 22, 789, 10.1016/0020-7519(92)90129-9

Reynecke, 2011, Dynamics of the free-living stages of sheep intestinal parasites on pasture in the North Island of New Zealand. 2. Weather variables associated with development, Vet. J., 59, 287

Leathwick, 2012, Managing anthelmintic resistance—Use of a combination anthelmintic and leaving some lambs untreated to slow the development of resistance to ivermectin, Parasitology, 187, 285

Dobson, 2011, A multi-species modelto assess the effect of refugia on worm control and anthelmintic resistance insheep grazing systems, Aust. Vet. J., 89, 200, 10.1111/j.1751-0813.2011.00719.x

Laurenson, 2013, Modelling the short- and long-term impacts of drenching frequency and targeted selective treatment on the performance of grazing lambs and the emergence of anthelmintic resistance, Parasitology, 140, 780, 10.1017/S0031182012002181

Fox, 2011, Predicting impacts of climate change on Fasciola hepatica risk, PLoS One, 6, e16126, 10.1371/journal.pone.0016126

Jackson, 2006, Alternative approaches to control—Quo vadit?, Vet. Parasitol., 139, 371, 10.1016/j.vetpar.2006.04.025

Kaplan, 2004, Drug resistance in nematodes of veterinary importance: A status report, Trends Parasitol., 20, 477, 10.1016/j.pt.2004.08.001

Familton, 2001, Anthelmintic-resistant Cooperia species in cattle, Vet. Rec., 149, 719

Lee, D.L. (2002). The Biology of Nematodes, Taylor and Francis.

Sutherland, 2010, Anthelmintic resistance in nematode parasites of cattle—A global issue?, Trends Parasitol, 27, 176, 10.1016/j.pt.2010.11.008

Demeler, 2009, Monitoring the efficacy of ivermectin and albendazole against gastro intestinal nematodes of cattle in Northern Europe, Vet. Parasitol., 160, 109, 10.1016/j.vetpar.2008.10.030

Charlier, 2010, The use of a simplified faecal egg count reduction test for assessing anthelmintic efficacy on Belgian and German cattle farms, Vet. Parasitol., 169, 352, 10.1016/j.vetpar.2010.01.015

Bartley, 2004, Characterisation of two triple resistant field isolates of Teladorsagia from Scottish lowland sheep farms, Vet. Parasitol., 123, 189, 10.1016/j.vetpar.2004.06.018

Sargison, 2007, Observations on the emergence of multiple anthelmintic resistance in sheep flocks in the south-east of Scotland, Vet. Parasitol., 45, 65, 10.1016/j.vetpar.2006.10.024

Wolstenholme, 2004, Drug resistance in veterinary helminths, Trends Parasitol., 20, 469, 10.1016/j.pt.2004.07.010

Kaminsky, 2008, A new class of anthelmintics effective against drug-resistant nematodes, Nature, 452, 176, 10.1038/nature06722

Little, 2010, Field efficacy and safety of an oral formulation of the novel combination anthelmintic, derquantel-abamectin, in sheep in New Zealand, N. Z. Vet. J., 58, 121, 10.1080/00480169.2010.67513

Steinfeld, H., Gerber, P., Wassenaar, T., Castel, V., Rosales, M., and de Haan, C. (2006). Livestock’s Long Shadow: Environmental Issues and Options, Report presented to the Food and Agricultural Organisation of the United Nations (FAO).

Gill, 2010, Mitigating climate change: The role of domestic livestock, Animal, 4, 323, 10.1017/S1751731109004662

Thornton, 2010, Livestock production: Recent trends, future prospects, Philos. Trans. R. Soc. B Biol. Sci., 365, 2853, 10.1098/rstb.2010.0134

Taylor, 2002, Anthelmintic resistance detection methods, Vet. Parasitol., 103, 183, 10.1016/S0304-4017(01)00604-5

Gasser, 2008, Toward practical, DNA-based diagnostic methods for parasitic nematodes of livestock—Bionomic and biotechnical implications, Biotechnol. Adv., 26, 325, 10.1016/j.biotechadv.2008.03.003

Zarlenga, 2001, A multiplex PCR assay for differentiating economically important gastrointestinal nematodes of cattle, Vet. Parasitol., 97, 199, 10.1016/S0304-4017(01)00410-1

Wimmer, 2004, Non-invasive assessment of parasitic nematode species diversity in wild Soay sheep using molecular markers, Int. J. Parasitol., 34, 625, 10.1016/j.ijpara.2003.11.022

Learmount, 2009, Development and validation of real-time PCR methods for diagnosis of Teladorsagia circumcincta and Haemonchus contortus in sheep, Vet. Parasitol., 166, 268, 10.1016/j.vetpar.2009.08.017

Dobson, 2009, Geometric means provide a biased efficacy result when conducting a faecal egg count reduction test (FECRT), Vet. Parasitol., 161, 162, 10.1016/j.vetpar.2008.12.007

Coles, 2006, The detection of anthelmintic resistance in nematodes of veterinary importance, Vet. Parasitol., 136, 167, 10.1016/j.vetpar.2005.11.019

Blackhall, 2007, Single nucleotide polymorphism (SNP) markers for benzimidazole resistance in veterinary nematodes, Parasitology, 134, 1077, 10.1017/S0031182007000054

Walsh, 2009, Molecular detection of benzimidazole resistance in Haemonchus contortus using real-time PCR and pyrosequencing, Parasitology, 136, 349, 10.1017/S003118200800543X

Skuce, 2010, Benzimidazole resistance allele haplotype diversity in United Kingdom isolates of Teladorsagia circumcincta supports a hypothesis of multiple origins of resistance by recurrent mutation, Int. J. Parasitol., 40, 1247, 10.1016/j.ijpara.2010.03.016

Gustaffson, 2009, Anthelmintic resistance in Swedish sheep flocks based on a comparison of the results from the faecal egg count reduction test and resistant allele frequencies of the beta-tubulin gene, Vet. Parasitol., 161, 60, 10.1016/j.vetpar.2008.12.001

Beech, 2010, Anthelmintic resistance: Markers for resistance, or susceptibility?, Parasitology, 138, 160, 10.1017/S0031182010001198

Gilleard, 2006, Understanding anthelmintic resistance: The need for genomics and genetics, Int. J. Parasitol., 36, 1227, 10.1016/j.ijpara.2006.06.010

Vignali, 2000, Multiplexed particle-based flow cytometric assays, J. Immunol. Methods, 243, 243, 10.1016/S0022-1759(00)00238-6

Pickering, 2002, Comparison of a multiplex flow cytometric assay with Enzyme-Linked Immunosorbent Assay for quantification of antibodies to Tetanus, Diphtheria and Haemophilus influenza Type b, Clin. Diagn. Lab. Immunol., 9, 872

Dunbar, 2003, Quantitative, multiplexed detection of bacterial pathogens: DNA and protein applications of the Luminex LabMAPTM system, J. Microbiol. Methods, 53, 245, 10.1016/S0167-7012(03)00028-9

Morgan, 2004, Cytometric bead array: A multiplexed assay platform with applications in various areas of biology, Clin. Immunol., 110, 252, 10.1016/j.clim.2003.11.017

Dunbar, 2006, Application of Luminex xMAPTM technology for rapid, high-throughput multiplexed nucleic acid detection, Clinia Chim. Acta, 363, 71, 10.1016/j.cccn.2005.06.023

Charlier, 2009, Evaluation of anti-Ostertagia ostertagi antibodies in individual milk samples as decision parameter for selective anthelmintic treatment in dairy cows, Prev. Vet. Med., 93, 147, 10.1016/j.prevetmed.2009.10.002

McCann, 2010, Seroprevalence and spatial distribution of Fasciola hepatica-infected dairy herds in England and Wales, Vet. Rec., 166, 612, 10.1136/vr.b4836

Andersen, 2013, SvSXP: A Strongylus vulgaris antigen with potential for prepatent diagnosis, Parasites Vectors, 6, 84, 10.1186/1756-3305-6-84

Ganheim, 2004, Acute phase proteins in response to Dictyocaulus viviparus infection in calves, Acta Vet. Scand., 45, 79, 10.1186/1751-0147-45-79

Charlier, 2011, Serum pepsinogen levels to monitor gastrointestinal nematode infections in cattle revisited, Res. Vet. Sci., 90, 451, 10.1016/j.rvsc.2010.06.029

Bandyopadhyay, 2007, Rapid microsphere assay for identification of Cryptosporidium hominis and Cryptosporidium parvum in stool and environmental samples, J. Clin. Microbiol., 45, 2835, 10.1128/JCM.00138-07

Li, 2010, A novel multiplex PCR coupled with Luminex assay for the simultaneous detection of Cryptosporidium spp., Cryptosporidium parvum and Giardia duodenalis, Vet. Parasitol, 173, 11, 10.1016/j.vetpar.2010.05.024

Stark, 2010, An evaluation of a multiplex tandem real-time PCR for the detection of Cryptosporidium spp, Dientamoeba fragilis, Entamoeba histolytica, and Giardia intestinalis from clinical stool samples, J. Clin. Microbiol., 49, 257, 10.1128/JCM.01796-10

Iseki, 2007, Development of a multiplex loop-mediated isothermal amplification (mLAMP) method for the simultaneous detection of bovine Babesia parasites, J. Microbiol. Methods, 71, 281, 10.1016/j.mimet.2007.09.019

Parida, 2008, Loop mediated isothermal amplification (LAMP): A new generation of innovative gene amplification technique; perspectives in clinical diagnosis of infectious diseases, Rev. Med. Virol., 18, 407, 10.1002/rmv.593

Aonuma, 2009, Loop-mediated isothermal amplification applied to filarial parasites detection in the mosquito vectors: Dirofilaria immitis as a study model, Parasites Vectors, 2, 15, 10.1186/1756-3305-2-15

Mori, 2009, Loop-mediated isothermal amplification (LAMP): A rapid, accurate and cost-effective diagnostic method for infectious diseases, J. Infect. Chemother., 15, 62, 10.1007/s10156-009-0669-9

Ollerenshaw, 1959, A method of forecasting the incidence of fascioliasis in Anglesey, Vet. Rec., 71, 591

Cornell, 2005, Modelling nematode populations: 20 years of progress, Trends Parasitol., 21, 542, 10.1016/j.pt.2005.08.019

Fuentes, 2006, Remote sensing and climate data as a key for understanding fasciolosis transmission in the Andes: Review and update of an ongoing interdisciplinary project, Geospat. Health, 1, 59, 10.4081/gh.2006.281

Rose, 2011, Modelling the impact of climate change on spatial patterns of disease risk: Sheep blowfly strike by Lucilia sericata in Great Britain, Int. J. Parasitol., 41, 739, 10.1016/j.ijpara.2011.01.012

Biggeri, 2007, Multivariate spatially-structured variability of ovine helminth infections, Geospat. Health, 2, 97, 10.4081/gh.2007.258

Durr, P., and Gatrell, A. (2004). GIS and Spatial Analysis in Vet. Science, CABI Publishing.

Rinaldi, 2006, New insights into the application of geographical information systems and remote sensing in veterinary parasitology, Geospat. Health, 1, 33, 10.4081/gh.2006.279

Bergquist, 2010, Health research based on geospatial tools: A timely approach in a changing environment, J. Helminthol., 84, 1, 10.1017/S0022149X09990484

Geospatial health: Health applications in geospatial science. Available online:http://www.geospatialhealth.unina.it.

Morgan, 2004, Ruminating on complexity: Macroparasites of wildlife and livestock, Trends Ecol. Evol., 19, 181, 10.1016/j.tree.2004.01.011

Morgan, 2012, Climate and the epidemiology of gastrointestinal nematode infections of sheep in Europe, Vet. Parasitol., 189, 8, 10.1016/j.vetpar.2012.03.028

David, 2008, Back to the future: Developing hypotheses on the effects of climate change on ovine parasitic gastroenteritis from historical data, Vet. Parasitol., 158, 73, 10.1016/j.vetpar.2008.08.006

Smith, 1994, Modeling of parasite populations—Gastrointestinal nematode models, Vet. Parasitol., 54, 127, 10.1016/0304-4017(94)90087-6

Morgan, 2010, Variation in the hatching behaviour of Nematodirus battus: Polymorphic bet hedging?, Int. J. Parasitol., 40, 675, 10.1016/j.ijpara.2009.11.002

Kenyon, 2009, The role of targeted selective treatments in the development of refugia-based approaches to the control of gastrointestinal nematodes of small ruminants, Vet. Parasitol., 164, 3, 10.1016/j.vetpar.2009.04.015

Cooper, 2012, ProSafeBeef and anthelmintic drug residues-a case study in collaborative application of multi-analyte mass spectrometry to enhance consumer safety, Anal. Bioanal. Chem., 404, 1623, 10.1007/s00216-012-6310-2

Imperiale, 2011, Residual concentrations of the flukicidal compound triclabendazole in dairy cows’ milk and cheese, Food Addit. Contam. Part A Chem. Anal. Control Expo. Risk Assess., 28, 438, 10.1080/19440049.2010.551422

Greer, 2009, Development and field evaluation of a decision support model for anthelmintic treatments as part of a targeted selective treatment (TST) regime in lambs, Vet. Parasitol., 164, 12, 10.1016/j.vetpar.2009.04.017

Cringoli, 2009, Evaluation of targeted selective treatments in sheep in Italy: Effects on faecal worm egg count and milk production in four case studies, Vet. Parasitol., 164, 36, 10.1016/j.vetpar.2009.04.010

Gallidis, 2009, The use of targeted selective treatments against gastrointestinal nematodes in milking sheep and goats in Greece based on parasitological and performance criteria, Vet. Parasitol., 164, 53, 10.1016/j.vetpar.2009.04.011

Morrison, 2009, Targeted selective treatments for gastrointestinal nematodes in first-season grazing cattle based on mid-season daily weight gains, Vet. Parasitol., 164, 80, 10.1016/j.vetpar.2009.04.016

Leask, 2013, The effect of application of the FAMACHA© system on selected production parameters in sheep, Small Rumin. Res., 110, 1, 10.1016/j.smallrumres.2012.07.026

Gaba, 2012, Can efficient management of sheep gastro-intestinal nematodes be based on random treatment?, Vet. Parasitol., 190, 178, 10.1016/j.vetpar.2012.06.011

Terrill, 2012, Experiences with integrated concepts for the control of Haemonchus contortus in sheep and goats in the United States, Vet. Parasitol., 186, 28, 10.1016/j.vetpar.2011.11.043

Reynecke, 2011, Blueprint for an automated specific decision support system for countering anthelmintic resistance in Haemonchus spp. at farm level, Vet. Parasitol., 177, 212, 10.1016/j.vetpar.2009.10.025

Gauly, 2013, Future consequences and challenges for dairy cow production systems arising from climate change in Central Europe—A review, Animal, 7, 843, 10.1017/S1751731112002352