A systematic review and meta-analysis of factors associated with anthelmintic resistance in sheep

Preventive Veterinary Medicine

Volumn 117, Issue 2, 2014, Pages 388-402

  Falzon, L C ^a   O'Neill, T J ^b   Menzies, P I ^c   Peregrine, A S ^c   Jones Bitton, A ^c   vanLeeuwen, J ^d   Mederos, A ^e  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF GUELPH   (Canada)

^d UNIVERSITY OF PRINCE EDWARD ISLAND   (Canada)

^e INSTITUTO NACIONAL DE INVESTIGACIÓN AGROPECUARIA INIA   (Uruguay)

Author keywords

Drench resistance; Evidence based recommendations; Gastro intestinal nematodes; Management practices; Qualitative and quantitative synthesis

Indexed keywords

ANTHELMINTIC AGENT;

ANIMAL; DRUG RESISTANCE; EVIDENCE BASED MEDICINE; GASTROINTESTINAL DISEASES; META ANALYSIS; NEMATODE; NEMATODE INFECTIONS; PARASITOLOGY; SHEEP; SHEEP DISEASES; VETERINARY;

ANIMALS; ANTHELMINTICS; DRUG RESISTANCE; EVIDENCE-BASED MEDICINE; GASTROINTESTINAL DISEASES; NEMATODA; NEMATODE INFECTIONS; SHEEP; SHEEP DISEASES;

EID: 84911443821     PISSN: 01675877     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.prevetmed.2014.07.003     Document Type: Article

References (116)

1. Abbott K.A., Taylor M.A., Stubbings L.A. Sustainable worm control strategies for sheep. A Technical Manual for Veterinary Surgeons and Advisers 2009, Sustainable Control of Parasites in Sheep (SCOPS), Leicestershire, United Kingdom, 51pp (printed by: Context Publications). Available from: 〈www.nationalsheep.org.uk〉. third ed.
2. Ancheta P.B., Dumilon R.A., Venturina V.M., Cerbito W.A., Dobson R.J., LeJambre L.F., Villar E.C., Gray G.D. Efficacy of benzimidazole anthelmintics in goats and sheep in the Philippines using a larval development assay. Vet. Parasitol. 2004, 120:107-121.
3. Barrere V., Falzon L.C., Shakya K.P., Menzies P.I., Peregrine A.S., Prichard R.K. Assessment of benzimidazole resistance in Haemonchus contortus in sheep flocks in Ontario, Canada: comparison of detection methods for drug resistance. Vet. Parasitol. 2013, 198:159-165.
4. Bartley D.J., Jackson E., Johnston K., Coop R.L., Mitchell G.B.B., Sales J., Jackson F. A survey of anthelmintic resistant nematode parasites in Scottish sheep flocks. Vet. Parasitol. 2003, 117:61-71.
5. Bartram D.J., Leathwick D.M., Taylor M.A., Geurden T., Maeder S.J. The role of combination anthelmintic formulations in the sustainable control of sheep nematodes. Vet. Parasitol. 2012, 186:151-158.
6. Belo V.S., Struchiner C.J., Werneck G.L., Barbosa D.S., de Oliveira R.B., Neto R.G.T., da Silva E.S. A systematic review and meta-analysis of the factors associated with Leishmania infantum infection in dogs in Brazil. Vet. Parasitol. 2013, 195:1-13.
7. Borenstein M., Hedges L.V., Higgins J.P.T., Rothstein H.R. Introduction to Meta-Analysis 2009, John Wiley & Sons Ltd., West Sussex, United Kingdom, 421pp. first ed.
8. Cabaret J., Benoit M., Laignel G., Nicourt C. Current management of farms and internal parasites by conventional and organic meat sheep French farmers and acceptance of targeted selective treatments. Vet. Parasitol. 2009, 164:21-29.
9. Calvete C., Calavia R., Ferrer L.M., Ramos J.J., Lacasta D., Uriarte J. Management and environmental factors related to benzimidazole resistance in sheep nematodes in Northeast Spain. Vet. Parasitol. 2012, 184:193-203.
10. Cawthorne R.J.G., Cheong F.H. Prevalence of anthelmintic resistant nematodes in sheep in south-east England. Vet. Rec. 1984, 114:562-564.
11. Chartier C., Pors I., Hubert J., Rocheteau D., Benoit C., Bernard N. Prevalence of anthelmintic resistant nematodes in sheep and goats in Western France. Small Ruminant Res. 1998, 29:33-41.
12. Clarke M. Interpreting the results of systematic reviews. Semin. Hematol. 2008, 45:176-180.
13. Cobo E., Cortés J., Ribera J.M., Cardellach F., Selva-O'Callaghan A., Kostov B., García L., Cirugeda L., Altman D.G., González J.A., Sànchez J.A., Miras F., Urrutia A., Fonollosa V., Rey-Joly C., Vilardell M. Effect of using reporting guidelines during peer review on quality of final manuscripts submitted to a biomedical journal: masked randomised trial. Br. Med. J. 2011, 343:d6783. 10.1136/bmj.d6783.
14. Cohen J. A coefficient of agreement for nominal scales. Educ. Psychol. Meas. 1960, 20:37-46.
15. Coles G.C. The future of veterinary parasitology. Vet. Parasitol. 2001, 98:31-39.
16. Coles G.C., Jackson F., Pomroy W.E., Prichard R.K., von Samson-Himmelstjerna G., Silvestre A., Taylor M.A., Vercruysse J. The detection of anthelmintic resistance in nematodes of veterinary importance. Vet. Parasitol. 2006, 136:167-185.
17. Corba J., Varady M., Konigova A. Anthelmintic resistance: the actual situation in Slovakia. Slov. Vet. Res. 2001, 26:145-150.
18. Craven J., Bjorn H., Barnes E.H., Henriksen S.A., Nansen P. A comparison of in vitro tests and a faecal egg count reduction test in detecting anthelmintic resistance in horse strongyles. Vet. Parasitol. 1999, 85:49-59.
19. DerSimonian R., Laird N. Meta-analysis in clinical trials. Controlled Clin. Trials 1986, 3:177-188.
20. Díez-Baños P., Pedreira J., Sánchez-Andrade R., Francisco I., Suárez J.L., Díaz P., Panadero R., Arias M., Painceira A., Paz-Silva A., Morrondo P. Field evaluation for anthelmintic-resistance ovine gastrointestinal nematodes by in vitro and in vivo assays. J. Parasitol. 2008, 94:925-928.
21. Dobson R.J., Besier R.B., Barnes E.H., Love S.C.J., Vizard A., Bell K., Le Jambre L.F. Principles for the use of macrocyclic lactones to minimise selection for resistance. Aust. Vet. J. 2001, 79:756-761.
22. Downes M.J., Dean R.S., Stavisky J.H., Adams V.J., Grindlay D.J.C., Brennan M.L. Methods used to estimate the size of the owned cat and dog populations: a systematic review. BMC Vet. Res. 2013, 9:121. 10.1186/1746-6148-9-121.
23. Downs S.H., Black N. The feasibility of creating a checklist for the assessment of the methodological quality both of randomised and non-randomised studies of health care interventions. J. Epidemiol. Community Health 1998, 52:377-384.
24. Echevarria F., Borba M.F.S., Pinheiro A.C., Waller P.J., Hansen J.W. The prevalence of anthelmintic resistance in nematode parasites of sheep in Southern Latin America: Brazil. Vet. Parasitol. 1996, 62:199-206.
25. Eddi C., Caracostantogolo J., Pena M., Schapiro J., Marangunich L., Waller P.J., Hansen J.W. The prevalence of anthelmintic resistance in nematode parasites of sheep in Southern Latin America: Argentina. Vet. Parasitol. 1996, 62:189-197.
26. Falzon L.C., Menzies P.I., Shakya K.P., Jones-Bitton A., Vanleeuwen J., Avula J., Stewart H., Jansen J.T., Taylor M.A., Learmount J., Peregrine A.S. Anthelmintic resistance in sheep flocks in Ontario, Canada. Vet. Parasitol. 2013, 193:150-162.
27. Gholamian A., Eslami A., Nabavi L., Rasekh A.R., Galedari H. A field survey on resistance to albendazole in gastrointestinal nematodes of sheep in Khozestan province of Iran. J. Vet. Res. 2007, 62:45-51.
28. Greenhalgh T. Papers that summarise other papers (systematic reviews and meta-analyses). Br. Med. J. 1997, 315:672-675.
29. Grégoire G., Derderian F., Le Lorier J. Selecting the language of the publications included in a meta-analysis: is there a Tower of Babel bias?. J. Clin. Epidemiol. 1995, 48:159-163.
30. Harbour R., Miller J. A new system for grading recommendations in evidence based guidelines. Br. Med. J. 2001, 323:334-336.
31. Higgins J.P.T. Commentary: heterogeneity in meta-analysis should be expected and appropriately quantified. Int. J. Epidemiol. 2008, 37:1158-1160.
32. Higgins J.P.T., Green S. Cochrane Handbook for Systematic Reviews of Interventions, Version 5.1.0 (updated: March 2011) 2011, The Cochrane Collaboration, 〈www.cochrane-handbook.org〉 (accessed 1 October 2013).
33. Higgins J.P.T., Altman D.G., Gotzche P.C., Jüni P., Moher D., Oxman A.D., Savovic J., Schulz K.F., Weeks L., Sterne J.A.C. The Cochrane Collaboration's tool for assessing risk of bias in randomized trials. Br. Med. J. 2011, 343:d5928. 10.1136/bmj.d5928.
34. Higgins J.P.T., Thompson S.G., Deeks J.J., Altman D.G. Measuring inconsistency in meta-analyses. Br. Med. J. 2003, 327:557-560.
35. Hootman J.M., Driban J.B., Sitler M.R., Harris K.P., Cattano N.M. Reliability and validity of three quality rating instruments for systematic reviews of observational studies. Res. Synth. Methods 2011, 2:110-118.
36. Hughes P.L., Dowling A.F., Callinan Resistance to macrocyclic lactone anthelmintics and associated risk factors on sheep farms in the lower North Island of New Zealand. N.Z. Vet. J. 2007, 55:177-183.
37. Ioannidis J., Patsopoulos N., Rothstein H. Reasons or excuses for avoiding meta-analysis in forest plots. Br. Med. J. 2008, 336:1413-1415.
38. Jackson F., Coop R.L. The development of anthelmintic resistance in sheep nematodes. Parasitology 2000, 120:S95-S107.
39. Kaplan R.M., Vidyashankar A.N. An inconvenient truth: global worming and anthelmintic resistance. Vet. Parasitol. 2012, 186:70-78.
40. Kenyon F., Greer A.W., Coles G.C., Cringoli G., Papadopoulos E., Cabaret J., Berrag B., Varady M., Van Wyk J.A., Thomas E., Vercruysse J., Jackson F. The role of targeted selective treatments in the development of refugia-based approaches to the control of gastrointestinal nematodes of small ruminants. Vet. Parasitol. 2009, 164:3-11.
41. Kettle P.R., Vlassoff A., Lukies J.M., Ayling J.M., McMurtry L.W. A survey of nematode control measures used by sheep farmers and of anthelmintic resistance on their farms Part 1. North Island and the Nelson region of South Island. N.Z. Vet. J. 1981, 29:81-83.
42. Kettle P.R., Vlassoff A., Ayling J.M., McMurtry L.W., Smith S.J., Watson A.J. A survey of nematode control measures used by sheep farmers and of anthelmintic resistance on their farms Part 2. South Island excluding the Nelson region. N.Z. Vet. J. 1982, 30:79-81.
43. Kim S.Y., Park J.E., Lee Y.J., Seo H.-J., Sheen S.-S., Hahn S., Jang B.-H., Son H.-J. Testing a tool for assessing the risk of bias for nonrandomized studies showed moderate reliability and promising validity. J. Clin. Epidemiol. 2013, 66:408-414.
44. Knox M.R., Besier R.B., Le Jambre L.F., Kaplan R.M., Torres-Acosta J.F.J., Miller J., Sutherland I. Novel approaches for the control of helminth parasites of livestock VI: Summary of discussions and conclusions. Vet. Parasitol. 2012, 186:143-149.
45. Kumar R., Yadav C.L. Prevalence of fenbendazole resistance in ovine nematodes in north West India. Trop. Anim. Health Prod. 1994, 26:230-234.
46. Lawrence K.E., Rhodes A.P., Leathwick D.M., Heuer C., Pomroy W.E., West D.M., Waghorn T.S., Moffat J.R. Farm management practices associated with macrocyclic lactone resistance on sheep farms in New Zealand. N.Z. Vet. J. 2006, 54:283-288.
47. Le Jambre L.F., Dobson R.J., Lenane I.J., Barnes E.H. Selection for anthelmintic resistance by macrocyclic lactones in Haemonchus contortus. Int. J. Parasitol. 1999, 29:1101-1111.
48. Lean I.J., Rabiee A.R., Duffield T.F., Dohoo I.R. Invited review: use of meta-analysis in animal health and reproduction: methods and application. J. Dairy Sci. 2009, 92:3545-3565.
49. Learmount J., Taylor M.A., Bartram D.J. A computer simulation study to evaluate resistance development with a derquantel-abamectin combination on UK sheep farms. Vet. Parasitol. 2012, 187:244-253.
50. Leathwick D.M., Vlassoff A., Barlow N.D. A model for nematodiasis in New Zealand lambs: the effect of drenching regime and grazing management on the development of anthelmintic resistance. Int. J. Parasitol. 1995, 25:1479-1490.
51. Leathwick D.M., Miller C.M., Atkinson D.S., Haack N.A., Alexander R.A., Oliver A.-M., Waghorn T.S., Potter J.F., Sutherland I.A. Drenching adult ewes: implications of anthelmintic treatments pre- and post-lambing on the development of anthelmintic resistance. N.Z. Vet. J. 2006, 54:297-304.
52. Leathwick D.M., Miller C.M., Atkinson D.S., Haack N.A., Waghorn T.S., Oliver A.-M. Managing anthelmintic resistance: untreated adult ewes as a source of unselected parasites, and their role in reducing parasite populations. N.Z. Vet. J. 2008, 56:184-195.
53. Leathwick D.M., Hosking B.C., Bisset S.A., McKay C.H. Managing anthelmintic resistance: is it feasible in New Zealand to delay the emergence of resistance to a new anthelmintic class?. N.Z. Vet. J. 2009, 57:203-207.
54. Leathwick D.M., Waghorn T.S., Miller C.M., Candy P.M., Oliver A.-M.B. Managing anthelmintic resistance-use of a combination anthelmintic and leaving some lambs untreated to slow the development of resistance to ivermectin. Vet. Parasitol. 2012, 187:285-294.
55. Leignel V., Silvestre A., Humbert J.F., Cabaret J. Alternation of anthelmintic treatments: a molecular evaluation for benzimidazole resistance in nematodes. Vet. Parasitol. 2010, 172:80-88.
56. Maingi N., Bjørn H., Dangolla A. The relationship between faecal egg count reduction and the lethal dose 50% in the egg hatch assay and larval development assay. Vet. Parasitol. 1998, 77:133-145.
57. Maroto R., Jimenez A.E., Romero J.J., De Oliveira J.B., Hernandez J. First report of anthelmintic resistance in gastrointestinal nematodes of sheep from Costa Rica. Vet. Med. Int. 2011, 1-4. 10.4061/2011/145312.
58. Martin P.J. Selection for thiabendazole resistance in Ostertagia spp. by low efficiency anthelmintic treatment. Int. J. Parasitol. 1989, 19:317-325.
59. Martin P.J., Anderson N., Jarrett R.G., Brown T.H., Ford G.E. Effects of a preventive and suppressive control scheme on the development of thiabendazole-resistance in Ostertagia spp. Aust. Vet. J. 1982, 58:185-190.
60. Martin P.J., Anderson N., Lwin T., Nelson G., Morgan T.E. The association between frequency of thiabendazole treatment and the development of resistance in field isolates of Ostertagia spp. of sheep. Int. J. Parasitol. 1984, 14:177-181.
61. Martínez-Valladares M., Martínez-Pérez J.M., Robles-Pérez D., Cordero-Pérez C., Famularo M.R., Fernández-Pato N., Castãnón-Ordónez L., Rojo-Vázquez F.A. The present status of anthelmintic resistance in gastrointestinal nematode infections of sheep in the northwest of Spain by in vivo and in vitro techniques. Vet. Parasitol. 2013, 191:177-181.
62. McGovern D.P.B., Valori R.M., Summerskill W.S.M., Levi M. Hierarchy of evidence. Evidence-based Medicine 2001, 14-17. BIOS Scientific Publishers, Texas, USA.
63. Mederos A., Waddell L., Sánchez J., Kelton D., Peregrine A.S., Menzies P., VanLeeuwen J., Rajic A. A systematic review-meta-analysis of primary research investigating the effect of selected alternative treatments on gastrointestinal nematodes in sheep under field conditions. Prev. Vet. Med. 2012, 104:1-14.
64. Menzies P. Handbook for the Control of Internal Parasites of Sheep 2012, Available from: 〈http://www.uoguelph.ca/~pmenzies/PDF/Handbook_Control_Internal_Parasites_Sheep_PMenzies.pdf〉 (accessed: 15th November, 2013).
65. Mitchell E.S.E., Hunt K.R., Wood R., McLean B. Anthelmintic resistance on sheep farms in Wales. Vet. Rec. 2010, 166:650-652.
66. Moayyedi P. Evidence-based medicine-the emperor's new clothes?. Am. J. Gastroenterol. 2008, 103:2965-2971.
67. Moher D., Liberati A., Tetzlaff J., Altman D.G. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA Statement. Int. J. Surg. 2010, 8:336-341. PRISMA Group.
68. Morgan E.R. The 125-year life cycle of parasite control. Vet. Rec. 2013, 173:89-91.
69. Morgan E.R., Coles G.C. Nematode control practices on sheep farms following an information campaign. Vet. Rec. 2010, 166:301-303.
70. Nari A., Salles J., Gil A., Waller P.J., Hansen J.W. The prevalence of anthelmintic resistance in nematode parasites of sheep in Southern Latin America: Uruguay. Vet. Parasitol. 1996, 62:213-222.
71. Niciura S.C.M., Verissimo C.J., Gromboni J.G.G., Rocha M.I.P., de Mello S.S., Barbosa C.M.P., Chiebao D.P., Cardoso D., Silva G.S., Otsuk I.P., Pereira J.R., Ambrosio L.A., Nardon R.F., Ueno T.E.H., Molento M.B. F200Y polymorphism in the β-tubulin gene in field isolates of Haemonchus contortus and risk factors of sheep flock management practices related to anthelmintic resistance. Vet. Parasitol. 2012, 190:608-612.
72. O'Connor A.M., Sargeant J.M., Gardner I.A., Dickson J.S., Torrence M.E., Dewey C.E., Dohoo I.R., Evans R.B., Gray J.T., Greiner M., Keefe G., Lefebvre S.L., Morley P.S., Ramirez A., Sischo W., Smith D.R., Snedeker K., Sofos J., Ward M.P., Wills R. The REFLECT statement: methods and processes of creating Reporting Guidelines for randomized controlled trials for livestock and food safety. Prev. Vet. Med. 2010, 93:11-18.
73. O'Neill T.J., Sargeant J.M., Poljak Z. The Effectiveness of Coxiella burnetti vaccines in occupationally exposed populations: a systematic review and meta-analysis. Zoonoses Public Health 2013, 10.1111/zph.12054.
74. Papadopoulos E., Gallidis E., Ptochos S. Anthelmintic resistance in sheep in Europe: a selected review. Vet. Parasitol. 2012, 189:85-88.
75. Petrie A., Watson P. Statistics for Veterinary and Animal Science 2013, John-Wiley and Sons Inc., United Kingdom, 412pp. third ed.
76. Praslicka J., Varady M., Corba J. Prevalence of resistant nematodes on sheep and goat farms in Slovakia. Slov. Vet. Res. 1994, 19:115-119.
77. Prichard R.K., Hall C.A., Kelly J.D., Martin I.C.A., Donald A.D. The problem of anthelmintic resistance in nematodes. Aust. Vet. J. 1980, 56:239-250.
78. Rendell D.K., Rentsch T.E., Smith J.M., Chandler D.S., Callinan A.P.L. Evidence that moxidectin is a greater risk factor than ivermectin in the development of resistance to macrocyclic lactones by Ostertagia spp. in sheep in south eastern Australia. N.Z. Vet. J. 2006, 54:313-317.
79. Sangster N.C. Anthelmintic resistance: past, present and future. Int. J. Parasitol. 1999, 29:115-124.
80. Sangster N.C., Gill J. Pharmacology of anthelmintic resistance. Parasitol. Today 1999, 15:141-146.
81. Sargeant J.M., Rajic A., Read S., Ohlsson A. The process of systematic review and its application in agri-food public health. Prev. Vet. Med. 2006, 75:141-151.
82. Sargeant J.M., Elgie R., Valour J., Saint-Onge J., Thompson A., Macynuk P., Snedeker K. Methodological quality and completeness of reporting in clinical trials conducted in livestock species. Prev. Vet. Med. 2009, 91:107-115.
83. Sargison N.D. Pharmaceutical control of endoparasitic helminth infections in sheep. Vet. Clin. Food Anim. 2011, 27:139-156.
84. Sargison N.D., Jackson F., Bartley D.J., Wilson D.J., Stenhouse L.H., Penny C.D. Observations on the emergence of multiple anthelmintic resistance in sheep flocks in the south-east of Scotland. Vet. Parasitol. 2007, 145:65-76.
85. Sargison N.D., Scott P.R., Wilson D.J., Macrae A.I., Penny C.D. Teladorsagia circumcincta resistance to moxidectin and multiple anthelmintic groups in ewes following use of the persistent drug before lambing. Vet. Rec. 2010, 167:523-527.
86. Schoenfeld P.S. EBM: an invaluable tool for medical practice. Am. J. Gastroenterol. 2008, 103:2965-2971.
87. Schulz K.F., Grimes D.A. Allocation concealment in randomised trials: defending against deciphering. Lancet 2002, 359:614-618.
88. Scott I., Pomroy W.E., Kenyon P.R., Smith G., Adlington B., Moss A. Lack of efficacy of monepantel against Teladorsagia circumcincta and Trichostrongylus colubriformis. Vet. Parasitol. 2013, 196:166-171.
89. Sczesny-Moraes E.A., Bianchin I., da Silva K.F., Catto J.B., Honer M.R., Paiva F. Resistência anti-helmíntica de nematóides gastrintestinais em ovinos, Mato Grosso do Sul. Pesq. Vet. Bras. 2010, 30:229-236.
90. Senn S.J. Overstating the evidence-double counting in meta-analysis and related problems. BMC Med. Res. Methodol. 2009, 10.1186/1471-2288-9-10.
91. Stear M.J., Singleton D., Matthews L. An evolutionary perspective on gastrointestinal nematodes of sheep. J. Helminthol. 2011, 85:113-120.
92. Stroup D.F., Berlin J.A., Morton S.C., Olkin I., Williamson G.D., Rennie D., Moher D., Becker B.J., Sipe T.A., Thacker S.B. Meta-analysis of observational studies in epidemiology. J. Am. Med. Assoc. 2000, 283:2008-2012.
93. Sustainable Worm Management Helminth Discussion Group initiated by the Department of Veterinary Tropical Diseases 2002, Faculty of Veterinary Science, University of Pretoria and Onderstepoort Veterinary Institute, under the auspices of and funded principally by Food and Agricultural Organization (FAO), 59pp.
94. Suter R.J., Besier R.B., Perkins N.R., Robertson I.D., Chapman H.M. Sheep-farm risk factors for ivermectin resistance in Ostertagia circumcincta in Western Australia. Prev. Vet. Med. 2004, 63:257-269.
95. Suter R.J., McKinnon E.J., Perkins N.R., Besier R.B. The effective life of ivermectin on Western Australian sheep farms-a survival analysis. Prev. Vet. Med. 2005, 72:311-322.
96. Sutherland I., Scott I. Gastrointestinal Nematodes of Sheep and Cattle. Biology and Control 2010, 1-60. John Wiley and Sons Ltd., West Sussex, UK.
97. Sutherland I.A., Brown A.E., Leathwick D.M. Selection for drug-resistant nematodes during and following extended exposure to anthelmintic. Parasitology 2000, 121:217-226.
98. Swarnkar C.P., Singh D. Worm-control practices, anthelmintic use and its implication on anthelmintic resistance in gastrointestinal nematodes of sheep in Rajasthan. Indian J. Anim. Sci. 2010, 80:593-600.
99. Taylor M.A. Emerging parasitic diseases of sheep. Vet. Parasitol. 2012, 189:2-7.
100. Taylor M.A., Hunt K.R., Goodyear K.L. Anthelmintic resistance detection methods. Vet. Parasitol. 2002, 103:183-194.
101. Torres-Acosta J.F.J., Mendoza-de-Gives P., Aguilar-Caballero A.J., Cuéllar-Ordaz Anthelmintic resistance in sheep farms: update of the situation in the American continent. Vet. Parasitol. 2012, 189:89-96.
102. Use of Drug Combinations FAO-University of Pretoria Electronic Conference 2007, Use of Drug Combinations, 52pp.
103. van Wyk J. Refugia-overlooked as perhaps the most potent factor concerning the development of anthelmintic resistance. Onderstepoort J. Vet. Res. 2001, 68:55-67.
104. van Wyk J.A., Stenson M.O., Van der Merwe J.S., Vorster R.J., Viljoen P.G. Anthelmintic resistance in South Africa: surveys indicate an extremely serious situation in sheep and goat farming. Onderstepoort J. Vet. Res. 1999, 66:273-284.
105. van Wyk J.A., Hoste H., Kaplan R.M., Besier R.B. Targeted selective treatment for worm management-how do we sell rational programs to farmers?. Vet. Parasitol. 2006, 139:336-346.
106. Vandenbroucke J.P., von Elm E., Altman D.G., Gøtzsche P.C., Mulrow C.D., Pocock S.T., Poole C., Schlesselman J.J., Egger M. Strengthening the reporting of observational studies in epidemiology (STROBE). Epidemiology 2007, 18:805-835.
107. Verissimo C.J., Niciura S.C., Alberti A.L.L., Rodrigues C.F.C., Barbosa C.M.P., Chiebao D.P., Cardoso D., da Silva G.S., Pereira J.R., Margatho L.F.F., da Costa R.L.D., Nardon R.F., Ueno T.E.H., Curci V.C.L.M., Molento M.B. Multidrug and multispecies resistance in sheep flocks from Sao Paulo state, Brazil. Vet. Parasitol. 2012, 187:209-216.
108. Viera A.J. Odds ratios and risk ratios: what's the difference and why does it matter?. South. Med. J. 2008, 101:731-734.
109. Voigt K., Scheuerle M., Hamel D. Triple anthelmintic resistance in Trichostrongylus spp. in a German sheep flock. Small Ruminant Res. 2012, 106:30-32.
110. Waghorn T.S., Leathwick D.M., Rhodes A.P., Lawrence K.E., Jackson R., Pomroy W.E., West D.M., Moffat J.R. Prevalence of anthelmintic resistance on sheep farms in New Zealand. N.Z. Vet. J. 2006, 54:271-277.
111. Waghorn T.S., Leathwick D.M., Miller C.M., Atkinson D.S. Brave or gullible: testing the concept that leaving susceptible parasites in refugia will slow the development of anthelmintic resistance. N.Z. Vet. J. 2008, 56:158-163.
112. Waghorn T.S., Miller C.M., Oliver A.-M.B., Leathwick D.M. Drench-and-shift is a high-risk practice in the absence of refugia. N.Z. Vet. J. 2009, 57:359-363.
113. Waller P.J., Donald A.D., Dobson R.J., Lacey E., Hennessy D.R., Allerton G.R., Prichard R.K. Changes in anthelmintic resistance status of Haemonchus contortus and Trichostrongylus colubriformis exposed to different anthelmintic selection pressures in grazing sheep. Int. J. Parasitol. 1989, 19:99-110.
114. Wells G.A., Shea B., O'Connell D., Peterson J., Welch W., Losos M., Tugwell P. The Newcastle-Ottawa Scale (NOS) for Assessing the Quality of Nonrandomised Studies in Meta-analyses 2009, Available at: 〈http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp〉 (accessed: 15th November 2013).
115. Zajac A.M. Gastrointestinal nematodes of small ruminants: life cycle, anthelmintics, and diagnosis. Vet. Clin. Food Anim. 2006, 22:529-541.
116. Zhang J., Yu K.F. What's the relative risk? A method of correcting the odds ratio in cohort studies of common outcomes. J. Am. Med. Assoc. 1998, 280:1690-1691.