The Use of Anti-Ostertagia Ostertagi Antibodies in Milk to Study the Epidemiology and Impact on Production of Gastrointestinal-Nematode Infections in Dairy Cows

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The Use of Anti-Ostertagia Ostertagi Antibodies in Milk to Study the Epidemiology and Impact on Production of Gastrointestinal-Nematode Infections in Dairy Cows THE USE OF ANTI-OSTERTAGIA OSTERTAGI ANTIBODIES IN MILK TO STUDY THE EPIDEMIOLOGY AND IMPACT ON PRODUCTION OF GASTROINTESTINAL-NEMATODE INFECTIONS IN DAIRY COWS Proefschrift ter verkrijging van de graad van doctor in de diergeneeskundige wetenschappen aan de faculteit diergeneeskunde Universiteit Gent, 2007 door Johannes Charlier Promotoren Prof. dr. J. Vercruysse Prof. dr. E. Claerebout Vakgroep Virologie, Parasitologie en Immunologie Faculteit Diergeneeskunde, Universiteit Gent Salisburylaan 133, B-9820 Merelbeke Zonder de medewerking van velen had deze thesis nooit tot stand kunnen komen. Aan hen spreek ik hier mijn oprechte dank uit. In de eerste plaats aan mijn promotoren prof. dr. Jozef Vercruysse en prof. dr. Edwin Claerebout. Zij bedachten het idee van de melkantistoffen, vonden de nodige fondsen en stimuleerden mij vervolgens om eigen invalshoeken aan het onderzoek te geven. Zij stimuleerden zowel mijn wetenschappelijk (wat is interessant) als pragmatisch (wat is haalbaar) denken, gaven mij een brede kijk op veterinaire parasitologie, lazen en verbeterden ongebreideld mijn manuscripten en gaven mij de kans naar internationale congressen te gaan. Een even grote dankbetuiging wil ik richten aan prof. dr. Luc Duchateau. Hij stond me bij met de statistische analyses, de interpretatie van de data en het verbeteren van de manuscripten. Bovendien stimuleerde hij me zelf kennis over statistische data-analyse te vergaren en had hij regelmatig een originele invalshoek in de aanpak van het onderzoek. Aan de andere leden van de begeleidingscommissie, prof. dr. Ian Dohoo, dr. Harm Ploeger en prof. dr. Dirk Berkvens die het manuscript doornamen en een belangrijke bijdrage leverden tot het finale resultaat. I also want to thank prof. dr. Ian Dohoo for the assistance of his department when we started performing the ELISAs. Aan de firma Merial, voor het financieel ondersteunen van dit project. J’adresse mes remerciements tout particuliers à Jean-Marc Lalloz qui a marqué sa sympathie pour le projet dès le début. Sa vision des implications pratiques de ces études s’est confirmée au cours du temps. Sincere thanks as well to Andy Forbes, whose contribution in the many scientific discussions proved to be very valuable and helpful. Een woord van dank ook aan Piet De Roose voor de praktische en logistieke steun bij het opzetten van de behandelingsproef . Aan Roland Bossuyt en Jean-Marie Van Crombrugge van het Melkcontrolecentrum Vlaanderen. Zij waren steeds present op belangrijke organisatorische vergaderingen van de proeven en verleenden hun volledige medewerking bij het verzamelen van de melkstalen. Aan Etienne De Mûelenaere en Kim Cattoir van de Vlaamse Rundveeteelt Vereniging. Zij steunden ons project, stelden de productiegegevens ter beschikking en motiveerden de melkcontroleurs voor het uitvoeren van de enquête. Aan dr. Luc De Meulemeester die ons in contact bracht met het Melkcontrolecentrum Vlaanderen, de Vlaamse Rundveeteelt Vereniging, en de medewerkende dierenartsen. Bovendien hielp hij mee aan de organisatie van verschillende studies. Aan al mijn collega’s op het werk voor de hulp, gezellige koffiekletsen en uitstappen. Ze hielpen mij ook door mij op het einde “gerust” te laten en taken over te nemen zodat ik ongestoord verder kon werken. Een speciaal dankwoord aan Iris die me wegwijs maakte in de ELISA wereld, Dirk, Mieke, Rudy, Stijn en Gert voor de technische ondersteuning. Aan prof. dr. Christian Burvenich en dr. Frédéric Vangroenweghe die mee de mastitis-studie mogelijk maakten. Aan de dierenartsen Adelin De Vlieger, Rony De Weweire, Peter Dhont, Raf Ide, Hendrik Keerman, Pieter Passchyn, Sylvie Rys en Tom Van Hulle en aan de veehouders die allen geïnteresseerd hebben meegewerkt aan het onderzoek. Ik zou ook m’n verloofde Inge willen bedanken voor de vele keren dat ze toestond dat ik m’n tijd besteedde aan deze thesis en niet met haar. En tenslotte m’n ouders voor het mogelijk maken van mijn studies en de stille aanmoedigingen bij het maken van dit werk. Mijn moeder dank ik bovendien voor de mooie tekeningen op de omslag van de thesis. List of abbreviations AUC Area under the curve BL Bovine leukaemia BVD Bovine viral diarrhoea CCC Concordance correlation coefficient CI Confidence interval Cmax Maximal concentration DIM Days in milk DNA Deoxyribonucleic acid ELISA Enzyme-linked immunosorbent assay EPG Eggs per gram EU European Union FEC Faecal egg count FSG First-season grazing GI Gastrointestinal GIS Geographical information system IBR Infectious bovine rhinotracheitis Ig Immunoglobulin Inj. Injectable L1 First-stage larva L2 Second-stage larva L3 Third-stage larva L4 Fourth-stage larva LL Lower limit MAP Mycobacterium avium subspecies paratuberculosis MCC Milk Control Centre ML Macrocyclic lactone NC Negative control OD Optical density ODR Optical-density ratio PBST Phosphate-buffered saline with 0.05 % Tween 20 PC Positive control RS Remote sensing UL Upper limit V.R.V. Flemish Cattle Breeding Association Table of contents List of abbreviations 4 GENERAL INTRODUCTION 9 1. INTRODUCTION 10 2. GASTROINTESTINAL-NEMATODE SPECIES AND THEIR RELATIVE IMPORTANCE IN DAIRY CATTLE 10 3. LIFE CYCLE AND EPIDEMIOLOGY OF OSTERTAGIA OSTERTAGI 11 4. PATHOGENESIS AND PATHOLOGY OF OSTERTAGIOSIS 13 6. REFERENCES 16 CHAPTER 1 17 THE DIAGNOSIS, IMPACT ON PRODUCTION AND CONTROL OF GASTROINTESTINAL NEMATODES IN DAIRY CATTLE 17 1. INTRODUCTION 18 2. DIAGNOSIS 20 2.1. INTRODUCTION 20 2.2. FAECAL EXAMINATION 20 2.3. SERUM-PEPSINOGEN DETERMINATION 21 2.4. MEASUREMENT OF SPECIFIC ANTIBODIES 22 2.5. OTHER TECHNIQUES 25 3. IMPACT ON PRODUCTION 26 3.1. INTRODUCTION 26 3.2. EFFECT ON WEIGHT GAIN AND CARCASS QUALITY 27 3.3. EFFECT ON MILK PRODUCTION 28 3.4. EFFECT ON REPRODUCTIVE PERFORMANCE 31 3.5. EFFECT ON IMMUNITY 32 4. CONTROL 33 4.1. INTRODUCTION 33 4.2. ANTHELMINTICS 33 4.3. CONTROL METHODS 37 5. CONCLUSIONS 40 6. REFERENCES 41 OBJECTIVES 53 CHAPTER 2 55 ASSESSMENT OF THE REPEATABILITY OF A MILK OSTERTAGIA OSTERTAGI ELISA AND EFFECTS OF SAMPLE PREPARATION 55 1. INTRODUCTION 56 2. MATERIALS AND METHODS 56 2.1. MILK SAMPLES 56 2.2. ELISA 57 2.3. EVALUATION STUDIES 58 2.4. STATISTICAL ANALYSIS 59 3. RESULTS 61 3.1. BORDER EFFECTS 61 3.2. REPEATABILITY OVER REPLICATES, PLATES AND DAYS 61 3.3. EFFECT OF SAMPLE PREPARATION 64 4. DISCUSSION 64 5. CONCLUSION 67 6. REFERENCES 68 CHAPTER 3 71 THE EFFECT OF AN EXPERIMENTALLY INDUCED ACUTE MASTITIS ON THE TEST RESULTS OF AN OSTERTAGIA OSTERTAGI MILK ELISA 71 1. INTRODUCTION 72 2. MATERIALS AND METHODS 72 2.1. EXPERIMENTAL ANIMALS AND STUDY FACILITIES 72 2.2. INTRAMAMMARY INOCULATION PROCEDURE 73 2.3. SAMPLE COLLECTION 73 2.4. LABORATORY METHODS 73 2.5. TITRATION EXPERIMENT 74 2.6. STATISTICAL ANALYSIS 74 3. RESULTS 75 3.1. O. OSTERTAGI ODR AND IGG ODR 75 3.2. TITRATION EXPERIMENT 77 4. DISCUSSION 77 5. REFERENCES 79 CHAPTER 4 81 A SURVEY TO DETERMINE RELATIONSHIPS BETWEEN BULK-TANK MILK ANTIBODIES AGAINST OSTERTAGIA OSTERTAGI AND MILK-PRODUCTION PARAMETERS 81 1. INTRODUCTION 82 2. MATERIALS AND METHODS 83 2.1. SELECTION OF FARMS AND SAMPLE COLLECTION 83 2.2. COLLECTION OF FARM AND PRODUCTION DATA 83 2.3. LABORATORY METHODS 84 2.4. STATISTICAL ANALYSIS 85 3. RESULTS 86 3.1. ODR VALUES OF THE SAMPLED HERDS 86 3.2. FARM DATA 87 3.3. RELATIONSHIP BETWEEN ODR AND MILK YIELD 87 3.4. RELATIONSHIP BETWEEN ODR AND MILK-SOLIDS CONTENT 89 4. DISCUSSION 90 5. REFERENCES 94 CHAPTER 5 97 ASSOCIATIONS BETWEEN DAIRY HERD MANAGEMENT FACTORS AND BULK-TANK MILK ANTIBODY LEVELS AGAINST OSTERTAGIA OSTERTAGI 97 1. INTRODUCTION 98 2. MATERIALS AND METHODS 99 2.1. DAIRY FARMS AND SAMPLE COLLECTION 99 2.2. COLLECTION OF HERD INFORMATION 99 2.3. ELISA PROCEDURE 100 2.4. STATISTICAL ANALYSIS 100 3. RESULTS 104 4. DISCUSSION 106 5. REFERENCES 110 CHAPTER 6 113 PREDICTING MILK-PRODUCTION RESPONSES AFTER AN AUTUMN TREATMENT OF PASTURED DAIRY HERDS WITH EPRINOMECTIN 113 1. INTRODUCTION 114 2. MATERIALS AND METHODS 115 2.1. HERD SELECTION 115 2.2. TREATMENT PROTOCOL 115 2.3. SAMPLE COLLECTION AND ELISA-PROCEDURE 116 2.4. COLLECTION OF FARM DATA 116 2.5. STATISTICAL ANALYSIS 117 3. RESULTS 118 3.1. FARMS AND ANIMALS 118 3.2. ANTI-OSTERTAGIA ANTIBODY LEVELS 119 3.3. OVERALL TREATMENT EFFECT ON MILK YIELD 120 3.4. THE RELATION BETWEEN THE PRE-TREATMENT ANTI-O. OSTERTAGI ANTIBODY LEVEL IN THE BULK-TANK MILK AND THE TREATMENT EFFECT 121 4. DISCUSSION 121 5. CONCLUSIONS 124 6. REFERENCES 125 CHAPTER 7 127 GENERAL DISCUSSION: THE USE OF MILK ANTIBODIES TO EVALUATE PARASITE-ASSOCIATED PRODUCTION LOSSES IN DAIRY CATTLE 127 1. INTRODUCTION 128 2. THE PRACTICAL USE BY VETERINARIANS OF THE OSTERTAGIA ELISA ON BULK-TANK MILK 128 3. THE LIMITATIONS/ADVANTAGES OF BULK-TANK MILK VERSUS INDIVIDUAL MILK 130 4. THE INTEGRATION OF MONITORING GASTROINTESTINAL-NEMATODE INFECTIONS IN A BROADER DAIRY HEALTH CONTEXT 132 5. THE USE OF MILK ELISAS AND GEOGRAPHICAL INFORMATION SYSTEMS TO DETERMINE THE REGIONAL ECONOMIC IMPORTANCE OF PARASITIC DISEASES 134 6. CONCLUSION 135 7. REFERENCES 136 SUMMARY 141 SAMENVATTING 149 General introduction 10 General introduction ____________________________________________________________________________________________ 1. Introduction Infection of livestock with gastrointestinal (GI) parasitic nematodes is a major constraint on production worldwide. All grazing cattle are exposed to infection with these parasites resulting in economic losses (mainly due to reduced productivity and costs of anthelmintic treatments). Traditionally, infections with GI nematodes were considered to be mainly important in first-season grazing (FSG) calves. The effects of clinical disease in this age group have been clearly demonstrated and are well known to both farmers and practitioners. In contrast, infections with GI nematodes in older cattle were for a long time considered to be of no major importance because of the absence of clinical symptoms and the lower fecal egg counts usually found in these animals. However, recently 2 reviews have demonstrated that subclinical GI-nematode infections can impair milk yield (Gross et al., 1999; Sanchez et al., 2004).
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