158,99 €
Fish farming, in seawater and in freshwater, in cages, tanks or ponds, makes an ever-increasing and significant contribution to the production of aquatic food in many regions of the world. During the last few decades there has been significant progress and expansion in the aquaculture sector, characterized by intensified production and the exploitation of many new species.
Aquaculture must be a sustainable bio-production, environmentally as well as economically. Disease prevention in order to reduce losses, and the use of antimicrobials is crucial in this perspective. Vaccination has, in a few years, become the most important method for disease prevention in aquaculture, and effective prophylaxis based on stimulation of the immune system of the fish is essential for further development of the industry.
This book provides general information about disease prevention in fish by vaccination, as well as specific descriptions of the correct use of vaccines against the most important bacterial and viral infectious diseases of aquatic animals. The book is written by some of the world’s leading experts in the subject, drawn from many countries where aquaculture is a significant and expanding part of the economy.
Fish Vaccination is an encyclopedia of fish vaccinology for every present and future aquaculturist. Professionals in the aquaculture sector, including fish veterinarians and fish biologists, within the industry, in scientific institutions and regulatory authorities will all find a huge wealth of commercially important knowledge within this book. Libraries in all universities where aquaculture, biological and veterinary sciences are studied and taught should have copies of this important book on their shelves.
Sie lesen das E-Book in den Legimi-Apps auf:
Seitenzahl: 1004
Veröffentlichungsjahr: 2014
Cover
Title Page
Copyright
Contributors
Preface
Chapter 1: The History of Fish Vaccination
Abstract
1.1 Introduction
1.2 Aquaculture
1.3 Immunology
1.4 Disease Prevention
1.5 Scientific Production – Reviews and Conferences
1.6 Successes and Failures
1.7 The Pioneers
1.8 Concluding Remarks
References
Chapter 2: Vaccination as a Preventive Measure
Abstract
2.1 Introduction
2.2 Biosecurity and Vaccination
2.3 Use of Vaccination in Aquaculture
2.4 Vaccination Against Different Diseases
2.5 Herd Immunity
2.6 Economic Considerations
2.7 Risk Assessment
2.8 The Market for Fish Vaccines
References
Chapter 3: Non-replicating Vaccines
Abstract
3.1 Introduction
3.2 Classification
3.3 Inactivated Vaccines – Methods of Inactivation
3.4 Evaluation of Inactivation Efficacy
3.5 Measures of Efficacy for Inactivated Vaccines
3.6 Mechanisms of Vaccine Protection
3.7 Antibodies as Correlates of Protective Immunity
3.8 Antigen Dose as Correlate of Protective Immunity
References
Chapter 4: Replicating Vaccines
Abstract
4.1 Introduction
4.2 Attenuation Strategies – Bacterial Vaccines
4.3 Attenuation Strategies – Viral Vaccines
4.4 Induction of Immunity
4.5 Vaccine Delivery
4.6 Vaccine Safety Considerations
4.7 Acknowledgement
References
Chapter 5: DNA Vaccines
Abstract
5.1 Introduction
5.2 Comparison of DNA Vaccines with Conventional Inactivated Products: Advantages and Disadvantages
5.3 DNA Vaccines for Veterinary Use
5.4 Biosecurity and Regulatory Considerations
References
Chapter 6: Mucosal Vaccination of Fish
Abstract
6.1 Introduction
6.2 History of “Mucosal” Vaccination
6.3 Mucosal versus Systemic Immunity in Fish
6.4 Immersion Vaccination
6.5 Oral Vaccination
6.6 Perspectives
References
Chapter 7: Adjuvants in Fish Vaccines
Abstract
7.1 Introduction
7.2 Vaccine Formulations
7.3 Principles of Adjuvant Actions
7.4 Antigenic Component
7.5 Adjuvants
7.6 Antigen Delivery Systems
7.7 Delivery Vehicles
7.8 Emulsion Vaccines
7.9 Biodegradable Particulate Delivery Systems
7.10 Fusion Protein Delivery System
7.11 Immunomodulators
7.12 Stabilizers
7.13 Concluding Remarks and Perspectives
7.14 Acknowledgements
References
Chapter 8: The Innate Immune Response in Fish
Abstract
8.1 Introduction
8.2 Innate Immunity: A
Sensing
and an
Effector
Arm
8.3 Professional Phagocytes: The Macrophages and the Neutrophilic Granulocytes
8.4 Natural Killer (NK)-Like Cells
8.5 The Sensing Arm of Innate Immunity
8.6 TLRs are the Best Studied PRRS in Fish
8.7 NOD-Like and RIG-I Receptors are Found in Fish
8.8 Lectins are Multifunctional Sensor Molecules for Carbohydrate Ligands
8.9 PRRs AND THE INDUCTION OF IMMUNITY
8.10 Cytokines in Innate Immunity
8.11 Interferons
8.12 The Complement System
8.13 Concluding Remarks and Perspectives
References
Chapter 9: The Adaptive Immune Response in Fish
Abstract
9.1 Introduction
9.2 Lymphocytes are the Key Cells of the Adaptive Immune System
9.3 Antigen Trapping and Activation of the Lymphocytes
9.4 Antigen Presenting Cells (APCS) of Myeloid Origin
9.5 Immunoglobulins and B Lymphocytes
9.6 T Lymphocytes
9.7 Cytotoxic T-Cells
9.8 Helper T-Cells
References
Chapter 10: Development, Production and Control of Fish Vaccines
Abstract
10.1 Introduction
10.2 Manufacturing License
10.3 Vaccine Development
10.4 Development of Tests
10.5 Transfers
10.6 Manufacturing
References
Chapter 11: Legal Requirements and Authorization of Fish Vaccines
Abstract
11.1 Introduction
11.2 Manufacturer Authorization
11.3 Food Safety – Maximum Residue Limits
11.4 Genetically Modified Organisms
11.5 DNA Vaccines
11.6 Prohibition of Use of Certain Vaccines
11.7 Use of Vaccines that are not Authorized
11.8 Autogenous Vaccines
11.9 Regional Rules and Competent Authorities
11.10 The European Union and Connected EEA Countries
11.11 United States of America
11.12 Japan
11.13 Other Relevant Organizations: OIE, FAO, WHO
References
Chapter 12: Vaccination Strategies and Procedures
Abstract
12.1 Introduction
12.2 Timing of Vaccination
12.3 Water Temperature
12.4 Size of Fish
12.5 Vaccination Methods
12.6 Time for Protection to Develop – Duration of Protection
12.7 Booster Vaccination
12.8 Vaccination Economy
References
Chapter 13: Side-Effects of Vaccination
Abstract
13.1 Introduction
13.2 Acute Side-Effects
13.3 Chronic Side-Effects
13.4 Injection Site Reactions
13.5 Extensive Abdominal Lesions
13.6 Lesions in Other Organs
13.7 Skeletal Lesions
13.8 Autoimmunity
13.9 Lesions in Non-Salmonid Species
References
Chapter 14: Future Fish Vaccinology
Abstract
14.1 Molecular Technologies
14.2 Recombinant Vaccines
14.3 Marker Vaccines
14.4 Mucosal Vaccination
14.5 Vaccines Against Parasitic Diseases
14.6 Vaccines for Controlling Reproduction
14.7 Improved Formulations
14.8 Immunomodulation
14.9 Cytokines and DAMPS (Danger-Associated Molecular Pattern) as Adjuvants
14.10 Concluding Remarks
References
Chapter 15: Vaccination against Vibriosis
Abstract
15.1 Vibriosis
15.2 Occurrence and Significance
15.3 Etiology
15.4 Pathogenesis
15.5 Vaccines
15.6 Vaccination Procedures
15.7 Vaccine Effect
15.8 Side-Effects
15.9 Regulations
References
Chapter 16: Vaccination against Furunculosis
Abstract
16.1 Introduction
16.2 Occurrence and Significance
16.3 Etiology
16.4 Pathogenesis and Virulence
16.5 Antigens
16.6 Vaccines
16.7 Vaccination Procedures
16.8 Effects
16.9 Side-Effects
16.10 Vaccination Against Atypical Furunculosis
16.11 Legal Aspects and Regulations
References
Chapter 17: Vaccination against Photobacteriosis
Abstract
17.1 Occurrence and Significance
17.2 Etiology
17.3 Pathogenesis
17.4 Vaccines
17.5 Vaccination Procedures
17.6 Effect
17.7 Side-Effects
17.8 Regulations
References
Chapter 18: Vaccination against Enteric Septicemia of Catfish
Abstract
18.1 Significance
18.2 Occurrence
18.3 Etiology
18.4 Pathogenesis
18.5 Virulence Factors
18.6 Vaccines and Immunity
18.7 Regulations (US)
18.8 Vaccination Practices
References
Chapter 19: Vaccination against Yersiniosis
Abstract
19.1 Yersiniosis
19.2 Occurrence and Significance
19.3 Etiology
19.4 Pathogenesis
19.5 Vaccines
19.6 Vaccination Procedures
19.7 Vaccine Effect
19.8 Side-Effects
19.9 Regulations
References
Chapter 20: Vaccination against Streptococcosis and Lactococcosis
Abstract
20.1 Occurrence
20.2 Significance
20.3 Etiology
20.4 Pathogenesis
20.5 Vaccines
20.6 Vaccination Procedures and Vaccine Effect
20.7 Side-Effects
20.8 Regulations
References
Chapter 21: Vaccination against Piscirickettsiosis
Abstract
21.1 Occurrence and Significance
21.2 Etiology
21.3 Pathogenesis
21.4 Vaccines and Vaccination
21.5 Current Vaccine Status
21.6 Future Perspectives
References
Chapter 22: Vaccination against Bacterial Kidney Disease
Abstract
22.1 Introduction
22.2 Occurrence
22.3 Significance
22.4 Etiology
22.5 Pathogenesis
22.6 Vaccines
22.7 Vaccination Procedures
22.8 Vaccine Effects and Side-Effects
22.9 Regulations
22.10 Future Directions
References
Chapter 23: Vaccination against Diseases Caused by Flavobacteriaceae Species
Abstract
23.1 Introduction
23.2 Bacterial Gill Disease (
Flavobacterium branchiophilum
)
23.3 Columnaris Disease (
Flavobacterium columnare
)
23.4 Bacterial Cold-Water Disease (
Flavobacterium psychrophilum
)
23.5 Tenacibaculosis (
Tenacibaculum maritimum
)
References
Chapter 24: Vaccination against Viral Hemorrhagic Septicemia and Infectious Hematopoietic Necrosis
Abstract
24.1 Occurrence and Significance
24.2 Etiology
24.3 Pathogenesis
24.4 Vaccines
24.5 Concluding Remarks
24.6 Acknowledgements
References
Chapter 25: Vaccination against Infectious Pancreatic Necrosis
Abstract
25.1 Occurrence and Significance
25.2 Etiology
25.3 Pathogenesis
25.4 Vaccines and Vaccine Effect
25.5 Vaccine-Induced Immune Responses
25.6 Regulations
References
Chapter 26: Vaccination against Infectious Salmon Anemia
Abstract
26.1 Occurrence and Significance
26.2 Etiology
26.3 Pathogenesis
26.4 Vaccines
26.5 Regulatory Issues
References
Chapter 27: Vaccination against Koi Herpesvirus Disease
Abstract
27.1 Occurrence and Significance
27.2 Etiology
27.3 Pathogenesis
27.4 Vaccine and Vaccination
27.5 Efficacy
27.6 Safety
27.7 Regulatory Issues
References
Chapter 28: Vaccination against Diseases Caused by Salmonid alphavirus
Abstract
28.1 Occurrence and Significance
28.2 Etiology
28.3 Pathogenesis
28.4 Immunity and Vaccine Development
References
Chapter 29: Vaccination against Diseases Caused by Betanodavirus
Abstract
29.1 Viral Encephalopathy and Retinopathy (VER)
29.2 Occurrence and Significance
29.3 Etiology
29.4 Pathogenesis
29.5 Immune Status and Response to NNV
29.6 Vaccines
29.7 Replicating Vaccines
29.8 Inactivated Virus
29.9 Recombinant Protein/Peptide
29.10 DNA Vaccines
29.11 Future Prospects and Recommendations
References
Chapter 30: Immunostimulation of Crustaceans
Abstract
30.1 Introduction
30.2 Immune System of Crustaceans
30.3 Immunostimulants of Crustaceans
30.4 Acknowledgements
References
Index
End User License Agreement
xv
xvi
xvii
xviii
xix
xx
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
61
62
63
64
65
66
67
68
69
70
71
72
73
74
75
76
77
78
79
80
81
82
83
84
85
86
87
88
89
90
91
92
93
94
95
96
97
98
99
100
101
102
103
104
105
106
107
108
109
110
111
112
113
114
115
116
117
118
119
120
121
122
123
124
125
126
127
128
129
130
131
132
133
134
135
136
137
138
139
140
141
142
143
144
145
146
147
148
149
150
151
152
153
154
155
156
157
158
159
160
161
162
163
164
165
166
167
168
169
170
171
172
173
174
175
176
177
178
179
180
181
182
183
184
185
186
187
188
189
190
191
192
193
194
195
196
197
198
199
200
201
202
203
204
205
206
207
208
209
210
211
212
213
214
215
216
217
218
219
220
221
222
223
224
225
226
227
228
229
230
231
232
233
234
235
236
237
238
239
240
241
242
243
244
245
246
247
248
249
250
251
252
253
254
255
256
257
258
259
260
261
262
263
264
265
266
267
268
269
270
271
272
273
274
275
276
277
278
279
280
281
282
283
284
285
286
287
288
289
290
291
292
293
294
295
296
297
298
299
300
301
302
303
304
305
306
307
308
309
310
311
312
313
314
315
316
317
318
319
320
321
322
323
324
325
326
327
328
329
330
331
332
333
334
335
336
337
338
339
340
341
342
343
344
345
346
347
348
349
350
351
352
353
354
355
356
357
358
359
360
361
362
363
364
365
366
367
368
369
370
371
373
374
375
376
377
378
379
380
381
382
383
Cover
Table of Contents
Preface
Chapter 1: The History of Fish Vaccination
Figure 1.1
Figure 2.1
Figure 5.1
Figure 6.1
Figure 8.1
Figure 8.2
Figure 8.3
Figure 9.1
Figure 9.2
Figure 10.1
Figure 10.2
Figure 10.3
Figure 11.1
Figure 11.2
Figure 12.1
Figure 12.2
Figure 12.3
Figure 12.4
Figure 12.5
Figure 13.1
Figure 13.2
Figure 13.3
Figure 13.4
Figure 14.1
Figure 22.1
Figure 22.2
Figure 27.1
Figure 27.2
Figure 27.3
Figure 27.4
Figure 27.5
Figure 28.1
Figure 28.2
Figure 28.3
Figure 30.1
Table 3.1
Table 3.2
Table 3.3
Table 3.4
Table 6.1
Table 7.1
Table 9.1
Table 15.1
Table 16.1
Table 16.2
Table 18.1
Table 18.2
Table 18.3
Table 18.4
Table 26.1
Table 29.1
Table 30.1
Table 30.2
Roar Gudding, Atle Lillehaug and Øystein Evensen
This edition first published 2014 © 2014 by John Wiley & Sons, Ltd
Registered office: John Wiley & Sons, Ltd, The Atrium, Southern Gate, Chichester, West Sussex, PO19 8SQ, UK
Editorial offices: 9600 Garsington Road, Oxford, OX4 2DQ, UK
The Atrium, Southern Gate, Chichester, West Sussex, PO19 8SQ, UK
111 River Street, Hoboken, NJ 07030-5774, USA
For details of our global editorial offices, for customer services and for information about how to apply for permission to reuse the copyright material in this book please see our website at www.wiley.com/wiley-blackwell.
The right of the author to be identified as the author of this work has been asserted in accordance with the UK Copyright, Designs and Patents Act 1988.
All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, recording or otherwise, except as permitted by the UK Copyright, Designs and Patents Act 1988, without the prior permission of the publisher.
Designations used by companies to distinguish their products are often claimed as trademarks. All brand names and product names used in this book are trade names, service marks, trademarks or registered trademarks of their respective owners. The publisher is not associated with any product or vendor mentioned in this book.
Limit of Liability/Disclaimer of Warranty: While the publisher and author(s) have used their best efforts in preparing this book, they make no representations or warranties with respect to the accuracy or completeness of the contents of this book and specifically disclaim any implied warranties of merchantability or fitness for a particular purpose. It is sold on the understanding that the publisher is not engaged in rendering professional services and neither the publisher nor the author shall be liable for damages arising herefrom. If professional advice or other expert assistance is required, the services of a competent professional should be sought.
Library of Congress Cataloging-in-Publication Data
Fish vaccination / edited by Roar Gudding, Atle Lillehaug, and Øystein Evensen.
pages cm
Includes bibliographical references and index.
ISBN 978-0-470-67455-0 (cloth)
1. Fishes— Vaccination. 2. Fishes— Diseases— Prevention. I. Gudding, Roar. II. Lillehaug, Atle, 1954- III. Evensen, Øystein, 1959-
SH171.F596 2014
571.9′51— dc23
2013034537
Wiley also publishes its books in a variety of electronic formats. Some content that appears in print may not be available in electronic books.
Inset photo: Vaccination of fish. Asgeir Østvik. Reproduced with permission.
Cover image: Main photo: Fishing farm. Tiny fishing farm in Ithaka, Greece. Courtesy of Margot Granitsas/Science Photo Library.
Cover design by Design Deluxe
Ofer Ashoulin
Dagon, Maagan Michael fish farm, Kibbutz Ma'agan Michael D.N. Menashe, Israel 37805
E-mail:
Stéphane Biacchesi
National Institute for Agricultural Research (INRA), 78352 Jouy en Josas, France
E-mail:
Eirik Biering
Norwegian Veterinary Institute, Tungasletta 2, 7485, Trondheim, Norway
E-mail:
Michel Brémont
National Institute for Agricultural Research (INRA), 78352 Jouy en Josas, France
E-mail:
Andrew Bridle
NCMCRS University of Tasmania, Locked Bag 1370, Launceston 7250, Tasmania, Australia
E-mail:
Jarl Bøgwald
Norwegian College of Fishery Science, UiT The Arctic University of Norway, 9037 Tromsø, Norway
E-mail:
Duncan J. Colquhoun
Norwegian Veterinary Institute, PO Box 750, 0106 Oslo, Norway
E-mail:
Roy A. Dalmo
Norwegian College of Fishery Science, UiT The Arctic University of Norway, 9037 Tromsø, Norway
E-mail:
Arnon Dishon
KoVax Ltd, Bynet Build. Har Hotzvim Ind. Park, PO Box 45212 Jerusalem, Israel 90836
E-mail:
Diane G. Elliott
U.S. Geological Survey, Western Fisheries Research Center, 6505 Northeast 65th Street, Seattle, Washington 98115, USA
E-mail:
Øystein Evensen
Norwegian School of Veterinary Science, PO Box 8146 Dep, 0033 Oslo, Norway
E-mail:
Knut Falk
Norwegian Veterinary Institute, PO Box 750, 0106 Oslo, Norway
E-mail:
Arne Marius Fiskum
Pharmaq, 7863 Overhalla, Norway
E-mail:
Thomas Goodrich
AquaTactics Fish Health, 12015 115th Avenue NE, Suite 120, Kirkland, Washington 98034, USA
E-mail:
Roar Gudding
Norwegian Veterinary Institute, PO Box 750, 0106 Oslo, Norway
E-mail:
K. Larry Hammell
Atlantic Veterinary College, University of Prince Edward Island, 550 University Avenue, Charlottetown, C1A4P3, Canada
E-mail:
Anja Holm
Danish Health and Medicines Authority, Axel Heides Gade 1, 2300 Copenhagen S, Denmark
E-mail:
Eva Högfors-Rönnholm
Laboratory of Aquatic Pathobiology, Environmental and Marine Biology, Department of Biosciences, Tykistökatu 6, Biocity, Åbo Akademi University, 20520 Turku, Finland
E-mail:
Jorunn B. Jørgensen
Norwegian College of Fishery Science, UiT The Arctic University of Norway, 9037 Tromsø, Norway
E-mail:
Indrani Karunasagar
Department of Fisheries Microbiology, Karnataka Veterinary, Animal and Fisheries Sciences University, College of Fisheries, Mangalore - 575002, India
E-mail:
Viswanath.Kiron
Aquatic Animal Health Unit, Faculty of Biosciences and Aquaculture, University of Nordland, PO Box 1490, 8049 Bodø, Norway
E-mail:
Phillip H. Klesius
USDA-ARS, Aquatic Animal Health Research Laboratory, 990 Wire Road, Auburn, Alabama 36832, USA
E-mail:
Dag Knappskog
MSD Animal Health, Thormøhlensgate 55, 5001 Bergen, Norway
E-mail:
Erling Olaf Koppang
Norwegian School of Veterinary Science, PO Box 8146 Dep, 0033 Oslo, Norway
E-mail:
Moshe Kotler
Department of Pathology, The Hebrew University–Hadassah Medical School, Jerusalem, 91120, Israel
E-mail:
Joseph Koumans
MSD Animal Health,Wim de Körverstraat 35, Post code 5381, AN Boxmeer, The Netherlands
E-mail:
Inger Kvitvang
Pharmaq, 7863 Overhalla, Norway
E-mail:
Atle Lillehaug
Norwegian Veterinary Institute, PO Box 750, 0106 Oslo, Norway
E-mail:
Biswajit Maiti
Department of Fisheries Microbiology, Karnataka Veterinary, Animal and Fisheries Sciences University, College of Fisheries, Mangalore - 575002, India
E-mail:
Sergio H. Marshall
Institute of Biology, Faculty of Sciences, Pontifical Catholic University of Valparaiso, PO Box 4059, 2340025 Valparaiso, Chile
E-mail:
Emilie Mérour
National Institute for Agricultural Research (INRA), 78352 Jouy en Josas, France
E-mail:
Paul J. Midtlyng
Norwegian School of Veterinary Science, PO Box 8146 Dep, 0033 Oslo, Norway
E-mail:
paul.midtlyng.aquamedic.no
Hetron Mweemba Munang'andu
Norwegian School of Veterinary Science, PO Box 8146 Dep, 0033 Oslo, Norway
E-mail:
hetronmweemba.munang'[email protected]
Stephen Mutoloki
Norwegian School of Veterinary Science, PO Box 8146 Dep, 0033 Oslo, Norway
E-mail:
Singaiah NaveenKumar
Department of Fisheries Microbiology, Karnataka Veterinary, Animal and Fisheries Sciences University, College of Fisheries, Mangalore - 575002, India
E-mail:
Audun H. Nerland
Department of Clinical Science, University of Bergen, 5021 Bergen, Norway
E-mail:
Ken Noda
Food Safety and Consumer Affairs Bureau, Ministry of Agriculture, Forestry and Fisheries, 1-2-1 Kasumigaseki Chiyoda-ku, Tokyo 100-8950, Japan
E-mail:
Barbara Nowak
NCMCRS University of Tasmania, Locked Bag 1370, Launceston 7250, Tasmania, Australia
E-mail:
Sonal Patel
Institute of Marine Research, Nordnesgaten 50, 5005 Bergen, Norway
E-mail:
Trygve T. Poppe
Norwegian School of Veterinary Science, PO Box 8146 Dep, 0033 Oslo, Norway
E-mail:
Julia W. Pridgeon
USDA-ARS, Aquatic Animal Health Research Laboratory, 990 Wire Road, Auburn, Alabama 36832, USA
E-mail:
Praveen Rai
Department of Fisheries Microbiology, Karnataka Veterinary, Animal and Fisheries Sciences University, College of Fisheries, Mangalore - 575002, India
E-mail:
Linda D. Rhodes
Northwest Fisheries Science Center, National Marine Fisheries Service, 2725 Montlake Boulevard East, Seattle, Washington 98112, USA
E-mail:
Espen Rimstad
Norwegian School of Veterinary Science, PO Box 8146 Dep, 0033 Oslo, Norway
E-mail:
Jesus L. Romalde
Department of Microbiology and Parasitology, CIBUS-Faculty of Biology, University of Santiago de Compostela, 15782 Santiago de Compostela, Spain
E-mail:
Jan H.W.M. Rombout
Aquatic Animal Health Unit, Faculty of Biosciences and Aquaculture, University of Nordland, PO Box 1490, 8049 Bodø, Norway
E-mail:
Byron E. Rippke
Center for Veterinary Biologics, USDA, 1920 Dayton Avenue, PO Box 844, Ames, Iowa 50010, USA
E-mail:
Kira Salonius
448 Boulter Loop, RR2, Prince Edward Island, Canada COA 1JO
E-mail:
Craig Shoemaker
USDA-ARS, Aquatic Animal Health Research Laboratory, 990 Wire Road, Auburn, Alabama 36832, USA
E-mail:
Krister Sundell
Laboratory of Aquatic Pathobiology, Environmental and Marine Biology, Department of Biosciences, Tykistökatu 6, Biocity, Åbo Akademi University, 20520 Turku, Finland
E-mail:
Carolina Tafalla
Animal Health Research Center (CISA-INIA), Carretera de Algete a El Casar km 8.1. Valdeolmos 28130, Madrid, Spain
E-mail:
Jaime A. Tobar
Centrovet Ltda, Avenida Salomon Sack 255, 9201310 Cerrillos, Santiago, Chile
E-mail:
E. Scott Weber III
University of California, 2108 Tupper Hall, Davis, California 95616, USA
E-mail:
Gregory D. Wiens
USDA-ARS, National Center for Cool and Cold Water Aquaculture, 11861 Leetown Rd, Kearneysville, West Virginia 25430, USA
E-mail:
Tom Wiklund
Laboratory of Aquatic Pathobiology, Environmental and Marine Biology, Department of Biosciences, Tykistökatu 6, Biocity, Åbo Akademi University, 20520 Turku, Finland
E-mail:
Rune Wiulsrød
Harbitzalléen 2A, Postbox 267 Skøyen, 0213 Oslo, Norway
E-mail:
Any intensive bioproduction – whether on land or at sea – will experience disease problems. Infections that occur in a wild fish as a sporadic event may cause severe mortality in fish-farming ponds or net-pens. Several regions with aquaculture have experienced great economic losses due to outbreaks of infectious diseases. Treatment with antimicrobials may have a negative impact on human health, the aquatic environment and even the confidence in products from aquaculture. Consequently, the expansion of commercial aquaculture has necessitated more emphasis on biosecurity measures, including disease prevention, in order to obtain a sustainable production.
Vaccination may contribute to both economic as well as environmental sustainability. The prevention of diseases using vaccines has a positive effect on the revenue for the fish farmer and the aquaculture industry by reducing morbidity, mortality and the costs of therapy, and by improving product quality. Vaccination may also improve animal welfare by reducing the suffering of diseased fish. Finally, reduction of the use of chemicals with potentialy detrimental ecological effects may be a prerequisite for further development.
The book aims at a complete coverage of the subject of fish vaccinology. The general part of the book gives science-based information about topics like the immune system of the fish, production and control of vaccines, and vaccination strategies and procedures. The use of vaccines may also have side-effects, and the mechanisms and appearances are described. The specific part includes chapters about vaccination against the most important bacterial and viral diseases in commercial fish species. One chapter about the stimulation of the immune system of crustaceans is also included.
The chapters dealing with specific diseases have a similar structure. These chapters include information that is relevant for vaccination, like the significance and occurrence of the diseases, the etiological agents, the most important antigens, as well as the specific vaccine products, the vaccination procedures, and finally the effects and possible side-effects of vaccination.
The scientific output in fish vaccinology has been substantial, especially during the last 20 years. The lists of references are consequently long, although the chapter authors have been encouraged to use review papers in order to reduce the length of the lists.
Fish vaccinology is a multidisciplinary science. The authors of the different chapters are selected from among leading experts in the different fields. While not compromising on scientific quality, we – as editors – have also placed some emphasis on selecting authors from different geographic regions.
As editors, our aim has been to produce a book that will contribute to the further sustainable development of global aquaculture. Fish farming is a rapidly growing industry in many parts of the world. It is expected that aquaculture will continue to grow both in freshwater and seawater, and contribute to the production of healthy and safe food, the development of local communities, and in some countries, even alleviation of poverty.
Roar GuddingAtle LillehaugØystein Evensen
Roar Gudding1 and Thomas Goodrich2
1Norwegian Veterinary Institute, Oslo, Norway
2AquaTactics Fish Health, Washington, USA
Effective and sustainable disease prevention using vaccines has been an important factor for the successful growth of aquaculture. The first vaccine for aquaculture, a yersiniosis vaccine for salmonid fish in the US, was licensed in 1976. Since then the use of vaccines has expanded to new countries and new species, simultaneous with the growth of the aquaculture industry.
This chapter gives a review of the history of fish vaccinology, including information about the achievements in research and presentation of some of the pioneers of the vaccine industry.
The knowledge of immunity is many hundreds of years old. Thucydides, a Greek historian living around 400 bc, described plague in his second book of the history of the Peloponnesian war. He noticed that a person who had recovered from plague was protected when exposed a second time (Humphrey and White, 1970).
The modern history of vaccination for prevention of infectious diseases started more than 200 years ago. In 1796, the English physician Edward Jenner inoculated a boy with infectious material from cowpox in order to induce immunity to smallpox. He had noticed that dairy farmers exposed to cowpox had become resistant to smallpox (Jenner, 1798). Jenner used the term “vaccine inoculation”, which was gradually changed to vaccination. Vaccine is derived from the Latin word vacca, which means cow.
Louis Pasteur and co-workers demonstrated that administration of attenuated and live microorganisms gave protection upon challenge with pathogenic microorganisms (Fenner et al., 1997). Their experiments with prevention of rabies were followed by research on various pathogenic microorganisms with great significance for human and animal health (Humphrey and White, 1970).
In a speech in 1881 Pasteur suggested that the word “vaccination” should be a general word for preventive inoculation of microorganisms as a tribute to the work of Jenner (Fenner et al., 1997). The word “vaccinology” is of more recent vintage. Salk and Salk (1977) introduced the term vaccinology in 1977 to describe the interdisciplinary dimension of disease prevention based upon microorganisms stimulating the immune system to prevent infectious diseases in individuals and populations.
Disease prevention by vaccination is one of the milestones of modern medicine. The use of prophylaxis based on vaccines is expanding in many ways. Vaccination is now considered to be a safe and efficient method for prevention of diseases in human as well as in veterinary medicine.
Compared with animal husbandry, fish farming is a relatively new method for bioproduction in many countries. When diseases appeared in aquaculture operations with salmonid fish, antibiotics or chemotherapeutics were used for disease treatment, and even for disease prevention. However, the need for efficacious immunoprophylaxis in hatcheries for salmonid fish was expressed as early as the late 1930s.
The first report of disease prevention using vaccines seems to have been by Snieszko et al. (1938) who published a paper about protective immunity in carp immunized with Aeromonas punctata. However, their paper was written in the Polish language which reduced the availability of the information. The first reports in English seem to have been written by Duff who showed protection against Aeromonas salmonicida in trout immunized by parenteral inoculation and by oral administration (Duff, 1939, 1942).
The most important reason for the disinterest in immunoprophylaxis was probably the availability of antimicrobial compounds in the years after World War II. A study by Snieszko and Friddle (1949) concluded that chemotherapy with sulfamerazine was superior to oral administration of a vaccine for the control of furunculosis. It was not until the 1970s that vaccines were applied in commercial aquaculture. Even in the scientific literature there are a limited number of reports about disease prevention by vaccination (Newman, 1993). In aquaculture, the first 30 years after World War II is therefore called the era of chemotherapy (Evelyn, 1997).
Vaccinology includes different disciplines. Immunology is one of them. During the last 150 years there have been various studies of fish immunology and biology with relevance to vaccinology, reviewed by Van Muiswinkel (2008). The background of these scientists has been varied, including biology, anatomy, hematology, physiology, ichthyology, microbiology, pathology, fish diseases and others. Research on the induction of humoral antibodies in immunized fish was published before World War II (Nybelin, 1935; Pliszka, 1939), and continued with studies of immunoglobulins and complement as well as the cellular basis of the immunological response (Ridgway et al., 1966; Cushing, 1970; Corbel, 1975; Press, 1998). Fish were also included in studies of comparative and developmental immunology in order to get a better understanding of the evolutionary development of the immune system (Ambrosius, 1967).
Different fish species, including carp and salmonid fish, were included in the immunological studies, and factors of importance in vaccinology, like temperature and other environmental factors, were also studied (Snieszko, 1974). The role of adjuvants in fish is important for progress in both immunology and vaccinology. Ambrosius and Lehmann (1965) found that adjuvants like aluminum hydroxide and Freund's adjuvant increased the quantity of immunoglobulins, the former slightly and the latter significantly.
The method of administration was also studied. Trout was found to produce a good immune response when injected with antigens from Aeromonas salmonicida (Krantz et al., 1963). However, parenteral introduction of antigens seemed to be economically prohibitive and might even be harmful to the fish. Oral immunization was therefore considered to be the only way for practical disease prevention (Snieszko, 1970).
This assessment was also influenced by results from studies on humans and terrestrial animals. The successful vaccination against poliomyelitis in humans and Newcastle disease in poultry by oral administration probably influenced priorities and the direction of research of scientists working with fish immunology and vaccinology (Stone et al., 1969; Sabin and Boulger, 1973). Industrial production of poultry and fish had similarities, and scientists working with different vertebrates shared information.
Experience from the poultry industry was probably also the basis for spray vaccination of fish as a method for administration of antigens. Spray vaccination of fish was given a US patent (Garrison et al., 1980), but the method was not widely used in the field.
Diseases are the final results of interactions between an agent, a host and the environment of the host and the pathogen (Snieszko, 1974) (see Figure 1.1). In a population of wild fish, diseases have been considered as part of a normal biological process. In cultures of fish this situation gradually changed. The number of fish and the density increased. Diseases that were considered to be a phenomenon in the wild fish population sometimes became a problem in a fish farm.
Fig 1.1 The health triangle. (Source: Adapted from Snieszko 1974. Reproduced with permission of John Wiley & Sons.)
Disease prevention should be based upon measures including all three interacting factors. However, aquaculture has some disadvantages compared with bioproduction of terrestrial animals. Pathogenic microorganisms may be transmitted through water. Furthermore, disinfection is difficult, or, as in the marine environment, even impossible. Furthermore, the side-effects and risks associated with chemotherapy reduce the use of antibiotics to therapeutic use, and even that should be limited. Some environmental factors might be controlled, but others, like water temperature, could not be influenced. The resistance of the fish, based on natural or acquired immunity, is therefore a crucial factor for the health of farmed fish.
During the short history of modern aquaculture it is accepted that disease prevention based on stimulation of the immune system has become an integrated part of the management of aquaculture operations. The history of fish vaccination consists of both success and failures. Due to scientific efforts and rapid transfer of scientific progress into practical measures, vaccination has become an important part of the development of the global aquaculture industry.
The scientific production in fish vaccinology and related areas has been considerable. A search on “fish vaccination” in scientific databases showed a total of around 10,000 papers (Science Direct, Blackwell). Most of them have been published during the last 20 years. The total number of publications was slightly above 100 at the end of the 1980s (Newman, 1993).
Fish vaccination has been the subject of many review articles (e.g., Snieszko, 1970; Harrell, 1979; Leong and Fryer, 1993; Newman, 1993; Press and Lillehaug, 1995; Ellis, 1997; Gudding et al., 1999; Vinitnantharat et al., 1999; Sommerset et al., 2005; Toranzo et al., 2009). Several international conferences on fish vaccinology and the proceedings from these have contributed to the progress (Anderson and Hennesen, 1981; de Kinkelin, 1984; Gudding et al., 1997; Midtlyng, 2005). Fish vaccination was also the subject of many dissertations before the turn of the century (e.g., Lamers, 1985; Erdal, 1990; Lillehaug, 1993; Kolb, 1994; Hoel, 1997; Joosten, 1997; Midtlyng, 1998). In addition, there are numerous dissertations on related subjects like fish immunology, fish bacteriology and disease prevention in fish farming. Disease prevention in aquaculture by vaccines has also been reviewed in textbooks and book chapters (e.g., Ellis, 1988; Tatner, 1993; Adams et al., 1997; Midtlyng, 1997).
Whereas research in fish immunology has included different fish species, studies on fish vaccinology have been mainly restricted to salmonid fish. In a chapter about furunculosis, the status in the late 1960s is summarized (Bullock et al., 1971). Under the heading Prophylactic chemotherapy the following statement is made:
“Although the practice of feeding low levels of drugs to control enzootic furunculosis may be useful, it must be done with caution to avoid toxicity to the fishes and alertness to possible appearance of drug resistant strains of
A. salmonicida
”.
As for vaccination, the authors concluded that oral immunization against furunculosis with antigens incorporated in the feed was the only feasible way for routine immunization. However, the authors indicated that the era of chemotherapy in aquaculture should come to an end and vaccination should be used for disease prevention.
An early presentation of vaccination against vibriosis was made by Hayashi et al. (1964). Based on immunization studies they concluded that injection of a concentrated vaccine might be a useful prophylactic way to control vibriosis in rainbow trout. One year later, Ross and Klontz (1965) showed that enteric redmouth disease (yersiniosis) could be prevented in fingerling rainbow trout fed pelleted food containing bacterial cells of the redmouth bacterium (Yersinia ruckeri).
During the 1970s immunoprophylaxis became recognized as method for prevention of infection caused by fish pathogenic species of Vibrio and Yersinia in aquaculture. The first product license for a fish vaccine was issued in 1976 when an enteric redmouth bacterin produced by Wildlife Vaccine Inc. was approved (Tebbit et al., 1981). The effect on morbidity and mortality was documented by both scientific studies as well as by experience from commercial operations. Protection could be achieved by inactivated vaccines without adjuvants, administered by injection or immersion (Bullock and Anderson, 1984; Evelyn, 1984).
In the 1980s a new costly disease initially named “Hitra disease” appeared in salmonid aquaculture in Norway. There was some dispute about the etiology of the disease. It was soon concluded that the disease was an infectious disease caused by a new pathogenic bacterium, Vibrio salmonicida (Egidius et al., 1986). Since 1988 most Atlantic salmon and rainbow trout in Norway have been vaccinated (initially via immersion) against this disease, which was given the name cold-water vibriosis.
In salmonids the great challenge in disease prevention was furunculosis caused by Aeromonas salmonicida. Based on the positive experience with prevention of Vibrio-infections using immersion vaccines, there were great expectations for similar effects with a furunculosis vaccine. However, immersion of furunculosis bacterins was found to give insufficient protection. Injection of simple whole-cell culture bacterins stimulated a protective immunity, but the magnitude and duration were less than desired.
In vaccines for terrestrial animals, adjuvants had been added to vaccines for decades. Al-hydrogel, which was used in vaccines for both man and animals, provided improved protection also when used in fish vaccines (Erdal and Reitan, 1992; Lillehaug, 1993). However, in order to achieve a long-lasting effect, oil adjuvants like mineral oils were found to reduce morbidity and mortality to an acceptable level, both in challenge tests as well as in aquaculture operations (Midtlyng, 1998). The local reactions caused by adjuvants were recognized as serious side-effects, but effective disease prevention was considered more important than animal welfare by authorities as well as by the industry and consumers.
Bacterins produced with antigens from V. anguillarum, V. salmonicida and A. salmonicida and added mineral oil adjuvants contributed to effective control of diseases, which without immunoprophylaxis would have caused great losses to the industry. The large amount of antimicrobials for disease treatment before introduction of vaccines was not acceptable for an industry that claimed to be sustainable. The impact of vaccination on the success of Norwegian aquaculture was expressed by a senior in the industry as follows: “The industry might have survived with the economic losses due to high mortality, but it could not survive with the negative effects of high use of antibiotics”. Vaccination was consequently one of the factors contributing to the development of the salmonid aquaculture industry. The figures for use of antibiotics in Norwegian aquaculture represent a success story in the history of vaccinology (Gudding, 2014).
The reasons for the success in fish vaccinology in Norway are many. Innovative scientists in public and private institutions and companies deserve to be acknowledged. However, good cooperation between the scientific community, authorities and the industry were also important contributing factors. Vaccines for fish diseases were developed, produced and tested experimentally in the field at a high speed.
Even the approval of vaccines by the authorities was a fast process in Norway with little bureaucracy. During early years of fish vaccination, licensing of fish vaccines was the responsibility of the Ministry of Agriculture. The regulatory requirements were few and approval of fish vaccines was considered to be a part of the learning process. Safety and efficacy in the field were emphasized. The transfer of responsibility to the Norwegian Medicines Agency in 1993 represented a change to a more comprehensive regulatory framework in line with international rules. However, retrospectively it can be stated that the simplistic but effective regulatory work during the first years of aquaculture in Norway contributed significantly to the decrease in antibiotic use in the industry without causing significant negative effects (Midtlyng et al., 2011).
During the early years of aquaculture, major viral diseases included infectious pancreatic necrosis, viral hemorrhagic septicemia and infectious hematopoietic necrosis. For the latter two viral diseases, biosecurity has mainly been based on eradication of diseased populations, and research on vaccination was not prioritized. The first successful experiments on vaccination against these diseases included live vaccines, either avirulent or attenuated strains (Fryer, 1976; Vestergaard-Jørgensen, 1976; Hill et al., 1980). The live vaccines provided acceptable or even good protection under experimental conditions, but safety considerations stopped further work. Some of the vaccines showed residual virulence to groups of vaccinated fish at an unacceptable level. The safety concern for other fish species in the aquatic environment also contributed to limit research on vaccines that could be used in commercial operations.
Inactivated viral vaccines for fish have provided some effect, especially under experimental conditions. However, the protective immunity in the field from inactivated vaccines has been relatively low compared with the protection achieved by most of the bacterial vaccines. Consequently, the aquaculture industry has not been satisfied with the efficacy (Biering et al., 2005).
The success with fish farming of salmonids stimulated aquaculture of marine fish species. In the Mediterranean countries, production of sea bass, sea bream and turbot increased, and so did disease-related problems. In the US, bacterial diseases were a challenge for the channel catfish industry. Vaccines were introduced in many countries and continents for disease prevention (Håstein et al., 2005). Some of these were commercial vaccines with national or international licenses, while some were autogenous or experimental vaccines used in a few fish farms.
Two important bacterial diseases for Mediterranean farmed species were vibriosis and pasteurellosis. Inactivated vaccines with the same antigenic composition as the microorganisms causing disease were found to provide acceptable to good protection (Santos et al., 1991; Gravningen et al., 1998). Vaccination against these diseases is now a part of the biosecurity programme in many regions with production of sea bass, sea bream and turbot.
Bacterial diseases were the primary concern in the US channel catfish industry. The primary bacterial pathogens in this industry are Edwardsiella ictaluri, Flavobacterium columnare and Aeromonas hydrophila. Vaccines have had limited use due to the extensive nature of the husbandry. Current vaccines against infections caused by E. ictaluri and F. columnare consist of attenuated live immersion vaccines (Shoemaker et al., 2009).
Most of the global aquaculture is located in countries in Asia. So far vaccination has not become an integral part of biosecurity in that region. However, there is a growing interest in disease prevention by vaccines in production of tilapia, pangasius and other species. The first commercial vaccine against a disease in pangasius was licensed in Vietnam in 2011.
The history of fish vaccination is generally a story of success. The fact that a small fish can be protected against an infectious disease by immersion for a few seconds in a diluted vaccine solution is one example of the remarkable ability of living organisms to cope with biological challenges.
However, there have also been obstacles in the use of the fish immune system for disease prevention. Studies of various fish species have showed that the basic mechanisms of immunity in fish, birds and mammals are similar. However, the history of fish vaccinology also includes results of studies showing differences between species with great influence on the strategy and methods for immunoprophylaxis.
Maternal immunity is a fundamental part of protection against infectious diseases in newborn individuals of mammals and birds. It would be reasonable to believe that a similar mechanism existed for fish. Maternal immunity has been found to be transferred from immunized mothers to offspring in the ovoviviparous guppy (Takahashi and Kawahara, 1987). In salmonid fish the transfer of maternal antibodies seems to be at very low levels and insufficient to provide protection for the offspring against infections (Lillehaug et al., 1996).
The failure of passive immunization is compensated by the early maturation of the immune system. Fish at a size of 2 g were protected after immersion vaccination (Johnson et al., 1982b). The duration of immunity and the development of immunological memory, both crucial in vaccinology, increased with size (Johnson et al., 1982a). Maximum duration of protection was achieved in rainbow trout immersion vaccinated at a size of 4 g. In commercial aquaculture, the duration of protection needed is directly related to the length of the production cycle, that is, the period between vaccination and harvest.
Effective prevention of several bacterial infections in fish by vaccination is well documented in the literature. However, infections caused by intracellular microorganisms are a challenge. This includes both viruses and intracellular bacteria. Attenuated vaccines and/or DNA vaccines seem to be a possible solution.
The history of fish vaccination includes the achievements by many scientists working in universities and research institutes. Their production is presented and documented in the scientific literature.
Vaccines are also commercial products, developed, produced and marketed by private companies. Manufacturers of fish vaccines were generally small businesses with a few enthusiastic pioneers involved in many parts of the process, from ideas to use of the vaccine in the field. These industrial entrepreneurs were important for progress in the early days of vaccinology. In addition to know-how about the product, they contributed with knowledge about the correct use of the vaccines.
Many of the early pioneers were excellent scientists who combined theoretical expertise and practical knowledge about disease prevention using vaccines with a commercial interest. A list of companies and pioneers can never be complete and fair for those involved.
The Colorado company Wildlife Vaccines, with Guy Tebbit, John Rohovec and Thomas Goodrich as experts, was the first manufacturer with a licensed fish vaccine. The company produced bacterins for the domestic and international market. Tavolek Inc., a subsidiary of Johnson & Johnson, was the second company with a licensed fish vaccine. Keith Johnson and Don Amend were technical experts involved in most parts of the development and production of the enteric redmouth vaccine and other bacterins. However, Tavolek Inc., and Wildlife Vaccines operated at a time when the market was too small for a profitable business.
In the 1980s Biomed Research Laboratories in Seattle entered the market. Stephen Newman, Tony Novotny, James Nelson and Robert Busch were a competent group of aquaculturists and vaccinologists, with expertise on disease prevention in hatcheries in the Northwestern US and from the manufacture of bacterins.
Two other small companies deserve to be mentioned in the history of vaccinology. Aqua Health Inc., with William Patterson as technical and scientific expert, and Aquaculture Vaccines Ltd., started as a subsidiary of Wildlife Vaccines, with Patrick Smith as expert, played significant roles in the early days of fish vaccination.
The growth of salmon production in Europe was the basis for the establishment of vaccine companies near the markets. Apothekernes Laboratorium, later Alpharma, was an international pharmaceutical company with headquarters in Oslo. The company saw a commercial potential in aquaculture and started fish vaccine production in Tromsø and later in Overhalla. In the early 1990s the company merged with Biomed Research Laboratories as part of the Alpharma group. The aquaculture part of the company was later separated from the parent company under the name Pharmaq.
In Bergen, Norbio was established with the scientists from the university as experts. Norbio was sold to the Dutch company, Intervet, which later merged with Shering-Plough which had also absorbed Aquaculture Vaccines Ltd. The fish vaccine production has from 2011 been a part of Merck Sharp Dome.
Trading of companies is not unusual in the vaccine industry, and some pharmaceutical companies and investors see the economic potential in fish vaccine production. The international pharmaceutical company Novartis has grown in the fish vaccine business, based on competence acquired with the Canadian company Aqua Health Inc.
In countries with a growing aquaculture industry, vaccine companies have been established based on a possible economic potential. Companies like Centrovet in Chile and Kovax in Israel are examples of regional fish vaccine manufacturers with the goal to provide efficacious and safe vaccines for the aquaculture industry.
The history of fish vaccinology is a documentation of how the immune system of fish can be stimulated by vaccines to prevent the accidental effects of pathogenic microorganisms. In a few years scientists in universities, research institutes and industry have produced basic and applied knowledge about the biology of microorganisms and the immune system of fish species in aquaculture, and this knowledge has been used for development, production, marketing and use of important products for the aquaculture industry.
Fish vaccinology is still in its infancy. Most of the products are first-generation vaccines, but a comprehensive scientific production and valuable practical experience are a good basis for development of improved products that will contribute to environmental, social and economic sustainability in global aquaculture.
Adams, A., Thompson, K.D. and Roberts, R.J. 1997. Fish vaccines, in
Vaccine Manual
.
The Production and Quality Control of Veterinary Vaccines for Use in Developing Countries
(eds N. Mowat and M. Rweyemanu). FAO Animal Production and Health Services No. 35. Rome, FAO, 127–42.
Ambrosius, H. 1967. Untersuchungen über die Immunglobuline niederer Wirbeltiere.
Allerg Asthma
13
: 111–19.
Ambrosius, H. and Lehmann, R. 1965. Beiträge zur Immunbiologie poikilothermer Wirbeltiere. III Der Einfluss von Adjuvanten auf de Antikörper-produktion.
Acta Biol Med Ger
14
: 830–44.
Anderson, D.P. and Hennesen, W. (eds) 1981. Fish biologics: serodiagnostics and vaccines.
Dev Biol Stand
49
: 496 pp.
Biering, E., Villoing, S., Sommerset, I. and Christie, K.E. 2005. Update on viral vaccines for fish.
Dev Biol (Basel)
121
: 97–113.
Bullock, G.L. and Anderson, D.P. 1984. Immunization against
Yersinia ruckeri
, cause of enteric red mouth, in
Symposium on Fish Vaccination
(ed. P. de Kinkelin). Paris, OIE, 151–66.
Bullock, G.L., Conroy, D.A. and Sniezko, S.F. 1971.
Bacterial disease of fishes, in Diseases of Fishes
(eds S.F. Snieszko and H.R. Axelrod). Jersey City, TFH Publications 10, 139.
Corbel, M.J. 1975. The immune response of fish: A review.
J Fish Biol.
7
: 539–63.
Cushing, J.E. 1970. Immunology of fish, in
Fish Physiology
, Vol. 4. (eds W.S. Hoar and D.J. Randall). New York, Academic Press, 465–500.
de Kinkelin, P. (ed.) 1984.
Symposium on fish vaccination: theoretical background and practical results on immunization against infectious diseases
. Paris, OIE.
Duff, D.C.B. 1939. Some serological relationships of the S, R, and G phases of
Bacillus salmonicida
.
J Bacteriol
38
: 91–100.
Duff, D.C.B. 1942. The oral immunization of trout against
Bacterium salmonicida
.
J Immunol
44
: 87–94.
Egidius, E., Wiik, R., Andersen, K.,
et al
., 1986.
Vibrio salmonicida
sp. nov., a new fish pathogen.
Int J Syst Evol Microbiol
36
: 518–20.
Ellis, A.E. (ed.) 1988.
Fish Vaccination
. London, Academic Press.
Ellis, A. 1997. Vaccines for farmed fish, in
Veterinary Vaccinology
(eds P.P. Pastoret, J. Blancou, P. Vannier and C. Verschueren). Amsterdam, Elsevier, 411–17.
Erdal, J.E. 1990.
Immune responses and protection after vaccination of farmed Atlantic salmon against bacterial diseases
. PhD thesis, Norwegian College of Veterinary Medicine, Oslo.
Erdal, J.E. and Reitan, L.J. 1992. Immune response and protective immunity after vaccination of Atlantic salmon (
Salmo salar
L) against furunculosis.
Fish Shellfish Immunol
2
: 99–108.
Evelyn, T.P.T. 1997. A historical review of fish vaccinology.
Dev Biol Stand
90
: 3–12.
Evelyn, T.P.T. 1984. Immunization against pathogenic Vibrios, in
Symposium on Fish Vaccination
(ed. P. de Kinkelin). Paris, OIE, 121–50.
Fenner, F., Pastoret, P.P., Blancou, J. and Terre, J. 1997. Historical introduction, in
Veterinary Vaccinology
(eds P.P. Pastoret, J. Blancou, P. Vannier and C. Verschueren). Amsterdam, Elsevier, 3–19.
Fryer, J.L., Rohovec, J.S., Tebbit, G.L.,
et al
., 1976. Vaccination for control of infectious diseases in Pacific salmon.
Fish Pathol
10
: 155–64.
Garrison, R.L., Gould, R.W., O'Leary, P.J. and Fryer, J.L. 1980. Spray immunization of fish.
US Patent No.
4, 223,014.
Gravningen, K., Thorarinsson, R., Johansen, L.H.,
et al
., 1998. Bivalent vaccines for sea bass (
Dicentrachus labrax
) against vibriosis and pasteurellosis.
J Appl Ichthyol
14
: 159–62.
Gudding, R. 2014. Vaccination as a preventive measure, in
Fish Vaccination
(eds R. Gudding A. Lillehaug and Ø. Evensen). Chichester, John Wiley & Sons Ltd., 12–21.
Gudding, R., Lillehaug, A. and Evensen, Ø. 1999. Recent developments in fish vaccinology.
Vet Immunol Immunpathol
72
: 203–12.
Gudding, R., Lillehaug, A., Midtlyng, P.J. and Brown, F. (eds) 1997. Fish vaccinology.
Dev Biol Stand
90
: 484 pp.
Harrell, L.W. 1979. Immunization of fishes in world mariculture: A review.
Proc World Maricult Soc
10
: 534–44.
Hayashi, K., Kobayashi, S., Kamata, T. and Ozaki, H. 1964. Studies on the vibrio disease of rainbow trout. II. Prophylactic vaccination against the vibrio disease.
J Fac Fish Prefect Univ Mie - Tsu
6
: 181–91.
Hill, B.J., Dorson, D.M. and Dixon, P.F. 1980. Studies on the immunization of trout against IPN, in
Fish Diseases
(ed. W. Ahne). Berlin, Springer Verlag, 29–36.
Hoel, K. 1997.
Adjuvant effects of bacterial components in fish vaccines
. PhD thesis, Norwegian College of Veterinary Medicine, Oslo.
Humphrey, J.H. and White, R.G. 1970.
Immunology for Students of Medicine
, 3rd edn. Oxford, Blackwell Scientific Publications, 1–34.
Håstein, T., Gudding, R. and Evensen, Ø. 2005. Bacterial vaccines for fish – an update of the current situation worldwide.
Dev Biol (Basel)
121
: 55–74.
Kolb, C. 1994.
Die Vakzination von Fischen
. PhD thesis, Justus-Liebig-Universität, Giessen.
Krantz, G.E., Reddecliff, J.M. and Heist, C.E. 1963. Development of antibodies against
Aeromonas salmonicida
in trout.
J Immunol
91
: 757–60.
Jenner, E. 1798.
An inquiry into the causes and effects of the variolae vaccinae, a disease discovered in some of the western counties of England particularly Gloucestershire, and known by the name of cow pox
. London, Sampson Low.
Johnson, K.A., Flynn, J.K. and Amend, D.F. 1982a. Duration of immunity in salmonids vaccinated by direct immersion with
Yersinia ruckeri
and
Vibrio anguillarum
bacterins.
J Fish Dis
5
: 207–13.
Johnson, K.A., Flynn, J.K. and Amend, D.F. 1982b. Onset of immunity in salmonid fry vaccinated by direct immersion in
Vibrio anguillarum
and
Yersinia ruckeri
bacterins.
J Fish Dis
5
: 197–205.
Joosten, E. 1997.
Immunological aspects of oral vaccination in fish
. PhD thesis, University of Wageningen.
Lamers, C.H.J. 1985.
The reaction of the immune system of fish to vaccination
. PhD thesis, University of Wageningen.
Leong, J.C. and Fryer, J.L. 1993. Viral vaccines for aquaculture.
Annu Rev Fish Dis
3
: 225–40.
Lillehaug, A. 1993.
Effects and side-effects of vaccination of salmonid fish
. PhD thesis, Norwegian College of Veterinary Medicine, Oslo.
Lillehaug, A., Sevatdal, S. and Endal, T. 1996. Passive transfer of specific maternal immunity does not protect Atlantic salmon (
Salmo salar
L.) fry against yersiniosis.
Fish Shellfish Immunol
6
: 521–35.
Midtlyng, P.J. 1997. Vaccination against furunculosis, in
Furunculosis – Multidisciplinary Fish Disease Research
(eds E.M. Bernoth, A.E. Ellis, P.J. Midtlyng, G. Olivier and P. Smith). San Diego, Academic Press, 382–404.
Midtlyng, P.J. 1998.
Evaluation of furunculosis vaccines in Atlantic salmon
. PhD thesis, Norwegian College of Veterinary Medicine, Oslo.
Midtlyng, P.J. 2005. Progress in fish vaccinology.
Dev Biol (Basel)
121
: 335 pp.
Midtlyng, P.J., Grave, K. and Horsberg, T.E. 2011. What has been done to minimize the use of antibacterial and antiparasitic drugs in Norwegian aquaculture.
Aquac Res
42: 28–34.
Newman, S.G. 1993. Bacterial vaccines for fish.
Annu Rev Fish Dis
3
: 145–85.
Nybelin, O. 1935. Über Agglutininbildung bei Fischen.
Z Immunitätsforsch
84
: 74–9.
Pliszka, F. 1939. Untersuchungen über die Agglutininbildung bei Fischen.
Zbl Bakt Abt
1 143: 262–4.
Press, CMcL. 1998. Immunology of fishes, in
Handbook of Vertebrate Immunology
(eds P.P. Pastoret, P. Griebel, H. Bazin and A. Govaerts). San Diego, Academic Press, 3–62.
Press, C. and Lillehaug, A. 1995. Vaccination in European salmonid aquaculture: a review of practices and prospects.
Br Vet J
151
: 46–69.
Ridgway, G.J., Hodgins, H.O. and Klontz, G.W. 1966. The immune response in teleosts, in
Phylogeny of Immunity
(eds R.T. Smith, P.A. Miescher and R.A. Good). Gainesville, FL, University of Florida Press, 199–208.
Ross, A.J. and Klontz, G.W. 1965. Oral immunization of rainbow trout (
Salmo gairdneri
) against an etiologic agent of “red mouth disease”.
J Fish Res Bd Can
22
: 713–19.
Sabin, A.B. and Boulger, L.R. 1973. History of Sabin attenuated poliovirus oral live vaccine strains.
J Biol Stand
1
: 115–18.
Salk, J. and Salk, D. 1977. Control of influenza and poliomyelitis with killed virus vaccines.
Science
195
: 834–47.
Santos, Y., Bandin, I., Nunez, S.,
et al
., 1991. Protection of turbot
Scophthalmus maximus
(L.), and rainbow trout,
Oncorhynchus mykiss
(Richardson), against vibriosis using two different vaccines.
J Fish Dis
14
: 407–11.
Shoemaker, C.A., Klesius, P.H., Evans, J.J. and Aria, C.R. 2009. Use of modified live vaccines in aquaculture.
J World Aquac Soc
40
: 573–85.
Snieszko, S.F. 1970. Immunization of fishes: a review.
J Wildl Dis
6
: 24–30.
Snieszko, S.F. 1974. The effects of environmental stress on outbreaks of infectious diseases of fishes.
J Fish Biol
6
: 197–208.
Snieszko, S.F. and Friddle, S.B. 1949. Prophylaxis of furunculosis in brook trout (
Salvelinus fontinalis
) by oral immunization and sulfamerazine.
Progress Fish Cult
11
: 161–8.
Snieszko, S., Piotrowska, W., Kocylowski, B. and Marek, K. 1938. Badania bakteriologiczne i serogiczne nad bakteriami posocznicy karpi. Memoires de l'Institut d'Ichtyobiologie et Pisciculture de la Station de Pisciculture Experimentale a Mydlniki de l'Universite Jagiellonienne a Cracovie Nr
38
.
Sommerset, I., Krossøy, B., Biering, E. and Frost, P. 2005. Vaccines for fish in aquaculture.
Exp Rev Vaccines
4
: 89–101.
Stone, H.D., Ritchie, A.E. and Boney, W.A. 1969. Immunization of chickens against Newcastle disease with beta-propiolactone-killed virus antigen administered in drinking water.
Avian Dis
13
: 568–78.
Takahashi, Y. and Kawahara, E. 1987. Maternal immunity in newborn fry of ovoviviparous guppy.
Nippon Suis Gakk
53
: 721–35.
Tatner, M.F. 1993. Fish vaccines, in
Vaccines for Veterinary Applications
(ed. A.R. Peters). Oxford, Butterworth-Heinemann, 199–224.
Tebbit, G.L., Erickson, J.D. and Van de Water, R.B. 1981. Development and use of
Yersinia ruckeri
bacterins to control enteric redmouth disease.
Dev Biol Stand
49
: 395–401.
Toranzo, A.E., Romalde, J.L., Magariños, B. and Barja, J.L. 2009. Present and future aquaculture vaccines against bacterial fish diseases.
Op Méditerr
86
: 155–76.
Van Muiswinkel, W.B. 2008. A history of fish immunology and vaccination I. The early days.
Fish Shellfish Immunol
25
: 397–408.
Vestergaard-Jørgensen, P.E. 1976. Partial resistance of rainbow trout (
Salmo gairdneri
) to viral haemorrhagic septicaemia (VHS) following exposure to non-virulent Egtved-virus.
Nord Vet Med
28
: 570–1.
Vinitnantharat, S., Gravningen, K. and Greger, E. 1999. Fish vaccines.
Adv Vet Med
41
: 539–50.
