A new approach to the management of emerging diseases of aquatic animals.

Since 1970, aquaculture has grown at a rate of between 5% and 10% per annum. It has achieved this by expanding into new areas, farming new (often non-native) species and intensifying production. These features of aquaculture, combined with large-scale movements of animals, have driven disease emergence, with negative consequences for both production and biodiversity. Efforts to improve the management of emerging diseases of aquatic animals must include actions to reduce the rate of disease emergence, enhance disease detection and reporting, and improve responses to prevent disease spread. The rate of disease emergence can be reduced by understanding the underpinning mechanisms and developing measures to mitigate them. The three principal mechanisms of disease emergence, namely, host switching, decreased host immunocompetence and increased pathogen virulence, have many drivers. The most important of these drivers are those that expose susceptible hosts to novel pathogens (e.g. the introduction of non-native hosts, translocation of pathogens, and increased interaction between wild and farmed populations), followed by host switching. Exposure to wild populations can be reduced through infrastructure and management measures to reduce escapes or exclude wild animals (e.g. barrier nets, filtration and closed-confinement technology). A high standard of health management ensures immunocompetence and resistance to putative new pathogens and strains, and thus reduces the rate of emergence. Appropriate site selection and husbandry can reduce the likelihood of pathogens developing increased virulence by preventing their continuous cycling in geographically or temporally linked populations. The under-reporting of emerging aquatic animal diseases constrains appropriate investigation and timely response. At the producer level, employing information and communications technology (e.g. smartphone applications and Cloud computing) to collect and manage data, coupled with a farmer-centric approach to surveillance, could improve reporting. In addition, reporting behaviours must be understood and disincentives mitigated. At the international level, improving the reporting of emerging diseases to the World Organisation for Animal Health allows Member Countries to implement appropriate measures to reduce transboundary spread. Reporting would be incentivised if the global response included the provision of support to low-income countries to, in the short term, control a reported emerging disease, and, in the longer term, develop aquatic animal health services. Early detection and reporting of emerging diseases are only of benefit if Competent Authorities' responses prevent disease spread. Effective responses to emerging diseases are challenging because basic information and tools are often lacking. Consequently, responses are likely to be sub-optimal unless contingency plans have been developed and tested, and decision-making arrangements have been well established.

Depuis les années 1970, l'aquaculture connaît un taux de croissance de 5 % à 10 % par an. Cette croissance a été rendue possible par le développement de nouvelles filières, l'élevage d'espèces nouvelles (et souvent non autochtones) et l'intensification de la production. Ces caractéristiques du secteur, associées à des transferts massifs d'espèces aquatiques ont entraîné l'émergence de maladies nouvelles, avec des effets négatifs aussi bien sur la production que sur la biodiversité. Les efforts d'amélioration de la gestion des maladies émergentes des animaux aquatiques doivent comporter des mesures visant à réduire l'incidence des maladies émergentes, à améliorer la détection et la notification des maladies et à optimiser les réponses déployées en cas de maladies afin d'en prévenir la propagation. Il est possible de réduire le taux d'émergence des maladies dès lors que les mécanismes sous-jacents à leur survenue sont bien compris et que les mesures appropriées sont prises pour les contrecarrer. Les trois principaux mécanismes d'émergence de maladies, à savoir la colonisation de nouveaux hôtes par des agents pathogènes, la baisse de l'immunocompétence des hôtes et la virulence accrue des agents pathogènes ont plusieurs facteurs déclenchants. Parmi ceux-ci, les plus importants sont ceux qui exposent les hôtes sensibles à des agents pathogènes nouveaux (par exemple l'introduction d'espèces hôtes non autochtones, les transferts d'agents pathogènes et les interactions accrues entre les populations sauvages et d'élevage), suivis par la colonisation de nouvelles espèces hôtes par des agents pathogènes. L'exposition aux populations sauvages peut être atténuée au moyen d'infrastructures appropriées et de mesures de gestion visant à limiter les évasions ou à exclure les espèces sauvages (par exemple, filets de retenue, filtration des eaux et technologies de confinement en système fermé). Une gestion sanitaire de haut niveau qualitatif permet de préserver l'immunocompétence et la résistance à de nouveaux agents et souches pathogènes potentiels, réduisant ainsi le taux d'émergence de nouvelles maladies. Une sélection appropriée du site de production et des techniques d'élevage permet de réduire la probabilité que les agents pathogènes puissent acquérir une virulence accrue, en les empêchant de prolonger leur cycle dans des populations spatialement ou temporellement reliées. La sous-déclaration de maladies émergentes des animaux aquatiques limite les possibilités de procéder à des enquêtes appropriées et d'organiser la réponse en temps voulu. Au niveau des producteurs, le niveau de notification peut être amélioré en recourant aux technologies de l'information et de la communication (par exemple les applications sur téléphonie mobile et l'informatique en nuage) pour la collecte et la gestion des données et en leur associant une méthodologie de la surveillance centrée sur l'éleveur. En outre, il est essentiel de comprendre les comportements en matière de notification et d'atténuer les facteurs de dissuasion. Au niveau international, la notification de maladies émergentes à l'Organisation mondiale de la santé animale permet aux Pays membres de mettre en place des mesures appropriées pour réduire leur propagation transfrontalière. Une méthode incitative envisageable pour améliorer la notification consiste à ce que la réponse mondiale prévoie d'apporter aux pays à faible revenu le soutien nécessaire pour que ceux-ci puissent, à court terme, lutter contre chaque maladie émergente notifiée et, à plus long terme, créer des Services nationaux chargés de la santé des animaux aquatiques. La détection précoce et la notification rapide des maladies émergentes ne portent leurs fruits que si les réponses mises en place par les Autorités compétentes empêchent toute propagation de ces maladies. Le déploiement de réponses efficaces en cas de maladie émergente est difficile, car les pays manquent souvent d'informations et d'outils de base. En conséquence, les réponses sont souvent inadéquates, à moins que des plans d'urgence n'aient été élaborés et testés, soutenus par des instruments décisionnels bien établis.

Desde 1970 la acuicultura ha registrado una tasa de crecimiento anual de entre el 5% y el 10%, cosa que ha logrado expandiéndose a nuevos territorios, cultivando nuevas especies (a menudo no autóctonas) e intensificando la producción. Estas características de la acuicultura, combinadas con los desplazamientos a gran escala de animales, han provocado la aparición de enfermedades y su cortejo de efectos negativos sobre la producción y la diversidad biológica. Las iniciativas para gestionar más eficazmente las enfermedades emergentes de los animales acuáticos deben incluir medidas que reduzcan la tasa de aparición de enfermedades, ayuden a detectarlas y notificarlas y mejoren las respuestas destinadas a impedir que se propaguen. La tasa de aparición de enfermedades se puede reducir entendiendo los mecanismos que subyacen al proceso e implantando medidas para contrarrestarlos. Los tres principales de esos mecanismos (a saber, el cambio de hospedador, la menor inmunocompetencia de los organismos hospedadores y la mayor virulencia de los patógenos) resultan de la suma de muchos factores. Los más importantes son aquellos que entrañan la exposición de un hospedador sensible a nuevos patógenos (p.ej. la introducción de hospedadores no autóctonos, el traslado de patógenos y el aumento de las interacciones entre poblaciones salvajes y poblaciones de cultivo) y aquellos que desembocan en un cambio de hospedador. Para reducir los niveles de exposición a poblaciones salvajes se pueden implantar medidas de gestión o de infraestructura que hagan difícil que los animales escapen o los aíslen de la fauna salvaje (como redes de barrera, filtración y tecnología de confinamiento cerrado). Una gestión sanitaria de buena calidad asegura la inmunocompetencia y la resistencia a cepas y patógenos supuestamente nuevos, reduciendo con ello la tasa de aparición de enfermedades emergentes. La selección de emplazamientos apropiados y el uso de métodos de cría convenientes pueden reducir la probabilidad de que los patógenos adquieran mayor virulencia porque evitan la continuidad de sus ciclos reproductivos entre poblaciones conectadas entre sí, ya sea geográfica o temporalmente. La insuficiente notificación de enfermedades emergentes de los animales acuáticos supone un lastre para estudiarlas debidamente y responder a ellas con celeridad. Las soluciones para mejorar los niveles de notificación trabajando desde la propia explotación podrían pasar por el uso de las tecnologías de información y comunicación (como las aplicaciones de teléfono inteligente o la informática «en nube¼) para obtener y gestionar datos, combinado con fórmulas de vigilancia cuya figura central sea el productor. Es preciso además entender los comportamientos ligados al hecho de notificar o no una enfermedad y restar peso a aquellos factores que desincentiven la notificación. A escala internacional, una más eficaz notificación de enfermedades emergentes a la Organización Mundial de Sanidad Animal permite a los Países Miembros aplicar medidas apropiadas para reducir la propagación transfronteriza. Algo que incentivaría la notificación es que entre las medidas mundiales de respuesta estuviera la prestación de apoyo a los países de renta baja para ayudarlos, a corto plazo, a controlar la enfermedad emergente notificada y, a más largo plazo, a dotarse de buenos servicios de sanidad acuícola. La pronta detección y notificación de enfermedades emergentes solo resulta provechosa si la respuesta de las autoridades competentes evita que la enfermedad se propague. Lo que dificulta una respuesta eficaz a las enfermedades emergentes es la frecuente falta de información y herramientas básicas. Lo más probable, por lo tanto, es que las respuestas no sean las idóneas a menos que se tengan elaborados y ensayados planes de emergencia y se tengan bien implantados mecanismos decisorios al respecto.

Introduction: Improved aquatic animal health management is vital to aquaculture's role in global food security.

Global food security and nutrition depend heavily on aquaculture, the continued growth of which is crucial as the world heads towards a human population of at least 9 billion by 2050, while harvests from wild capture will, at best, stabilise at current levels. Thus, a fundamental question is: how can we sustainably increase aquatic food production? It is clear that aquatic animal diseases present a substantial threat and, consequently, aquatic animal health management has a critical role in food security. An ecosystem approach to aquaculture will mitigate impacts on ecosystem services and biodiversity, and provide the necessary resilience to future disease threats, including those exacerbated by climate change. Due to the nature of aquatic production systems, this approach must encompass fisheries and other sectors that share the same resources. Improved aquatic animal health management must be a key component of aquaculture's future. At the national level, public-private partnerships are vital in achieving objectives of common benefit. Improved disease reporting and response is critical in the control of listed and emerging diseases and can only be achieved through government, industry and stakeholder collaboration. Great potential exists to improve biosecurity from the farm to national level, but this will only be achieved through collaboration. Industry cannot develop effective biosecurity without a clear government strategy and support, specifically legislation which provides an effective framework for safe trade. Governments have a key role in creating a regulatory environment that supports effective biosecurity and is attractive to investment; such as one that supports the development and regulatory approval of therapeutics. The improved control of transboundary diseases requires the wider and more consistent implementation of OIE standards, particularly on disease notification. This can only be achieved through improved collaboration between trading partners and by supporting low- and middle-income countries to strengthen their aquatic animal health services. There is incredible potential for aquaculture to continue its rapid growth and increase its contribution to global food security. However, sustainable growth of aquaculture is threatened by both known diseases, which we cannot effectively control, and new diseases, which may become pandemic. Recent pandemics have shown that global production systems are epidemiologically connected and, consequently, aquatic animal diseases present a shared global threat that demands global solidarity. The world now depends on a sustainable future for aquaculture and improved aquatic animal health management is critical to its continued and growing contribution to global food security.

La sécurité alimentaire et nutritionnelle mondiale dépend fortement de l'aquaculture, dont l'impératif de croissance continue est d'autant plus vital que la population mondiale devrait dépasser les 9 milliards d'habitants d'ici 2050, tandis que le produit des captures en mer se maintiendra, dans le meilleur des cas, aux niveaux actuels. Par conséquent, la question fondamentale est celle de savoir comment accroître les capacités de production durable de denrées alimentaires d'origine aquatique. Il est évident que les maladies des animaux aquatiques présentent une menace importante et que la gestion de la santé des animaux aquatiques joue un rôle déterminant pour la sécurité alimentaire. Une approche de l'aquaculture basée sur les écosystèmes permettra d'atténuer l'impact des maladies sur les services écosystémiques et sur la biodiversité et d'assurer la résilience nécessaire vis-à-vis des futures menaces sanitaires, y compris celles que le changement climatique risque d'amplifier. Compte tenu de la nature des systèmes de production aquatique, cette approche doit couvrir la pêche mais aussi d'autres secteurs partageant les mêmes ressources. L'amélioration de la gestion de la santé des animaux aquatiques est donc une composante essentielle de l'avenir de l'aquaculture. À l'échelle nationale, les partenariats public­privé sont déterminants pour la réussite d'objectifs d'intérêt commun. L'amélioration de la notification des maladies et de la réponse qui leur est apportée est essentielle pour lutter contre les maladies listées et émergentes et ne peut se faire qu'avec la collaboration des gouvernements, du secteur lui-même et des parties prenantes. Il y a une grande marge potentielle d'amélioration de la biosécurité en aquaculture, depuis la ferme jusqu'au niveau national, mais elle ne pourra se réaliser qu'en mettant en place une collaboration effective. La filière aquacole ne peut assurer une biosécurité efficace si elle ne dispose pas du soutien stratégique des gouvernements, en particulier sous forme d'une législation apportant un cadre effectif à la sécurité sanitaire des échanges. Le rôle des gouvernements est déterminant en ce qu'ils instaurent un contexte réglementaire propice à la biosécurité et attractif pour les investisseurs, par exemple en soutenant le développement et l'autorisation réglementée de nouveaux agents thérapeutiques. Fondamentalement, l'amélioration de la lutte contre les maladies transfrontalières passe par une mise en œuvre plus large et cohérente des normes de l'OIE, en particulier celles relatives à la notification des maladies. Cela ne peut se faire qu'à travers une meilleure collaboration entre partenaires commerciaux et le soutien apporté aux pays à revenu faible et intermédiaire afin qu'ils puissent renforcer leurs services chargés de la santé des animaux aquatiques. L'aquaculture a un potentiel de croissance énorme et devrait pouvoir contribuer encore plus à la sécurité alimentaire mondiale. Néanmoins, la croissance durable de l'aquaculture est menacée par des maladies connues mais que nous ne savons pas encore maîtriser efficacement, ainsi que par des maladies nouvelles qui risquent de prendre une dimension pandémique. Les pandémies récentes ont montré l'interconnexion des systèmes de production mondiaux au plan épidémiologique et la menace mondiale que représentent les maladies des animaux aquatiques, menace qui nous concerne tous et exige une solidarité planétaire. Le monde dépend désormais de la possibilité pour l'aquaculture d'avoir un avenir durable, de sorte qu'il est vital d'améliorer la gestion des maladies des animaux aquatiques afin que le secteur puisse continuer à renforcer sa participation à la sécurité alimentaire mondiale.

La nutrición y la seguridad alimentaria del mundo dependen en buena medida de la acuicultura, cuyo continuo crecimiento es esencial cuando el planeta se encamina hacia una población de al menos 9 000 millones de seres humanos para 2050 y cuando la producción resultante de la pesca de captura quedará estancada, en el mejor de los casos, en los niveles actuales. Ello abre un interrogante fundamental: el de cómo incrementar de modo sostenible la producción de alimentos de origen acuático. Está claro que las enfermedades de los animales acuáticos representan una importante amenaza y que, por consiguiente, la gestión de su estado de salud cumple una función básica para la seguridad alimentaria. El hecho de considerar la acuicultura en clave ecosistémica atenuará el impacto de esta actividad sobre los servicios y la diversidad biológica de los ecosistemas y aportará la necesaria resiliencia ante futuras amenazas infecciosas, en particular aquellas que el cambio climático va a exacerbar. Por la propia naturaleza de los sistemas de producción acuícola, esta lógica ecosistémica debe abarcar tanto la pesca como otros sectores que comparten los mismos recursos. Un aspecto clave del porvenir de la acuicultura debe ser una mejor gestión de la sanidad de los animales acuáticos. A escala nacional, las alianzas publicoprivadas son vitales para cumplir una serie de objetivos de interés general. Para combatir las patologías inscritas en las listas, así como las enfermedades emergentes, es fundamental contar con mecanismos más eficaces para notificarlas y responder a ellas, lo que pasa necesariamente por la colaboración entre los poderes públicos, la industria y otras partes interesadas. Hay mucho margen para reforzar la seguridad biológica a todos los niveles, desde el de la explotación hasta el nacional, pero el ingrediente insoslayable para ello es la colaboración. El sector no puede instaurar una seguridad biológica eficaz sin contar con el apoyo y con una estrategia clara de los poderes públicos, y más concretamente sin una legislación que encuadre eficazmente la seguridad del comercio. Los gobiernos tienen una función básica que cumplir estableciendo condiciones reglamentarias que, además de propiciar medidas eficaces de seguridad biológica, atraigan las inversiones, por ejemplo, apoyando los procesos de desarrollo y aprobación reglamentaria de productos terapéuticos. Un factor clave para combatir más eficazmente las enfermedades transfronterizas es una aplicación más extendida y coherente de las normas de la OIE, sobre todo en materia de notificación de enfermedades, lo que pasa necesariamente por una colaboración más estrecha entre socios comerciales y por el apoyo a los países de renta baja y mediana para ayudarlos a fortalecer sus servicios de sanidad de los animales acuáticos. La acuicultura encierra un potencial increíble para seguir creciendo con rapidez y contribuyendo cada vez más a la seguridad alimentaria mundial. Su crecimiento sostenible, empero, está amenazado por las enfermedades, ya se trate de patologías conocidas que no sabemos combatir eficazmente o de nuevas enfermedades que pueden llegar a ser pandémicas. Las últimas pandemias han puesto de relieve que los sistemas productivos mundiales están epidemiológicamente conectados y que por lo tanto las enfermedades de los animales acuáticos constituyen un peligro planetario que a todos amenaza y que exige una respuesta mundial solidaria. El mundo depende ahora de que la acuicultura pueda crecer sosteniblemente en el futuro. En este sentido, una gestión más eficaz de la sanidad acuícola es crucial para que el sector siga contribuyendo, y lo haga cada vez más, a la seguridad alimentaria mundial.

The aquatic animal pandemic crisis.

The growth of aquaculture over the past 50 years has been accompanied by the emergence of aquatic animal diseases, many of which have spread to become pandemic in countries or continents. An analysis of 400 emerging disease events in aquatic animals that were logged by the Centre for Environment, Fisheries and Aquaculture Science between 2002 and 2017 revealed that more than half were caused by viruses. However, in molluscs, most events were parasitic. Categorising these events indicated that the key processes underpinning emergence were the movement of live animals and host switching. Profiles of key pathogens further illustrate the importance of wild aquatic animals as the source of new infections in farmed animals. It is also clear that the spread of new diseases through the largescale movement of aquatic animals for farming, for food and for the ornamental trade has allowed many to achieve pandemic status. Many viral pathogens of fish (e.g. infectious salmon anaemia, viral haemorrhagic septicaemia) and shrimp (e.g. white spot syndrome virus) affect a large proportion of the global production of key susceptible species. Wild aquatic animal populations have also been severely affected by pandemic diseases, best exemplified by Batrachochytrium dendrobatidis, a fungal infection of amphibians, whose emergence and spread were driven by the movement of animals for the ornamental trade. Batrachochytrium dendrobatidis is now widespread in the tropics and subtropics and has caused local extinctions of susceptible amphibian hosts. Given the rising demand for seafood, aquacultural production will continue to grow and diseases will continue to emerge. Some will inevitably achieve pandemic status, having significant impacts on production and trade, unless there are considerable changes in global monitoring and the response to aquatic animal diseases.

Au cours des 50 dernières années, la forte croissance qu'a connue l'aquaculture est allée de pair avec l'émergence de nombreuses maladies affectant les animaux aquatiques, dont certaines se sont propagées jusqu'à devenir pandémiques à l'échelle nationale ou continentale. L'analyse de 400 événements sanitaires survenus chez des animaux aquatiques et consignés entre 2002 et 2017 par le Centre for Environment, Fisheries and Aquaculture Science a déterminé l'origine virale de plus de la moitié d'entre eux. Toutefois, chez les mollusques la plupart des événements analysés étaient d'ordre parasitaire. Le classement des événements par catégories a montré que les principaux processus sous-jacents à cette émergence étaient liés aux transferts d'animaux vivants et à la colonisation de nouveaux hôtes par les agents pathogènes. Les profils des agents pathogènes majeurs illustrent le rôle des espèces aquatiques sauvages en tant que sources d'infections nouvelles chez les animaux aquatiques d'élevage. Il apparaît clairement que la propagation de nouvelles maladies à la faveur des transferts massifs d'animaux aquatiques à des fins d'élevage, de production alimentaire ou de commerce d'espèces d'ornement a conféré un statut pandémique à nombre de ces maladies. De nombreux virus affectant les poissons (par ex., le virus de l'anémie infectieuse du saumon, le virus de la septicémie hémorragique virale) et les crevettes (par ex., le virus du syndrome des points blancs) ont une incidence majeure sur de vastes segments de la production mondiale d'espèces sensibles cruciales. Les populations sauvages d'animaux aquatiques sont également touchées par des maladies pandémiques, dont l'exemple type est l'infection à Batrachochytrium dendrobatidis, une affection fongique des amphibiens dont l'émergence et la propagation sont le fruit des transferts d'animaux aquatiques destinés au commerce aquariophile. Batrachochytrium dendrobatidis est désormais largement présent dans les eaux tropicales et subtropicales où il est responsable d'extinctions locales parmi les espèces d'amphibiens sensibles. La croissance de la production aquacole se poursuivra afin de répondre à une demande toujours plus forte en poissons et fruits de mer, entraînant l'émergence continue de nouvelles maladies. Si des changements déterminants ne sont pas introduits dans la surveillance exercée au niveau mondial sur les maladies des animaux aquatiques et dans la réponse qui leur est apportée, certaines de ces maladies vont inéluctablement acquérir une dimension pandémique avec des conséquences importantes sur la production et le commerce.

El crecimiento de la acuicultura en los últimos 50 años se ha acompañado de la aparición de enfermedades de los animales acuáticos, que en muchos casos se han propagado hasta llegar a ser pandémicas en ciertos países o continentes. Tras analizar 400 episodios de enfermedades emergentes de animales acuáticos registrados entre 2002 y 2017 por el Centre for the Environment, Fisheries and Aquaculture Science, los autores constataron que más de la mitad de esos episodios fueron causados por virus, si bien en el caso de los moluscos la mayoría de ellos eran parasitarios. De la clasificación de esos episodios se desprende que los procesos básicos que subyacen a su aparición son los desplazamientos de animales vivos y los cambios de anfitrión. El perfil de los principales patógenos revela además la importancia que revisten los animales acuáticos silvestres como fuente de nuevas infecciones de los animales de acuicultura. También está claro que la propagación de nuevas enfermedades por el movimiento a gran escala de animales acuáticos con fines de producción acuícola, consumo alimentario o comercio de animales ornamentales ha propiciado que muchas de ellas adquieran carácter pandémico. Muchos patógenos víricos de los peces (como el virus de la anemia infecciosa del salmón o el de la septicemia hemorrágica viral) y camarones (como el virus del síndrome de las manchas blancas) afectan a una gran parte de la producción mundial de las principales especies sensibles. Las poblaciones silvestres de animales acuáticos también se han visto afectadas de gravedad por enfermedades pandémicas, como ejemplifica perfectamente la infección por Batrachochytrium dendrobatidis, micosis de los anfibios cuya aparición y propagación fue alimentada por el comercio y el consiguiente movimiento de animales con fines ornamentales. Este hongo, muy extendido ahora en las regiones tropicales y subtropicales, ha causado la extinción en ciertas áreas de especies anfibias sensibles. Habida cuenta de la creciente demanda de alimentos de origen marino, la producción acuícola seguirá creciendo y también seguirán surgiendo enfermedades. Inevitablemente, algunas de ellas se harán pandémicas y resultarán muy dañinas para la producción y el comercio, a menos que haya cambios de calado en los sistemas mundiales de vigilancia y respuesta ante las enfermedades de los animales acuáticos.

Epidemiology of Bonamia in the UK, 1982 to 2012.

Bonamiasis, caused by Bonamia ostreae, was confirmed in native flat oysters Ostrea edulis L. in England in 1982. Hudson & Hill (1991; Aquaculture 93:279-285) documented investigations into the initial spread of the disease in wild and cultivated stocks of native oysters in the UK. They also described the controls that were initially applied to prevent the further spread of the pathogen. This paper reports on subsequent controls and associated monitoring applied in the UK and reports on the epidemiology of the disease in the 30 yr from 1982 to 2012. Bonamiasis remained confined to the zones in England as documented by Hudson & Hill (1991) until 2005, when it was confirmed in Lough Foyle, Northern Ireland. In 2006 it was found in 2 new areas, one in Wales and one in Scotland. Subsequent further spread to additional areas in all parts of the UK has resulted in 9 zones being currently designated as infected with the disease. In addition, a single oyster from one area has tested positive for the closely related B. exitiosa. In general, analysis of the results of the monitoring programme in England and Wales shows no clear trend in infection levels over time, although there has been an apparent decrease in the level of infection in some fishery areas. In an autumn sampling programme the highest levels of infection were detected in October.

Acute dermatitis in farmed trout: an emerging disease.

A new skin condition, known as puffy skin disease (PSD), emerged in farmed rainbow trout Oncorhynchus mykiss (Walbaum) in 2002. The number of new cases increased considerably from 2006. Clinical signs include white or grey skin patches, which become raised and red with excessive mucous production and scale loss. Fish are inappetant and lose condition. Histologically, the key feature is epithelial hyperplasia. We undertook a questionnaire study of trout farmers in England and Wales to investigate prevalence and risk factors. PSD was reported on 37% (n = 49) of rainbow trout sites, located in 28 river catchments. The increase in cases from 2006 onwards was mirrored by the increase in red mark syndrome (RMS). Prevalence and severity of PSD were highest in the summer months. The presence of PSD was associated with RMS (OR = 9.7, P < 0.001). Sites receiving live rainbow trout in the previous 12 months were considerably more likely to have PSD (OR = 5.3. P < 0.01), which suggests an infectious aetiology. The size of affected fish and prevalence varied between farms, indicating that farm-level factors are important. Future research should further investigate the aetiology of PSD and practices to manage the disease.

Differential characterization of emerging skin diseases of rainbow trout--a standardized approach to capturing disease characteristics and development of case definitions.

Farmed and wild salmonids are affected by a variety of skin conditions, some of which have significant economic and welfare implications. In many cases, the causes are not well understood, and one example is cold water strawberry disease of rainbow trout, also called red mark syndrome, which has been recorded in the UK since 2003. To date, there are no internationally agreed methods for describing these conditions, which has caused confusion for farmers and health professionals, who are often unclear as to whether they are dealing with a new or a previously described condition. This has resulted, inevitably, in delays to both accurate diagnosis and effective treatment regimes. Here, we provide a standardized methodology for the description of skin conditions of rainbow trout of uncertain aetiology. We demonstrate how the approach can be used to develop case definitions, using coldwater strawberry disease as an example.

Farm level bio-economic modelling of aquatic animal disease and health interventions.

A farm level bio-economic model, for aquatic animal production, of the relationships between inputs (e.g. purchased animals), outputs (e.g. harvested animals) and gross margin (GM) was developed to assess ex-ante the economics of disease and animal health interventions. Feed costs were calculated from estimates of food conversion ratio (FCR), animals harvested and mortality. The model was applied to a typical grow-out rainbow trout (Oncorhynchus mykiss) farm on Lake Titicaca, Peru and a typical shrimp (Paenus vannamei) farm in the Mekong Delta, Vietnam. The model was used in two analyses. Firstly, an approach to assess the burden of disease developed by the Global Burden of Animal Diseases (GBADs) project was adopted. Output under conditions of 'ideal health' was estimated by reducing mortality to zero and removing health costs. GM in both systems increased by approximately 25% when production was kept constant (and stocking rates reduced) and more than doubled if production was allowed to rise (and initial stocking increased). The increase in GM under conditions of ideal compared with current production provided an estimate of the maximum possible benefit from improved health management. Secondly, break-even analysis was used to assess the economics of vaccination against infectious pancreatic necrosis (IPN) vaccine (rainbow trout - RBT) and probiotics (shrimp). If initial stocking was kept constant, and production allowed to rise, break-even points for the intervention (when GM was the same with and without the intervention) were achieved when mortality was reduced by 16% in RBT fry and juvenile and 28% in shrimp. If production was kept constant and benefit realised by reduced initial stocking, the break-even point was achieved for i) vaccination of RBT when mortality in fry and juveniles was reduced by 39%, and ii) probiotics in shrimp production when there was a 15% reduction in mortality (nursery and grow-out), 10% increase in shrimp weight at harvest and 10% improvement in FCR. The results demonstrate how relatively simple models, parameterised with basic farm production data, can assess the burden of disease and quantify ex-ante the potential benefit of interventions. In the absence of trial data, these analyses support decision-making by farmers. The models can be adapted for many aquaculture systems. Farm level results can be extrapolated to estimate disease burden, and benefits of interventions, at regional or national level and thus support informed decision-making and allocation of resources to health management.

Disease will limit future food supply from the global crustacean fishery and aquaculture sectors.

Seafood is a highly traded food commodity. Farmed and captured crustaceans contribute a significant proportion with annual production exceeding 10 M metric tonnes with first sale value of $40bn. The sector is dominated by farmed tropical marine shrimp, the fastest growing sector of the global aquaculture industry. It is significant in supporting rural livelihoods and alleviating poverty in producing nations within Asia and Latin America while forming an increasing contribution to aquatic food supply in more developed countries. Nations with marine borders often also support important marine fisheries for crustaceans that are regionally traded as live animals and commodity products. A general separation of net producing and net consuming nations for crustacean seafood has created a truly globalised food industry. Projections for increasing global demand for seafood in the face of level or declining fisheries requires continued expansion and intensification of aquaculture while ensuring best utilisation of captured stocks. Furthermore, continued pressure from consuming nations to ensure safe products for human consumption are being augmented by additional legislative requirements for animals (and their products) to be of low disease status. As a consequence, increasing emphasis is being placed on enforcement of regulations and better governance of the sector; currently this is a challenge in light of a fragmented industry and less stringent regulations associated with animal disease within producer nations. Current estimates predict that up to 40% of tropical shrimp production (>$3bn) is lost annually, mainly due to viral pathogens for which standard preventative measures (e.g. such as vaccination) are not feasible. In light of this problem, new approaches are urgently required to enhance yield by improving broodstock and larval sourcing, promoting best management practices by farmer outreach and supporting cutting-edge research that aims to harness the natural abilities of invertebrates to mitigate assault from pathogens (e.g. the use of RNA interference therapeutics). In terms of fisheries losses associated with disease, key issues are centred on mortality and quality degradation in the post-capture phase, largely due to poor grading and handling by fishers and the industry chain. Occurrence of disease in wild crustaceans is also widely reported, with some indications that climatic changes may be increasing susceptibility to important pathogens (e.g. the parasite Hematodinium). However, despite improvements in field and laboratory diagnostics, defining population-level effects of disease in these fisheries remains elusive. Coordination of disease specialists with fisheries scientists will be required to understand current and future impacts of existing and emergent diseases on wild stocks. Overall, the increasing demand for crustacean seafood in light of these issues signals a clear warning for the future sustainability of this global industry. The linking together of global experts in the culture, capture and trading of crustaceans with pathologists, epidemiologists, ecologists, therapeutics specialists and policy makers in the field of food security will allow these issues to be better identified and addressed.

A seafood risk tool for assessing and mitigating chemical and pathogen hazards in the aquaculture supply chain.

Intricate links between aquatic animals and their environment expose them to chemical and pathogenic hazards, which can disrupt seafood supply. Here we outline a risk schema for assessing potential impacts of chemical and microbial hazards on discrete subsectors of aquaculture-and control measures that may protect supply. As national governments develop strategies to achieve volumetric expansion in seafood production from aquaculture to meet increasing demand, we propose an urgent need for simultaneous focus on controlling those hazards that limit its production, harvesting, processing, trade and safe consumption. Policies aligning national and international water quality control measures for minimizing interaction with, and impact of, hazards on seafood supply will be critical as consumers increasingly rely on the aquaculture sector to supply safe, nutritious and healthy diets.

The spread of pathogens through trade in aquatic animals and their products.

It is well known that the transboundary spread of infectious diseases is aided by trade in live animals and the consequences can be severe if, as a result, a pathogen broadens its host range to new species. Trade in aquatic animal species is increasing, and aquaculture is also expanding to meet the growing human population's demands for animal protein. Moreover, it is clear that aquaculture has created potential new pathways by which pathogens and diseases may be introduced or spread to new areas. The risk of pathogen transfer is generally considered greater for the movement of live aquatic animals than for the movement of processed and dead products. The currently available health standards support the concept of minimising the risk of disease and pathogen incursion while, at the same time, avoiding unjustifiable or unnecessary impediments to trade. Nevertheless, the international spread of diseases through the movement of animals still occurs, despite these standards. Consequently, this paper considers the evidence linking international trade in aquatic animals and aquatic animal-derived products with the transmission and spread of diseases. The authors provide examples of pathogen transfer leading to disease spread and considerthe situation of emerging diseases, as well as the need for a holistic approach to deal with risk-based threats at their source.

Koi herpesvirus: distribution and prospects for control in England and Wales.

Koi herpesvirus (KHV) causes a highly virulent disease affecting carp, Cyprinus carpio L., and poses a serious socio-economic threat to the UK carp industry. This study aimed to determine the geographic distribution and prevalence of KHV exposed fish in England and Wales through ELISA antibody testing. Only three of the 82 farms sampled produced positive results, suggesting fish farms provide a relatively safe source of fish. Of the 71 'high-risk' fisheries tested, 26 were positive. All eight geographic areas within England and Wales studied had at least one KHV positive site. Twelve consignments of imported koi carp from seven S.E. Asian countries were tested for KHV antibody. Six consignments from six different countries were positive. Although a high proportion of consignments were positive, the results indicate that lower risk stocks of fish exist that could be sourced by the ornamental carp sector. The study provides evidence that KHV is widespread and prevalent in 'high-risk' fisheries. There are, however, prospects for controlling KHV as English and Welsh farms appear to be relatively free of the virus, and in most cases fish are not moved from fisheries to other waters.

Comparative assessment of live cyprinid and salmonid movement networks in England and Wales.

Disease poses a significant threat to aquaculture. While there are a number of factors contributing to pathogen transmission risk, movement of live fish is considered the most important. Understanding live fish movement patterns for different aquaculture sectors is therefore crucial to predicting disease occurrence and necessary for the development of effective, risk-based biosecurity, surveillance and containment policies. However, despite this, our understanding of live movement patterns of key aquaculture species, namely salmonids and cyprinids, within England and Wales remains limited. In this study, networks reflecting live fish movements associated with the cyprinid and salmonid sectors in England and Wales were constructed. The structure, composition and key attributes of each network were examined and compared to provide insight into the nature of trading patterns and connectedness, as well as highlight sites at a high risk of spreading disease. Connectivity at both site and catchment level was considered to facilitate understanding at different resolutions, providing further insight into disease outbreaks, with industry wide implications. The study highlighted that connectivity through live fish movements was extensive for both industries. The salmonid and cyprinid networks comprised 2533 and 3645 nodes, with a network density of 5.81 × 10-4 and 4.2 × 10-4, respectively. The maximum network reach of 2392 in the salmonid network was higher, both in absolute terms and as a proportion of the overall network, compared to maximum network reach of 2085 in the cyprinid network. However, in contrast, the number of sites in the cyprinid network with a network reach greater than one was 513, compared to 171 in the salmonid network. Patterns of connectivity indicated potential for more frequent yet smaller scale disease outbreaks in the cyprinid industry and less frequent but larger scale outbreaks in the salmonid industry. Further, high connectivity between river catchments within both networks was shown, posing challenges for zoning at the catchment level for the purpose of disease management. In addition to providing insight into pathogen transmission and epidemic potential within the salmonid and cyprinid networks, the study highlights the utility of network analysis, and the value of accessible, accurate live fish movement data in this context. The application of outputs from this study, and network analysis methodology, to inform future disease surveillance and control policies, both within England and Wales and more broadly, is discussed.

Sustainable aquaculture through the One Health lens.

Aquaculture is predicted to supply the majority of aquatic dietary protein by 2050. For aquaculture to deliver significantly enhanced volumes of food in a sustainable manner, appropriate account needs to be taken of its impacts on environmental integrity, farmed organism health and welfare, and human health. Here, we explore increased aquaculture production through the One Health lens and define a set of success metrics - underpinned by evidence, policy and legislation - that must be embedded into aquaculture sustainability. We provide a framework for defining, monitoring and averting potential negative impacts of enhanced production - and consider interactions with land-based food systems. These metrics will inform national and international science and policy strategies to support improved aquatic food system design.

Assessment of exotic fish disease introduction and establishment in the United Kingdom via live fish transporters.

Live fish transporters returning empty from mainland Europe may mechanically introduce exotic pathogens and parasites to the UK. A qualitative risk assessment approach was adopted to investigate the likelihood of introduction and establishment in rainbow trout farms of viral haemorrhagic septicaemia (VHS), infectious haematopoietic necrosis (IHN) and Gyrodactylus salaris via this route. A scenario tree was developed and estimates made for the likelihood of each step based on a review of the available information. The level of uncertainty associated with each step was qualitatively assessed. The likelihood of a lorry becoming contaminated with any of the 3 hazards was only greater than negligible if the lorry made movements between farms in mainland Europe. In these circumstances, the overall likelihood of introduction and establishment was extremely low (would occur very rarely), extremely low to negligible and very low (would occur rarely) for VHS, IHN and G. salaris, respectively. A high level of uncertainty existed due to the lack of data on farm-level prevalence, minimum infectious dose (of the viral hazards) and the large variability in duration and conditions of transport. A telephone survey of live fish transporters found that cleaning and disinfection practices after return to the UK were implemented. Currently, no UK-based transporters make movements between farms in mainland Europe. Thus, the likelihood that UK-owned transporters may become infected is negligible. Changes in the way in which UK-based live fish transporters operate in mainland Europe need to be monitored and development of a code of practice to minimise the risk of disease introduction considered.

Demonstrating freedom from Gyrodactylus salaris (Monogenea: Gyrodactylidae) in farmed rainbow trout Oncorhynchus mykiss.

This paper describes an approach to demonstrate freedom of individual rainbow trout farms from Gyrodactylus salaris Malmberg, 1957. The infection status of individual farms is relevant should G. salaris be introduced into a country or zone previously known to be free of the parasite. Trade from farms where G. salaris may have been introduced would be restricted until freedom had been demonstrated. Cage, fish and parasite sample sizes were calculated based on the minimum detectable prevalence (P*), test characteristics, population size, and Type I and II errors. Between 5 and 23 cages per farm would need to be sampled to demonstrate freedom at a cage level P* of 10%. The number of fish sampled per cage depended mainly on the test sensitivity (probability of correctly identifying an infected fish). Assuming a test sensitivity of 99% at the fish level, 59 fish per cage are needed (P* = 5%). Since G. salaris may exist in mixed infection with G. derjavini, testing a sample of gyrodactylid parasites may not result in the parasite being detected when present. Test sensitivity at the fish level depends on the number of gyrodactylids on the fish, the proportion of which are G. salaris and the number examined. Assuming a P* of 5% (i.e. G. salaris are at least 5% of the gyrodactylid population), between 20 and 73 parasites per fish would need to be sampled (depending on abundance) to maintain the Type I error at 0.01 (thus a fish level test sensitivity of 99%). This work identifies the critical information, and further research, needed to assess freedom from G. salaris with a known level of confidence; this is essential to provide a sound scientific basis for decision-making about disease control measures.

Emergence of cold water strawberry disease of rainbow trout Oncorynchus mykiss in England and Wales: outbreak investigations and transmission studies.

Cold water strawberry disease (CWSD), or red mark syndrome (RMS), is a severe dermatitis affecting the rainbow trout Oncorynchus mykiss. The condition, which presents as multifocal, raised lesions on the flanks of affected fish, was first diagnosed in Scotland in 2003 and has since spread to England and Wales. Results of field investigations indicated the condition had an infectious aetiology, with outbreaks in England linked to movements of live fish from affected sites in Scotland. Transmission trials confirmed these results, with 11 of 149 and 106 of 159 naive rainbow trout displaying CWSD-characteristic lesions 104 to 106 d after being cohabited with CWSD-affected fish from 2 farms (Farm B from England and Farm C from Wales, respectively). The condition apparently has a long latency, with the first characteristic lesions in the previously naive fish not definitively observed until 65 d (650 day-degrees) post-contact with affected fish. Affected fish from both outbreak investigations and the infection trial were examined for the presence of viruses, oomycetes, parasites and bacteria using a combination of techniques and methodologies (including culture-independent cloning of PCR-amplified bacterial 16S rRNA genes from lesions), with no potentially causative infectious agent consistently identified. The majority of the cloned phylotypes from both lesion and negative control skin samples were assigned to Acidovorax-like beta-Proteobacteria and Methylobacterium-like alpha-Proteobacteria.

An assessment of the variation in the prevalence of renal myxosporidiosis and hepatitis in wild brown trout, Salmo trutta L., within and between rivers in South-West England.

The prevalence of renal myxosporidiosis in wild brown trout, Salmo trutta, in seven river catchments in South-West England was investigated. Three hundred and twenty-seven fish were sampled from 16 sites, of which 54 (16.5%) were found, by histological examination of the kidney, to be infected with Tetracapsuloides bryosalmonae, the causative agent of proliferative kidney disease. No T. bryosalmonae infected fish were found in one river catchment, in other catchments the prevalence ranged from 2.5% to 36%. Hepatitis was strongly associated with the presence of T. bryosalmonae (odds ratio = 20.2, P < 0.001). Chloromyxum schurovi was found in 25% of fish and in six of seven river catchments, where the prevalence ranged from 2.4% to 63%. There was a strong negative association between the presence of T. bryosalmonae and C. schurovi (odds ratio = 0.10, P < 0.001). A hierarchical binomal model of the variance indicated that for T. bryosalmonae most of the variance existed at the site level, whereas for C. schurovi most variance existed at the river catchment level, suggesting that prevalence of T. bryosalmonae infection is determined largely by site level factors (e.g. presence of alternate host). The intraclass correlation coefficients (ICC) were 0.2 and 0.4 for T. bryosalmonae and C. schurovi, respectively, indicating the latter has higher effective transmission because of a higher level of infectiousness and/or abundance of alternate oligochaete hosts. These values can be used in future studies to estimate the sample sizes required to generate prevalence estimates with the required precision.

The application of risk analysis in aquatic animal health management.

Risk analysis has only been regularly used in the management of aquatic animal health in recent years. The Agreement on the Application of Sanitary and Phytosanitary measures (SPS) stimulated the application of risk analysis to investigate disease risks associated with international trade (import risk analysis-IRA). A majority (9 of 17) of the risk analyses reviewed were IRA. The other major focus has been the parasite of Atlantic salmon--Gyrodactylus salaris. Six studies investigated the spread of this parasite, between countries, rivers and from farmed to wild stocks, and clearly demonstrated that risk analysis can support aquatic animal health policy development, from international trade and biosecurity to disease interaction between wild and farmed stocks. Other applications of risk analysis included the spread of vertically transmitted pathogens and disease emergence in aquaculture. The Covello-Merkhofer, risk analysis model was most commonly used and appears to be a flexible tool not only for IRA but also the investigation of disease spread in other contexts. The limitations of the identified risk assessments were discussed. A majority were qualitative, partly due to the lack of data for quantitative analysis, and this, it can be argued, constrained their usefulness for trade purposes (i.e. setting appropriate sanitary measures); in other instances, a qualitative result was found to be adequate for decision making. A lack of information about the disease hazards of the large number of fish species traded is likely to constrain quantitative analysis for a number of years. The consequence assessment element of a risk analysis was most likely to be omitted, or limited in scope and depth, rarely extending beyond examining the evidence of susceptibility of farmed and wild species to the identified hazard. The reasons for this are discussed and recommendations made to develop guidelines for a consistent, systematic and multi-disciplinary approach to consequence assessment. Risk analysis has improved decision making in aquatic animal health management by providing a transparent method for using the available scientific information. The lack of data is the main constraint to the application of risk analysis in aquatic animal health. The identification of critical parameters is an important output from risk analysis models which should be used to prioritise research.

A Simple Model to Rank Shellfish Farming Areas Based on the Risk of Disease Introduction and Spread.

The European Union Council Directive 2006/88/EC requires that risk-based surveillance (RBS) for listed aquatic animal diseases is applied to all aquaculture production businesses. The principle behind this is the efficient use of resources directed towards high-risk farm categories, animal types and geographic areas. To achieve this requirement, fish and shellfish farms must be ranked according to their risk of disease introduction and spread. We present a method to risk rank shellfish farming areas based on the risk of disease introduction and spread and demonstrate how the approach was applied in 45 shellfish farming areas in England and Wales. Ten parameters were used to inform the risk model, which were grouped into four risk themes based on related pathways for transmission of pathogens: (i) live animal movement, (ii) transmission via water, (iii) short distance mechanical spread (birds) and (iv) long distance mechanical spread (vessels). Weights (informed by expert knowledge) were applied both to individual parameters and to risk themes for introduction and spread to reflect their relative importance. A spreadsheet model was developed to determine quantitative scores for the risk of pathogen introduction and risk of pathogen spread for each shellfish farming area. These scores were used to independently rank areas for risk of introduction and for risk of spread. Thresholds were set to establish risk categories (low, medium and high) for introduction and spread based on risk scores. Risk categories for introduction and spread for each area were combined to provide overall risk categories to inform a risk-based surveillance programme directed at the area level. Applying the combined risk category designation framework for risk of introduction and spread suggested by European Commission guidance for risk-based surveillance, 4, 10 and 31 areas were classified as high, medium and low risk, respectively.

Investigation of risk factors for clinical mastitis in British dairy herds with bulk milk somatic cell counts less than 150,000 cells/ml.

A sample of dairy farms in Great Britain with a monthly bulk milk somatic cell count of less than 150,000 cells/ml was enrolled into a 12-month prospective study. At the end of the study, a questionnaire on milking practice and other farm management practices was sent to the 482 farmers who had collected data on the occurrence of mastitis throughout the 12 months. The response rate was 93 per cent. The reported mean incidence of clinical mastitis was 36.9 cases per 100 cow-years. Factors associated with an increase in the incidence of clinical mastitis were cleaning out the straw yard less frequently than every six weeks, more than 5 per cent of cows leaking milk outside the parlour, checking the foremilk, wearing gloves during milking, an average annual milk yield of more than 7000 litres per cow, dipping or spraying teats before milking and keeping milk with a high somatic cell count out of the bulk tank. Factors associated with a decrease in the incidence of clinical mastitis were using a cloth to dry the teats after washing them as part of premilking preparation, using calving boxes for less than 40 per cent of calvings, and using both cubicles and straw yards to house dry cows, as opposed to other housing.