The application of epidemiology in aquatic animal health -opportunities and challenges

ABSTRACT: Over recent years the growth in aquaculture, accompanied by the emergence of new and transboundary diseases, has stimulated epidemiological studies of aquatic animal diseases. Great potential exists for both observational and theoretical approaches to investigate the processes driving emergence but, to date, compared to terrestrial systems, relatively few studies exist in aquatic animals. Research using risk methods has assessed routes of introduction of aquatic animal pathogens to facilitate safe trade (e.g. import risk analyses) and support biosecurity. Epidemiological studies of risk factors for disease in aquaculture (most notably Atlantic salmon farming) have effectively supported control measures. Methods developed for terrestrial livestock diseases (e.g. risk-based surveillance) could improve the capacity of aquatic animal surveillance systems to detect disease incursions and emergence. The study of disease in wild populations presents many challenges and the judicious use of theoretical models offers some solutions. Models, parameterised from observational studies of host pathogen interactions, have been used to extrapolate estimates of impacts on the individual to the population level. These have proved effective in estimating the likely impact of parasite infections on wild salmonid populations in Switzerland and Canada (where the importance of farmed salmon as a reservoir of infection was investigated). A lack of data is often the key constraint in the application of new approaches to surveillance and modelling. The need for epidemiological approaches to protect aquatic animal health will inevitably increase in the face of the combined challenges of climate change, increasing anthropogenic pressures, limited water sources and the growth in aquaculture. TABLE OF CONTENTS: 1 Introduction 42 The development of aquatic epidemiology 73 Transboundary and emerging diseases 93.1 Import risk analysis (IRA) 103.2 Aquaculture and disease emergence 113.3 Climate change and disease emergence 133.4 Outbreak investigations 134 Surveillance and surveys 154.1 Investigation of disease prevalence 154.2 Developments in surveillance methodology 164.2.1 Risk-based surveillance and scenario tree modelling 164.2.2 Spatial and temporal analysis 164.3 Test validation 175 Spread, establishment and impact of pathogens 185.1 Identifying routes of spread 185.1.1 Ex-ante studies of disease spread 195.1.2 Ex-post observational studies 215.2 Identifying risk factors for disease establishment 235.3 Assessing impact at the population level 245.3.1 Recording mortality 245.3.2 Farm health and production records 265.3.3 Assessing the impact of disease in wild populations 276 Conclusions 317 Competing interests 328 Authors' contributions 329 Acknowledgements 3310 References 33.     

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.     

Global trade in ornamental fish from an Australian perspective: the case for revised import risk analysis and management strategies

Over 1 billion ornamental fish comprising more than 4000 freshwater and 1400 marine species are traded internationally each year, with 8-10 million imported into Australia alone. Compared to other commodities, the pathogens and disease translocation risks associated with this pattern of trade have been poorly documented. The aim of this study was to conduct an appraisal of the effectiveness of risk analysis and quarantine controls as they are applied according to the Sanitary and Phytosanitary (SPS) agreement in Australia. Ornamental fish originate from about 100 countries and hazards are mostly unknown; since 2000 there have been 16-fold fewer scientific publications on ornamental fish disease compared to farmed fish disease, and 470 fewer compared to disease in terrestrial species (cattle). The import quarantine policies of a range of countries were reviewed and classified as stringent or non-stringent based on the levels of pre-border and border controls. Australia has a stringent policy which includes pre-border health certification and a mandatory quarantine period at border of 1-3 weeks in registered quarantine premises supervised by government quarantine staff. Despite these measures there have been many disease incursions as well as establishment of significant exotic viral, bacterial, fungal, protozoal and metazoan pathogens from ornamental fish in farmed native Australian fish and free-living introduced species. Recent examples include Megalocytivirus and Aeromonas salmonicida atypical strain. In 2006, there were 22 species of alien ornamental fish with established breeding populations in waterways in Australia and freshwater plants and molluscs have also been introduced, proving a direct transmission pathway for establishment of pathogens in native fish species. Australia's stringent quarantine policies for imported ornamental fish are based on import risk analysis under the SPS agreement but have not provided an acceptable level of protection (ALOP) consistent with government objectives to prevent introduction of pests and diseases, promote development of future aquaculture industries or maintain biodiversity. It is concluded that the risk analysis process described by the Office International des Epizooties under the SPS agreement cannot be used in a meaningful way for current patterns of ornamental fish trade. Transboundary disease incursions will continue and exotic pathogens will become established in new regions as a result of the ornamental fish trade, and this will be an international phenomenon. Ornamental fish represent a special case in live animal trade where OIE guidelines for risk analysis need to be revised. Alternatively, for countries such as Australia with implied very high ALOP, the number of species traded and the number of sources permitted need to be dramatically reduced to facilitate hazard identification, risk assessment and import quarantine controls.     

Epidemiological approach to aquatic animal health management: opportunities and challenges for developing countries to increase aquatic production through aquaculture

Aquaculture appears to have strongest potential to meet the increasing demands for aquatic products in most regions of the world. The world population is on the increase, as is the demand for aquatic food products. Production from capture fisheries at a global level is levelling off. Potential contributions from aquaculture to local food security, livelihoods and nutrition can be highly significant, especially in many remote and resource-poor rural areas. One of the major constraints to aquaculture production is the losses due to diseases. Over the decades, the sector has faced significant problems with disease outbreaks and epidemics which caused significant economic losses. The use of sound epidemiological principles and logical and science-based approach to identify and manage risks comprise two of the most important components of an effective biosecurity program. The maintenance of effective biosecurity in aquaculture is becoming more and more essential. There will be more demand for aquatic animal epidemiologists as well as epidemiological tools/resources in the region. The use of epidemiology will significantly improve health management, risk analysis and disease control. Although there are clear limitations and complications in the use of epidemiology for controlling aquatic animal pathogens, some positive results have recently emerged from a series of studies and trials to control diseases affecting the small-scale shrimp farming sector in southern India. This paper summarises the results of one such study which emphasizes the significant benefit of close collaboration with farmers, both individually and as groups, and capacity and awareness building among them and the importance of understanding the risk factors and implementing better management practices.     

SARS-CoV-2 in animals: potential for unknown reservoir hosts and public health implications

Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2, previously 2019-nCoV) is suspected of having originated in 2019 in China from a coronavirus infected bat of the genus Rhinolophus. Following the initial emergence, possibly facilitated by a mammalian bridge host, SARS-CoV-2 is currently transmitted across the globe via efficient human-to-human transmission. Results obtained from experimental studies indicate that animal species such as cats, ferrets, raccoon dogs, cynomolgus macaques, rhesus macaques, white-tailed deer, rabbits, Egyptian fruit bats, and Syrian hamsters are susceptible to SARS-CoV-2 infection, and that cat-to-cat and ferret-to-ferret transmission can take place via contact and air. However, natural infections of SARS-CoV-2 have been reported only in pet dogs and cats, tigers, lions, snow leopards, pumas, and gorillas at zoos, and farmed mink and ferrets. Even though human-to-animal spillover has been reported at several instances, SARS-CoV-2 transmission from animals-to-humans has only been reported from mink-to-humans in mink farms. Following the rapid transmission of SARS-CoV-2 within the mink population, a new mink-associated SARS-CoV-2 variant emerged that was identified in both humans and mink. The increasing reports of SARS-CoV-2 in carnivores indicate the higher susceptibility of animal species belonging to this order. The sporadic reports of SARS-CoV-2 infection in domestic and wild animal species require further investigation to determine if SARS-CoV-2 or related Betacoronaviruses can get established in kept, feral or wild animal populations, which may eventually act as viral reservoirs. This review analyzes the current evidence of SARS-CoV-2 natural infection in domestic and wild animal species and their possible implications on public health.     

Disease and health management in Asian aquaculture

Asia contributes more than 90% to the world's aquaculture production. Like other farming systems, aquaculture is plagued with disease problems resulting from its intensification and commercialization. This paper describes the various factors, providing specific examples, which have contributed to the current disease problems faced by what is now the fastest growing food-producing sector globally. These include increased globalization of trade and markets; the intensification of fish-farming practices through the movement of broodstock, postlarvae, fry and fingerlings; the introduction of new species for aquaculture development; the expansion of the ornamental fish trade; the enhancement of marine and coastal areas through the stocking of aquatic animals raised in hatcheries; the unanticipated interactions between cultured and wild populations of aquatic animals; poor or lack of effective biosecurity measures; slow awareness on emerging diseases; the misunderstanding and misuse of specific pathogen free (SPF) stocks; climate change; other human-mediated movements of aquaculture commodities. Data on the socio-economic impacts of aquatic animal diseases are also presented, including estimates of losses in production, direct and indirect income and employment, market access or share of investment, and consumer confidence; food availability; industry failures. Examples of costs of investment in aquatic animal health-related activities, including national strategies, research, surveillance, control and other health management programmes are also provided. Finally, the strategies currently being implemented in the Asian region to deal with transboundary diseases affecting the aquaculture sector are highlighted. These include compliance with international codes, and development and implementation of regional guidelines and national aquatic animal health strategies; new diagnostic and therapeutic techniques and new information technology; new biosecurity measures including risk analysis, epidemiology, surveillance, reporting and planning for emergency response to epizootics; targeted research; institutional strengthening and manpower development (education, training and extension research and diagnostic services).     

Selective breeding in fish and conservation of genetic resources for aquaculture

To satisfy increasing demands for fish as food, progress must occur towards greater aquaculture productivity whilst retaining the wild and farmed genetic resources that underpin global fish production. We review the main selection methods that have been developed for genetic improvement in aquaculture, and discuss their virtues and shortcomings. Examples of the application of mass, cohort, within family, and combined between-family and within-family selection are given. In addition, we review the manner in which fish genetic resources can be lost at the intra-specific, species and ecosystem levels and discuss options to best prevent this. We illustrate that fundamental principles of genetic management are common in the implementation of both selective breeding and conservation programmes, and should be emphasized in capacity development efforts. We highlight the value of applied genetics approaches for increasing aquaculture productivity and the conservation of fish genetic resources.     

Piscirickettsiosis and piscirickettsiosis-like infections in fish: a review

Piscirickettsia salmonis was the first "rickettsia-like" bacteria to be recognized as a pathogenic agent of fish. Since the first reports of piscirickettsiosis emerged from Chile in the late 1980s, Piscirickettsia-like bacteria have been recognized with increasing frequency in a variety of fish species, from both fresh and saltwaters around the world. Although the first reported incidents of Piscirickettsia were in salmonids, Piscirickettsia-like bacteria are now being frequently associated with disease syndromes in non-salmonid fish. Mortalities have occurred in white seabass (Atactoscion noblis), black seabass (Dicentrarchus sp.), tilapia (Oreochromis, Tilapia and Sarotherodon spp.) and blue-eyed plecostomus (Panaque suttoni). Piscirickettsiosis and piscirickettsiosis-like diseases have affected aquaculture productivity, profitability, the species of fish compatible with commercial rearing, and transportation of fish from site to site. Piscirickettsiosis and syndromes caused by similar bacteria are an emerging disease complex that will increasingly inhibit fish production.     

State of the art and future trends of European and Italian aquaculture

This paper describes the main features of fish aquaculture in Europe and Italy focusing attention on single sectors of the farmed species and their trend for the future. Over recent years, European and Italian aquaculture have shown a markedly different trend from that of world aquatic production. Asia, particularly China, has recorded a constant and rapid growth and Latin America a moderate development. Nowadays, European farmers are concerned with adapting their product to market demand and diversifying the fish species reared. After a discussion about the main European production statistics regarding finfish aquaculture production, we consider the most important aspects in the promotion of production and consequent consumption of farmed fish.     

State of the art and future trends of European and Italian aquaculture

This paper describes the main features of fish aquaculture in Europe and Italy focusing attention on single sectors of the farmed species and their trend for the future. Over recent years, European and Italian aquaculture have shown a markedly different trend from that of world aquatic production. Asia, particularly China, has recorded a constant and rapid growth and Latin America a moderate development. Nowadays, European farmers are concerned with adapting their product to market demand and diversifying the fish species reared. After a discussion about the main European production statistics regarding finfish aquaculture production, we consider the most important aspects in the promotion of production and consequent consumption of farmed fish.     

Emerging viral diseases of fish and shrimp

The rise of aquaculture has been one of the most profound changes in global food production of the past 100 years. Driven by population growth, rising demand for seafood and a levelling of production from capture fisheries, the practice of farming aquatic animals has expanded rapidly to become a major global industry. Aquaculture is now integral to the economies of many countries. It has provided employment and been a major driver of socio-economic development in poor rural and coastal communities, particularly in Asia, and has relieved pressure on the sustainability of the natural harvest from our rivers, lakes and oceans. However, the rapid growth of aquaculture has also been the source of anthropogenic change on a massive scale. Aquatic animals have been displaced from their natural environment, cultured in high density, exposed to environmental stress, provided artificial or unnatural feeds, and a prolific global trade has developed in both live aquatic animals and their products. At the same time, over-exploitation of fisheries and anthropogenic stress on aquatic ecosystems has placed pressure on wild fish populations. Not surprisingly, the consequence has been the emergence and spread of an increasing array of new diseases. This review examines the rise and characteristics of aquaculture, the major viral pathogens of fish and shrimp and their impacts, and the particular characteristics of disease emergence in an aquatic, rather than terrestrial, context. It also considers the potential for future disease emergence in aquatic animals as aquaculture continues to expand and faces the challenges presented by climate change.     

A survey of the transmission of infectious diseases/infections between wild and domestic ungulates in Europe

ABSTRACT: The domestic animals/wildlife interface is becoming a global issue of growing interest. However, despite studies on wildlife diseases being in expansion, the epidemiological role of wild animals in the transmission of infectious diseases remains unclear most of the time. Multiple diseases affecting livestock have already been identified in wildlife, especially in wild ungulates. The first objective of this paper was to establish a list of infections already reported in European wild ungulates. For each disease/infection, three additional materials develop examples already published, specifying the epidemiological role of the species as assigned by the authors. Furthermore, risk factors associated with interactions between wild and domestic animals and regarding emerging infectious diseases are summarized. Finally, the wildlife surveillance measures implemented in different European countries are presented. New research areas are proposed in order to provide efficient tools to prevent the transmission of diseases between wild ungulates and livestock.     

MHC class II is an important genetic risk factor for canine systemic lupus erythematosus (SLE)-related disease: implications for reproductive success

Major histocompatibility complex (MHC) class II genes are important genetic risk factors for development of immune-mediated diseases in mammals. Recently, the dog (Canis lupus familiaris) has emerged as a useful model organism to identify critical MHC class II genotypes that contribute to development of these diseases. Therefore, a study aimed to evaluate a potential genetic association between the dog leukocyte antigen (DLA) class II region and an immune-mediated disease complex in dogs of the Nova Scotia duck tolling retriever breed was performed. We show that DLA is one of several genetic risk factors for this disease complex and that homozygosity of the risk haplotype is disadvantageous. Importantly, the disease is complex and has many genetic risk factors and therefore we cannot provide recommendations for breeders exclusively on the basis of genetic testing for DLA class II genotype.     

All creatures great and minute: a public policy primer for companion animal zoonoses

Approximately 63% of US households have at least one pet, a large percentage of which are considered family members. Pet owners can derive substantial physical and psychological benefits from interaction with companion animals. However, pet ownership is not without risks; zoonotic diseases are increasingly drawing the attention of healthcare professionals, policy makers and the general public. While zoonoses of 'traditional' pets are widely recognized and their prevention and treatment factors are generally known, the growing popularity of 'non-traditional' pets has the potential to facilitate human exposure to novel zoonoses. However, the greatest risk of zoonoses probably arises from animals taken directly from the wild to serve as pets. Non-governmental organizations, state veterinary associations and others have been calling for increased regulation of animal imports, some proposing that all 'exotics' be banned from the pet trade. Because zoonotic diseases of companion animals are influenced by interacting factors of ecological, technical, socio-economic, and political origin, efforts to minimize their impact need be multi-dimensional, simultaneously addressing both the ecological and socio-political drivers of disease emergence and transmission. This study is intended to serve as a primer for animal care professionals seeking to engage with policy makers and the pet industry on the prevention of companion animal zoonoses. We provide background on the human-animal bond, risks of zoonoses associated with groups of companion animals, and the public policy context, as well as identify the factors needed to build a comprehensive approach to companion animal zoonoses risk management. Also included are examples of innovative, non-regulatory initiatives designed to limit the spread and impact of companion animal zoonoses, including a reptile salmonella poster, the National Reptile Improvement Plan, Habitattitude campaign, Pet Zoonoses Committee, and a wildlife disease surveillance initiative known as Project TripWire.     

Prevalence of the Bacterium Coxiella burnetii in Wild Rodents from a Canadian Natural Environment Park

Zoonotic diseases impact both wild and domestic animal populations and can be transmitted to humans through close contact with animal species. Reservoir species acting as vectors are major traffickers of disease. Rodents contribute to the transmission of Coxiella burnetii although little is known about its prevalence in wild animal populations. DNA was extracted from genital swabs collected from woodland jumping mice, deer mice, Southern red‐backed voles, Eastern chipmunks, North American red squirrels, as well as Southern and Northern flying squirrels collected from Algonquin Park, Canada. The presence of C. burnetii was determined through real‐time PCR. All species sampled had some prevalence of infection, except Eastern chipmunks, indicating wild rodents in Algonquin Park are reservoirs for C. burnetii. Emerging zoonotic diseases are linked to increasing globalization. Contact amongst individuals increases as crowding, habitat loss and fragmentation increase within wild spaces. Parks often act as a last refuge for wildlife but may also be an important transmission zone of wildlife disease to humans. Investigations that attempt to discover wild reservoir species of zoonotic disease are critically important to understanding the risk of pathogen exchange between wild and human populations.     

Paratuberculosis in farmed and free-living wild ruminants in the Czech Republic (1999-2001)

Due to the occurrence of the infection of Mycobacterium avium subspecies paratuberculosis among domestic ruminants and the rapid development of farmed deer industry and the market of cloven-hoofed game we have carried surveys of paratuberculosis, beginning in 1997, in the most common four species of wild ruminants in the Czech Republic [Pavlik et al., Vet. Microbiol. 77 (2000) 231-251]. From 1999 the prevalence of paratuberculosis has been slightly reduced in all three types of husbandry of wild ruminants. Nevertheless paratuberculosis has been diagnosed in wild ruminants in three districts, in four game parks and in five farms. M. a. paratuberculosis was isolated from 128 (5.3%) out of 2,403 wild ruminants of four animal species: 106 red deer, 2 roe deer, 4 fallow deer and 16 mouflons. In red deer farms, the highest number of clinical paratuberculosis cases was in yearling deer. RFLP type B-C1 of M. a. paratuberculosis predominated during the second period (1999-2001) in all types of husbandry with no relationship to wild ruminant species. New "cattle" RFLP types B-C5 and B-C16 of M. a. paratuberculosis were described in infected farmed red deer and one "intermediate" RFLP type R-I4 in fallow deer from one game park. The survival of M. a. paratuberculosis was found to be 4 months during winter in the pasture after destocking of all cattle infected with paratuberculosis. We found that non-vertebrates, wild ruminants or non-ruminant wildlife can be vectors and potentially become a risk factor in the spread of M. a. paratuberculosis infection.     

Mechanisms of viral emergence

A number of virologic and environmental factors are involved in the emergence and re-emergence of viral disease. Viruses do not conservatively occupy a single and permanent ecological niche. Rather, due to their intrinsic capacity for genetic change, and to the evolvability of fitness levels, viruses display a potential to parasitize alternative host species. Mutation, recombination and genome segment reassortment, and combination of these molecular events, produce complex and phenotypically diverse populations of viruses, which constitute the raw material on which selection acts. The majority of emerging viral diseases of humans have a zoonotic origin. Sociologic and ecologic factors produce diverse and changing environments in which viral subpopulations have ample opportunities to be selected from intrinsically heterogeneous viral populations, particularly in the case of RNA viruses. In this manner, new human, animal and plant viruses have emerged periodically and, from all evidence, will continue to emerge. This article reviews some of the mechanisms that have been identified in viral emergence, with a focus on the importance of genetic variation of viruses, and on the general concept of biological complexity.     

Stratospheric ozone depletion and animal health.

There is an increasing concern over ozone depletion and its effects on the environment and human health. However, the increase in ultraviolet-B radiation (UV-B) that would result from significant losses of ozone is also potentially harmful to animals. Any increase in disease in domestic species would not only have serious animal welfare implications but may also be economically important. The diseases which are likely to increase if ozone depletion continues include the squamous cell carcinomas of the exposed, non-pigmented areas of cats, cattle, sheep and horses. Uberreiter's syndrome in dogs is also associated with exposure to UV-B and may be expected to increase, as may the severity of conditions such as infectious keratoconjunctivitis (New Forest eye) in cattle. Aquaculture systems in which fish often have little or no protection by shading may also be at risk. Cataracts and skin lesions have been associated with the exposure of farmed fish to ultraviolet radiation and have resulted in significant losses.