Assigning cause for emerging diseases of aquatic organisms

Hutson, Kate S.; Davidson, Ian; Bennett, Jerusha; Poulin, Robert; Cahill, Patrick

doi:10.1016/j.tim.2023.01.012

Cited by 15 publications

(8 citation statements)

References 91 publications

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“…In Aotearoa New Zealand, outbreaks of disease in Chinook salmon associated with skin infections were first reported in 2012 in sea pens located in the Marlborough Sounds and have been consistently reported thereafter [28, 31, 54, 55]. Assigning disease causation and confirming whether a ubiquitous microorganism is an infectious agent or is commensal flora of the host remains a challenge for diagnostic microbiologists, specifically for topical diseases [38, 56, 57]. Although most salmonids are susceptible to tenacibaculosis [15], it was reported that Pacific salmon species in the Pacific Northwest were resistant to mouth-rot disease caused by T. maritimum [see 8].…”

Section: Discussionmentioning

confidence: 99%

“…and environmental factors such as warming seawater, harmful algae and biofouling organisms [33-35]. The Henle–Koch postulates [36, 37] to prove causality of disease have been successfully applied to several aquatic diseases [see 38 for review]. Some examples include shrimp white faeces syndrome [39], francisellosis in Atlantic cod ( Gadus morhua ) [see 40], amoebic gill disease in Atlantic salmon [41], bacterial and fungal diseases in marine seaweed [42, 43], streptococcosis in whiteleg shrimp ( Litopenaeus vannamei ) [see 44], and heart- and skeletal muscle inflammation in Atlantic salmon [45].…”

Section: Introductionmentioning

confidence: 99%

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Experimental challenge of Chinook salmon withTenacibaculum maritimumandTenacibaculum dicentrarchifulfils Koch’s postulates

Kumanan,

Carson,

Hunter

et al. 2024

Preprint

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The bacterial skin disease tenacibaculosis, caused byTenacibaculumspecies, can compromise numerous species of economically important marine fish, including salmonids. While tenacibaculosis is a known threat to Atlantic salmon (Salmo salar) aquaculture, the pathogenesis ofTenacibaculum maritimumandTenacibaculum dicentrarchion Chinook salmon (Oncorhynchus tshawytscha) has not yet been investigated. In this study, three molecular O-AGC types ofT. maritimum(O-AGC Type 3-0, Type 2-1 and Type 3-2) andT. dicentrarchiisolated during a disease outbreak of farmed Chinook salmon in Aotearoa New Zealand were assessed for their ability to induce tenacibaculosis in salmon smolts under controlled conditions. Naive Chinook salmon were exposed toT. maritimumorT. dicentrarchiby immersion. Clinical signs of tenacibaculosis were apparent post-exposure and observed in 100% of all three molecular O-AGC types ofT.-maritimum-challenged fish, with 100% morbidity in O-AGC Type 2-1 and Type 3-2 and 60% in O-AGC Type 3-0. Chinook salmon exposed toT. dicentrarchishowed characteristic clinical signs of disease in 51% of the challenged population, with 28% morbidity. Common gross pathological signs observed for bothTenacibaculumspecies were congruent with observations on farmed fish in the field, including scale loss, erythematous skin lesion, skin ulcers, fin necrosis, mouth erosion and gill ulceration. Exophthalmia was observed only inT. maritimum-challenged fish, while skin ulcers appeared grossly more severe with exposed musculature inT. dicentrarchi-challenged fish. PureT. maritimumandT. dicentrarchicultures were reisolated from the skin and gills of the challenged fish and their identity was confirmed by species-specific PCR and molecular O-AGC typing. Challenge experiments and associated field surveillance (forT. maritimum) did not show the presence of culturableT. maritimumcells in the anterior kidney. This provides compelling evidence that tenacibaculosis in farmed Chinook salmon is an external infectious disease, and thatTenacibaculumis a marine obligate organism that is unable to survive in fish body fluids and does not cause septicaemia. This has repercussions for approaches to experimental challenges withTenacibaculumspecies, which must occur by immersion rather than intraperitoneal or intramuscular inoculation, to replicate the natural transmission pathway and to ensure a successful challenge model. This study fulfilled modernised Koch’s postulates for the three molecular O-AGC types ofT. maritimumand single strain ofT. dicentrarchias aetiological agents of tenacibaculosis in Chinook salmon that cause mortalities with considerable external abnormalities.Author summaryChinook salmon,Oncorhynchus tshawytscha, is the most significant species of Pacific salmon for its large size and nutritional content which makes it a premium choice for aquaculture. In Aotearoa|New Zealand, Chinook salmon is the only marine salmon species farmed. For a decade, the industry was impacted by an undiagnosed skin disease resulting in high mortalities. Disease susceptibility in Chinook salmon is scarcely studied and added to the challenge for a timely diagnosis. This novel research provides insight on disease susceptibility of Chinook salmon and confirmsTenacibaculumspecies identified in New Zealand pose a high threat to the aquaculture industry. This research has global implications and contributes valuable insights and approaches to disease management that can be applied in British Columbia and Canada where Chinook salmon populations are in decline.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Experimental challenge of Chinook salmon withTenacibaculum maritimumandTenacibaculum dicentrarchifulfils Koch’s postulates

Kumanan,

Carson,

Hunter

et al. 2024

Preprint

Self Cite

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“…Additionally, it is also important to consider whether relevant policies and regulations can provide a sufficient guarantee for safe species introduction [ 43 , 44 , 45 ]. The risk of infectious diseases should include a risk assessment of pathogen exposure; hazards to indigenous species (including becoming direct victims and pathogen vectors); consequences of disease outbreak; impacts on human health, social economy, and ecological environment; and other relevant factors [ 46 , 47 , 48 ]. Regarding the internationally advanced risk assessment system, we determined the indices of the risk assessment model system for the introduction of aquatic animals (see Table 1 ).…”

Section: Methodsmentioning

confidence: 99%

Risk Assessment Model System for Aquatic Animal Introduction Based on Analytic Hierarchy Process (AHP)

Zhang

Zhao

et al. 2023

Animals

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The spread of invasive species (IS) has the potential to upset ecosystem balances. In extreme cases, this can hinder economical utilization of both aquatic (fisheries) and terrestrial (agricultural) systems. As a result, many countries regard risk assessment of IS as an important process for solving the problem of biological invasion. Yet, some IS are purposefully introduced for what is seen as their potential economic benefits. Thus, conducting IS risk assessments and then formulating policies based on scientific information will allow protocols to be developed that can reduce problems associated with IS incursions, whether occurring purposefully or not. However, the risk assessment methods currently adopted by most countries use qualitative or semiquantitative methodologies. Currently, there is a mismatch between qualitative and quantitative assessments. Moreover, most assessment systems are for terrestrial animals. What is needed is an assessment system for aquatic animals; however, those currently available are relatively rudimentary. To fill this gap, we used the analytic hierarchy process (AHP) to build a risk assessment model system for aquatic IS. Our AHP has four primary indexes, twelve secondary indexes, and sixty tertiary indexes. We used this AHP to conduct quantitative risk assessments on five aquatic animals that are typically introduced in China, which have distinct biological characteristics, specific introduction purposes, and can represent different types of aquatic animals. The assessment results show that the risk grade for Pterygoplichthys pardalis is high; the risk grade for Macrobrachium rosenbergii, Crassostrea gigas, and Trachemys scripta elegans is medium; and the grade risk for Ambystoma mexicanum is low. Risk assessment of the introduction of aquatic animals using our AHP is effective, and it provides support for the introduction and healthy breeding of aquatic animals. Thus, the AHP model can provide a basis for decision-making risk management concerning the introduction of species.

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“…Microbial diseases that do not conform to traditional definitions are widespread in the oceans but are often poorly characterised and have unresolved aetiology (Hutson et al., 2023 ). These diseases include those involving more than one aetiological agent (e.g.…”

Section: Question 2: What Constitutes a Pathogen In A Changing Marine...mentioning

confidence: 99%

Marine diseases and the Anthropocene: Understanding microbial pathogenesis in a rapidly changing world

Hudson,

Egan

2024

Microbial Biotechnology

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Healthy marine ecosystems are paramount for Earth's biodiversity and are key to sustaining the global economy and human health. The effects of anthropogenic activity represent a pervasive threat to the productivity of marine ecosystems, with intensifying environmental stressors such as climate change and pollution driving the occurrence and severity of microbial diseases that can devastate marine ecosystems and jeopardise food security. Despite the potentially catastrophic outcomes of marine diseases, our understanding of host‐pathogen interactions remains an understudied aspect of both microbiology and environmental research, especially when compared to the depth of information available for human and agricultural systems. Here, we identify three avenues of research in which we can advance our understanding of marine disease in the context of global change, and make positive steps towards safeguarding marine communities for future generations.

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Assigning cause for emerging diseases of aquatic organisms

Cited by 15 publications

References 91 publications

Experimental challenge of Chinook salmon withTenacibaculum maritimumandTenacibaculum dicentrarchifulfils Koch’s postulates

Experimental challenge of Chinook salmon withTenacibaculum maritimumandTenacibaculum dicentrarchifulfils Koch’s postulates

Risk Assessment Model System for Aquatic Animal Introduction Based on Analytic Hierarchy Process (AHP)

Marine diseases and the Anthropocene: Understanding microbial pathogenesis in a rapidly changing world

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