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Review

A Review of Winter Ulcer Disease and Skin Ulcer Outbreaks in Atlantic Salmon (Salmo salar)

by
Maryam Ghasemieshkaftaki
Department of Ocean Sciences, Memorial University of Newfoundland, St. John’s, NL A1C 5S7, Canada
Hydrobiology 2024, 3(3), 224-237; https://doi.org/10.3390/hydrobiology3030015
Submission received: 8 March 2024 / Revised: 22 July 2024 / Accepted: 5 August 2024 / Published: 11 August 2024
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Abstract

:
Winter ulcer disease (WUD) is widely recognized as a serious threat to animal welfare and a major contributor to revenue loss within the aquaculture sector, particularly affecting the salmon-farming industry. This highlights the significant impact of WUD on both animal well-being and the economic sustainability of fish farming. WUD causes hemorrhagic signs and results in dermal lesions and ulcers. This disease can lead to higher mortality rates and a considerable decline in the fish’s market value. Moritella viscosa, a Gram-negative bacterium, is predominantly, but not exclusively, correlated with the emergence of WUD, mostly during the colder seasons. Waterborne transmission is the primary way for spreading the bacterium within a population. However, there is remarkable variation in the prevalence and characteristics of WUD in different regions. In Europe, this disease often occurs in the winter, and the intensity and occurrence of outbreaks are influenced by water temperature and salinity. In contrast, outbreaks are typically observed in the summer and mid-autumn in Eastern Canada. Despite the administration of various polyvalent vaccines, outbreaks of skin ulcers have been documented in Canada, and studies have highlighted the possible roles of other bacterial pathogens in Atlantic salmon. This review discusses the etiology, pathogenesis, and potential mitigation or prevention strategies for WUD, mainly in Atlantic salmon. Moreover, it underscores the necessity of conducting further investigations to discover the potential unknown causative agents of ulcerative disease and design appropriate vaccines or preventive strategies for these pathogens.

1. Introduction

Winter ulcer disease (WUD) is a prominent health challenge in the salmon-farming industry [1]. The clinical symptoms include superficial skin lesions that can evolve into long-lasting ulcers, affecting the underlying tissues or internal organs and ultimately leading to septicemia or mortality [2,3,4]. The initial reports of ulcerative disease in Atlantic salmon (Salmo salar) in Norwegian aquaculture back to 1980 [5], and these conditions continue to represent a critical health and economic problem within the North Atlantic territory. The east coast of Canada is relatively new to the phenomenon of skin ulcers, and little information has been published about this condition [6,7,8]. This review discusses the causative agents of ulcerative disease in different areas, mainly in Atlantic salmon, and addresses some measures for tackling these problems. To be more precise, this review covers the Canadian aquaculture sector, M. viscosa and WUD, co-infection, and regional variations. Additionally, it outlines the vaccines for ulcerative disease and available treatments.
Moritella viscosa is the primary agent responsible for causing winter ulcer disease [9,10,11,12]. It is a pathogenic microorganism that targets fish skin, which serves as the primary defense against waterborne infections [13]. The epidermis is the initial barrier of skin against aquatic microbes. M. viscosa commences its infectious cycle by settling on the scale surface [13]. This bacterium has been isolated from Atlantic salmon (Salmo salar), rainbow trout (Oncorhynchus mykiss) [3], turbot (Scophthalmus maximus) [14], and halibut (Hippoglossus hippoglossus) [15]. It has also been collected from farmed cod (Gadus morhua) [16], and lumpsucker (Cyclopterus lumpus) [17]. Although it was previously believed that M. viscosa is homogenous, recent research has revealed heterogeneity among strains of this pathogen [18].
Several studies have focused on ulcerative disease in Atlantic salmon (Table 1). Although M. viscosa is the main causal agent for this disease, a recent study has revealed the emergence of a new Vibrio sp. affecting vaccinated Atlantic salmon in Eastern Canada [6].
Bacterial infection can cause mortality in fish [6]. Koch’s postulates, considered the fundamental criteria for identifying the causative agents of diseases, have been applied in previous studies on fish [6,19,20,21]. Koch’s postulates were formulated based on and specify that a microorganism must be present in all cases, absent in healthy individuals, and capable of causing the disease when re-incubated after isolation in a pure culture. Also, the microorganism should be isolated again from the host that was experimentally infected, ensuring it is the same organism originally linked to the disease [22]. A recent investigation validated Koch’s postulates in the novel Vibrio sp. detected in Atlantic salmon exhibiting skin ulcers [6].
An increase in blood leukocyte levels has been reported after bacterial infections and challenges in different fish species, indicating an immune response after encountering pathogenic strains [23,24,25,26,27]. Although mortality has been observed in Atlantic salmon following the M. viscosa infection [28,29], a recent study confirmed a high percentage of survival in vaccinated Atlantic salmon after the challenge with this pathogen [1] (Figure 1 and Table 1). Increases in blood leukocyte and IgM levels were observed following the challenge which revealed that the ALPHA JECT micro IV vaccine is effective [1].
Table 1. Mortality rates of Atlantic salmon after bacterial infections/challenges.
Table 1. Mortality rates of Atlantic salmon after bacterial infections/challenges.
Host (S) Marine Fish Bacterial StrainDose Infection/Challenge RouteMortality RateReferences
Atlantic salmonVibrio sp. J383108 CFU/doseIP22.5%[6]
Atlantic salmonVibrio sp. J383107 CFU/doseIP5%[6]
Atlantic salmonVibrio sp. J383106 CFU/doseIP0%[6]
Atlantic salmonM. viscosa7 × 105 CFU/mLBath33%[28]
Atlantic salmonV. marinus3.5 × 103 CFU/doseIM50%[2]
Atlantic salmonM. viscosa-co cultivated106 CFU/mLBath96%[29]
Atlantic salmonM. viscosa and Alivibrio wodanis(106/106 CFU/mL)Bath94%[29]
Atlantic salmonM. viscosa and Alivibrio wodanis(106/106 CFU/mL)Bath98%[29]
Atlantic salmonAlivibrio wodanis then M. viscosa(106 + 106 CFU/mL)Bath84%[29]
Atlantic salmonAlivibrio wodanis co-cultivated1.5 × 106 CFU/mLBath8%[29]
Atlantic salmonM. viscosa106 CFU/doseIP5.64%[1]
Atlantic salmonM. viscosa106 CFU/mLBath2.82%[1]
IP: Intraperitoneal. IM: Intramuscular.

2. Canadian Aquaculture Industry

The Canadian aquaculture industry, established in 1970, has experienced dramatic growth over the past 50 years. Initially, this industry’s production was less than 10,000 tonnes in 1980. It then saw a substantial rise, reaching 49,500 tonnes by 1991, with a value of approximately CAD 233.6 million [31]. By 2009, Canadian aquaculture production ranked 20th globally, with Atlantic salmon farming accounting for nearly 70% of the national output and Canada being the fourth largest producer of farmed salmon worldwide [32].
Canadian aquaculture has continued to increase. In 2011, the industry accounted for 162,000 tonnes, about 0.25% of global aquaculture production. A significant portion of this production, 60%, was attributed to British Columbia. New Brunswick and Newfoundland and Labrador also emerged as important provinces in salmon production [32]. Farmed salmon production, a key economic driver in rural and coastal areas, was Canada’s third-largest seafood export at the time. This industry has played a pivotal role in provinces like Newfoundland and Labrador, New Brunswick, Nova Scotia, Prince Edward Island, and British Columbia [33]. Globally, Canada has been recognized as the fourth-largest producer of farmed Atlantic salmon (Salmo salar), highlighting its significant contribution to sustainable seafood production [34]. In 2021, farmed salmon production amounted to around 118,861 tonnes, with a value exceeding CAD 999 million [35]. The Canadian aquaculture industry, especially Atlantic salmon farming, is experiencing rapid growth, and its contribution to enhancing economic development and employment opportunities has been highlighted [36].

3. Global Status of Winter Ulcer Disease in Atlantic Salmon

Winter ulcer disease affects Atlantic salmon at cold water temperatures [37,38]. According to previous studies, infection can happen at lower water temperatures, typically when the ocean temperature falls below 7–8 °C [3,18,30,39,40]. This disease shows up as superficial skin lesions on scaled areas, and these lesions can turn into skin ulcers [30,38]. Winter ulcer disease poses a serious threat to Norwegian salmonid farming. It is the primary bacterial infection that has not been prevented by immunization and antibiotics [28,41]. Winter ulcer disease has a negative economic impact on Norway and Iceland [42]. Downgrading of fillet quality and mortalities cause severe financial losses [3,42]. Winter ulcer disease leads to less than 10% mortality rate during an epidemic [38,43]. However, one study suggested that mortality rates could exceed 40% [44]. When temperatures rise over 8 °C [38] or salinity drops below 12–15%, fish can recover [28]. Although this disease can affect juvenile and adult fish, it usually affects fish in their first year at sea in Norway [41,45]. Winter ulcer disease in salmon weighing 2–3 kg was reported in Scotland [9]. However, a lower frequency was observed among fish weighing over 1 kg [45]. Similarly, farm-raised Atlantic salmon on Canada’s east coast frequently develop ulcers when they weigh less than 1 kg [8].
Several investigations have been carried out to identify the source(s) of bacterial infection leading to ulcer formation. An investigation conducted on Atlantic salmon showed that bacteria in the seawater were the primary cause of skin ulcers [46]. Skin ulcers formed after a bath infection with M. viscosa in Norwegian Atlantic salmon [28]. Also, they mainly occurred at the injection site following intraperitoneal or intramuscular challenges [14,15].
There are not many documented descriptions of Atlantic salmon winter ulcer epidemics. Most studies have discussed outbreak-related facts without going into detail about the actual occurrence. For instance, Coyne et al. (2006) claim that post-smolts in their first year at sea are particularly susceptible to outbreaks, but they give no further details about the occurrence [41]. The first outbreak of winter ulcer in farmed Scottish Atlantic salmon was described by Bruno et al. (1998) [9]. It was observed that market-size Atlantic salmon experienced mortality at low temperatures [9]. Another study described the characteristics of winter ulcer in British Columbia [47]. Also, a comprehensive descriptive examination of ulcer diagnosis in Atlantic salmon farms in New Brunswick was provided by MacKinnon et al. (2019) [8]. However, these ulcers were not directly comparable to winter ulcers observed in farmed Atlantic salmon in BC or Europe since the water temperatures in the east of Canada were between around 10 and 13 °C when the outbreak occurred. Further studies should prioritize conducting comprehensive, geographically focused case studies to enhance data comparability and investigating diverse environmental impacts on the disease dynamics. Such efforts may enhance our knowledge about ulcer disease in Atlantic salmon in different regions.

4. Moritella viscosa, the Main Causative Agent of Winter Ulcer Disease

Winter ulcer disease, caused mainly by the bacterium Moritella viscosa, is a severe problem in the salmon-farming sector [28,46,48,49,50,51]. This bacterium is found in farmed Atlantic salmon in the Northern Atlantic Ocean and can be isolated from the marine environment. Moritella was initially recognized and distinguished from the genus Vibrio [52]. It is a halophilic, psychotropic, motile bacterium that has a fermentative and oxidative metabolism and produces oxidase. The colonies are yellow and round on Trypticase Soy Agar (TSA) supplemented with 2% NaCl [10]. The genome of M. viscosa consists of one chromosome (5.1 Mb) and two small cryptic plasmids called pMVIS41 (4.1 kb) and pMVIS39 (3.9 kb) [53]. This bacterium affects different organs of fish; hemorrhagic signs can be seen in the gills, on the head, and on different parts of the skin. There are also reports of internal organ necrosis or muscle deterioration [28]. Fish with chronic infections may experience a severe inflammatory response that changes their muscle tissue and endothelial cells in the hypodermis [38]. There are currently limited definitive findings regarding the causative agent of skin ulcers in Canada. It has been speculated that either multiple opportunistic pathogens or the primary pathogen M. viscosa cause this disease [8].
M. viscosa’s virulence factors are not well known. However, it has been described that extracellular cytotoxic products (ECPs) play a significant role in causing skin ulcers in Atlantic salmon. These extracellular products may clarify the pathology related to M. viscosa [39]. The extracellular metallopeptidase MvP1 has been isolated from ECPs of M. viscosa and characterized [54,55]. Also, MvOmp1 acts as an antigen for protection in M. viscosa, and further studies can be conducted to detect the ability of this protein to serve as a subunit vaccine [56]. Furthermore, it has been described that M. viscosa oligosaccharides and an antigen weighing 17–19 kDa in the outer membrane increases the antigenicity of this bacterium and might be essential virulence factors [18]. More research is required to determine if the antigens and virulence factors of this bacterium can function as immune stimulants in fish.

5. The Role of Co-Infection in Winter Ulcer Disease

In fish, co-infections affect survival rates, compromise the effectiveness of disease control strategies, and have an impact on the immune system and treatment outcomes. However, there is a lack of research in this area [57].
M. viscosa is the cause of winter ulcers; however, other environmental bacteria may also contribute to outbreaks of this disease [29,42]. The most frequent bacteria are Aliivibrio wodanis [12] and Tenacibaculum sp., which have been collected from cases of ulcer disease. Tenacibaculum may attack skin lesions and co-infect wounds caused by M. viscosa [43]. The pathogen Tenacibaculum finnmarkense has been identified as a novel species within the genus Tenacibaculum [58].
Although it was suggested that A. wodanis may inhibit the healing and recovery of skin ulcers resulting from a first infection with M. viscosa [37], another study showed that A. wodanis may restrict the growth of M. viscosa [53]. Furthermore, simultaneous infection with both M. viscosa and A. wodanis does not elevate the mortality rate of fish in comparison to infection solely with M. viscosa [29]. Moreover, A. wodanis infection can diminish the virulence of M. viscosa, as the initial infection with A. wodanis decreases mortality for subsequent infections with M. viscosa [29]. The reason behind this phenomenon could be associated with A. wodanis’ ability to modify the gene expression profile of M. viscosa, possibly due to competition for identical habitats and nutrients, such as the sequestration of iron through siderophore-mediated interspecies competition. Additionally, the inhibition of M. viscosa growth might occur through the secretion of inhibitory effectors like bacteriocins [29,53,59]. Additional research is necessary to investigate how other bacteria might co-infect Atlantic salmon with M. viscosa.

6. Regional Distinctions

Ulcerative disease was first noted in Canada in New Brunswick (NB) in 1990 [60], but it was also reported in British Columbia (BC) in 2011 [47]. Winter ulcer has been known to exist in Norway since 1980 [5,38]. Ulcerative disease caused by M. viscosa infection in BC resemble those seen in farmed Atlantic salmon in European countries. The fundamental traits of this disease and corresponding infection are comparable in these two regions, including shallow wounds, isolation of M. viscosa, onset at temperatures below 8 °C, and recovery or no incidence of infection at higher temperatures [2,9,38,47].
The infection observed on Canada’s eastern coast is notably more intricate. Whitman et al. (2001) reported that ulcerative disease was primarily responsible for the mortality that persisted until the end of September [60]. Even with antibiotic therapy, around 31% mortality was reported during the outbreak [60]. A Vibrio was also recovered from this investigation in New Brunswick; its biochemical and SDS-Page characteristics matched Allivibrio wodanis [60].
Recent research has focused on specific knowledge gaps related to skin ulcers in Eastern Canada [8,61]. MacKinnon et al. (2019) examined the factors contributing to the development of skin ulcers in farmed Atlantic salmon. They demonstrated that the prevalence increases in the summer and autumn at temperatures above 10 °C. This study investigated the incidence of skin ulcers by analyzing clinical signs that varied in severity but did not identify the pathogen. The main objective was to identify the disease-related factors [8]. According to MacKinnon et al. (2019), farms near one another have occasionally experienced epidemics at the same periods. At other times, geographically separate farms reported skin ulcers a week apart. Average mortality during epidemics was eight weeks; however, in certain cages, it was higher, ranging up to 26 weeks. The water temperature during the epidemics fluctuated between 10.06 °C and 13.36 °C [8].
The prevalence of WUD in Europe exhibits a notable difference compared to Eastern Canada. In European farms, WUD is observed at temperatures under 7 °C [62]. However, in the east of Canada, skin ulcers often appear in warmer months when the water temperatures vary between around 10 and 13 °C [8] (Figure 2). The clades of this pathogen in these two areas are different. Two primary clades have been described in M. viscosa, which are categorized as ‘typical’ and ‘variant’ [63]. ‘Typical M. viscosa has mostly been separated from Atlantic salmon farmed in European regions. ‘Variant’ M. viscosa has been observed in Atlantic salmon cultured in Canada and Iceland [63] (Figure 3). Antigenic heterogeneity suggests that M. viscosa is serologically diverse [18].
It is proposed that genetic elements within M. viscosa have advanced compatibility factors that adjust the ‘typical’ M. viscosa to host-specific virulence [64]. Norwegian farms experienced below 10% mortality in winter, and the fish that showed skin ulcer recovered in the spring, when the water temperature reached 8 °C [38]. However, skin ulcers on saltwater net-pen-raised Atlantic salmon can result in high mortality rates and financial losses in Atlantic Canada [8]. In Eastern Canada, the presence of skin ulcer disease is relatively new, and less accessible information about it is available for Atlantic salmon. In saltwater, these skin ulcers may rapidly deteriorate. Fish may initially exhibit only subtle signs of laterally raised scales, and, shortly after, mortality can occur, characterized by a single massive circular ulcerative lesion or wound [7,8].

7. Vaccines against WUD

Vaccination is an effective management strategy for fish health that decreases disease outbreaks and minimizes the use of antibiotics in the aquaculture industry [65]. The first vaccination trials against M. viscosa started in 1993 for Atlantic salmon. After the introduction of vaccines, antibiotic use decreased in the salmonid-farming industry [66]. The vaccine’s structure was based on formalin, which deactivated the bacteria and was injected with an oil adjuvant into salmon. This method of vaccine development has been accepted in Norway and Iceland. This formulation provided salmon with some protection against M. viscosa [67]. However, it has been suggested that the polyvalent oil-based vaccine against M. viscosa was more efficient than the monovalent vaccine. Polyvalent vaccines contain at least two or more strains of the antigen [14,66].
The assessment of vaccine efficacy in test challenges is complex. The occurrence of lesions and infections in fish was not measured, and the efficacy of the vaccine was only evaluated based on the relative percentage survival (RPS) and the mean days to death (MDD) [66]. However, on salmon farms, skin ulcers and wound infections cause mortality and low-quality flesh; therefore, establishing a new strategy for evaluating a vaccine is necessary. Even though international surveys have suggested that immunization against WUD is effective, several studies have reported the occurrence of winter mortality and WUD in vaccinated fish. Thus, it appears that current vaccines need to be modified and/or new vaccines must be developed. Vaccination against only one serotype of M. viscosa is insufficient [66]. Although several vaccines have been tested, lesions and ulcers are frequently reported during outbreaks of this disease, so designing a more effective vaccine that provides better protection and reduces skin infections is required. Over the past decade, vaccine development’s primary purpose has been focused on identifying a novel technology that enhances vaccine effectiveness [68]. Modern vaccine studies focus on using specific pathogen components to produce a vaccine that contains new antigens [69]. Attenuated vaccines are more effective than killed vaccines due to their ability to induce the cellular immune response in the host. These vaccines are designed using attenuated bacteria or natural strains with low virulence factors [70,71]. However, there is a concern associated with live attenuated vaccines due to the possibility of the bacteria returning to their virulent version [70,72], so the majority of approved vaccines for aquaculture are composed of inactivated pathogenic microbes combined with an adjuvant, and they may include either one or multiple microorganisms [71,73].
The vaccine containing M. viscosa antigen demonstrated high efficacy in protecting farmed Atlantic salmon, leading to a marked decrease in both mortality and skin ulcers [50]. Another study demonstrated that the ALPHA JECT micro IV (Pharmaq, Norway) vaccine offered high percentages of survival against M. viscosa in farmed Atlantic salmon [1]. Also, M. viscosa outer membrane vesicles (OMVs) were used in vaccine preparation for Atlantic salmon [1]. OMVs are spherical lipid vesicles derived from the outer membranes of Gram-negative bacteria. OMVs assist in communication between bacteria in different growth environments and influence the host’s immune response [74,75]. They carry antigens and are promising candidates for new vaccine formulations. These vesicles efficiently engage antigen-presenting cells due to their surface antigens, contain a variety of pathogen-associated molecular patterns (PAMPs) that activate and support immune responses [76], and exhibit self-adjuvant effects [77]. One study used OMVs of M. viscosa as the key component in the vaccine to boost the vaccinated Atlantic salmon. This comprehensive study revealed the high immunogenicity of M. viscosa OMVs in vaccinated farmed Atlantic salmon [1]. However, further investigations should use M. viscosa OMVs as a vaccine component in the absence of extra boosting. Using this method would offer insightful information about how well M. viscosa OMVs work as an independent potential vaccine for Atlantic salmon.

8. Treatments and Mitigating Strategies

Antibiotic prescriptions were used in Norwegian Atlantic salmon farming; however, they did not substantially reduce disease-related mortality [28,41,78]. This may be partially attributable to a diseased fish’s tendency to stop feeding, which prevents them from ingesting the antibiotic [42,47]. It is crucial that antibiotic also target the skin because this disease may not develop in a systemic infection [47]. Immunization against bacterial diseases such as enteric redmouth, vibriosis, furunculosis [79], and winter ulcer disease has decreased antibiotic usage in the fish industry [66]. In Canada, oxytetracycline hydrochloride (Terramycin-Aqua), trimethoprim and sulphadiazine powder (Tribressen 40% powder), sulfadimethoxine and ormetoprim (Romet 30), and florfenicol (Aquaflor) are approved for use in aquaculture [80].
Oral administration of oxolinic acid (OXA) was employed by Coyne et al. (2004) as an experimental protocol to treat winter ulcer disease in Atlantic salmon. They measured OXA concentrations in plasma and internal organs 24 h after the end of exposure to antibiotics in a fish farm with different kinds of fish populations (sick and healthy). They found that the administration of OXA was beneficial for healthy fish; however, it had little or no impact on moribund fish. Also, the findings did not indicate a significant positive impact on reducing mortality trends over time [78]. They also conducted another study on the concentration of florfenicol (FF) and found that it was compatible with their previous study. Although M. viscosa was susceptible to FF, looking at the mortality rate before, during, and even after the period of administration did not provide clear proof that this antibiotic was effective in reducing the mortality rates at the cage site [41].
One study investigated the effects of dietary β-1,3/1,6-glucans on the survival of Atlantic salmon when challenged with Moritella viscosa. The results indicated that β-glucan supplementation reduced the mortality rates in both unvaccinated and vaccinated salmon, enhancing the effectiveness of the vaccine against this pathogen [81]. Therefore, it can be used as a potential strategy for mitigating the impact of winter ulcer disease in the salmon-farming industry. However, conducting large-scale field trials in aquaculture is crucial to confirm these findings. Also, future studies should assess the practical implementation and optimal dose of β-glucan supplementation to prevent winter ulcer disease.
Research has examined the benefits of adding urea to feed to minimize osmotic stress [82,83]. The research indicates that osmotic imbalance might be a factor in the emergence of winter ulcers in farmed salmon. Adding urea to the diet seems to affect plasma osmolality, aiding in reducing this imbalance [83]. Also, trimethylamine oxide was used to improve fat digestibility to prevent winter ulcers in rainbow trout. These mitigating strategies have positive effects [82]. However, further research is required to determine the impact of trimethylamine on Atlantic salmon.

9. Comparative Bacterial Genomics for Vaccine Advancements in Ulcerative Disease

Fish immunization and the corresponding research in this field was started in the 1940s to prevent diseases [84,85]. Aquatic vaccines constitute the most reliable strategy for preventing disease and thereby maintaining the healthiness and sustainability of aquaculture [86]. Vaccines currently consist of inactivated bacterial pathogens and are the most efficient way of preventing infectious disease in fish. Vaccines are produced with or without adjuvants, such as mineral oils, which are added mainly to increase the immune response of the immunized fish [68,87,88].
Novel vaccine research has utilized live-attenuated, subunit, or recombinant DNA and RNA particle vaccines with new antigenic components [70,71]. DNA vaccination involves the use of pathogen genes instead of antigens to stimulate an immune response. These vaccines often consist of bacterial plasmids that carry genes and are designed to replicate in bacteria and express in the recipient [89,90].
Comparative bacterial genomics is a beneficial tool for vaccine development that uses genome-sequenced data to describe different biological aspects (bacterial evolution, physiology, and pathogenesis) of microorganisms [91,92]. Genomic research (e.g., classic microbiology, molecular microbiology, and host–pathogen interactions) can provide comprehensive information about pathogenesis and a host’s immune response to control an infectious disease [93,94,95].
Recently, a comparative genomic analysis of a new causative agent of ulcerative disease provided comprehensive knowledge about this pathogen [6], information that can potentially be utilized to develop a new preventive measure for the salmon-farming industry in Eastern Canada. However, more studies need to be carried out to define these strategies.

10. Conclusions

Research on Atlantic salmon from Europe has noticeably contributed to our understanding of winter ulcer, which is primarily caused by M. viscosa. However, few of these studies have included isolates of M. viscosa from Canada. Furthermore, differences in the temperatures at which ulcerative outbreaks occur suggest that different pathogens might be involved. In Atlantic Canada, this disease has a significant economic impact, but there are few published data on the appearance or causes of skin ulcers for Atlantic salmon reared in this region. M. viscosa is thought to be a principal causative agent of winter ulcer disease; however, recent studies reported that vaccination provided strong protection against this pathogen. This finding suggests that unknown bacterial infections might lead to ulcerative disease and mortality in farmed Atlantic salmon. As a result, it may be more difficult and problematic to treat or prevent this disease. While some vaccines showed high protection, further research could focus on enhancing vaccine formulations to increase efficacy against different strains of M. viscosa and to determine the other potential causative agents of ulcerative disease. Also, co-infections with various bacteria might cause skin ulcers. There is limited data on how different pathogens interact and the effects of these interactions on ulcer formation. Future research should aim to explore these interactions in greater detail and their potential impact on the development of ulcers. It can provide the aquaculture industry with effective preventive strategies or vaccines against these pathogens.

Funding

This review received no external funding.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

Some parts of this manuscript are directly derived from the author’s thesis, which was previously submitted to the Memorial University of Newfoundland, so the author sincerely appreciates the help provided by Anthony Kurt Gamperl as a committee member for his valuable comments and feedback. The author also thanks Javier Santander, thesis supervisor, for his insightful suggestions.

Conflicts of Interest

The author declares no conflict of interest.

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Figure 1. (A) Mortality and clinical signs reported in Atlantic salmon after challenge with M. viscosa [28,29]. This bacterium can affect Atlantic salmon at lower temperatures [30]. (B) Atlantic salmon were vaccinated and then challenged with M. viscosa. A significant increase in WBC levels was observed after the challenge [1]. Increasing levels of lymphocytes and low mortality rates indicated the appropriate functioning of the adaptive immune response in Atlantic salmon immunized with ALPHA JECT micro IV vaccine. This illustration was created by the author using BioRender (https://biorender.com/) (accessed on 17 April 2024).
Figure 1. (A) Mortality and clinical signs reported in Atlantic salmon after challenge with M. viscosa [28,29]. This bacterium can affect Atlantic salmon at lower temperatures [30]. (B) Atlantic salmon were vaccinated and then challenged with M. viscosa. A significant increase in WBC levels was observed after the challenge [1]. Increasing levels of lymphocytes and low mortality rates indicated the appropriate functioning of the adaptive immune response in Atlantic salmon immunized with ALPHA JECT micro IV vaccine. This illustration was created by the author using BioRender (https://biorender.com/) (accessed on 17 April 2024).
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Figure 2. The occurrence of ulcer disease is different in European countries and Eastern Canada. In European cases, when the water temperature rises above 8 °C, the ulcers disappear, and fish can survive [38]. However, in Eastern Canada, the ulcerative disease occurs at between around 10 and 13 °C and will be persistent until summer or mid-autumn [8]. In both scenarios, bacterial adhesion leads to lesions and ulcers. This figure was designed by the author utilizing BioRender (https://biorender.com/) (accessed on 28 February 2024).
Figure 2. The occurrence of ulcer disease is different in European countries and Eastern Canada. In European cases, when the water temperature rises above 8 °C, the ulcers disappear, and fish can survive [38]. However, in Eastern Canada, the ulcerative disease occurs at between around 10 and 13 °C and will be persistent until summer or mid-autumn [8]. In both scenarios, bacterial adhesion leads to lesions and ulcers. This figure was designed by the author utilizing BioRender (https://biorender.com/) (accessed on 28 February 2024).
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Figure 3. This map shows the distribution of M. viscosa clades in different regions. ‘Typical’ M. viscosa has mostly been isolated from Atlantic salmon farmed in Norway, Scotland, and the Faroe Islands. ‘Variant’ M. viscosa has been observed in Atlantic salmon cultured in Canada and Iceland [63]. This figure was designed by the author utilizing BioRender (https://biorender.com/) (accessed on 9 April 2024).
Figure 3. This map shows the distribution of M. viscosa clades in different regions. ‘Typical’ M. viscosa has mostly been isolated from Atlantic salmon farmed in Norway, Scotland, and the Faroe Islands. ‘Variant’ M. viscosa has been observed in Atlantic salmon cultured in Canada and Iceland [63]. This figure was designed by the author utilizing BioRender (https://biorender.com/) (accessed on 9 April 2024).
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Ghasemieshkaftaki, M. A Review of Winter Ulcer Disease and Skin Ulcer Outbreaks in Atlantic Salmon (Salmo salar). Hydrobiology 2024, 3, 224-237. https://doi.org/10.3390/hydrobiology3030015

AMA Style

Ghasemieshkaftaki M. A Review of Winter Ulcer Disease and Skin Ulcer Outbreaks in Atlantic Salmon (Salmo salar). Hydrobiology. 2024; 3(3):224-237. https://doi.org/10.3390/hydrobiology3030015

Chicago/Turabian Style

Ghasemieshkaftaki, Maryam. 2024. "A Review of Winter Ulcer Disease and Skin Ulcer Outbreaks in Atlantic Salmon (Salmo salar)" Hydrobiology 3, no. 3: 224-237. https://doi.org/10.3390/hydrobiology3030015

APA Style

Ghasemieshkaftaki, M. (2024). A Review of Winter Ulcer Disease and Skin Ulcer Outbreaks in Atlantic Salmon (Salmo salar). Hydrobiology, 3(3), 224-237. https://doi.org/10.3390/hydrobiology3030015

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