Six articles reported on one or more salmonid factors that contributed to infection with T. maritimum ( Table 3 , Supplementary Table 1 ) (Soltani et al., 1996; Handlinger et al., 1997; van Gelderen et al., 2011; Downes et al., 2018; Bateman et al., 2021; Bass et al., 2022). Two studies reported an increased prevalence of infection during the first year of production at sea when the fish are smaller (Downes et al., 2018; Bateman et al., 2021), with a possible factor being the softness of scales at a young age (van Gelderen et al., 2011). In one study, the size of fish was investigated by comparing the mass of wild fish (kg) to their current length (cm) during their first year at sea (Bass et al., 2022). Authors reported that fish with a higher bacterial load of T. maritimum had a lower-than-expected mass for their length, which was identified as a function of decreased feeding rates and feed consumption in fish infected with the bacteria (Bass et al., 2022).

A challenge trial to assess the fish species effect found that a T. maritimum challenge concentration of 1.6 x 10⁶ cells/mL was significantly (p<0.05) associated with higher mortality in Atlantic salmon (74.9%) compared to Rainbow trout (50.0%); there were no differences at other challenge concentrations (1.8 x 10³, 2.3 x 10⁴, 2.3 x 10⁵, and 1.6 x 10⁷ cells/mL) (Soltani et al., 1996). When salmonids were compared to non-salmonids such as greenback flounder, there was significantly higher mortality (10% vs 2%) and morbidity with lesions (20% vs 0%) in Atlantic salmon (Soltani et al., 1996). Another study reported species-specific variability in the response to infection with T. maritimum (Handlinger et al., 1997). Greenback flounder showed mild to moderate erosions on the fins and tail with minimal histological lesions compared to the higher susceptibility and more severe lesions observed in rainbow trout and Atlantic salmon (Handlinger et al., 1997).

Most of the 15 articles that mentioned management factors ( Table 3 , Supplementary Table 1 ) investigated gill/body abrasion (n=8) (Handlinger et al., 1997; Powell et al., 2004; Powell et al., 2005; Olsen et al., 2011; van Gelderen et al., 2011; Apablaza et al., 2017; Smage et al., 2017; Nowlan et al., 2021a) or pen elements (netting, cleaning systems) (n=3) (van Gelderen et al., 2011; Rud et al., 2017; Nowlan et al., 2021a). Abrasion of the gills was reported to disturb respiration, which ultimately enhanced the progression of disease from T. maritimum (Powell et al., 2004; Apablaza et al., 2017; Wynne et al., 2020). Bodily abrasion, which could be a result of contact with netting or other pen elements, was reported to enhance the rate and severity of infection (Olsen et al., 2011; van Gelderen et al., 2011). Skin lesions were commonly found in areas that were more prone to abrasion or movement, such as dorsal and pectoral fins (van Gelderen et al., 2011). Other studies reported that abrasion allowed bacterial proliferation below the epidermis (van Gelderen et al., 2011) and that the infiltration of T. maritimum was restricted to necrotic tissue (Handlinger et al., 1997). One article reported that infection with T. maritimum appeared to occur only after abrasion of the skin (Olsen et al., 2011). However, another study reported that at high concentrations, the fish became infected with T. maritimum and died after 72 hours with no prior abrasion to the epithelium, and little sign of erosion (van Gelderen et al., 2011).

Contact with pen elements (van Gelderen et al., 2011), other fish (van Gelderen et al., 2011), or jellyfish (Smage et al., 2017), or net pen cleaning (Nowlan et al., 2021a), could have introduced T. maritimum, as it was reported that T. maritimum exists in several reservoirs such as tank walls, net pens, and water samples (van Gelderen et al., 2011; Rud et al., 2017; Nowlan et al., 2021a). Studies also reported on transfer from freshwater to saltwater (Smage et al., 2017; Nowlan et al., 2021a), and time since transfer to saltwater between three to eight weeks (Frelier et al., 1994), and one week and one year, as factors for T. maritimum infection (Downes et al., 2018; Nowlan et al., 2021a). The prevalence of T. maritimum in dead and dying salmon (from all causes) was also found to be the highest in the first year after ocean entry (Bateman et al., 2021). Other management factors such as vaccines were examined (van Gelderen et al., 2009; Frisch et al., 2018). A vaccine developed for yellow mouth using isolates from western Canada was reported to be unsuccessful in protecting fish under experimental challenge conditions (Frisch et al., 2018). In another vaccination study on marine flexibacteriosis, authors reported that naïve Atlantic salmon had significantly better survival rates when injected with vaccine and adjuvant than the control group or vaccine only group (van Gelderen et al., 2009).

Environmental factors were reported by 16 of the included studies ( Tables 3 – 5 , Supplementary Table 1 ). One study reported that infection with T. maritimum did not always result in clinical signs, therefor other environmental factors might be necessary to result in clinical disease (Brosnahan et al., 2019). Water temperature was the most frequently reported environmental factor (n=10) ( Tables 3 , 4 ) (Frelier et al., 1994; Handlinger et al., 1997; Barker et al., 2009; Olsen et al., 2011; van Gelderen et al., 2011; Apablaza et al., 2017; Downes et al., 2018; Brosnahan et al., 2019; Nowlan et al., 2021a; Ghosh et al., 2022). An increased water temperature was reported to result in a greater prevalence of T. maritimum in the gill arches of farmed salmon (Downes et al., 2018) or an increased frequency of application of florfenicol treatments (Nowlan et al., 2021a). The remaining eight articles reported a potential connection between water temperature and T. maritimum (Frelier et al., 1994; Handlinger et al., 1997; Barker et al., 2009; Olsen et al., 2011; van Gelderen et al., 2011; Apablaza et al., 2017; Brosnahan et al., 2019; Ghosh et al., 2022). Some studies reported an increased number of disease outbreaks of disease caused by T. maritimum during periods of warmer water temperatures (Barker et al., 2009; Olsen et al., 2011; Downes et al., 2018). One study reported that infection during periods of warmer water temperature was the result of increased stress on fish and increased bacterial growth (van Gelderen et al., 2011). In contrast, one study reported that the prevalence of T. maritimum did not appear to have a strong correlation with warmer water, although no statistical analysis was presented (Brosnahan et al., 2019). Another reported an overgrowth of Tenacibaculum species in the fecal microbiota of salmonids undergoing low-temperature water treatment, however, the species could not be confirmed as T. maritimum (Ghosh et al., 2022). Increases in water temperature were reported to be associated with algal blooms (van Gelderen et al., 2011; Apablaza et al., 2017), which have been hypothesized to be a risk factor for T. maritimum infection.

Seasonality was reported in numerous studies and relationships to other factors such as water temperature, salinity, and dissolved oxygen were considered (n=7) ( Tables 3 , 5 ) (Frelier et al., 1994; Barker et al., 2009; van Gelderen et al., 2011; Downes et al., 2018; Nowlan et al., 2021a; Bass et al., 2022). Ultraviolet irradiation from the sun was reported as a possible cause of skin lesions that then propagate the growth of T. maritimum (Handlinger et al., 1997). One study found that increased numbers of all Tenacibaculum species, higher fish mortality, and increased tenacibaculosis outbreaks were recorded in the spring and summer compared to the fall and winter months (Nowlan et al., 2021a). Mortalities and antimicrobial applications to treat yellow mouth outbreaks during the spring and summer months were also identified to be indirectly correlated with increased temperature and decreased dissolved oxygen (Nowlan et al., 2021a). Another study reported decreased dissolved oxygen to be an environmental stressor (Apablaza et al., 2017) that could result from events such as algal blooms, contributing to an increased prevalence of infection with T. maritimum. The prevalence of T. maritimum found in sea lice surrounding farmed salmonid pens was also highest in the summer at times with the highest water temperature and lowest dissolved oxygen (Nowlan et al., 2021a). Another study stated that decreased levels of T. maritimum in Chinook salmon were associated with decreased mortality in fall and winter (Bass et al., 2022).

An increase in water salinity was reported as another factor associated with the application of antimicrobials (Nowlan et al., 2021a). Outbreaks have been described to occur during periods where salinity levels were between 29-32% (Frelier et al., 1994). One study reported that they found no association between the bacterial load of T. maritimum in salmonid-parasitizing sea lice and changes in water salinity, however, the statistical significance of these results was not reported (Barker et al., 2009).

Vectors of T. maritimum have also been reported as factors of infection. Horizontal transmission of T. maritimum between smolts has been experimentally reported (Frisch et al., 2018). Other proposed vectors include sea lice (Barker et al., 2009; Llewellyn et al., 2017; Nowlan et al., 2021a), lumpsuckers (Frisch et al., 2018), and from farmed onto wild salmonids (Bateman et al., 2022). One study reported that salmon infected with sea lice (Lepeophtheirus salmonis) did not have increased levels of T. maritimum compared to control fish (Llewellyn et al., 2017). Jellyfish have also been proposed as a vector, however, two studies reported that they were not suspected as the original source of T. maritimum infection (Smage et al., 2017; Downes et al., 2018). However, one article reported that jellyfish species do have the ability to carry T. maritimum and deposit it on or into the epidermis of fish upon contact (Ferguson et al., 2010).

Microbial factors were reported by 14 of the included studies ( Tables 3 , 6 , Supplementary Table 1 ). Several studies reported that T. maritimum is a natural part of the microbial community on the surface of salmonid skin, mucosal layer, and the oral cavity (van Gelderen et al., 2011; Reid et al., 2017; Wynne et al., 2020; Nowlan et al., 2021a; Ghosh et al., 2022). One study also reported that T. maritimum was able to form a biofilm on different surfaces such as tank walls (Frisch et al., 2018). Reports also suggested that endotoxins may be involved in the pathogenesis of disease from T. maritimum, since there was a lack of inflammatory markers found at the site of lesions (Handlinger et al., 1997; van Gelderen et al., 2011).

Fish microbiota has been reported to shift according to stressors such as temperature or co-infection, which may predispose fish to growth of T. maritimum (Reid et al., 2017). The amount of T. maritimum exposure, or bacterial load, has been reported as a possible factor for infection (Powell et al., 2004; van Gelderen et al., 2011). In two experimental studies, higher concentrations (2.3 x 10⁵ cells/mL & 1 x 10⁸ cells/mL) of T. maritimum in a bath challenge at constant salinity and temperature were reported to result in 100% mortality from yellow mouth within 3 days, whereas lower concentrations (< 2.3 x 10⁵ cells/mL) only resulted in mortalities after days to weeks (Soltani et al., 1996; van Gelderen et al., 2011).

In skin lesions on the dorsal and pectoral fins, it was observed that T. maritimum was restricted to the necrotic areas of the epithelium and did not infiltrate the musculature of salmon at any concentration (van Gelderen et al., 2011). The size of skin lesions was reported to be smaller in challenges with higher doses, and larger as doses decreased, although in the highest dose (1 x 10⁸ cells/mL) lesions across dorsal, lateral, and pectoral areas were found in similar percentages as the other doses (van Gelderen et al., 2011). This finding was similarly reported in another study, which stated that superficial lesions were common in early mortalities with a higher challenge concentration (2.3 x 10⁵ – 1.6 x 10⁷ cells/mL) and later mortalities had eroded ulcers (Soltani et al., 1996). Another study reported that wild salmon with a higher T. maritimum load had reduced lower-than-expected mass for their measured length (Bass et al., 2022).

Co-infection with other pathogens such as salmonid alphavirus (SAV) has been reported to increase the bacterial load of Tenacibaculum species on the skin of fish in a dose-dependent manner (Reid et al., 2017). This may be a response to a change in the microbial makeup of the skin, which allowed for T. maritimum to act as an opportunistic pathogen (Reid et al., 2017). One study also found higher levels of T. maritimum in dead and dying fish when compared to live fish collected from various salmon farm locations across British Columbia (Bateman et al., 2021). In cases of yellow mouth, it has been reported that T. maritimum is the dominant bacteria found in the oral cavity, although it is also one of the common bacteria in the mouths of unaffected or recovered salmon as well (Wynne et al., 2020). Co-infection with T. maritimum and Vibrio species was significantly associated only in salmon with yellow mouth, where Vibrio spp. load significantly increased in fish with clinical signs of yellow mouth when compared to healthy fish (Wynne et al., 2020). It was also reported that amoebic gill disease in salmon was not found to be a significant risk factor for the development of yellow mouth (Downes et al., 2018).

The age and size of salmonids appear to be a contributing factor of T. maritimum infection. Younger fish, particularly during their first year at sea when they are smaller and have softer scales, are reported as more susceptible to infection (van Gelderen et al., 2011; Downes et al., 2018; Bateman et al., 2021). Due to its lack of host specificity, disease from T. maritimum has been described in many other species such as dover sole, sea bass, red/black sea bream, and turbot, with a wide geographic range (Bernardet et al., 1994). In red/black sea bream, younger and smaller fish are reported to have more severe clinical signs than older and larger (>60 mm long) fish (Wakabayashi et al., 1984). Infection in these fish only occurred between 1-2 weeks following transfer from freshwater to saltwater (Wakabayashi et al., 1984). In Dover sole, the condition has also been described to be more common in younger fish, specifically during 60-100 days after hatching (McVicar and White, 1979). Decreased size as a function of increased T. maritimum load was also reported by a study, where it was concluded that this was a result of a decreased feeding rate (Bass et al., 2022). This is consistent with previous research indicating that T. maritimum infected fish become anorexic, making treatment with oral antimicrobials difficult (Soltani et al., 1995; Avendano-Herrera et al., 2006b).

The comparison between different salmonid species (Atlantic salmon and Rainbow trout) and non-salmonids (like greenback flounder) highlights variations in susceptibility, with Atlantic salmon showing significantly higher mortality and morbidity rates than greenback flounder, and similar morbidity/mortality to Rainbow trout (Soltani et al., 1996; Handlinger et al., 1997). There were no studies comparing morbidity and mortality in Atlantic and Pacific (including Chinook and Coho) salmon. However, in one study comparing Atlantic salmon and Rainbow trout at different bacterial concentrations, there was only a significant difference in mortalities at a concentration of 1.6 x 10⁶ cells/mL, not at any of the other concentrations, including a higher concentration of and 1.6 x 10⁷ cells/mL (Soltani et al., 1996). This result was not discussed by the authors, and based on the results of the other challenges, Rainbow trout and Atlantic salmon are assumed to show similar patterns of infection; consistent with other studies (Soltani et al., 1996; Handlinger et al., 1997). This information is crucial to understand the vulnerability of fish of different species, sizes, and ages to T. maritimum, which can inform infection risk.

Management practices likely play a pivotal role in T. maritimum infection and subsequent prevention. T. maritimum has been shown to be a part of the microbial community in both healthy and yellow mouth-affected salmonids (Wynne et al., 2020). This emphasizes its role as an opportunistic pathogen that could cause disease in immunocompromised fish (Wynne et al., 2020; Bateman et al., 2021). Management events such as transfer from fresh to saltwater, pen cleaning resulting in abrasion, and aggression from high stocking densities could all be stressful events resulting in infection (Wynne et al., 2020). Although at high enough concentrations, disease from T. maritimum has been demonstrated in the absence of abrasion (van Gelderen et al., 2011), many studies report that abrasion of the gills and body results in an increased severity of infection and mortality (Powell et al., 2004; Olsen et al., 2011; van Gelderen et al., 2011; Apablaza et al., 2017; Wynne et al., 2020). This was reported in another study involving sea bass, when scarified and smeared with Flexibacter maritimus broth culture, total mortality occurred within four days, with no mortality occurring in fish injected with the bacteria (Bernardet et al., 1994). The potential role of pen cleaning events in introducing T. maritimum emphasizes the need for careful maintenance of aquaculture facilities (van Gelderen et al., 2011). Higher stocking densities and improper feeding practices could result in aggressive behavior in Atlantic salmon (van Gelderen et al., 2011) who have been shown to bite and charge, resulting in abrasions (Mork et al., 1999). Reduced mortality due to T. maritimum has been demonstrated in Tasmania, where changed management procedures such as feeding practices and stocking densities were decreased (Handlinger et al., 1997).

Transfer from freshwater to saltwater was also identified as a factor (Smage et al., 2017; Nowlan et al., 2021a), especially during the first year at sea (Frelier et al., 1994; Downes et al., 2018; Nowlan et al., 2021a). This transfer is a stressful event that can pre-dispose fish to infection with T. maritimum (Wakabayashi et al., 1984; Frisch et al., 2018). This change has also been shown to alter the microbial community of the salmonid gut (Dehler et al., 2017), which could lead to dysbiosis and the overgrowth of opportunistic pathogens such as T. maritimum. Future research investigating microbial indicators could identify salmonids at risk for dysbiosis and disease (Dehler et al., 2017).

Vaccine development is a crucial management tool that could decrease T. maritimum outbreaks and thus antimicrobial use. AMR is a problem that exists at the interface of humans, animals, and the environment, therefore, we must consider it from a One Health perspective (Collignon and McEwen, 2019). With AMU in aquaculture, there comes the risk of AMR bacterial strains and genes developing in the aquatic environment and spreading to the terrestrial environment (Collignon and McEwen, 2019). By developing vaccines to prevent disease outbreaks or reduce morbidity/mortality of fish due to yellow mouth, the environmental and economic damages associated with yellow mouth can be modulated. Currently, the only vaccine approved for use against T. maritimum is for turbot in Spain (Nowlan et al., 2021b). In a vaccination study conducted in Tasmania and published in 2009, naïve Atlantic salmon had significantly better survival rates when injected with vaccine and adjuvant (Freund’s incomplete adjuvant), than the control group or vaccine-only group when challenged with T. maritimum (van Gelderen et al., 2009). This suggests the necessity for an adjuvant to demonstrate protection, however, the adjuvant group developed areas of melanin with granulomas and cysts focused in the fundic region (van Gelderen et al., 2009). These side-effects could lead to growth impairment and feed impaction (van Gelderen et al., 2009). A more recent study developed a vaccine for yellow mouth using isolates from western Canada that was able to elicit an antibody response, however, in a challenge scenario protection was not observed (Frisch et al., 2018). A difficulty in the development of a vaccine for salmonids may be due to the lack of repeatable and reliable challenge models (Nowlan et al., 2021b). Further, clinical signs of tenacibaculosis may be attributable to several Tenacibaculum species, making strain and species selection a challenge (Wynne et al., 2020; Nowlan et al., 2021b). This emphasizes the need for a reliable challenge model for T. maritimum in salmonids, and further vaccine development research.

Environmental conditions could significantly impact the amount of T. maritimum in the environment and therefor increase the risk of T. maritimum infection. Water temperature was reported as a factor of infection in many studies, with a consistent theme being that warmer water increases the prevalence of T. maritimum. The optimum growth range for T. maritimum is between 15-30°C, with temperatures above 15°C and higher salinities between 30-35% described as risk factors for tenacibaculosis (Avendano-Herrera et al., 2006b; Downes et al., 2018). Outbreaks in both salmonids and other farmed fish such as wedge sole have been reported to occur at water temperatures between 15-20°C, which may be the result of an increased stress response in fish and increased bacterial growth (van Gelderen et al., 2011; Mabrok et al., 2023). In adult Chinook salmon, warmer water temperature (16-24°C) has been associated with decreased growth and impaired smoltification (Carter, 2005). In salmonids, it is suggested that risk from all diseases is limited at temperatures between 12-13°C, with risk increasing from 14-17°C and high from 18-20°C (Carter, 2005). Exposure to temperatures outside of optimum rearing ranges may result in increased stress, which has immunosuppressive action (Abram et al., 2017). There is an observed suppression of the immune system when fish are exposed to cold stress due to overwintering strategies (Abram et al., 2017). This could explain why outbreaks of tenacibaculosis have also been observed in the winter months, why another study described an overgrowth of Tenacibaculum species in the fecal microbiota of salmonids undergoing low-temperature water treatment (Ghosh et al., 2022), or why decreased levels of T. maritimum in Chinook salmon in the fall and winter months were associated with decreased mortality (Bass et al., 2022). This further highlights the multiplicity of considerations at play even within one environmental factor of interest.

It has been postulated that factors such as UV irradiation, changes in salinity, and dissolved oxygen levels are associated with yellow mouth in salmonids (Wade and Weber, 2020). Decreasing the salinity and/or temperature in a pen has previously been shown to reduce yellow mouth mortality in affected salmonids (Soltani and Burke, 1995), however, subsequent studies found that freshwater treatments had no significant effect on the presence of the bacteria (Downes et al., 2018). Outbreaks of yellow mouth are significantly correlated with seasonality, with increasing prevalence in the summer, followed by a decline in outbreaks over the winter months (Downes et al., 2018). The predisposing source of tissue damage by UV irradiation and subsequent T. maritimum infiltration has been supported by several outbreak cases where spongy changes, as reported by Bullock et al., 1988, were observed to be the likely result of UV damage (Bullock, 1988; Handlinger et al., 1997). In natural infections, eye and dorsal surface lesions were more common in comparison to experimental conditions, which could also confirm the importance of UV irradiation (Handlinger et al., 1997). However, this is not the sole predisposing factor, since disease with similar lesions in different locations has been found in fish in settings with controlled lighting (Handlinger et al., 1997). Algal blooms have been suggested as a factor in T. maritimum infection outbreaks, since algal blooms decrease oxygenation and increase stress on fish (Riisberg and Edvardsen, 2008; Apablaza et al., 2017). Higher water temperatures which are conducive to the growth of T. maritimum also lead to algal blooms, which could result in a multiplicity of stressors leading to infection (Riisberg and Edvardsen, 2008; Apablaza et al., 2017). Recognizing these environmental factors can aid in predicting and mitigating T. maritimum outbreaks, especially in regions where aquaculture is prevalent.

T. maritimum has no host specificity and can transmit horizontally, therefore vectors are a factor of interest. Potential vectors for transmission in salmonids could be sea lice (Barker et al., 2009; Llewellyn et al., 2017; Nowlan et al., 2021a), jellyfish (Smage et al., 2017; Downes et al., 2018), and lumpsuckers (Frisch et al., 2018). However, none of the included studies were able to demonstrate that the vector of interest was the original source of T. maritimum. Instead, vectors such as jellyfish or plankton may play a role in tissue damage leading to abrasion, which could allow T. maritimum to proliferate (Ferguson et al., 2010; Apablaza et al., 2017). T. maritimum has been detected in Pelagia quadtrata and Muggiaea atlantica and Pelagia notiluca jellyfish species which are known to cause gill damage leading to disease in salmon (Delannoy et al., 2011; Fringuelli et al., 2012). The transmission of T. maritimum between wild and farmed salmonids in BC has also been a concern in the recent years, due to the decline of Sockeye salmon in the region (Bateman et al., 2022). In a study screening Sockeye salmon smolts as they migrate past salmon farms in the Discovery Islands region, there was a peak of 12.7 times the background level of T. maritimum prevalence (Bateman et al., 2022). However, this could not be confirmed because of interaction with farmed fish, as the region is described as a hydrographic funnel that forces migrating salmon into a higher density and could magnify all sources of T. maritimum pressure (Bateman et al., 2022).

T. maritimum is part of the natural microbial community on the surface of salmonids (van Gelderen et al., 2011; Reid et al., 2017; Wynne et al., 2020; Nowlan et al., 2021a; Ghosh et al., 2022). Based on previous bacterial culture reports, T. maritimum is difficult to culture in non-sterile seawater, which may suggest that its growth is inhibited in the natural aquatic environment due to inhibition of other bacteria (Avendano-Herrera et al., 2006a). Understanding the microbial makeup of fish skin, mucus, and oral cavity is essential in assessing the risk of T. maritimum infections. Fish microbiota can shift and undergo dysbiosis because of challenges from stress such as temperature, fresh to saltwater transfer, and co-infection (Reid et al., 2017; Ghosh et al., 2022). Under experimental conditions, it has been demonstrated that temperature has a significant effect on the salmonid gut microbiota, skin mucous, and water microbiota (Ghosh et al., 2022). This dysbiosis allows for pathogenic and opportunistic bacteria to proliferate, for example, salmonid alphavirus infection can increase the bacterial load of Tenacibaculum species on the skin of infected fish (Reid et al., 2017). Differences in microbial load challenge studies, such as number of data replicates must also be considered. Studies have also reported strong and significant positive correlations between T. maritimum and many other infectious agents in farmed Atlantic salmon in BC (Bateman et al., 2021). Tenacibaculum dicentrarchi and Tenacibaculum finnmarkense have also been linked to tenacibaculosis outbreaks in Chile and Canada (Avendano-Herrera et al., 2020; Nowlan et al., 2021a). These bacteria are often found together and may result in disease displaying similar clinical signs such as mouth erosions and frayed fins (Wynne et al., 2020; Nowlan et al., 2021a; Mabrok et al., 2023). Therefore, it is becoming increasingly important to understand the natural microbial community of salmonids and the pathogenic source of outbreaks, to further develop treatment and control strategies.