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. 2024 Dec 15;48(4):e14067. doi: 10.1111/jfd.14067

First Report of ‘Soft Flesh’ Induced by the Parasite Kudoa thyrsites (Myxosporea) in Commercial Codfish From Norway

Lucilla Giulietti 1,✉, Arne Levsen 1, Miguel Bao 1, Egil Karlsbakk 1,2, Julia E Storesund 1, Hui‐Shan Tung 1, Paolo Cipriani 1,3
PMCID: PMC11907682  PMID: 39676448

ABSTRACT

Kudoa thyrsites is a myxosporean parasite that infects the skeletal muscle of various teleost fish species globally. Severe infections lead to ‘soft flesh’ in fish fillets, resulting in food spoilage and subsequent discard. While K. thyrsites has previously been identified in migratory Atlantic mackerel in the northern Northeast Atlantic Ocean, it has not been observed in resident or farmed fish species in Norwegian waters until now. This study presents the first evidence of K. thyrsites infection and the associated ‘soft flesh’ condition in resident commercially important gadoid species from Norwegian waters, including Norwegian coastal cod (NCC), Northeast Arctic cod (NEA) and tusk. Molecular analyses confirmed the parasitic infection in ‘soft flesh’‐affected fish sampled from multiple coastal locations in Norway. The life cycle of Kudoa remains unknown but likely involves an alternating annelid host as in other myxosporeans. These findings in resident hosts suggest that the parasite completes its life cycle also at higher latitudes, in northern Norway. Consequently, there is a risk for the Norwegian fishing industry, as the effect of the parasite on fish fillet texture can occasionally occur and impact both consumer acceptance and industry revenues.

Keywords: Brosme brosme , cod, codfish, Gadus morhua , Kudoa thyrsites , soft flesh, tusk

1. Introduction

Kudoa thyrsites is a widespread myxosporean parasite that infects the skeletal muscle of several teleost species worldwide, including economically valuable farmed salmonids such as farmed Atlantic salmon ( Salmo salar ) (reviewed by Henning, Hoffman, and Manley (2013) and Levsen (2015). In the northern Northeast Atlantic, this species has been found in migratory commercial‐sized Atlantic mackerel ( Scomber scombrus ), but it has not been found in resident fish species or farmed fish so far (Giulietti, Karlsbakk, et al. 2022; Højgaard, Homrum, and Salter 2022; Levsen, Jørgensen, and Mo 2008; Soares et al. 2023). This parasite has been sporadically reported in sea trout ( Salmo trutta ) and farmed Atlantic salmon from Ireland, southern England and France (Holliman 1994; Palmer 1994; Prudhomme and Pantaleon 1959), where also migratory hosts such as mackerel could acquire infections (Giulietti, Karlsbakk, et al. 2022). Kudoa thyrsites may cause liquefaction of fish skeletal muscle, also known as ‘soft‐flesh’ or ‘jelly fish’, in heavily infected fish after death, leading to food spoilage and discard (Giulietti, Karlsbakk, et al. 2022; Moran, Whitaker, and Kent 1999a; St‐Hilaire, Hill, et al. 1997). The condition results from the enzymatic degradation of the fish flesh (Funk et al. 2008), emerging 6–48 h post mortem (Giulietti, Karlsbakk, et al. 2022; St‐Hilaire, Hill, et al. 1997) or even after several days or weeks in initially frozen and subsequently thawed fillets (A. Levsen, personal observation). As a result, infected intact fish prone to develop ‘soft flesh’ may reach retailers or consumers and be discarded, potentially jeopardising the fishing industry's reputation and causing loss of revenue (Giulietti, Karlsbakk, et al. 2022; reviewed by Levsen 2015). Although no foodborne disease cases have been reported for K. thyrsites, antibodies against Kudoa have been found in individuals with allergic reactions to fish, suggesting potential hypersensitivity related to K. thyrsites (EFSA BIOHAZ Panel 2024; Martínez de Velasco et al. 2008).

Gadoid fish species, commonly referred to as codfish, are the most commercially important wild species in Norway (Strand et al. 2024; Straume et al. 2024). Among them, the Atlantic cod ( Gadus morhua ) is the most economically valuable wild fish in Europe, with Norway landing about 290,000 t in 2023 (EUMOFA 2023; Directorate of Fisheries 2023). The Northeast Arctic cod (NEA) (or skrei) is the largest stock, supporting a Barents Sea fishery valued at over 790 million Euros (Directorate of Fisheries 2023). Unlike other migratory fish, the NEA cod remain in northern waters, migrating seasonally within Norwegian waters to spawn near Lofoten Archipelago each spring, while Norwegian coastal cod (NCC) reside in fjords year‐round (Jakobsen 1987; Olsen et al. 2010). Cod is processed into various products, including fillets and dry‐salted fish (clipfish) for export (Sogn‐Grundvåg et al. 2021; Straume et al. 2020). Tusk ( Brosme brosme ) is a deepwater fish found at depths of 60–400 m in the Northeast Atlantic, exhibiting limited migration and genetic variations (ICES 2023; Knutsen et al. 2009). Primarily caught as bycatch, tusk is less consumed than cod but is valued for its taste and exported as dry‐salted clipfish to Brazil, Italy and Portugal (Norwegian Seafood Council 2023; Tveit et al. 2023). Recent efforts aim to enhance the value of tusk fisheries through increased investment in fillet production (Tveit et al. 2023).

Texture quality of fish fillet is an important factor for consumer acceptance. Mechanical damage during fishing operations, large catch size and autolytic changes, as well as infections with bacteria and parasites, can cause undesired softening or gaping of the fillets, adversely affecting product quality and marketability (reviewed by Bolin et al. 2021; Cheng et al. 2014 and Sogn‐Grundvåg et al. 2022). The present study reports cases of softening and liquefaction in the musculature of economically important fish stocks from Norwegian waters, including NCC, NEA and tusk, which are all associated with K. thyrsites infections.

2. Material and Methods

In total, 78 NCC, 30 NEA and 33 tusks were collected during Institute of Marine Research (IMR) research surveys and by local fishermen using bottom trawl and longline (see Figure 1 and Table 1). Fish were frozen at sea (−20°C) and sent to IMR in Bergen, Norway, for parasitological inspection.

FIGURE 1.

FIGURE 1

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Catch localities of Norwegian coastal cod (NCC), Northeast Arctic cod (NEA) and tusk, in Norwegian waters. (SK) Skaggerak—off Helgøya, (HO) Hordaland—off Grasøyane, (TR) SørTrøndelag—off Hitra, (NO) Nordaland—off Kvalnes and (VE) Vestfjord—off the Lofoten archipelago.

TABLE 1.

Catching locality, sampling month and year, sample size and biometric data of Norwegian coastal cod (NCC), Northeast Arctic cod (NEA) and tusk collected from Norwegian waters.

Fish hosts Catching locality, coordinates and sampling date
Norwegian coastal cod (NCC) Overall (SK) Skaggerak—off Helgøya (HO) Hordaland—off Grasøyane (NO) Nordaland—off Kvalnes (VE) Vestfjord—off the Lofoten archipelago

58°2.4′ N

7°51.6′ E

62°26.262′ N

5°44.43′ E

65°57′ N

12°45.4′ E

67°35.4′ N

13°9.8298′ E
Early October 2023 Early January 2024 Late October 2023 Early November 2023
Sample size (N) N = 78 N = 30 N = 25 N = 19 N = 4
N ‘soft flesh’ affected fish 6 1 1 3 1
Occurrence ‘soft flesh’ (%) 7.7% 3.3% 4% 15.8% 25%
Biometrics—all fish examined
TL 586 ± 120 (425–850) 668 ± 57 (585–795) 486 ± 168 (230–690) 588 ± 189 (330–730)
TW 2447 ± 1600 (808–7505) 3305 ± 1139 (2001–6470) 1716 ± 1363 (210–3857) 2428 ± 1714 (373–3886)
Biometrics—‘soft flesh’ affected fish
TL 585 ± 138 (230–850) 450 n.a. 410 ± 182 (300–620) 720
TW 2603 ± 1507 (210–7505) 994 2318 1285 ± 1812 (227–3377) 3565
Northeast Arctic cod (NEA) (VE) Vestfjord—off Lofoten archipelago
68°2.88′ N 13°50.868′ E
Mid‐March 2024
Sample size (N) N = 30
N ‘soft flesh’ affected fish 1
Occurrence ‘soft flesh’ (%) 3.3%
Biometrics—all fish examined
TL 912 ± 55 (795–1015)
TW 7223 ± 998 (5200–9014)
Biometrics—‘soft flesh’ affected fish
TL 912
TW 7244
Tusk (TR) SørTrøndelag—off Hitra
63°33′ N 8°16.8′ E
Mid‐September 2023
Sample size (N) N = 33
N ‘soft flesh’ affected fish 1
Occurrence ‘soft flesh’ (%) 3%
Biometrics—all fish examined
TL 532 ± 94 (400–730)
TW 1995 ± 1198 (642–4761)
Biometrics—‘soft flesh’ affected fish
TL 527
TW 1916
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Note: Total body length (TL, mm) and total body weight (TW, g) are presented as mean ± SD (range).

Abbreviation: n.a., not acquired.

After thawing, fish were measured (total body length—TL) and weighed (total body weight—TW). Routine inspections for ascaridoid parasites, conducted approximately 48 h after thawing, revealed several fish specimens with abnormally soft and liquefied fillets. Consequently, all the remaining fish were examined for Kudoa‐induced ‘soft flesh’ using manual texture testing and visual inspection, following the procedure detailed by Levsen, Jørgensen, and Mo (2008). Muscle samples from liquefied areas were prepared on glass slides, moistened with saline, minced (St‐Hilaire, Ribble, et al. 1997) and examined microscopically at 400–1000× magnification for microparasites. Liquefied muscle tissue was stored in vials at −20°C for molecular analyses.

Soft muscle samples were tested for Kudoa spp. infections by molecular analysis. DNA was extracted from 40 mg of liquefied tissue with the DNeasy Blood and Tissue Kit (Qiagen). Kudoa spp. small subunit ribosomal RNA (SSU rRNA) gene sequences were amplified with PCR using primers Ksp18SF and Ksp18SR (Giulietti et al. 2020). For samples with weak bands, a nested PCR was performed using SSUfor1 (Levsen, Jørgensen, and Mo 2008) and a reverse primer from Funk et al. (2007). PCR reactions were conducted in a 25‐μL volume following the procedure reported by Giulietti et al. (2020). Purification and sequencing of PCR products were performed by Eurofins (Cologne, Germany). Sequences were assembled with ChromasPro 2.1.8 and aligned using ClustalX 2.0 (Larkin et al. 2007). Sequence similarity was checked using the Nucleotide Basic Local Alignment Search Tool (BLAST).

The occurrence of ‘soft flesh’ was calculated as the proportion of affected fish among those examined and confirmed infected by molecular analysis (Giulietti et al. 2024).

3. Results

In Atlantic cod, ‘soft flesh’ was found in 3.3% (1/30) of NEA cod from the Lofoten archipelago (VE) and in 7.7% (6/78) of NCC cod caught in the area from Skagerrak (SK) to VE (Table 1 and Figure 1). In tusk, 3% (1/33) of the fish caught from off Hitra in SørTrøndelag (TR) displayed ‘soft flesh’ (Table 1 and Figure 1). In all cases, infected specimens generally retained an intact myomere structure, with localised muscle degradation in the upper hypaxial musculature (upper belly flaps) (Figure 2a–c). In some NCC cod, a complete rupture of the myomere structure resulted in total liquefaction (Figure 2d).

FIGURE 2.

FIGURE 2

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Illustration of Kudoa‐induced ‘soft flesh’ condition in fillet of tusk (a), and Northeast Arctic cod (NEA) (b) and Norwegian coastal cod (NCC) (c, d) caught in Norwegian waters. Most specimens exhibited a muscle degradation focally localised in the belly flap (a–c), while a few NCC cod specimens showed a complete rupture of the segmental myomere structure throughout the flesh, resulting in complete liquefaction without any firmness (d).

Microscopic analysis revealed myxosporean plasmodia in the skeletal muscle of tusk, along with a few small immature spores (approximately 4 μm). No plasmodia or spores were detected in the liquefied muscle of NCC and NEA cod. All eight soft fish specimens were found infected with K. thyrsites. The eight partial SSU rDNA sequences (377‐1289 bp) were identical (GenBank accession number PQ659029‐PQ659031). They were also identical to K. thyrsites sequences from its type host African snoek ( Thyrsites atun ) from South Africa (AY078430), as well as from Atlantic mackerel in southern Norwegian waters (MT913636‐7) and other hosts from the Atlantic (GenBank accession numbers AY542482, OM200072 and PQ164243).

4. Discussion

For the first time, we recorded K. thyrsites infection and the associated ‘soft flesh’ condition in Atlantic cod and tusk. Kudoa thyrsites infects various teleost species globally, but reports from Gadiformes are limited (Henning, Hoffman, and Manley 2013; Levsen 2015). Documented infections leading to ‘soft flesh’ have occurred in several hake species, including Pacific hake ( Merluccius productus ) and South African hake ( Merluccius capensis ) (Henning, Hoffman, and Manley 2013). Kudoa thyrsites has also been reported in Alaska pollock ( Gadus chalcogrammus ) from British Columbia and blue whiting ( Micromesistius poutassou ) from Portugal (Cavaleiro et al. 2021; Kabata and Whitaker 1984). In the late 1980s, anecdotal reports of abnormally rapid autolysis in cod flesh from the Oslo fjord area in Eastern Norway and along the Swedish west coast suggested a condition caused by Kudoa parasites (Jensen 1987). The present discovery in Atlantic cod and tusk broadens the known host range of K. thyrsites supporting its low host specificity (Henning, Hoffman, and Manley 2013; Levsen 2015).

This study provides evidence of Kudoa thyrsites transmission within Norwegian waters, marking the northernmost record of infection in resident fish species and expanding the known distribution of this parasite to northern Norway, above the Arctic Circle.

The life cycle of Kudoa spp. is unknown (Moran, Whitaker, and Kent 1999b; Yokoyama et al. 2015), but it is assumed to involve a definitive annelid host and an intermediate fish host (Eszterbauer et al. 2015). For instance, Sphaerospora dicentrarchi, a related kudoid parasite (Casal et al. 2019), uses the polychaete Capitella sp. as invertebrate host (Rangel et al. 2009). Fish likely become infected through their skin, fins or gills via actinospores released from the annelid host (Eszterbauer et al. 2015). To date, in the northern Northeast Atlantic, K. thyrsites has been exclusively documented in migratory Atlantic mackerel from Scottish waters, the Faroe Islands, the North Sea and the southern Norwegian Sea (Giulietti, Karlsbakk, et al. 2022; Højgaard, Homrum, and Salter 2022; Levsen, Jørgensen, and Mo 2008; Soares et al. 2023). Due to the absence of K. thyrsites infections in resident fish from Nordic seas, Giulietti, Karlsbakk, et al. (2022) proposed that migrating mackerel might acquire it in southern regions, such as off the Iberian Peninsula and the British Isles, areas where the unknown definitive invertebrate hosts are likely found. Reports of K. thyrsites infections in sea trout and farmed Atlantic salmon from these regions indicate potential transmission there (Barja and Toranzo 1993; Holliman 1994; Palmer 1994; Prudhomme and Pantaleon 1959). However, our novel finding of K. thyrsites in resident fish species from coastal Norway provides evidence that this parasite can be transmitted in these waters and indicates that it can complete its life cycle there. Species such as tusk, NCC cod and NEA cod are primarily confined to Norwegian waters and do not migrate south (ICES 2023; Johansen et al. 2020; Knutsen et al. 2009). Hence, these species likely acquire K. thyrsites infections through exposure to infective stages present in Norwegian coastal waters. Transmission through predation on infected mackerel is unlikely, as fish‐to‐fish transmission via ingestion of infected tissue has been unsuccessful (Moran, Whitaker, and Kent 1999b; Yokoyama et al. 2015). Thus, infections in these resident species likely arise from direct environmental exposure to infective actinospore stages rather than from predation on infected migratory species.

It remains unclear whether the parasite is endemic to Norwegian waters or has more recently spread. Similar to other parasites moving from temperate and subtropical regions to northern waters (Dupouy‐Camet 2016), changes in the NE Atlantic ecosystem could have facilitated its northward spread. Alternatively, infections may have been overlooked, with cases of ‘soft flesh’ misattributed to handling or storage issues, as the parasite is typically noted in heavily infected hosts, while many cases may remain undetected (Giulietti, Karlsbakk, et al. 2022; St‐Hilaire, Hill, et al. 1997).

In NCC and NEA cod affected by ‘soft flesh’, neither plasmodia nor spores were observed in the liquefied muscle tissue. A similar finding was reported in heavily liquefied Atlantic mackerel infected with K. thyrsites (Giulietti, Johansen Nedberg, et al. 2022). This has led to the suggestion that prolonged storage of liquefied muscle under laboratory conditions may degrade parasite spores due to proteolytic enzymes in the fish flesh (Giulietti, Johansen Nedberg, et al. 2022), which could explain the absence of spores and plasmodia in the cod samples.

The occurrence of K. thyrsites–induced ‘soft flesh’ may present challenges for the fishery industry in Norway, if impacting the quality and consumer perception of gadoid fillet products. This condition compromises fillet quality, leading to decreased consumer acceptance (Sogn‐Grundvåg et al. 2021) and potentially resulting in reduced prices and reputational damage in both domestic and international markets (Levsen 2015). The rapid onset of ‘soft flesh’ shortly after harvest—observable even in frozen products upon thawing (A. Levsen, personal observation)—limits opportunities for value‐added processing and marketing. This issue is particularly critical given the economic significance of gadoid species to the fish processing sector in Norway (Sogn‐Grundvåg et al. 2021; Tveit et al. 2023). Recent examples illustrate the impact of this quality issue; K. thyrsites infections have negatively affected the Norwegian mackerel industry (Giulietti, Karlsbakk, et al. 2022), while Kudoa musculoliquefaciens has caused significant economic losses in the broadbill swordfish fishery in Australia (Bolin et al. 2021). In British Columbia, K. thyrsites resulted in substantial losses in salmonid aquaculture, amounting to 50 million Canadian dollars in 2002 (Funk et al. 2007; Marshall et al. 2016). Although extensive salmonid and cod farming occurs in Norway, there are no reports of K. thyrsites infections in Norwegian farmed fish. However, cases of K. thyrsites infection and associated ‘soft flesh’ condition may have been overlooked, as the condition can develop up to 48 h post mortem (Giulietti, Karlsbakk, et al. 2022; St‐Hilaire, Hill, et al. 1997) and could be misattributed to handling or storage issues.

Now there is a need to expand our knowledge regarding the prevalence and density of this parasite in commercially important gadoids and farmed salmonids in Norwegian waters and Nordic seas.

Author Contributions

Lucilla Giulietti: conceptualization, methodology, validation, formal analysis, investigation, data Curation, project administration, writing – original draft and writing – review and editing. Arne Levsen: formal analysis, investigation, conceptualization, writing – review and editing and supervision. Miguel Bao: writing – review and editing. Egil Karlsbakk: writing – review and editing. Julia E. Storesund: writing – review and editing and visualization. Hui‐Shan Tung: formal analysis. Paolo Cipriani: conceptualization, methodology, validation, formal analysis, investigation, data curation, visualization, writing – original draft and writing – review and editing.

Conflicts of Interest

The authors declare no conflicts of interest.

Acknowledgements

We thank Stig Mæhle for his assistance and help with the molecular analyses. We further thank Aina Bruvik and Rebeca Perez Garcia for their help with sample preparation. The study is based on data collected within the project ‘Monitoring of parasites in commercially important wild fish in Norway’ financed by the Institute of Marine Research (IMR), Norway, and the Norwegian Fiskeriforskningsavgiften (FFA).

Funding: This work was supported by the Institute of Marine Research (IMR) and the Norwegian Fiskeriforskningsavgiften (FFA).

Contributor Information

Lucilla Giulietti, Email: lucilla.giulietti@hi.no.

Arne Levsen, Email: arne.levsen@hi.no.

Miguel Bao, Email: miguel.bao@hi.no.

Egil Karlsbakk, Email: egil.karlsbakk@uib.no.

Julia E. Storesund, Email: julia.storesund@hi.no.

Hui‐Shan Tung, Email: hui-shan.tung@hi.no.

Paolo Cipriani, Email: paolo.cipriani@hi.no.

Data Availability Statement

All data generated or analysed during this study are included in this published article. Sequences data are made available in NCBI: http://www.ncbi.nlm.nih.gov/genbank.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

All data generated or analysed during this study are included in this published article. Sequences data are made available in NCBI: http://www.ncbi.nlm.nih.gov/genbank.

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