Gallbladders with mucosal outpouchings (diverticula) were found in a population of Atlantic salmon farmed in sea water. Soft tissue calcification affected the skin, skeletal muscle and gut, as identified by histological observations. In addition, inflammation of muscle and intestinal tissue and lymphocytic and fibrous reaction were present in the liver. The general fish population was characterized by poor growth and unspecified mortalities. Here we describe the observed lesions and discuss them in the light of the general health status of the population.Lesions of the biliary system in Atlantic salmon (Salmo salar L.)publishedVersio

Chikwati, Elvis Mashingaidze

Dalum, Alf Seljenes

Einen, Olai

Kortner, Trond M.

Mørkøre, Turid

Ravndal, Jarle

Sveen, Lene

English

NOFIMA Repository

J Fish Dis. 2022;00:1–5.   | 1wileyonlinelibrary.com/journal/jfdReceived: 31 July 2022  | Revised: 6 October 2022  | Accepted: 11 October 2022DOI: 10.1111/jfd.13724  S H O R T  C O M M U N I C A T I O NLesions of the biliary system in Atlantic salmon (Salmo salar L.)Lene R. Sveen1  |   Elvis Chikwati2 |   Alf Dalum1 |   Trond M. Kortner2 |   Jarle Ravndal3 |   Olai Einen4 |   Turid Mørkøre51Norwegian Institute of Food Fisheries and Aquaculture Research (Nofima), Tromsø, Norway2Department of Paraclinical Sciences, Faculty of Veterinary Medicine, Norwegian University of Life Sciences, Ås, Norway3Cargill Aqua Nutrition, Bergen, Norway4Cermaq Group AS, Oslo, Norway5Department of Animal and Aquacultural Sciences, Faculty of Biosciences, Norwegian University of Life Sciences, Ås, NorwayCorrespondenceLene R. Sveen, Nofima AS, Osloveien 1, Post box 210, NO- 1431 Ås, Norway.Email: lene.sveen@nofima.noFunding informationCargill; Cermaq; Norges Forskningsråd, Grant/Award Number: 296296; RFF ARKTISKeywords: Atlantic salmon, calcification, gallbladder, inflammation, pathologyGallbladders with mucosal outpouchings (diverticula) were found in a population of Atlantic salmon farmed in sea water. Soft tissue cal-cification affected the skin, skeletal muscle and gut, as identified by histological observations. In addition, inflammation of muscle and intestinal tissue and lymphocytic and fibrous reaction were present in the liver. The general fish population was characterized by poor growth and unspecified mortalities. Here we describe the observed lesions and discuss them in the light of the general health status of the population.1  |  STUDY POPUL ATIONThis study was part of a feeding trial in Finnmark county, northern Norway. The fish used were 147 g Atlantic salmon smolts transferred to six commercial seawater cages in November 2018 (68,415 salmon per cage) and harvested in May 2020 (2.9 kg). The fish were fed ac-cording to nutritional requirements with either a constant or sea-sonal adjusted EPA + DHA regimes in triplicates.In October 2019 (11 months at sea) and May 2020 (at harvest), fish were randomly selected from each of the sea cages (n = 10) for biometric determinations. Tissue samples from four fish per sea cage waere collected from pyloric caeca, distal intestine and liver (liver only from May sampling), while skin with attached red and white skeletal muscle was collected from five fish per sea cage. In May, gallbladders with visual pathological changes were collected from four individuals. Tissue samples were fixed in 10% phosphate- buffered formalin and stained with haematoxylin and eosin (H&E) according to Li et al. (2019), Alcian blue and PAS (AB/PAS) according to Sveen et al. (2021) and Von Kossa according to Culling et al. (2014). For registered pathologies, the reader is re-ferred to Appendix S1.2  |  RESULTSAfter 17.5 months in sea, growth was poorer than expected with 2.9 kg average harvest weight, whereas the expected slaughter weight for Atlantic salmon is 4– 5 kg (Barrett et al., 2022). The cu-mulative mortality for the production was 13.3% with the weekly number of mortalities per cause given in Figure 1. Skin ulcers and unspecified mortalities were the main causes of losses, followed by mechanical delousing operations and some cases of heart and skel-etal muscle inflammation (HSMI), with no dietary effects.Gross pathology of the gall bladder ranged from minor to severe enlargement of the organ with numerous dark bulging lesions on the surface (Figure 2). The condition affected 4% of the sampled fish in October and 7% of the sampled fish in May. Microscopic findings This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.© 2022 The Authors. Journal of Fish Diseases published by John Wiley & Sons Ltd. 13652761, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jfd.13724 by Nofima, Wiley Online Library on [01/11/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License2  |    SVEEN et al.F I G U R E  1  Weekly number of mortalities. Mortalities per cause (stacked bars) as recorded by the local fish health personnel and accumulated mortality (red line). Total initial farm inventory 410,490.F I G U R E  2  Pathology of the gall bladder. (a, b) Photos of gall bladders with lesions (c– i). Tissue sections of diverticula with characteristic connective tissue formation, eosinophilic granular cells (white arrow), melanized foci (black arrow), mucus (pattern arrow) response in the columnar epithelial tissue and lumen. Tissue sections stained with AB/PAS. 13652761, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jfd.13724 by Nofima, Wiley Online Library on [01/11/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License    |  3SVEEN et al.showed diverticula of the mucosal wall, thickening of the fibro-muscular layer, with the presence of eosinophilic granular cells and melanized foci (Figure 2f). An excessive mucus response was noted in the columnar epithelial tissue and lumen in some of the diverticula (Figure 2g– i).Mild to severe lipid accumulation (steatosis) was observed within the enterocytes in pyloric caeca affecting 92% of the sam-ples in October 2019 and 38% in May 2020. In the distal intestine, 70% of the samples had mild to marked inflammation in October, whereas in May, 50% of the samples were characterized by infil-tration of the submucosa and lamina propria by a mixed popula-tion of inflammatory cells, shortening of mucosal folds and loss of supranuclear vacuoles in the enterocytes (Figure 3). In the liver, a peribiliary lymphocytic and fibrous reaction was observed as the main pathological finding (Figure 3), affecting 46% of the samples at harvest.Mineralized foci were present in the skin, skeletal muscle, py-loric caeca and the distal intestine. In October 2018, 73% of the skin F I G U R E  3  Lesions of the liver and distal intestine. (a) Peribiliary lymphocytic infiltration and fibrosis in the liver bile ducts (white asterisks), fibrous and lymphocytic infiltration (black arrow) and degeneration of the epithelium (white arrow). (b) Normal morphology of the distal intestine. (c) Moderate enteritis. (d) Multifocal lesions of soft tissue calcification in muscularis (black arrows), circular well- defined calcified lesions accompanied by no tissue reaction (e) Magnified insert. Tissue sections stained with H&E.F I G U R E  4  Calcification of skin and muscle tissue. (a– c) Calcified lesions (black arrow) were found in skin (Ski) dermis, myosepta (Myo), red and white muscle tissue (Mu). (d– f) Red and white muscle tissue with inflammation (white arrow) and vacuolization (pattern filled arrow). Tissue section (a– c) stained with Von Kossa, (d– f) with AB/PAS 13652761, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jfd.13724 by Nofima, Wiley Online Library on [01/11/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License4  |    SVEEN et al.dermis- , myosepta- and muscle tissue were affected, accompanied by inflammation and vacuolization of red muscle tissue (Figure 4). In May 2020, 70% of the skin samples, 38% of distal intestine and 8% of the pyloric caeca samples had calcified lesions (Figures 3 and 4), while only one fish had inflammation in red muscle tissue.3  |  DISCUSSIONHere we present findings from a population of A. salmon, which upon harvest was characterized by poor growth, unspecified mor-talities, incidences of calcinosis and lesions of the digestive and biliary system (Figure 5). The recorded causes of mortality and the average mortality rate represent the general trend in the industry (Sommerset et al., 2020). The large size of the diverticula suggests that this condition must have persisted for some time. The nature of the calcified foci and fibrosis of the hepatic duct further suggests a chronic state of the lesions. Such a chronic disease progression likely reduces the fitness of the animals and overlaps well in time with the unspecified mortalities recorded for this production. The high incidences of lesions in the gut and the biliary system likely af-fected nutrient digestion and absorption negatively, which may have contributed to the poor growth observed for the population.The lesions of the gallbladders resemble that of intramural di-verticulosis described in humans (Mark & Melnick, 1964; Ross et al., 1955). Ross et al. describe these diverticula as a likely con-sequence of chronic inflammation and increased luminar pressure, resulting in pulsion diverticula into the loose stroma of the gallblad-der wall. Here, the high percentage of lesions in the biliary system and gut may indicate that these events are connected. Bile acids are further vital for the absorption of dietary fat and fat- soluble vitamins such as Vitamin D. Dysregulation of vitamin D is related to calcifica-tion processes (Black & Kanat, 1985); hence, it is plausible that the biliary lesions may be connected to the calcified foci. Unfortunately, liver/gut and skin/gallbladder samples were collected from different individuals, and this hypothesis needs further elucidation.The samples for this study were collected from random fish at a commercial production site; hence, we believe that the findings are representative for the population. The series of lesions may repre-sent a health problem which may have been overlooked previously.ACKNOWLEDG EMENTSThe authors express their gratitude to Mira Hansen at the Veterinary Institute laboratory at Harstad for excellent histological processing of tissue samples.FUNDING INFORMATIONThis work was funded by the project ‘Omega- 3 for salmon under Arctic conditions – optimization of use and effects on fish health and fillet quality’ which was supported by Researcsh Council of Norway grant no 296296 – RFF ARKTIS and the industrial partners Cermaq and Cargill.CONFLIC T OF INTERE S TThe authors declare that there are no conflicts of interest associated with this publication.DATA AVAIL ABILIT Y S TATEMENTThe data that support the findings of this study are available on re-quest from the corresponding author. The data are not publicly avail-able due to privacy or ethical restrictions.ORCIDLene R. Sveen  https://orcid.org/0000-0003-3394-3462 R E FE R E N C E SBarrett, L., Oldham, T., Kristiansen, T. S., Oppedal, F., & Stien, L. H. (2022). Declining size- at- harvest in Norwegian salmon aquaculture: Lice, disease, and the role of stunboats. Aquaculture, 559, 738440.Black, A., & Kanat, I. (1985). A review of soft tissue calcifications. The Journal of Foot Surgery, 24(4), 243– 250.Culling, C. F. A., Allison, R., & Barr, W. (2014). Cellular pathology technique. Elsevier.Li, Y., Kortner, T. M., Chikwati, E. M., Munang'andu, H. M., Lock, E. J., & Krogdahl, Å. (2019). Gut health and vaccination response in pre- smolt Atlantic salmon (Salmo salar) fed black soldier fly (Hermetia illucens) larvae meal. Fish & Shellfish Immunology, 86, 1106– 1113.Mark, J. B. D., & Melnick, G. S. (1964). Diverticulosis of the gallblad-der: Clinical and radiographic features. Archives of Surgery, 88(3), 498– 500.Ross, W. D., Finby, N., & Evans, J. A. (1955). Intramural diverticulosis of the gallbladder. Radiology, 64(3), 366– 372.Sommerset, I., Jensen, B. B., Bornø, G., Haukaas, A., & Brun, E. (2020). In Norwegian "Fiskehelserapporten 2020". Veterinærinstituttet.F I G U R E  5  Pathological findings at harvest. The percentage of lesions is given as (n of lesions/n of samples analysed) separately for each tissue. The percentage of nodular gall bladders is given by (n observations/total number of fish sampled at harvest). 13652761, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jfd.13724 by Nofima, Wiley Online Library on [01/11/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License    |  5SVEEN et al.Sveen, L., Krasnov, A., Timmerhaus, G., & Bogevik, A. S. (2021). Responses to Mineral Supplementation and Salmon Lice (Lepeophtheirus sal-monis) Infestation in Skin Layers of Atlantic Salmon (Salmo salar L.). Genes, 12(4), 602.SUPPORTING INFORMATIONAdditional supporting information can be found online in the Supporting Information section at the end of this article.How to cite this article: Sveen, L. R., Chikwati, E., Dalum, A., Kortner, T. M., Ravndal, J., Einen, O., & Mørkøre, T. (2022). Lesions of the biliary system in Atlantic salmon (Salmo salar L.). Journal of Fish Diseases, 00, 1–5. https://doi.org/10.1111/jfd.13724 13652761, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jfd.13724 by Nofima, Wiley Online Library on [01/11/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License

Lesions of the biliary system in Atlantic salmon (Salmo salar L.)

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Gallbladders with mucosal outpouchings (diverticula) were found in a population of Atlantic salmon farmed in sea water. Soft tissue calcification affected the skin, skeletal muscle and gut, as identified by histological observations. In addition, inflammation of muscle and intestinal tissue and lymphocytic and fibrous reaction were present in the liver. The general fish population was characterized by poor growth and unspecified mortalities. Here we describe the observed lesions and discuss them in the light of the general health status of the population

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Lesions of the biliary system in Atlantic salmon (Salmo salar L.)

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