{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,19]],"date-time":"2026-08-19T17:37:01Z","timestamp":1787161021427,"version":"build-2736575974"},"reference-count":47,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2019,10,6]],"date-time":"2019-10-06T00:00:00Z","timestamp":1570320000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Landesfischereiverband Bayern e.V.","award":["-"],"award-info":[{"award-number":["-"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>For many years, brown trout (Salmo trutta fario) mortalities within the pre-alpine Isar River in Germany were reported by the Bavarian Fisheries Association (Landesfischereiverband Bayern e.V.) and local recreational anglers during August and September. Moribund fish seemed to be affected by proliferative darkening syndrome (PDS). In addition, proliferative kidney disease (PKD) caused by Tetracapsuloides bryosalmonae was discussed. To investigate this phenomenon, the present field study monitored brown trout mortalities by daily river inspection in 2017 and 2018. Moribund brown trout (n = 31) were collected and examined using histology, immunohistochemistry, qPCR, and quantitative stereology. Our investigations identified 29 (93.5%) brown trout affected by PKD. Four brown trout (12.9%) displayed combined hepatic and splenic lesions fitting the pathology of PDS. The piscine orthoreovirus 3, suspected as causative agent of PDS, was not detectable in any of the samples. Quantitative stereological analysis of the kidneys revealed a significant increase of the renal tissue volumes with interstitial inflammation and hematopoietic hyperplasia in PKD-affected fish as compared to healthy brown trout. The identified T. bryosalmonae strain was classified as part of the North American clade by phylogenetical analysis. This study highlights PKD and PDS as contributing factors to recurrent autumnal brown trout mortalities.<\/jats:p>","DOI":"10.3390\/pathogens8040177","type":"journal-article","created":{"date-parts":[[2019,10,7]],"date-time":"2019-10-07T03:34:01Z","timestamp":1570419241000},"page":"177","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":17,"title":["Proliferative Kidney Disease and Proliferative Darkening Syndrome are Linked with Brown Trout (Salmo trutta fario) Mortalities in the Pre-Alpine Isar River"],"prefix":"10.3390","volume":"8","author":[{"given":"Daniela","family":"Arndt","sequence":"first","affiliation":[{"name":"Institute for Infectious Diseases and Zoonoses, LMU Munich, 80539 Munich, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1149-1613","authenticated-orcid":false,"given":"Robert","family":"Fux","sequence":"additional","affiliation":[{"name":"Institute for Infectious Diseases and Zoonoses, LMU Munich, 80539 Munich, Germany"},{"name":"German Center for Infection Research (DZIF), Partner Site Munich, 80539 Munich, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andreas","family":"Blutke","sequence":"additional","affiliation":[{"name":"Research Unit Analytical Pathology, Helmholtz Zentrum Munich, 85764 Neuherberg, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Julia","family":"Schwaiger","sequence":"additional","affiliation":[{"name":"Bavarian Environment Agency, Unit Aquatic Toxicology, 82407 Wielenbach, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mansour","family":"El-Matbouli","sequence":"additional","affiliation":[{"name":"Clinical Division of Fish Medicine, University of Veterinary Medicine, 1210 Vienna, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6143-082X","authenticated-orcid":false,"given":"Gerd","family":"Sutter","sequence":"additional","affiliation":[{"name":"Institute for Infectious Diseases and Zoonoses, LMU Munich, 80539 Munich, Germany"},{"name":"German Center for Infection Research (DZIF), Partner Site Munich, 80539 Munich, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7014-0277","authenticated-orcid":false,"given":"Martin C.","family":"Langenmayer","sequence":"additional","affiliation":[{"name":"Institute for Infectious Diseases and Zoonoses, LMU Munich, 80539 Munich, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2019,10,6]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"487","DOI":"10.1186\/s13071-016-1759-z","article-title":"An epidemiological model for proliferative kidney disease in salmonid populations","volume":"9","author":"Carraro","year":"2016","journal-title":"Parasit. Vectors"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1017\/S0031182017001482","article-title":"Temperature-related parasite infection dynamics: The case of proliferative kidney disease of brown trout","volume":"145","author":"Strepparava","year":"2018","journal-title":"Parasitology"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1007\/s11259-006-0019-7","article-title":"Climatic variations related to fish diseases and production","volume":"30","author":"Alborali","year":"2006","journal-title":"Vet. Res. Com."},{"key":"ref_4","unstructured":"Amlacher, E. (1981). Taschenbuch der Fischkrankheiten, Jena VEB Gustav Fischer Verlag."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1016\/0959-8030(93)90039-E","article-title":"Proliferative kidney disease of salmonid fish","volume":"3","author":"Hedrick","year":"1993","journal-title":"Annu. Rev. Fish Dis."},{"key":"ref_6","unstructured":"Schwaiger, J., Ferling, H., Dembek, G., Gerst, M., and Scholz, K. (2013). Ursachenermittlung nach dem Ausschlussverfahren-Versuchsans\u00e4tze an der Iller und anderen Gew\u00e4ssern. Bachforellensterben in Bayern-Auf den Spuren eines ungekl\u00e4rten Ph\u00e4nomens, 12 July 2013, M\u00fcnchen Landesfischereiverband, Bayern e.V."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"463","DOI":"10.1007\/s00027-009-0110-6","article-title":"Immune deficiency causes annual late summer brown trout (Salmo trutta) mortality in Austrian prealpine river systems","volume":"71","author":"Lahnsteiner","year":"2009","journal-title":"Aquat. Sci."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Kuehn, R., Stoeckle, B.C., Young, M., Popp, L., Taeubert, J.E., Pfaffl, M.W., and Geist, J. (2018). Identification of a piscine reovirus-related pathogen in proliferative darkening syndrome (PDS) infected brown trout (Salmo trutta fario) using a next-generation technology detection pipeline. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0206164"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Fux, R., Arndt, D., Langenmayer, M.C., Schwaiger, J., Ferling, H., Fischer, N., Indenbirken, D., Grundhoff, A., Dolken, L., and Adamek, M. (2019). Piscine Orthoreovirus 3 is not the causative pathogen of proliferative darkening syndrome (PDS) of brown trout (Salmo trutta fario). Viruses, 11.","DOI":"10.3390\/v11020112"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"117","DOI":"10.3354\/dao02993","article-title":"First proliferative kidney disease outbreak in Austria, linking to the aetiology of black trout syndrome threatening autochthonous trout populations","volume":"119","author":"Gorgolione","year":"2016","journal-title":"Dis. Aquat. Organ."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1111\/j.1365-2761.1984.tb01201.x","article-title":"Proliferative kidney disease of salmonid fish: A review","volume":"7","author":"Bucke","year":"1984","journal-title":"J. Fish Dis."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1111\/j.1365-2761.1979.tb00161.x","article-title":"Epidemiological aspects of proliferative kidney disease amongst rainbow trout Salmo gairdneri Richardson in Northern Ireland","volume":"2","author":"Ferguson","year":"1979","journal-title":"J. Fish Dis."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"S95","DOI":"10.1017\/S0031182003003767","article-title":"The expression of immune-regulatory genes in rainbow trout, Oncorhynchus mykiss, during a natural outbreak of proliferative kidney disease (PKD)","volume":"126","author":"Holland","year":"2003","journal-title":"Parasitology"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1111\/j.1365-2761.1984.tb00939.x","article-title":"Haematological studies in proliferative kidney disease of rainbow trout, Salmo gairdneri Richardson","volume":"7","author":"Hoffmann","year":"1984","journal-title":"J. Fish Dis."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1111\/j.1365-2761.1987.tb01081.x","article-title":"A study of the sequential clinical and pathological changes during proliferative kidney disease in rainbow trout, Salmo gairdneri Richardson","volume":"10","author":"Bucke","year":"1987","journal-title":"J. Fish Dis."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"221","DOI":"10.3354\/dao057221","article-title":"Infection of bryozoans by Tetracapsuloides bryosalmonae at sites endemic for salmonid proliferative kidney disease","volume":"57","author":"Tops","year":"2003","journal-title":"Dis. Aquat. Organ."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"61","DOI":"10.3354\/dao045061","article-title":"Induction of proliferative kidney disease (PKD) in rainbow trout Oncorhynchus mykiss via the bryozoan Fredericella sultana infected with Tetracapsula bryosalmonae","volume":"45","author":"Feist","year":"2001","journal-title":"Dis. Aquat. Organ."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"133","DOI":"10.3354\/dao01894","article-title":"Transmission of Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea) to Fredericella sultana (Bryozoa: Phylactolaemata) by various fish species","volume":"79","author":"Grabner","year":"2008","journal-title":"Dis. Aquat. Organ."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1046\/j.1365-2761.2000.00227.x","article-title":"Immunohistochemical and PCR studies of wild fish for Tetracapsula bryosalmonae (PKX), the causative organism of proliferative kidney disease","volume":"23","author":"Morris","year":"2000","journal-title":"J. Fish Dis."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1111\/j.1365-2761.1987.tb01094.x","article-title":"Further consideration of the haematology of proliferative kidney disease (PKD) in rainbow trout, Salmo gairdneri Richardson","volume":"10","author":"Bucke","year":"1987","journal-title":"J. Fish Dis."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"254","DOI":"10.1111\/j.1550-7408.1985.tb03047.x","article-title":"PKX, the causative agent of proliferative kidney disease (PKD) in pacific salmonid fishes and its affinities with the Myxozoa","volume":"32","author":"Kent","year":"1985","journal-title":"J. Protozool."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1007\/s00436-003-0986-3","article-title":"Malacosporean-like spores in urine of rainbow trout react with antibody and DNA probes to Tetracapsuloides bryosalmonae","volume":"92","author":"Hedrick","year":"2004","journal-title":"Parasitol. Res."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"151","DOI":"10.3354\/dao03200","article-title":"Tetracapsuloides bryosalmonae persists in brown trout Salmo trutta for five years post exposure","volume":"127","author":"Soliman","year":"2018","journal-title":"Dis. Aquat. Organ."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"23","DOI":"10.3354\/dao02580","article-title":"Complex interaction between proliferative kidney disease, water temperature and concurrent nematode infection in brown trout","volume":"104","author":"Steiner","year":"2013","journal-title":"Dis. Aquat. Organ."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1186\/1297-9716-44-55","article-title":"Immune gene expression profiling of proliferative kidney disease in rainbow trout Oncorhynchus mykiss reveals a dominance of anti-inflammatory, antibody and T helper cell-like activities","volume":"44","author":"Gorgoglione","year":"2013","journal-title":"Vet. Res."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"207","DOI":"10.3354\/dao02417","article-title":"Kidney pathology and parasite intensity in rainbow trout Oncorhynchus mykiss surviving proliferative kidney disease: Time course and influence of temperature","volume":"97","author":"Bettge","year":"2012","journal-title":"Dis. Aquat. Organ."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"67","DOI":"10.3354\/dao01989","article-title":"Proliferative kidney disease in rainbow trout: Time- and temperature-related renal pathology and parasite distribution","volume":"83","author":"Bettge","year":"2009","journal-title":"Dis. Aquat. Organ."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1016\/j.vetpar.2005.07.022","article-title":"Development of Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea) in bryozoan hosts (as examined by light microscopy) and quantitation of infective dose to rainbow trout (Oncorhynchus mykiss)","volume":"135","author":"Morris","year":"2006","journal-title":"Vet. Parasitol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1729","DOI":"10.1098\/rspb.2004.2677","article-title":"The phylogeography of salmonid proliferative kidney disease in Europe and North America","volume":"271","author":"Henderson","year":"2004","journal-title":"Proc. Biol. Sci."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"392","DOI":"10.1002\/biuz.201410552","article-title":"Fremde Fische in Fl\u00fcssen und Seen","volume":"44","author":"Holm","year":"2014","journal-title":"Biol. Unserer Zeit"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1111\/j.1865-1682.2010.01150.x","article-title":"Assessing the impact of climate change on disease emergence in freshwater fish in the United Kingdom","volume":"57","author":"Gale","year":"2010","journal-title":"Transbound. Emerg. Dis."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"2184","DOI":"10.1111\/j.1095-8649.2008.02054.x","article-title":"Role of altitude and water temperature as regulating factors for the geographical distribution of Tetracapsuloides bryosalmonae infected fishes in Switzerland","volume":"73","author":"Wahli","year":"2008","journal-title":"J. Fish Biol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"193","DOI":"10.3354\/dao03102","article-title":"Comparative study of proliferative kidney disease in grayling Thymallus thymallus and brown trout Salmo trutta fario: An exposure experiment","volume":"123","author":"Ros","year":"2017","journal-title":"Dis. Aquat. Organ."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Lewisch, E., Unfer, G., Pinter, K., Bechter, T., and El-Matbouli, M. (2018). Distribution and prevalence of T. bryosalmonae in Austria: A first survey of trout from rivers with a shrinking population. J. Fish Dis.","DOI":"10.1111\/jfd.12863"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"139","DOI":"10.3354\/dao02855","article-title":"Proliferative kidney disease in brown trout: Infection level, pathology and mortality under field conditions","volume":"114","author":"Hirschi","year":"2015","journal-title":"Dis. Aquat. Organ."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"139","DOI":"10.3354\/dao02731","article-title":"Proliferative kidney disease (PKD) agent Tetracapsuloides bryosalmonae in brown trout populations in Estonia","volume":"109","author":"Dash","year":"2014","journal-title":"Dis. Aquat. Organ."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/j.aanat.2013.04.011","article-title":"Design-based stereology: Planning, volumetry and sampling are crucial steps for a successful study","volume":"196","author":"Tschanz","year":"2014","journal-title":"Ann. Anat."},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Howard, C.V., and Reed, M. (2005). Unbiased Stereology, QTP Publications. [2nd ed.].","DOI":"10.4324\/9780203006399"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"499","DOI":"10.1046\/j.1365-2761.2003.00485.x","article-title":"Melano-macrophage centres and their role in fish pathology","volume":"26","author":"Agius","year":"2003","journal-title":"J. Fish Dis."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"827","DOI":"10.3389\/fimmu.2017.00827","article-title":"Melanomacrophage centers as a histological indicator of immune function in fish and other poikilotherms","volume":"8","author":"Steinel","year":"2017","journal-title":"Front. Immunol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"41","DOI":"10.3354\/dao02768","article-title":"Persistence of Tetracapsuloides bryosalmonae (Myxozoa) in chronically infected brown trout Salmo trutta","volume":"111","author":"Kumar","year":"2014","journal-title":"Dis. Aquat. Organ."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"292","DOI":"10.1016\/j.yhbeh.2009.06.006","article-title":"Melanin-based skin spots reflect stress responsiveness in salmonid fish","volume":"56","author":"Kittilsen","year":"2009","journal-title":"Horm. Behav."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"7036","DOI":"10.1021\/jf100723b","article-title":"Seasonal variations in skin pigmentation and flesh quality of Atlantic Salmon (Salmo salar L.): Implications for quality management","volume":"58","author":"Leclercq","year":"2010","journal-title":"J. Agric. Food Chem."},{"key":"ref_44","unstructured":"(2019, April 08). Bavarian Agency of Environment. Available online: https:\/\/www.lfu.bayern.de\/analytik_stoffe\/fischsterben\/festgestellte_ursachen\/index.htm."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"200","DOI":"10.1016\/j.vetpar.2009.07.028","article-title":"Comparison of the susceptibility of brown trout (Salmo trutta) and four rainbow trout (Oncorhynchus mykiss) strains to the myxozoan Tetracapsuloides bryosalmonae, the causative agent of proliferative kidney disease (PKD)","volume":"165","author":"Grabner","year":"2009","journal-title":"Vet. Parasitol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1577\/1548-8667(1998)010<0012:RDSAOI>2.0.CO;2","article-title":"Ribosomal DNA sequence analysis of isolates of the PKX Myxosporean and their relationship to members of the genus Sphaerospora","volume":"10","author":"Kent","year":"1998","journal-title":"J. Aquat. Anim. Health"},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Blutke, A., and Wanke, R. (2018). Sampling strategies and processing of Biobank tissue samples from porcine biomedical models. J. Vis. Exp.","DOI":"10.3791\/57276-v"}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/8\/4\/177\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T13:27:57Z","timestamp":1760189277000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/8\/4\/177"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,10,6]]},"references-count":47,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2019,12]]}},"alternative-id":["pathogens8040177"],"URL":"https:\/\/doi.org\/10.3390\/pathogens8040177","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,10,6]]}}}