High prevalence of infections and pathological changes in burbot (Lota lota) from a polluted lake (Lake Mjøsa, Norway)

Chemosphere

Volumn 90, Issue 5, 2013, Pages 1711-1718

  Berg, Vidar ^a   Zerihun, Mulualem A ^b   Jørgensen, Anders ^b   Lie, Elisabeth ^a   Dale, Ole B ^b   Skaare, Janneche Utne ^b   Lyche, Jan L ^b  

^a NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^b NORWEGIAN VETERINARY INSTITUTE   (Norway)

Author keywords

DDTs; Fish; Mycobacteriosis; Pathology; PBDEs; PCBs

Indexed keywords

FISH; FISHERIES; FLAME RETARDANTS; LAKES; ORGANIC POLLUTANTS; PATHOLOGY; POLYCHLORINATED BIPHENYLS;

BROMINATED FLAME RETARDANTS; DDTS; INDUSTRIAL ACTIVITIES; MYCOBACTERIOSIS; PBDES; PERSISTENT ORGANIC POLLUTANTS; POLYBROMINATED DIPHENYL ETHER (PBDES); POLYCHLORINATED BIPHENYL (PCBS);

LAKE POLLUTION;

CHLORPHENOTANE; FLAME RETARDANT; LIPID; POLYBROMINATED DIPHENYL ETHER; POLYCHLORINATED BIPHENYL;

BACTERIAL DISEASE; DDT; DISEASE PREVALENCE; GADOID; HEALTH STATUS; HISTOPATHOLOGY; HUMAN ACTIVITY; INDUSTRIAL LOCATION; INFECTIVITY; LAKE POLLUTION; ORGANIC POLLUTANT; PARASITE; PATHOLOGY; PBDE; PCB; POLLUTION EXPOSURE; WILD POPULATION;

ARTICLE; BACTERIAL INFECTION; BORBOT; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; FISH; GRANULOMA; HISTOPATHOLOGY; INDUSTRIAL WASTE; LAKE; LIPID LIVER LEVEL; LOTA LOTA; MYCOBACTERIUM; MYCOBACTERIUM SALMONIPHILUM; NONHUMAN; NORWAY; PARASITOSIS; POLLUTANT; WATER POLLUTION;

LAKE LOSNA; LAKE MJOSA; NORWAY; OPPLAND;

BACTERIA (MICROORGANISMS); LOTA; LOTA LOTA; MYCOBACTERIUM;

EID: 84872276742     PISSN: 00456535     EISSN: 18791298     Source Type: Journal    
DOI: 10.1016/j.chemosphere.2012.10.017     Document Type: Article

References (71)

1. Anderson T.D., MacRae J.D. Polybrominated diphenyl ethers in fish and wastewater samples from an area of the Penobscot River in Central Maine. Chemosphere 2006, 62:1153-1160.
2. Arkoosh M.R., Clemons E., Huffman P., Kagley A.N. Increased susceptibility of juvenile chinook salmon to vibriosis after exposure to chlorinated and aromatic compounds found in contaminated urban estuaries. J. Aquat. Animal Health 2001, 13:257-268.
3. Arkoosh M.R., Boylen D., Dietrich J., Anulacion B.F., Ylitalo G., Bravo C.F., Lyndal L., Loge F.J., Collier T.K. Disease susceptibility of salmon exposed to polybrominated diphenyl ethers (PBDEs). Aquat. Toxicol. 2010, 98:51-59.
4. Au D.W.T. The application of histo-cytopathological biomarkers in marine pollution monitoring: a review. Mar. Pollut. Bull. 2004, 48:817-834.
5. Belas R., Faloon P., Hannaford A. Potential applications of molecular biology to the study of fish mycobacteriosis. Ann. Rev. Fish Dis. 1995, 5:133-173.
6. Berg V., Lyche J.L., Karlsson C., Stavik B., Nourizadeh-Lillabadi R., Hårdnes N., Skaare J.U., Alestrøm P., Lie E., Ropstad E. Accumulation and effects of natural mixtures of persistent organic pollutants (POP) in Zebrafish after two generations of exposure. J. Toxicol. Environ. Health A 2011, 74:405-423.
7. Birchmeier K.L., Smith K.A., Passino-Reader D.R., Sweet L.I., Chernyak S.M., Adams J.V., Omann G.M. Effects of selected polybrominated diphenyl ether flame retardants on lake trout (Salvelinus namaycush) thyomcyte viability, apoptosis, and necrosis. Environ. Toxicol. Chem. 2005, 24:1518-1522.
8. Bishop P.J., Neuman G. The history of the Ziehl-Neelsen stain. Tubercle 1970, 51:196-206.
9. Bruno D.W., Griffiths J., Mitchell G.C., Wood B.P., Fletcher Z.J., Drobniewski F.A., Hastings T.S. Pathology attributed to Mycobacterium chelonae infection among farmed and laboratory-infected Atlantic salmon Salmo salar. Dis. Aquat. Org. 1998, 33:101-109.
10. Costa P.M., Caeiro S., Lobo J., Martins M., Ferreira A.M., Cateno M., Vale C., DelValls T.á., Costa M.H. Estuarine ecological risk based on hepatic histopathological indices from laboratory and in situ tested fish. Mar. Pollut. Bull. 2011, 62:55-65.
11. Cuesta A., Meseguer J., Esteban M.á. Effects of the organochlorine p,p'-DDE and lindane on gilthead seabream leucocyte immune parameters and gene expression. Fish Shellfish Immunol. 2008, 25:682-688.
12. Darnerud P.O., Eriksen G.S., Jóhannesson T., Larsen P.B., Viluksela M. Polybrominated diphenyl ethers: occurrence, dietary exposure, and toxicology. Environ. Health Prespect. 2001, 109(Suppl. 1):49-68.
13. de Boer J., Dao Q.T., van Leeuwen P.J.S., Kotterman M.J.J., Schobben J.H.M. Thirty year monitoring of PCBs, organochlorine pesticides and tetrabromodiphenoldiphenylether in eel from The Netherlands. Environ. Pollut. 2010, 158:1228-1236.
14. de Wit C.A., Herzke D., Vorkamp K. Brominated flame retardants in the Arctic environment - trends and new candidates. Sci. Total Environ. 2010, 408:2885-2918.
15. Duffy J.E., Zelikoff T. The relationship between nonplanar PCB-induced immunotoxicity and hepatic CYP1A induction in a fish model. J. Immunotoxicol. 2006, 3:39-47.
16. Duffy-Whritenour J.E., Kurzman R.Z., Kennedy S., Zelikoff J.T. Non-coplanarpolychlorinated biphenyl (PCB)-induced immunotoxicity is coincident with alterations in the serotonergic system. J. Immunotoxicol. 2010, 7:318-326.
17. Eljarrat E., de la Cal A., Raldua D., Duran C., Barcelo D. Occurrence and bioavailability of polybrominated diphenyl ethers and hexabromocyclododecane in sediment and fish from the Cinca River, a tributary of the Ebro River (Spain). Environ. Sci. Technol. 2004, 38:2603-2608.
18. Ekman E., Åkerman G., Balk L., Norrgren L. Impact of PCB on resistance to Flavobacterium psychrophilum after experimental infection of rainbow trout Onchorhynchus mykiss eggs by nanoinjection. Dis. Aquat. Organ. 2004, 60:31-39.
19. Fjeld, E., Schlabach, M., Rognerud, S., Källberg, G., 2004. Miljøgifter i sedimenter og fisk i Mjøsa, Drammensvassdraget og Drammensfjorden. KLIF/SFT report TA 2051 ISBN82-577-4583-9. Klif.no. (Norwegian).
20. Fjeld, E., Rognerud, S., 2009. Miljøgifter i Ferskvannsfisk, 2008. Kvikksølv i abbor og organiske miljøgifter i ørret. Klif Report TA-2544. 978-82-577-5586-7. Klif.no. (Norwegian).
21. Fonnum F., Mariussen E. Mechanisms involved in the neurotoxic effects of environmental toxicants such as polychlorinated biphenyls and brominated flame retardants. J. Neurochem. 2009, 111:1327-1347.
22. Förlin L., Norrgren L. Physiological and morphological studies of feral perch before and after remediation of a PCB contaminated lake: Järnsjön. Ambio 1998, 27:418-424.
23. Geeraerts C., Focant J.-F., Eppe G., Pauw E.D., Belpaire C. Reproduction of European eel jeopardized by high levels of dioxins and dioxin-like PCBs?. Sci. Total. Environ. 2011, 409:4039-4047.
24. Gregoraszczuk E., Milczarek K., Wójtowicz A.K., Berg V., Skaare J.U., Ropstad E. Steroid secretion following exposure of ovarian follicular cells to three different natural mixtures of persistent organic pollutants (POPs). Reprod. Toxicol. 2008, 25:58-66.
25. Hale R.C., La Guardia M.J., Harvey E.P., Mainor T.M., Duff W.H., Gaylor M.O. Polybrominated diphenyl ether flame retardants in Virginia freshwater fishes (USA). Environ. Sci. Technol. 2001, 35:4585-4591.
26. Hartmann P.C., Burkhardt-Holm P., Giger W. Occurrence of polybrominated diphenyl ethers (PBDEs) in brown trout bile and liver from Swiss rivers. Environ. Pollut. 2007, 146:107-113.
27. Isosaari P., Hallikainen A., Kiviranta H., Vuorinen P.J., Parmanne R., Koistinen J., Vartiainen T. Polychlorinated dibenzo-p-dioxins, dibenzofurans, biphenyls, napthalenes and polybrominated diphenyl ethers in the edible fish caught from the Baltic Sea and lakes in Finland. Environ. Pollut. 2006, 141:213-225.
28. Iwanowicz L.R., Lerner D.T., Blazer V.S., McCormick S.D. Aqueous exposure to Aroclor 1254 modulates the mitogenic response of Atlantic salmon anterior kidney T-cells: Indications of short- and long-term immunomodulation. Aquat. Toxicol. 2005, 72:305-314.
29. Iwanowicz L.R., Blazer V.S., McCormick S.D., VanVeld P.A. Arochlor 1248 exposure leads to immunomodulation, decreased disease resistance and endocrine disruption in brown bullhead, Ameiurus nebulosus. Aquat. Toxicol. 2009, 93:70-82.
30. Jørgensen E.H., Vijayan M.M., Killie J.-E., Aluru N., Aas-Hansen Ø., Maule A. Toxicokinetics and effects of PCBs in Arctic fish: A review of studies on Arctic charr. J. Toxicol. Environ. Health A 2006, 69:37-52.
31. Koehler A. The gender-specific risk to liver toxicity and cancer of flounder (Platichthys flesus (L.)) at the German Wadden Sea coast. Aquat. Toxicol. 2004, 70:257-276.
32. Köhler A., Wahl E., Söffker K. Functional and morphological changes of lysosomes as prognostic biomarker of toxic injury in a marine flatfish Platichthus flesus (L.). Environ. Toxicol. Chem. 2002, 21:2434-2444.
33. Koponen K., Myers M.S., Ritola O., Huuskonen S.E., Lindström-Seppä P. Histopathology of feral fish from a PCB-contaminated freshwater lake. Ambio 2001, 30:122-126.
34. Kraugerud M., Doughty R.W., Lyche J.L., Berg V., Tremoen N.H., Alestrøm P., Alexandersen M., Ropstad E. Natural mixtures of persistent organic pollutants (POPs) suppress ovarian follicle development, liver vitellogenin immunostaining and hepatocyte proliferation in female zebrafish (Danio rerio). Aquat. Toxicol. 2012, 116-117:16-23.
35. Law R.J., Allchin C.R., de Boer J., Covaci A., Herzke D., Leåpom P., Morris S., Tronczynski J., de Wit C.A. Levels and trends of brominated flame retardants in the European environment. Chemosphere 2006, 64:187-208.
36. Letcher R.J., Bustnes J.O., Dietz R., Jenssen B.M., Jørgensen E.H., Sonne C., Verreault J., Vijayan M.M., Gabrielsen G.W. Exposure and effects assessments of persistent organohalogen contaminants in arctic wildlife and fish. Sci. Total Environ. 2010, 408:2995-3040.
37. Linderoth M., Hansson T., Liewenborg B., Sundberg H., Noaksson E., Hansson M., Zebühr Y., Balk L. Basic physiological biomarkers in adult female perch (Perca fluviatilis) in a cronic polluted gradient in the Stockholm recipient (Sweden). Mar. Pollut. Bull. 2006, 53:437-450.
38. Lukin A., Sharova J., Belicheva L., Camus L. Assessment of fish health status in the Pechora river: effects of contamination. Ecotoxicol. Environ. Saf. 2011, 74:355-365.
39. Luna L.G. Manual of Histologic Staining Methods of the Armed Forces Institute of Pathology 1968, McGraw-Hill, New York.
40. Luo Q., Cai Z.W., Wong M.H. Polybrominated diphenyl ethers in fish and sediment from river polluted by electronic waste. Sci. Total Environ. 2007, 383:115-127.
41. Lyche J., Larsen H., Skaare J.U., Tverdal A., Dahl E., Johansen G., Ropstad E. Effects of perinatal exposure to low doses of PCB 153 and PCB 126 on lymphocyte proliferation and hematology in goat kids. J. Toxicol. Environ. Health A 2004, 67:889-904.
42. Lyche J.L., Oskam I.C., Skaare J.U., Reksen O., Sweeney T., Dahl E., Farstad W., Ropstad E. Effects of gestational and lactational exposure to low doses of PCBs 126 and 153 on anterior pituitary and gonadal hormones and on puberty in female goats. Reprod. Toxicol. 2004, 19:87-95.
43. Lyche J.L., Larsen H.J., Skaare J.U., Tverdal A., Johansen G.M., Ropstad E. Perinatal exposure to low doses of PCB 153 and PCB 126 affects maternal and neonatal immunity in goat kids. J. Toxicol. Environ. Health A 2006, 69:139-158.
44. Lyche J.L., Nourizadeh-Lillabadi R., Almaas C., Stavik B., Berg V., Skåre J.U., Alestrøm P., Ropstad E. Natural mixtures of persistent organic pollutants (POP) increase weight gain, advance puberty, and induce changes in gene expression associated with steroid hormones and obesity in female zebrafish. J. Toxicol. Environ. Health A 2010, 73:1032-1057.
45. Lyche J.L., Nourizadeh-Lillabadi R., Karlsson C., Stavik B., Berg V., Skåre J.U., Alestrøm P., Ropstad E. Natural mixtures of POPs affected body weight gain and induced transcription of genes involved in weight regulation and insulin signalling. Aquat. Toxicol. 2011, 102:197-204.
46. Mariussen E., Fjeld E., Breivik K., Steinnes E., Borgen A., Kjellberg G., Schlabach M. Elevated levels of polybrominated diphenyl ethers (PBDEs) in fish from Lake Mjøsa, Norway. Sci. Total Environ. 2008, 390:132-141.
47. Misumi I., Vella A.T., Leong J.-A.C., Nakanishi T., Schreck C.B. P,p-DDE depresses the immune competence of Chinook salmon (Oncorhynchus tshawytscha) leukocytes. Fish Shellfish Immunol. 2005, 19:97-114.
48. Mulder P.J., Lie E., Eggen G.S., Ciesielski T.M., Berg T., Skaare J.U., Jenssen B.M., Sørmo E.G. Mercury in molar excess of selenium interferes with thyroid hormone function in free-ranging freshwater fish. Environ. Sci. Technol 2012, 46:9027-9037.
49. Murvoll K.M., Skaare J.U., Moe B., Anderssen E., Jenssen B.M. Spatial trends and associated biological responses of organochlorines and brominated flame retardants in hatchlings of North-Atlantic kittiwakes (Rissa tridactyla). Environ. Toxicol. Chem. 2006, 25:1648-1656.
50. Newbold R.R., Padilla-Banks E., Jefferson W.N., Heindel J.J. Effects of endocrine disruptors on obesity. Int. J. Androl. 2008, 31:201-208.
51. Noga E.J. Skin ulcers in fish: Pfiesteria and other etiologies. Environ. Pathol. 2000, 28:807-823.
52. Nourizadeh-Lillabadi R., Lyche J.L., Almaas C., Stavik B., Moe S.J., Alexandersen M., Berg V., Jakobsen K.S., Stenseth N.C., Skaare J.U., Alestrøm P., Ropstad E. Transcriptional regulation in liver and testis associated with developmental and reproductive effects in male zebrafish exposed to natural mixtures of persistent organic pollutants (POP). J. Toxicol. Environ. Health A 2009, 72:112-130.
53. Prophet E.B., Mills B., Arrington J.B., Sobin L.H. Laboratory methods in histotechnology 1994, Armed Forces Institute of Pathology, American Registry of Pathology, Washington, DC.
54. Pulliainen E., Korhonen K., Kankaanranta L., Mäki K. Non spawning burbot on the northern coast of the Bothnian Bay. Ambio 1992, 21:170-175.
55. Raldúa D., Francesc Padrós F., Montserrat Solé M., Eljarrat E., Barceló D., Riva M.C., Barata C. First evidence of polybrominated diphenyl ether (flame retardants) effects in feral barbel from the Ebro River basin (NE, Spain). Chemosphere 2008, 73:56-64.
56. Randak T., Zlabek V., Pulkrabova J., Kolarova J., Kroupova H., Siroka Z., Velisek J., Svobodova Z., Hajslova J. Effects of pollution on chub in the River Elbe, Czech Republic. Ecotoxicol. Environ. Saf. 2009, 72:737-746.
57. Ricker W.E. Computation and interpretation of biological statistics of fish populations. Bull. Fish. Res. Board Can. 1975, 191:1-382.
58. Ross A.J. Mycobacterium salmoniphilum sp. nov. from salmonid fishes. Am. Rev. Respir. Dis. 1960, 81:241-250.
59. Ryan M.J., Stern G.A., Diamond M., Croft M.V., Roach P., Kidd K. Temporal trends of organochlorine contaminants in burbot and lake trout from three selected Yukon lakes. Sci. Total Environ. 2005, 351-352:501-522.
60. Sellström U., Jansson B., Kierkegaard A., de Wit C., Odsjö T., Olsson M. Polybrominated diphenyl ethers (PBDE) in biological samples from the Swedish environment. Chemosphere 1993, 26:1703-1718.
61. Sørmo E.G., Jenssen B.M., Lie E., Skaare J.U. Brominated flame retardants in aquatic organisms from the North Sea in comparison with biota from the high Arctic marine environment. Environ. Toxicol. Chem. 2009, 28:2082-2090.
62. Stapanian M.A., Paragamian V.L., Madenjian C.P., Jackson J.R., Lappalainen J., Evenson M.J., Neufeld M.D. Worldwide status of burbot and conservation measures. Fish Fish 2010, 11:34-56.
63. Sures B., Knopf K. Individual and combined effects of cadmium and 3,3',4,4',5-pentachlorobiphenyl (PCB 126) on the humoral immune response in European eel (Anguilla Anguilla) experimentally infected with larvae of Anguillicola crassus (Nematoda). Parasitology 2004, 128:445-454.
64. Szlinder-Richert J., Barska I., Usydus Z., Grabic R. Polybrominated diphenyl ethers (PBDEs) in selected fish species from the southern Baltic Sea. Chemosphere 2010, 78:695-700.
65. Thomsen C., Knutsen H.K., Liane V.H., Frøshaug M., Kvalem H.E., Haugen M., Meltzer H.M., Alexander J., Becher G. Consumption of fish from a contaminated lake strongly affects the concentrations of polychlorinated diphenyl ethers and hexabromocyclododecane in serum. Mol. Nutr. Food Res. 2008, 52:228-237.
66. Turyk M., Anderson H., Knobeloch L., Imm P., Persky V. Organochlorine exposure and incidence of diabetes in a cohort of Great Lakes sport fish consumers. Environ. Health Perspect. 2009, 117:1076-1082.
67. Xiaofei Q., Xijuan X., Yan L., Yaxian Z., Zhongzhi Y., Shan F., Mi T., Xingru Z., Zhanfen Q., Xiaobai X., Yongjian Y. Ecotoxicological effects of mixed pollutants resulted from e-wastes recycling and bioaccumulation of polybrominated diphenyl ethers in Chinese loach (Misgurnus anguillicaudatus). J. Environ. Sci. 2009, 21:1695-1701.
68. Zerihun M.A., Nilsen H., Hodneland S., Colquhoun D.J. Mycobacterium salmoniphilum infection in farmed Atlantic salmon Salmo salar. J. Fish Dis. 2011, 34:769-781.
69. Zerihun M.A., Berg V., Lyche J.L., Dunchan J.C., Poppe T.T. Mycobacterium salmoniphilum infection in burbot Lota lota. Dis. Aquat. Org. 2011, 95:57-64.
70. Zimmer K.E., Montaño M., Olsaker I., Dahl E., Berg V., Karlsson C., Murk A.J., Skaare J.U., Ropstad E., Verhagen S. In vitro steroidogenic effects of mixtures of persistent organic pollutants (POPs) extracted from burbot (Lota lota) caught in two Norwegian lakes. Sci. Total Environ. 2011, 409:2040-2048.
71. Zhulidov A.V., Robarts R.D., Headley J.V., Liber K., Zhulidov D.A., Zhulidova O.V., Pavlov D.F. Levels of DDT and hexachlorocyclohexane in burbot (Lota lota L.) from Russian Arctic rivers. Sci. Total Environ. 2002, 292:231-246.