Fish Physiology and Biochemistry

, Volume 39, Issue 2, pp 143–158 | Cite as

Multi-organ histological observations on juvenile Senegalese soles exposed to low concentrations of waterborne cadmium

  • P. M. Costa
  • S. Caeiro
  • M. H. Costa


A histopathological screening was performed on juvenile Senegalese soles exposed to environmentally realistic concentrations of waterborne Cd (0.5, 5 and 10 μg L−1) for 28 days. The severity and dissemination of histopathological changes were variable and limited to the kidney, liver, spleen, gills and skin goblet cells. Contradicting available literature that refers the liver as the most affected organ upon acute exposure and the kidney following chronic exposure, the liver was the most impacted organ (even at the lowest concentration), in a trend that could relate to the duration of exposure and Cd concentration. The most noticeable hepatic alterations related to inflammation, although hepatocellular alterations like lipidosis and eosinophilic foci also occurred. The trunk kidney of exposed fish endured moderate inflammation, apoptosis and necrosis, however, without a clear time-dependent effect. The spleen of fish subjected to the highest concentrations revealed diffuse necrotic foci accompanied by melanomacrophage intrusion. The gills, albeit the most important apical uptake organ of dissolved toxicants, sustained only moderate damage, from epithelial hyperplasia and pavement cell detachment to the potentially more severe chloride cell alterations. In the skin, an increase in goblet cell size occurred, most notoriously correlated to Cd concentration at earlier stages of exposure. The results show that a metal-naïve juvenile fish can endure deleterious effects when exposed to low, ecologically relevant, concentrations of a common toxic metal and that the pattern of Cd-induced histopathological alterations can be complex and linked to organ-specific responses and metal translocation within the organism.


Histopathology Metal Solea senegalensis Sub-lethal exposure Bioassays 



P.M. Costa is supported by the Portuguese Science and Technology Foundation (FCT) through the grant SFRH/BPD/72564/2010. The present research is financed by FCT and co-financed by the European Community FEDER through the program COMPETE (project reference PTDC/SAU-ESA/100107/2008). The authors also acknowledge P. Pousão and his team (IPIMAR–INRB) for supplying the animals tested during the present work.


  1. Agius C, Roberts RJ (2003) Melano-macrophage centres and their role in fish pathology. J Fish Dis 26:499–509PubMedCrossRefGoogle Scholar
  2. Alvarado NE, Quesada I, Hylland K, Marigómez I, Soto M (2006) Quantitative changes in metallothionein expression in target cell-types in the gills of turbot (Scophthalmus maximus) exposed to Cd, Cu, Zn and after a depuration treatment. Aquat Toxicol 77:64–77PubMedCrossRefGoogle Scholar
  3. Arellano JM, Storch V, Sarasquete C (1999) Histological changes and copper accumulation in liver and gills of the Senegalese sole, Solea senegalensis. Ecotoxicol Environ Safe 44:62–72CrossRefGoogle Scholar
  4. Au DWT (2004) The application of histo-cytopathological biomarkers in marine pollution monitoring: a review. Mar Pollut Bull 48:817–834PubMedCrossRefGoogle Scholar
  5. Berntssen MHG, Aspholm OØ, Hylland K, Bonga SEW, Lundebye A-K (2001) Tissue metallothionein, apoptosis and cell proliferation responses in Atlantic salmon (Salmo salar L.) parr fed elevated dietary cadmium. Comp Biochem Physiol C 128:299–310CrossRefGoogle Scholar
  6. Brumbaugh WG, Schmitt CJ, May TW (2005) Concentrations of cadmium, lead, and zinc in fish from mining-influenced waters of Northeastern Oklahoma: sampling of blood, carcass, and liver for aquatic biomonitoring. Arch Environ Contam Toxicol 49:76–88CrossRefGoogle Scholar
  7. Cabral HN (2000) Comparative feeding ecology of sympatric Solea solea and S. senegalensis, within the nursery areas of the Tagus estuary, Portugal. J Fish Biol 57:1550–1562CrossRefGoogle Scholar
  8. Cerdá J, Douglas S, Reith M (2010) Genomic resources for flatfish research and their applications. J Fish Biol 77:1045–1070PubMedCrossRefGoogle Scholar
  9. Costa PM, Costa MH (2008) Biochemical and histopathological endpoints of in vivo cadmium toxicity in Sparus aurata. Cienc Mar 34:349–361Google Scholar
  10. Costa PM, Diniz MS, Caeiro S, Lobo J, Martins M, Ferreira AM, Caetano M, Vale C, DelValls TÀ, Costa MH (2009) Histological biomarkers in liver and gills of juvenile Solea senegalensis exposed to contaminated estuarine sediments: a weighted indices approach. Aquat Toxicol 92:202–212CrossRefGoogle Scholar
  11. Costa PM, Caeiro S, Diniz MS, Lobo J, Martins M, Ferreira AM, Caetano M, Vale C, DelValls TÀ, Costa MH (2010) A description of chloride cell and kidney tubule alterations in the flatfish Solea senegalensis exposed to moderately contaminated sediments from the Sado estuary (Portugal). J Sea Res 64:465–472CrossRefGoogle Scholar
  12. Costa PM, Caeiro S, Lobo J, Martins M, Ferreira AM, Caetano M, Vale C, DelValls TÀ, Costa MH (2011) Estuarine ecological risk based on hepatic histopathological indices from laboratory and in situ tested fish. Mar Pollut Bull 62:55–65PubMedCrossRefGoogle Scholar
  13. Dayeh V, Lynn DH, Bols NC (2005) Cytotoxicity of metals common in mining effluent to rainbow trout cell lines and to the ciliated protozoan, Tetrahymena thermophila. Toxicol in Vitro 19:399–410PubMedCrossRefGoogle Scholar
  14. Dorian C, Gattone VH, Klaassen CD (1995) Discrepancy between the nephrotoxic potencies of cadmium–metallothionein and cadmium chloride and the renal concentration of cadmium in the proximal convoluted tubules. Toxicol Appl Pharmacol 130:161–168PubMedCrossRefGoogle Scholar
  15. Eggleton J, Thomas KV (2004) A review of factors affecting the release and bioavailability of contaminants during sediment disturbance events. Environ Int 30:973–980PubMedCrossRefGoogle Scholar
  16. Escobar MC, Souza V, Bucio L, Hernández E, Gómez-Quiroz LE, Ruiz MCG (2009) MAPK activation is involved in Cadmium-induced Hsp70 expression in HepG2 cells. Toxicol Mech Meth 19:503–509CrossRefGoogle Scholar
  17. Falciani F, Diab AM, Sabine V, Williams TD, Ortega F, George SG, Chipman JK (2008) Hepatic transcriptomic profiles of European flounder (Platichthys flesus) from field sites and computational approaches to predict site from stress gene responses following exposure to model toxicants. Aquat Toxicol 90:92–101PubMedCrossRefGoogle Scholar
  18. Faucher K, Fichet D, Miramand P, Lagardére J-P (2008) Impact of chronic cadmium exposure at environmental dose on escape behaviour in sea bass (Dicentrarchus labrax L.; Teleostei, Moronidae). Environ Pollut 151:148–157PubMedCrossRefGoogle Scholar
  19. Giari L, Manera M, Simoni E, Dezfuli BS (2007) Cellular alterations in different organs of European sea bass Dicentrarchus labrax (L.) exposed to cadmium. Chemosphere 67:1171–1181PubMedCrossRefGoogle Scholar
  20. Groten JP, Sinkeldam EJ, Luten JB, van Bladeren PJ (1991) Cadmium accumulation and metallothionein concentrations after 4-week dietary exposure to cadmium chloride or cadmium-metallothionein in rats. Toxicol Appl Pharmacol 111:504–513PubMedCrossRefGoogle Scholar
  21. Häcker G (2000) The morphology of apoptosis. Cell Tissue Res 301:5–17PubMedCrossRefGoogle Scholar
  22. Hamada T, Tanimoto A, Sasaguri Y (1997) Apoptosis induced by cadmium. Apoptosis 2:359–367PubMedCrossRefGoogle Scholar
  23. Handy RD (1992) The assessment of episodic metal pollution. I. Uses and limitations of tissue contaminant analysis in rainbow trout (Oncorhynchus mykiss) after short waterborne exposure to cadmium or copper. Arch Environ Contam Toxicol 22:74–81PubMedCrossRefGoogle Scholar
  24. Hawkes JW (1974) The Structure of fish skin. I. General characterization. Cell Tissue Res 149:147–158PubMedCrossRefGoogle Scholar
  25. Horiguchi H, Oguma E, Kayama F (2011) Cadmium induces anemia through interdependent progress of hemolysis, body iron accumulation, and insufficient erythropoietin production in rats. Toxicol Sci 122:198–210PubMedCrossRefGoogle Scholar
  26. Iger Y, Lock RAC, van der Meij JCA, Bonga SEW (1994) Effects of water-borne cadmium on the skin of the common carp (Cyprinus carpio). Arch Environ Contam Toxicol 26:342–350PubMedCrossRefGoogle Scholar
  27. Isani G, Andreani G, Cocchioni F, Fedeli D, Carpené E, Falcioni G (2009) Cadmium accumulation and biochemical responses in Sparus aurata following sub-lethal Cd exposure. Ecotoxicol Environ Safe 72:224–230CrossRefGoogle Scholar
  28. Johansson-Sjöbeck ML, Larsson A (1978) The effect of cadmium on the hematology and on the activity of δ-aminolevulinic acid dehydratase (ALA-D) in blood and hematopoietic tissues of the flounder, Pleuronectes flesus L. Environ Res 17:191–204PubMedCrossRefGoogle Scholar
  29. Kalman J, Riba I, DelValls TÀ, Blasco J (2010) Comparative toxicity of cadmium in the commercial fish species Sparus aurata and Solea senegalensis. Ecotoxicol Environ Safe 73:306–311CrossRefGoogle Scholar
  30. Karnaky KJ, Ernst SA, Philpott CW (1976a) Teleost chloride Cell I. Response of pupfish Cyprinodon variegatus gill Na, K-ATPase and chloride cell fine structure to various high salinity environments. J Cell Biol 70:144–156PubMedCrossRefGoogle Scholar
  31. Karnaky KJ, Kinter LB, Kinter WB, Stirling CE (1976b) Teleost chloride cell II. Autoradiographic localization of gill Na, K-ATPase in killifish Fundulus heteroclitus adapted to low and high salinity environments. J Cell Biol 70:157–177PubMedCrossRefGoogle Scholar
  32. Kiernan JA (2008) Histological and histochemical methods. Theory and practice, 4th edn. Scion Publishing, BloxhamGoogle Scholar
  33. Lemaire-Gony S, Lemaire P, Pulsford AL (1995) Effects of cadmium and benzo(a)pyrene on the immune system, gill ATPase and EROD activity of European sea bass Dicentrarchus labrax. Aquat Toxicol 31:297–313CrossRefGoogle Scholar
  34. Li H, Zhang S (2001) In vitro cytotoxicity of the organophosphorus pesticide parathion to FG-9307 cells. Toxicol in Vitro 15:643–647PubMedCrossRefGoogle Scholar
  35. Lizardo-Daudt HM, Kennedy C (2008) Effects of cadmium chloride on the development of rainbow trout Oncorhynchus mykiss early life stages. J Fish Biol 73:702–718CrossRefGoogle Scholar
  36. Martoja R, Martoja M (1967) Initiation aux techniques de l’histologie animal. Masson, ParisGoogle Scholar
  37. Maunder RJ, Buckley J, Val AL, Sloman KA (2011) Accumulation of dietary and aqueous cadmium into the epidermal mucus of the discus fish Symphysodon sp. Aquat Toxicol 103:205–212PubMedCrossRefGoogle Scholar
  38. Mézin LC, Hale RC (2000) Effects of contaminated sediment on the epidermis of mummichog, Fundulus heteroclitus. Environ Toxicol Chem 19:2779–2787Google Scholar
  39. Muylle F, Robbens J, De Coen W, Timmermans J-P, Blust R (2006) Cadmium and zinc induction of ZnT-1 mRNA in an established carp cell line. Comp Biochem Physiol C 143:242–251Google Scholar
  40. Myers MS, Johnson LL, Hom T, Collier TK, Stein JE, Varanasi U (1998) Toxicopathic hepatic Lesions in subadult English Sole (Pleuronectes vetulus) from Puget Sound, Washington, USA: relationships with other biomarkers of contaminant exposure. Mar Environ Res 45:46–67CrossRefGoogle Scholar
  41. Nawrot TS, Staessen JA, Roels HA, Munters E, Cuypers A, Richart T, Ruttens A, Smeets K, Clijsters H, Vangronsveld J (2010) Cadmium exposure in the population: from health risks to strategies of prevention. Biometals 23:769–782PubMedCrossRefGoogle Scholar
  42. Nordberg GF (2009) Historical perspectives on cadmium toxicology. Toxicol Appl Pharmacol 238:192–200PubMedCrossRefGoogle Scholar
  43. Power M, Attrill MJ, Thomas RM (1999) Heavy metal concentration trends in the Thames estuary. Water Res 33:1672–1680CrossRefGoogle Scholar
  44. Soengas JL, Agra-Lago MJ, Carballo B, Andrés MD, Veira JAR (1996) Effect of an acute exposure to sublethal concentrations of cadmium on liver carbohydrate metabolism of Atlantic salmon (Salmo salar). Bull Environ Contam Toxicol 57:625–631PubMedCrossRefGoogle Scholar
  45. Thophon S, Kruatrachue M, Upatham ES, Pokethitiyook P, Sahaphong S, Jaritkhuan S (2003) Histopathological alterations of white seabass, Lates calcarifer, in acute and subchronic cadmium exposure. Environ Pollut 121:307–320PubMedCrossRefGoogle Scholar
  46. van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149PubMedCrossRefGoogle Scholar
  47. van Kerkhove E, Pennemans V, Swennen Q (2010) Cadmium and transport of ions and substances across cell membranes and epithelia. Biometals 23:823–855PubMedCrossRefGoogle Scholar
  48. Vethaak AD, Wester PW (1996) Diseases of flounder Platichthys flesus in Dutch coastal and estuarine waters, with particular reference to environmental stress factors. II. Liver histopathology. Dis Aquat Org 26:99–116CrossRefGoogle Scholar
  49. Vigliano FA, Bermúdez R, Nieto JM, Quiroga MI (2009) Development of rodlet cells in the gut of turbot (Psetta maxima L.): relationship between their morphology and S100 protein immunoreactivity. Fish Shellfish Immunol 26:146–153PubMedCrossRefGoogle Scholar
  50. Vogelbein WK, Fournie JW, van Held PA, Huggett RJ (1990) Hepatic neoplasms in the mummichog Fundulus heteroclitus from a creosote-contaminated site. Cancer Res 50:5978–5986PubMedGoogle Scholar
  51. Waeles M, Riso RD, Maguer J-F, Le Corre P (2004) Distribution and chemical speciation of dissolved cadmium and copper in the Loire estuary and North Biscay continental shelf, France. Est Coastal Shelf Sci 59:49–57CrossRefGoogle Scholar
  52. Wester PW, van der Ven TM, Vethaak AD, Grinwis GCM, Vos JG (2002) Aquatic toxicology: opportunities for enhancement through histopathology. Environ Toxicol Pharmacol 11:289–295PubMedCrossRefGoogle Scholar
  53. Yamamoto T, Kawai K, Oshima S (2011) Distribution of mucous cells on the body surface of Japanese flounder Paralichthys olivaceus. J Fish Biol 78:848–859PubMedCrossRefGoogle Scholar
  54. Zar JH (1998) Biostatistical analysis, 4th edn. Prentice Hall, Upper Saddle RiverGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  1. 1.IMAR–Instituto do Mar, Departamento de Ciências e Engenharia do AmbienteFaculdade de Ciências e Tecnologia da Universidade Nova de LisboaCaparicaPortugal
  2. 2.Departamento de Ciências e TecnologiaUniversidade AbertaLisbonPortugal
  3. 3.CENSE – Centre for Environmental and Sustainability Research, Departamento de Ciências e Engenharia do AmbienteFaculdade de Ciências e Tecnologia da Universidade Nova de LisboaCaparicaPortugal

Personalised recommendations