Abstract
In this review the biochemical, metabolic and toxicological significance of porphyrins in birds is examined, and their use as biomarkers of exposure to xenobiotics and heavy metals is explored. Laboratory studies pinpointing the main classes of compounds that alter porphyrin profiles are described, as well as those which defined the resulting porphyrin profiles and target organs. Field studies in which the biomarker was validated on natural populations of several species of birds are then reviewed. We finally illustrate their potential as a non-destructive biomarker suitable for situations in which destructive sampling of natural populations must be avoided, suggesting the implementation of this approach.
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Akins, J.M., Hooper, M.J., Miller, H. and Woods, J.S. (1993). Porphyrin profiles in the nestling European starling (Sturnus vulgaris): a potential biomarker of field contaminant exposure. J. Toxicol. Environ. Health 40(1), 47-59.
Bernard, A. and Lauwerys, R. (1987). Metal-induced alterations of δ-aminolevulinc acid dehydratase. Ann. N.Y. Acad. Sci. 514, 41.
Bishop, C.A., Mahony, N.A., Trudeau, S. and Pettit, K.E. (1999). Reproductive and physiological responses to chlorinated hydrocarbons in tree swallow (Tachyneta bicolor) in areas of concern in the Great Lakes-St. Laurence River basin. Environ. Toxicol. Chem. 18, 263-71.
Blus, L.J., Henny, C.J., Hoffman, D.J. and Grove, R.A. (1993). Accumulation and effects of lead and cadmium on wood ducks near a mining and smelting complex in Idaho. Ecotoxicology 2, 139-54.
Cantoni, L., dal Fiume, D., Rizzardini, M. and Ruggieri, R. (1984). In vitro inhibitory effect on porphyrinogen decarboxylase of liver extracts from TCDD treated mice. Toxicol. Lett. 20(2), 211-7.
Carpenter, H.M., Williams, D.E. and Buhler, D.R. (1985). Hexaclorobenzene-induced porphyria in japanese quail: changes in microsomal enzymes. J. Toxicol. Environ. Health 15, 431-44.
Casini, S. (1997). Effects of hexachlorobenzene and polychlorinated biphenyls on porphyrin metabolism: a potential application in ecotoxicological studies. Pharmacol. Res. 35(3), 221-2.
Casini, S., Fossi, M.C., Gavilan, J.F., Barra, R., Parra, O., Leonzio, C. and Focardi, S. (2001). Porphyrin levels in excreta of sea birds of the cilean coasts as nondestructive biomarker of exposure to environmental pollutants. Arch. Environ. Contam. Toxicol. 41(1), 65-72.
De Matteis, F. and Lim, C.K. (1994). Porphyrins as “Nondestructive” indicators of exposure to environmental Pollutants. In M.C. Fossi and C. Leonzio (eds) Nondestructive Biomarkers in Vertebrates, pp. 93-128. Boca Raton FL: Lewis Press.
De Verneuil, H., Sassa, S. and Kappas, A. (1983). Effects of polychlorinated biphenyl compounds, 2,3,7,8-tetrachlorodibenzo-p-dioxin, phenobarbital and iron on hepatic uroporphyrinogen decarboxylase. Biochem. J. 214, 145-51.
Den Besten, C., Bennik, M.H.J., Bruggeman, I., Schielen, P., Kuper, F., Brouwer, A., Koeman, J.H., Vos, J.G. and van Bladeren, P.J. (1993). The role of oxidative metabolism in hexachlorobenzene-induced porphyria and thyroid hormone homeostasis: a comparison with pentachlorobenzene in a 13-week feeding study. Toxicol. Appl. Pharmacol. 119, 181-94.
Elliott, J.E., Kennedy, S.W., Jeffrey, D. and Shutt, L. (1991). Polychlorinated biphenyl (PCBs) effects on hepatic mixed function oxidases and porphyria in birds: II. Amer. kestrel. Comp. Biochem. Physiol C. Comp. Pharmacol. Toxicol. 99(1–2), 141-6.
Elliott, J.E., Kennedy, S.W., Peakall, D.B. and Won, H. (1990). Polychlorinated biphenyl (PCBs) effects on hepatic mixed function oxidases and porphyria in birds: I. Japanese quail. Comp. Biochem. Phys C. Comp. Pharmacol. Toxicol. 96(1), 205-10.
Elliott, J.E., Norstrom, R.J., Lorenzen, A., Hart, L.E., Philibert, H., Kennedy, S.W., Stegeman, J.J., Bellward, G.D. and Cheng, K.M. (1996). Biological effects of polychlorinated dibenzo-p-dioxins, dibenzofurans, and biphenyls in bald eagle (Haliaeetus leucocephalus) chicks. Environ. Toxicol. Chem. 15, 762-93.
Fossi, M.C., Casini, S. and Marsili, L. (1996). Porphyrins in excreta: a nondestructive biomarker for the hazard assessment of birds contaminated with PCBs. Chemosphere 33(1), 29-42.
Fossi, M.C. and Leonzio, C. (eds) (1994). Nondestructive Biomarkers in Vertebrates. Boca Raton, FL: Lewis Publishers Press.
Fox, G.A., Kennedy, S.W., Norstrom, R.J. and Wigfield, D.C. (1988). Porphyria in herring gulls: a biochemical response to chemical contamination of Great Lakes food chains. Environ. Toxicol. Chem. 7, 831-9.
Gilbertson, M. and Fox, G.A. (1977). Pollutant-associated embryonic mortality of great lakes herring gulls. Environ. Pollut. 12, 211-16.
Goldstein, J.A., McKinney, J.D., Lucier, G.W., Hickman, P., Bergman, H. and Moore, J.A. (1976). Toxicological assessment of hexachlorobiphenyl isomers and 2,3,7,8-tetrachlorodibenzofuran in chicks. Toxicol. Appl. Pharmacol. 36, 81-92.
Grandchamp, B., Deybach, J.C., Grelier, M., De Verneuil, H. and Nordmand, Y. (1980). Studies of porphyrin synthesis in fibroblasts of patients with congenital erithropoietic porphyria and one patient with homozygous coproporphyria. Biochim. Biophys. Acta 620, 577-86.
Grasman, K.A., Scanlon, P.F. and Fox, G.A. (2000). Geographic variation in hematological variables in adult and prefledgling herring gulls (Larus argentatus) and possible associations with organochlorine exposure. Arch. Environ. Contam. Toxicol. 38, 244-53.
Henny, C.J., Lawrence, J.B., Hoffman, D.J., Grove, R.A. and Hatfield, J.S. (1991). Lead accumulation and Osprey production near a mining site on Cœur d'Alene river, Idaho. Arch. Environ. Contam. Toxicol. 21, 415-24.
Henriksen, E.O., Gabrielsen, G.W., Trudeau, S., Wolkers, J., Sagerup, K. and Skaare, J.U. (2000). Organochlorines and possible biochemical effects in glaucous gulls (Larus hyperboreus) from bjornoya, the Barents Sea. Arch. Environ. Contam. Toxicol. 38, 234-43.
Hoffman, D.J., Heinz, G.H., Sileo, L., Audet, D.J., Campbell, J.K. and Le Captain, L.J. (2000). Developmental toxicity of lead-contaminated sediment to mallad ducklings. Arch. Environ. Contam. Toxicol. 39, 221-32.
Jacobs, J.M., Sinclair, P.R., Bement, W.J., Lambrecht, R.W., Sinclair, J.F. and Goldstein, J.A. (1989). Oxidation of uroporphyrinogen by methylcholantrene-induced cytochrome P-450. Biochem. J. 258, 247-53.
Jacobs, J.M., Sinclair, P.R., Gorman, N., Jacobs, N.J., Sinclair, J.F., Bement, W.J. and Walton, H. (1992). Effects of diphenyl ether herbicides on porphyrin accumulation by cultured hepatocytes. J. Biochem. Toxicol. 7(2), 87-95.
Kennedy, S.W. and Fox, G.A. (1990). Highly carboxylated porphyrins as a biomarker of polyalogenated aromatic hydrocarbon exposure in wildlife: confirmation of their presence in great lakes herring gull chicks in the early 1970s and important methodological details. Chemosphere 21(3), 407-15.
Kennedy, S.W., Fox, G.A., Trudeau, S., Bastien, L.J. and Jones, S.P. (1998). Highly carboxylated porphyrin concentration: a biochemical biomarker of PCB exposure in herring gulls. Mar. Environ. Res. 46(1–5), 65-9.
Lambrecht, R.W., Sinclair, P.R., Bement, W.J. and Sinclair, J.F. (1988). Uroporphyrin accumulation in cultured chick embrio hepatocytes: comparison of 2,3,7,8-terìtrachlorodibenzo-p-dioxin and 3,4,3′,4′-tetrachlorobiphenyl. Toxicol. Appl. Pharm. 96, 507-16.
Leonzio, C., Bianchi, N., Casini, S., Fossi, M.C. and Focardi, S. (2001). A nondestructive approach to assess the health status of a rare species, the Eleonor's falcon. 11th Annual meeting of SETAC Europe, From basic science to decision-making: “The Environmental Odyssey”, Abstracts, 235.
Leonzio, C., Fossi, M.C. and Casini, S. (1995). Porphyrins as biomarkers of methylmercury and PCBs exposure in experimental quail. Bull. Environ. Contam. Toxicol. 56, 244-50.
Lim, C.K. (1991). Porphyrins. In T. Hanai (ed.) Journal of Chromatography Library. Liquid Chromatography in Biomedical Analysis, vol. 80, pp. 209-29. Elsevier.
Lim, C.K. and Peters, T.J. (1984). Urine and faecal porphyrin profiles by reversed-phase high-performance liquid chromatography in the porphyries. Clin. Chim. Acta 139, 55-63.
Lorenzen, A., Kennedy, S.W., Bastien, L.J. and Hahn, M.E. (1997b). Halogenated aromatic Hydrocarbon-mediated porphyrin accumulation and induction of cytochrome P4501A in chicken embryo hepatocytes. Biochem. Pharmacol. 53, 373-84.
Lorenzen, A., Shutt, J.L. and Kennedy, S.W. (1997a). Sensitivity of common tern (Sterna hirundo) embryo hepatocyte cultures to CYP1A induction and porphyrin accumulation by halogenated aromatic hydrocarbons and common tern egg extracts. Arch. Environ. Contam. Toxicol. 32, 126-34.
Marks, G.S. (1985). Exposure to toxic agents: the heme biosynthetic pathway and hemoproteins as indicator. CRC Crit. Rev. Toxicol. 15, 151-79.
Martinez, G., Cebrian, M., Chamorro, G. and Jague, O. (1983). Urinary uroporphyrin as a indicator of arsenic exposure in rats. Proc. Western Pharmacol. Soc. 26, 171-8.
Miranda, C.L., Henderson, M.C., Wang, J.L., Nakaue, H.S. and Buhler, D.R. (1986). Induction of acute renal porphyria in Japanese quail by Aroclor 1254. Biochem. Phamacol. 35(20), 3637-9.
Miranda, C.L., Henderson, M.C., Wang, J.L., Nakaue, H.S. and Buhler, D.R. (1987). Effects of polychlorinated biphenyls on porphyrin synthesis and cytochrome P-450-dependent monooxygenases in small intestine and liver of Japanese quail. J. Toxicol. Environ. Health 20, 27-35.
Miranda, C.L., Henderson, M.C., Wang, J.L., Nakaue, H.S. and Buhler, D.R. (1992). Comparative effects of the polychlorinated biphenyl mixture, aroclor 1242, on porphyrin and xenobiotic metabolism in kidney of Japanese quail and rat. Comp. Biochem. Physiol. 103c(1), 149-52.
Nichol, A.W., Elsbury, S., Elder, G.H., Jackson, A.H. and Rao, K.R.N. (1982). Separation of impurities in diazinon preparations and their effects on porphyrin biosynthesis in tissue culture. Biochem. Pharmacol. 31, 1033-8.
O'Halloran, J. and Duggan, P.F. (1988). Blood lead levels and free red blood cell protoporphyrin as measure of lead exposure in mute swans. Environ. Pollut. 52, 19-38.
Pain, D.J. (1989). Hematological parameters as predictor of blood lead and indicators of lead poisoning in the black duck (Anas rubripes). Environ. Pollut. 60, 67-81.
Poland, A. and Glover, E. (1973). 2,3,7,8-Tetrachlorodibenzo-(p)-dioxin: a potent inducer of δ-aminolevulinc acid synthetase. Science 179, 476-8.
Scheuehammer, A.M. (1989). Monitoring wild bird populations for lead exposure. J. Wildl. Manag. 53, 759-65.
Sinclair, P.R., Bement, W.J., Bonkovsky, H.L., Lambrecht, R.W., Frezza, J.E., Sinclair, J.F., Urquhart, A.J. and Elder, G.H. (1986). Uroporphyrin accumulation produced by halogenated biphenyls in chick-embrio hepatocytes. Biochem. J. 237, 63-71.
Sinclair, P.R., Bement, W.J., Bonkovsky, H.L. and Sinclair, P.R. (1984). Inhibition of uroporphyrinogen decarboxylase by halogenated biphenyls in chick hepatocyte cultures. Biochem. J. 222, 737-48.
Sinclair, P.R., Walton, H.S., Gorman, N., Jacobs, J.M. and Sinclair, J.F. (1997). Multiple roles of polyhalogenated biphenyls in causing increases in cytochrome P450 and uroporphyrin accumulation in cultured hepatocytes. Toxicol. Appl. Pharmacol. 147, 171-9.
Smith, A.G. and De Matteis, F. (1990). Oxidative injury mediated by the hepatic cytochrome P450 system in conjunction with cellular iron. Effects on the pathway of haem biosynthesis. Xenobiotica 20, 865-71.
Smith, A.G. and Francis, J.E. (1987). Chemically-induced formation of an inhibitor of hepatic uroporphyrinogen decarboxylase in inbred mice with iron overload. Biochem. J. 246, 221-6.
Strik, J.J.T.W.A. (1973a). Chemical porphyria in Japanese quail (Coturnix coturnix japonica). Enzyme 16, 211-23.
Strik, J.J.T.W.A. (1973b). Species differences in experimental porphyria caused by polyhalogenated aromatic compounds. Enzyme 16, 224-30.
Taira, M.C. and San Martin de Viale, L.C. (1980). Porphyrinogen carboxylyase from chick embrio liver—in vivo effect of heptachlor and Lindane. Int. J. Biochem. 12, 1033-41.
Trust, K.A., Rummel, K.T., Scheuhammer, A.M., Brisbin, I.L. and Hooper, M.J. (2000). Contaminant exposure and biomarker responses in spectacled eiders (Somateria fischeri) from St. Lawrence Island, Alaska. Arch. Environ. Contam. Toxicol. 38, 107-13.
Vos, J.G. and Koeman, J.H. (1970). Comparative toxicologic study with polychlorinated biphenyls in chickens with special reference to porphyria, edema formation, liver necrosis, and tissue residues. Toxicol. Appl. Pharmacol. 17, 656-68.
Vos, J.G., Strik, J.J.T.W.A. and Pennings, J.H. (1971). Polychlorinated biphenyls as inducers of hepatic porphyria in Japanese quail, with special references to delta-aminolevulinic acid synthetase activity, fluorescence, and residues in the liver. Toxicol. Appl. Pharmacol. 20(2), 232-40.
Wayland, W., Trudeau, S., Marchant, T., Parker, D. and Hobson, K.A. (1998). The effect of pulp and paper mill effluent on an insectivorous bird, the tree swallow. Ecotoxicology 7, 237-51.
Woods, J.S., Fowler, B.A. (1977). Renal porphyrinuria during chronic methyl mercury exposure. J. Lab. Clin. Med. 90, 266-72.
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Casini, S., Cristina Fossi, M., Leonzio, C. et al. Review: Porphyrins as Biomarkers for Hazard Assessment of Bird Populations: Destructive and Non-destructive Use. Ecotoxicology 12, 297–305 (2003). https://doi.org/10.1023/A:1022519214505
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DOI: https://doi.org/10.1023/A:1022519214505