Skip to main content
Log in

Thyroid Lesions and Dioxin Accumulation in the Livers of Jungle Crows (Corvus Macrorhynchos) in Urban and Suburban Tokyo

  • Published:
Archives of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

Wild jungle crows (Corvus macrorhynchos) captured from three different areas of Tokyo were examined to evaluate environmental contamination of dioxins. In addition to the pathologic examination of their whole body, accumulation of dioxins, mRNA expression of the aryl hydrocarbon receptor (AhR), and pentoxyresorufin-O-depenthylase (PROD) activity in the liver were determined. Marked histopathologic changes were observed in the thyroid glands, especially in the crows from the urban downtown area. Levels of dioxins and their toxic equivalents (TEQs) and AhR mRNA expression in the livers of the crows from the urban area were higher than those from the suburban area. There was a high correlation between the levels of TEQs and PROD activity. The results of the present study demonstrated that jungle crows possess AhR-mediated toxicologic pathways similar to those of mammals and suggest the possibility that the thyroidal changes observed in the adult crows from the urban areas are one of the toxic manifestations resulting from exposure to dioxins and other environmental chemicals.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.

Similar content being viewed by others

References

  • BD Abbott JE Schmid JG Brown CR Wood RD White AR Buckalew et al. (1999) ArticleTitleRT-PCR quantification of AHR, ARNT, GR, and CYP1A1 mRNA in craniofacial tissues of embryonic mice exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin and hydrocortisone Toxicol Sci 47 76–85 Occurrence Handle10.1093/toxsci/47.1.76 Occurrence Handle1:CAS:528:DyaK1MXjt1Wisro%3D Occurrence Handle10048155

    Article  CAS  PubMed  Google Scholar 

  • CH Bastomsky (1977) ArticleTitleEnhanced thyroxine metabolism and high uptake goiters in rats after a single dose of 2,3,7,8-tetrachlorodibenzo-p-dioxin Endocrinology 101 292–296 Occurrence Handle1:CAS:528:DyaE2sXksl2htLw%3D Occurrence Handle862558

    CAS  PubMed  Google Scholar 

  • BM Braune M Simon (2003) ArticleTitleDioxins, furans, and non-ortho PCBs in Canadian Arctic seabirds Environ Sci Technol 37 3071–3077 Occurrence Handle10.1021/es021082p Occurrence Handle1:CAS:528:DC%2BD3sXktlyqurc%3D Occurrence Handle12901652

    Article  CAS  PubMed  Google Scholar 

  • CC Capen SL Martin (1989) ArticleTitleThe effects of xenobiotics on the structure and function of thyroid follicular and C-cells Toxicol Pathol 17 266–293 Occurrence Handle1:CAS:528:DyaL1MXls1Ontr8%3D Occurrence Handle2675279

    CAS  PubMed  Google Scholar 

  • L Dong Q Ma Jr JP Whitlock (1996) ArticleTitleDNA binding by the heterodimeric Ah receptor. Relationship to dioxin-induced CYP1A1 transcription in vivo J Biol Chem 271 7942–7948 Occurrence Handle10.1074/jbc.271.14.7942 Occurrence Handle1:CAS:528:DyaK28XitFarsLc%3D Occurrence Handle8626473

    Article  CAS  PubMed  Google Scholar 

  • MA Franc R Pohjanvirta J Tuomisto AB Okey (2001) ArticleTitlePersistent, low-dose 2,3,7,8-tetrachlorodibenzo-p-dioxin exposure: Effect on aryl hydrocarbon receptor expression in a dioxin-resistance model Toxicol Appl Pharmacol 175 43–53 Occurrence Handle10.1006/taap.2001.9222 Occurrence Handle1:CAS:528:DC%2BD3MXlvFKgurc%3D Occurrence Handle11509025

    Article  CAS  PubMed  Google Scholar 

  • KS Guruge S Tanabe (1997) ArticleTitleCongener specific accumulation and toxic assessment of polychlorinated biphenyls in common cormorants, phalacrocorax carbo, from Lake Biwa, Japan Environ Pollut 96 425–433 Occurrence Handle10.1016/S0269-7491(97)00045-6 Occurrence Handle1:CAS:528:DyaK2sXlvVWgtL4%3D Occurrence Handle15093408

    Article  CAS  PubMed  Google Scholar 

  • JT Hamm CY Chen LS Birnbaum (2003) ArticleTitleA mixture of dioxins, furans, and non-ortho PCBs based upon consensus toxic equivalency factors produces dioxin-like reproductive effects Toxicol Sci 74 182–191 Occurrence Handle10.1093/toxsci/kfg107 Occurrence Handle1:CAS:528:DC%2BD3sXkvVSmurg%3D Occurrence Handle12730615

    Article  CAS  PubMed  Google Scholar 

  • T Iida H Hirakawa T Matsueda J Nagayama T Nagata (1999) ArticleTitlePolychlorinated dibenzo-p-dioxins and related compounds: Correlations of levels in human tissues and in blood Chemosphere 38 2767–2774 Occurrence Handle10.1016/S0045-6535(98)00478-0 Occurrence Handle1:CAS:528:DyaK1MXitlOltbw%3D Occurrence Handle10214714

    Article  CAS  PubMed  Google Scholar 

  • K Kannan KS Kumar H Nakata J Falandysz G Oehme S Masunaga (2003) ArticleTitlePolychlorinated biphenyls, dibenzo-p-dioxins, dibenzofurans, and p,p′-DDE in livers of white-tailed sea eagles from Eastern Germany, 1979-1998 Environ Sci Technol 37 1249–1255 Occurrence Handle1:CAS:528:DC%2BD3sXhsVaqurg%3D

    CAS  Google Scholar 

  • J Kanno C Matsuoka K Furuta H Onodera H Miyajima A Maekawa et al. (1990) ArticleTitleTumor promoting effect of goitrogens on the rat thyroid Toxicol Pathol 18 239–246 Occurrence Handle1:CAS:528:DyaK3MXit1eht74%3D Occurrence Handle1697977

    CAS  PubMed  Google Scholar 

  • SW Kennedy SP Jones LJ Bastien (1995) ArticleTitleEfficient analysis of cytochrome P4501A catalytic activity, porphyrins, and total proteins in chicken embryo hepatocyte cultures with a fluorescence plate reader Anal Biochem 226 362–370 Occurrence Handle10.1006/abio.1995.1237 Occurrence Handle1:CAS:528:DyaK2MXltVSrsb4%3D Occurrence Handle7793639

    Article  CAS  PubMed  Google Scholar 

  • M Machala J Vondráček L Bláha M Ciganek JV Neča (2001) ArticleTitleAryl hydrocarbon receptor-mediated activity of mutagenic polycyclic aromatic hydrocarbons determined using in vitro reporter gene assay Mutat Res 497 49–62 Occurrence Handle1:CAS:528:DC%2BD3MXmt1Krs7s%3D Occurrence Handle11525907

    CAS  PubMed  Google Scholar 

  • S Masunaga T Takasuga J Nakanishi (2001) ArticleTitleDioxin and dioxin-like PCB impurities in some Japanese agrochemical formulations Chemosphere 44 873–885 Occurrence Handle10.1016/S0045-6535(00)00310-6 Occurrence Handle1:CAS:528:DC%2BD3MXkvVehtbg%3D Occurrence Handle11482680

    Article  CAS  PubMed  Google Scholar 

  • J Mimura Y Fujii-Kuriyama (2003) ArticleTitleFunctional role of AhR in the expression of toxic effects by TCDD Biochim Biophys Acta 1619 263–268 Occurrence Handle1:CAS:528:DC%2BD3sXovFGrtg%3D%3D Occurrence Handle12573486

    CAS  PubMed  Google Scholar 

  • RD Moccia GA Fox A Britton (1986) ArticleTitleA quantitative assessment of thyroid histopathology of herring gulls (Larus argentatus) from the Great Lakes and a hypothesis on the causal role of environmental contaminants J Wildl Dis 22 60–70 Occurrence Handle1:STN:280:BimC2cvhslQ%3D Occurrence Handle3951063

    CAS  PubMed  Google Scholar 

  • N Nishimura Y Miyabara M Sato J Yonemoto C Tohyama (2002) ArticleTitleImmunohistochemical localization of thyroid stimulating hormone induced by a low oral dose of 2,3,7,8-tetrachlorodibenzo-p-dioxin in female Sprague-Dawley rats Toxicology 171 73–82 Occurrence Handle10.1016/S0300-483X(01)00559-5 Occurrence Handle1:CAS:528:DC%2BD38XhtVKmtbo%3D Occurrence Handle11836014

    Article  CAS  PubMed  Google Scholar 

  • M Peden-Adams K Alonso C Godard S Skipper W Mashburn J Hoover et al. (1998) ArticleTitleEffects of environmentally relevant concentrations of 2,3,7,8-TCDD on domestic chicken immune function and CYP450 activity: F1 generation and egg injection studies Chemosphere 37 1923–1939 Occurrence Handle10.1016/S0045-6535(98)00259-8 Occurrence Handle1:CAS:528:DyaK1cXmvV2kur4%3D Occurrence Handle9828320

    Article  CAS  PubMed  Google Scholar 

  • RS Pollenz MJ Santostefano E Klett VM Richardson B Necela LS Birnbaum (1998) ArticleTitleFemale Sprague-Dawley rats exposed to a single oral dose of 2,3,7,8-tetrachlorodibenzo-p-dioxin exhibit sustained depletion of aryl hydrocarbon receptor protein in liver, spleen, thymus, and lung Toxicol Sci 42 117–128 Occurrence Handle10.1006/toxs.1998.2439 Occurrence Handle1:CAS:528:DyaK1cXislKlsrs%3D Occurrence Handle9579024

    Article  CAS  PubMed  Google Scholar 

  • S Sakai K Hayakawa H Takatsuki I Kawakami (2001) ArticleTitleDioxin-like PCBs released from waste incineration and their deposition flux Environ Sci Technol 35 3601–3607 Occurrence Handle10.1021/es001945j Occurrence Handle1:CAS:528:DC%2BD3MXlslyksrk%3D Occurrence Handle11783634

    Article  CAS  PubMed  Google Scholar 

  • K Senthilkumar N Iseki S Hayama J Nakanishi S Masunaga (2002) ArticleTitlePolychlorinated dibenzo-p-dioxins, dibenzofurans, and dioxin-like polychlorinated biphenyls in livers of birds from Japan Arch Environ Contam Toxicol 42 244–255 Occurrence Handle10.1007/s00244-001-0030-5 Occurrence Handle1:STN:280:DC%2BD38%2FoslWhsg%3D%3D Occurrence Handle11815817

    Article  CAS  PubMed  Google Scholar 

  • PK Smith RI Krohn GT Hermanson AK Mallia FH Gartner MD Provenzano et al. (1985) ArticleTitleMeasurement of protein using bicinchoninic acid Anal Biochem 150 76–85 Occurrence Handle1:CAS:528:DyaL2MXlsFKksL0%3D Occurrence Handle3843705

    CAS  PubMed  Google Scholar 

  • PF Smith SJ Grossman RJ Gerson LR Gordon JG Deluca JA Majka RW Wang JI Germershausen JS MacDonald (1991) ArticleTitleStudies on the mechanism of simvastatin-induced thyroid hypertrophy and follicular cell adenoma in the rat Toxicol Pathol 19 197–205 Occurrence Handle1:CAS:528:DyaK38Xns1WgsA%3D%3D Occurrence Handle1780636

    CAS  PubMed  Google Scholar 

  • RJ Sommer KM Sojka RS Pollenz PS Cooke RE Peterson (1999) ArticleTitleAh receptor and ARNT protein and mRNA concentrations in rat prostate: Effects of stage of development and 2,3,7, 8-tetrachlorodibenzo-p-dioxin treatment Toxicol Appl Pharmacol 155 177–189 Occurrence Handle10.1006/taap.1998.8597 Occurrence Handle1:CAS:528:DyaK1MXhsVegtL0%3D Occurrence Handle10053172

    Article  CAS  PubMed  Google Scholar 

  • TN Takagi KA Matsui K Yamashita H Ohmori M Yasuda (2000) ArticleTitlePathogenesis of cleft palate in mouse embryos exposed to 2,3,7, 8-tetrachlorodibenzo-p-dioxin (TCDD) Teratog Carcinog Mutagen 20 73–86 Occurrence Handle10.1002/(SICI)1520-6866(2000)20:2<73::AID-TCM3>3.0.CO;2-M Occurrence Handle1:CAS:528:DC%2BD3cXhtF2mtb8%3D Occurrence Handle10679751

    Article  CAS  PubMed  Google Scholar 

  • M Berg ParticleVan den L Birnbaum AT Bosveld B Brunström P Cook M Feeley et al. (1998) ArticleTitleToxic equivalency factors (TEFs) for PCBs, PCDDs, PCDFs for humans and wildlife Environ Health Perspect 106 775–792 Occurrence Handle9831538

    PubMed  Google Scholar 

Download references

Acknowledgments

We thank Dr. Annamalai Subramanian for critical reading of the manuscript. We are also grateful to Drs. Mitsuru Nakamura and Nagahiro Nose for kindly providing the crows. This study was supported in part by Grant-in-Aid for COE from the Ministry of Education, Culture, Sports, Science, and Technology of Japan. Parts of this study were conducted as “Survey on the State of Dioxin Accumulation in Wildlife” by the Ministry of the Environment.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Y. Kashida.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kobayashi, M., Kashida, Y., Yoneda, K. et al. Thyroid Lesions and Dioxin Accumulation in the Livers of Jungle Crows (Corvus Macrorhynchos) in Urban and Suburban Tokyo. Arch Environ Contam Toxicol 48, 424–432 (2005). https://doi.org/10.1007/s00244-004-0101-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00244-004-0101-5

Keywords

Navigation