The neonicotinoid pesticide imidacloprid and the dithiocarbamate fungicide mancozeb disrupt the pituitary-thyroid axis of a wildlife bird

Chemosphere

Volumn 122, Issue , 2015, Pages 227-234

  Pandey, Surya Prakash ^a   Mohanty, Banalata ^a  

^a UNIVERSITY OF ALLAHABAD   (India)

Author keywords

Breeding phase; Dithiocarbamate; HPT axis; Neonicotinoid; TSH; Wildlife

Indexed keywords

BIRDS; CELL PROLIFERATION; CELLS; CYTOLOGY; INSECTICIDES;

BREEDING PHASE; DITHIOCARBAMATES; HPT AXIS; NEONICOTINOIDS; WILDLIFE;

CHEMICAL CONTAMINATION;

IMIDACLOPRID; LIOTHYRONINE; MANCOZEB; THYROTROPIN; THYROXINE; FUNGICIDE; IMIDAZOLE DERIVATIVE; MANEB; NITRO DERIVATIVE; THYROID HORMONE; ZINEB;

BIRD; COLLOID; ENDOCRINE DISRUPTOR; FUNGICIDE; GERM CELL; HOMEOSTASIS; METABOLISM; PESTICIDE; PLASMA; REPRODUCTIVE BIOLOGY; SEASONAL VARIATION; WILD POPULATION;

ADULT; ANIMAL EXPERIMENT; ARTICLE; BIRD; BLOOD LEVEL; BODY WEIGHT; BREEDING; COLLOID; CONTROLLED STUDY; EPITHELIUM CELL; HISTOPATHOLOGY; HYPOPHYSIS THYROID SYSTEM; LD 50; LIOTHYRONINE BLOOD LEVEL; MALE; MORPHOMETRICS; NEGATIVE FEEDBACK; NONHUMAN; NUCLEAR SIZE; OVARY CYCLE; STROMA CELL; THYROID FOLLICLE; THYROID GLAND; THYROID WEIGHT; THYROTROPIN BLOOD LEVEL; THYROXINE BLOOD LEVEL; WILDLIFE; ADVERSE EFFECTS; ANATOMY AND HISTOLOGY; ANIMAL; BLOOD; CYTOLOGY; DRUG EFFECTS; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL MONITORING; HYPOPHYSIS; METABOLISM; ORGAN SIZE; PHYSIOLOGY; SONGBIRD;

AMANDAVA AMANDAVA; AVES; HEXAPODA;

ANIMALS; BODY WEIGHT; CELL NUCLEUS SIZE; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL MONITORING; EPITHELIAL CELLS; FUNGICIDES, INDUSTRIAL; IMIDAZOLES; MALE; MANEB; NITRO COMPOUNDS; ORGAN SIZE; PASSERIFORMES; PITUITARY GLAND; STROMAL CELLS; THYROID GLAND; THYROID HORMONES; THYROTROPIN; ZINEB;

EID: 84920519304     PISSN: 00456535     EISSN: 18791298     Source Type: Journal    
DOI: 10.1016/j.chemosphere.2014.11.061     Document Type: Article

References (49)

1. Adamski Z., Błoszyk J., Piosik K., Tomczak K. Effects of difl ubenzuron and mancozeb on soil microarthropods: a long-term study. Biolog. Lett. 2009, 46:3-13. 10.2478/v10120-009-0008-y.
2. Anway M.D., Cupp A.S., Uzumcu M., Skinner M.K. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 2005, 308:1466-1469. 10.1126/science.1108190.
3. Axelstad M., Boberg J., Nellemann C., Kiersgaard M., Jacobsen P.R., Christiansen S., Hougaard K.S., Hass U. Exposure to widely used fungicide mancozeb causes thyroid hormone disruption in rat dams but no behavioral effects in the offsprings. Toxicol. Sci. 2011, 120:439-446. 10.1093/toxsci/kfr006.
4. Bal R., Naziroğlu M., Türk G., Yilmaz Ö., Kuloğlu T., Etem E., Baydas G. Insecticide imidacloprid induces morphological and DNA damage through oxidative toxicity on the reproductive organs of developing male rats. Cell Biochem. Funct. 2012, 10.1002/cbf.2826.
5. Baligar P.N., Kaliwal B.B. Induction of gonadal toxicity to female rats after chronic exposure to mancozeb. Ind. Health 2001, 39:235-243. 10.2486/indhealth.39.235.
6. Barrett P., Ebling F.J.P., Schuhler S., Wilson D., Ross A.W., Warner A., Jethwa P., Boelen A., Visser T.J., Ozanne D.M., Archer Z.A., Mercer J.G., Morgan P.J. Hypothalamic thyroid hormone catabolism acts as a gatekeeper for the seasonal control of body weight and reproduction. Endocrinology 2007, 148:3608-3617. 10.1210/en.2007-0316.
7. Bhardwaj S., Srivastava M.K., Kapoor U., Srivastava L.P. A 90 days oral toxicity of imidacloprid in female rats: morphological, biochemical and histopathological evaluations. Food Chem. Toxicol. 2010, 48:1185-1190. 10.1016/j.fct.2010.02.009.
8. Bhaskar R., Mohanty B. Pesticides in mixture disrupt metabolic regulation: in silico and in vivo analysis of cumulative toxicity of mancozeb and imidacloprid on body weight of mice. Gen. Comp. Endocrinol. 2014, 205:226-234. 10.1016/j.ygcen.2014.02.007.
9. Blacquie're T., Smagghe G., van Gestel C.A.M., Mommaerts V. Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology 2012, 21:973-992. 10.1007/s10646-012-0863-x.
10. Calviello G., Piccioni E., Boninsegna A., Tedesco B., Maggiano N., Serini S., Wolf F.I., Palozza P. DNA damage and apoptosis induction by the pesticide mancozeb in rat cells: involvement of the oxidative mechanism. Toxicol. Appl. Pharmacol. 2006, 211:87-96. 10.1016/j.taap.2005.06.001.
11. Cesh L.S., Elliott K.H., Quade S., Mckinney M.A., Maisoneuve F., Garcelon D.K., Sandau C.D., Letcher R.J., Williams T.D., Elliott J.E. Polyhalogenated aromatic hydrocarbons and metabolites: relation to circulating thyroid hormone and retinol in nestling bald eagles (Haliaes leucocephalus). Environ. Toxicol. Chem. 2010, 29:1301-1310. 10.1002/etc.165.
12. Corsini E., Viviani B., Birindelli S., Gilardi F., Torri A., Codecà I., Lucchi L., Bartesaghi S., Galli C.L., Marinovich M., Colosio C. Molecular mechanisms underlying mancozeb-induced inhibition of TNF-alpha production. Toxicol. Appl. Pharmacol. 2006, 212:89-98. 10.1016/j.taap.2005.07.002.
13. Costa C., Silvari V., Melchini A., Catania S., Heffron J.J., Trovato A., De Pasquale R. Genotoxicity of imidacloprid in relation to metabolic activation and composition of the commercial product. Mutat. Res. 2009, 672:40-44. 10.1016/j.mrgentox.2008.09.018.
14. Crane H.M., Pickford D.B., Hutchinson T.H., Brown J.A. Effects of ammonium perchlorate on thyroid function in developing fathead minnows, Pimephales promelas. Environ. Health Perspect. 2005, 113:396-401. 10.1289/ehp.7333.
15. Dawson A., Thapliyal J.P. The thyroid and photoperiodism. Avian Endocrinology 2001, 141-151. Narosa Publishing House, New Delhi. A. Dawson, C.M. Chaturvedi (Eds.).
16. Doerge D.R., Takazawa R.S. Mechanism of thyroid peroxidase inhibition by ethylenethiourea. Chem. Res. Toxicol. 1990, 3:98-101. 10.1021/tx00014a003.
17. Domico L.M., Zeevalk G.D., Bernard L.P., Cooper K.R. Acute neurotoxic effects of mancozeb and maneb in mesencephalic neuronal cultures are associated with mitochondrial dysfunction. Neurotoxicology 2006, 27:816-825. 10.1016/j.neuro.2006.07.009.
18. Fawcett D., Jensh R. Bloom & Fawcett's Concise Histology 2002, Arnold Publishers, New York, pp. 257-258, ISBN0-340-80677-X. second ed.
19. Flood D.E.K., Fernandino J.I., Langlois V.S. Thyroid hormones in male reproductive development: evidence for direct crosstalk between the androgen and thyroid hormone axes. Gen. Comp. Endocrinol. 2013, 192:2-14. 10.1016/j.ygcen.2013.02.038.
20. Hartoft-Nielsen M.L., Rasmussen A.K., Feldt-Rasmussen U., Buschard K., Bock T. Estimation of number of follicles, volume of colloid and inner follicular surface area in the thyroid gland of rats. J. Anat. 2005, 207:117-124. 10.1111/j.1469-7580.2005.00442.x.
21. Health and Consumer Protection Directorate General, 2009. Directorate D-Food Safety: Production and distribution chain. In: review report for the active substance mancozeb. European Commission, Brussels, pp1-62. (URL:
22. Jeschke P., Nauen R., Schindler M., Elbert A. Overview of the status and global strategy for neonicotinoids. J. Agric. Food Chem. 2011, 59:2897-2908. dx.doi.org/10.1021/jf101303g.
23. Kendeigh S., Wallin C., Harold E. Seasonal and taxonomic differences in the size and activity of the thyroid glands in birds. Ohio J. Sci. 1966, 66:368-379.
24. Kimura-Kuroda J., Komuta Y., Kuroda Y., Hayashi M., Kawano H. Nicotine-Like effects of the neonicotinoid insecticides acetamiprid and imidacloprid on cerebellar neurons from neonatal rats. PLoS ONE 2012, 7:e32432. 10.1371/journal.pone.0032432.
25. Koppad A.G., Umarbhadsha N.K. Effect of pre-sowing treatments on seed germination of babehi (Psoralea corylifolia) and senna (Cassia angustifolia) in nursery. Karnataka J. Agric. Sci. 2006, 19:441-442.
26. Kot B.C.W., Lau T.Y.H., Cheng S.C.H. Stereology of the thyroid gland in Indo-Pacific bottlenose dolphin (Tursiops aduncus) in comparison with human (Homo sapiens): quantitative and functional implications. PLoS ONE 2013, 8:e62060. 10.1371/journal.pone.0062060.
27. Ksheerasagar R.L., Kaliwal B.B. Temporal effects of mancozeb on testes, accessory reproductive organs and biochemical constituents in albino mice. Environ. Toxicol. Pharmacol. 2003, 15:9-17. 10.1016/j.etap.2003.08.006.
28. Laisi A., Tuominen R., Männistö P., Savolainen K., Mattila J. The effect of maneb, zineb, and ethylenethiourea on the humoral activity of the pituitary-thyroid axis in rat. Arch. Toxicol. 1985, 8:253-258. 10.1007/978-3-642-69928-3_37.
29. Lopez-Antia A., Ortiz-Santaliestra M.E., Mougeot F., Mateo R. Experimental exposure of red-legged partridges (Alectoris rufa) to seeds coated with imidacloprid, thiram and difenoconazole. Ecotoxicology 2012, 22:125-138. 10.1007/s10646-012-1009-x.
30. Mahadevaswami M.P., Jadaramkunti U.C., Hiremath M.B., Kaliwal B.B. Effect of mancozeb on ovarian compensatory hypertrophy and biochemical constituents in hemicastrated albino rat. Reprod. Toxicol. 2000, 14:127-134. 10.1016/S0890-6238(00)00064-2.
31. Maranghi F., De Angelis S., Tassinari R., Chiarotti F., Lorenzetti S., Moracci G., Morcoccia D., Gilardi E., Di Virgilio A., Eusepi A., Mantovani A., Olivieri A. Reproductive toxicity and thyroid effects in Sprague Dawley rats exposed to low doses of ethylenethiourea. Food Chem. Toxicol. 2013, 59:261-271. 10.1016/j.fct.2013.05.048.
32. Marteinson S.C., Kimmins S., Letcher R.J., Palace V.P., Bird D.M., Ritchie I.J., Fernie K.J. Diet exposure to technical hexabromocyclododecane (HBCD) affects testes and circulating testosterone and thyroxine levels in American kestrels (Falco sparverius). Environ. Res. 2011, 111:1116-1123. 10.1016/j.envres.2011.08.006.
33. Marteinson S.C., Bird D.M., Letcher R.J., Sullivan K.M., Ritchie I.J., Fernie K.J. Dietary exposure to technical hexabromocyclododecane (HBCD) alters courtship, incubation and parental behaviors in American kestrels (Falco sparverius). Chemosphere 2012, 89:1077-1083.
34. Mayne G.J., Bishop C.A., Martin P.A., Boermans H.J., Hunter B. Thyroid function in nestling tree swallows and eastern bluebirds exposed to non-persistent pesticides and p, p¢-DDE in apple orchards of Southern Ontario, Canada. Ecotoxicology 2005, 14:381-396. 10.1007/s10646-004-6372-9.
35. McNabb F.M.A. The Hypothalamic-pituitary-thyroid (HPT) axis in birds and its role in bird development and reproduction 2007, 37:163-193. 10.1080/10408440601123552.
36. Miller M.D., Crofton K.M., Rice D.C., Zoeller R.T. Thyroid-disrupting chemicals: interpreting upstream biomarkers of adverse outcomes. Environ. Health Perspect. 2009, 117:1033-1041. 10.1289/ehp.0800247.
37. Mishra A.C., Mohanty B. Effects of lactational exposure of olanzapine and risperidone on hematology and lymphoid organs histopathology: a comparative study in mice neonates. Eur. J. Pharmacol. 2010, 634:170-177. 10.1016/j.ejphar.2010.02.014.
38. Mondal S., Ghosh R.C., Mate M.S., Karmakar D.B. Effects of acetamiprid on immune system in female wistar rats. Proc. zool. Soc. 2009, 62:109-117. 10.1007/s12595-009-0012-6.
39. Nakao N., Ono H., Yoshimura T. Thyroid hormones and seasonal reproductive neuroendocrine interactions. Reproduction 2008, 136:1-8. 10.1530/REP-08-0041.
40. National Toxicology Program (NTP), 1992. Toxicology and carcinogenesis studies of etylene thiourea in rats and mice. In: Technical Report Series 388, US department of health and human services, National Institute of Health, research triangle park, NC, pp 1-261.
41. Overgaard A., Holst K., Mandrup K.R., Boberg J., Christiansen S., Jacobsen P.R., Hass U., Mikkelsen J.D. The effect of perinatal exposure to ethinyl oestradiol or a mixture of endocrine disrupting pesticides on kisspeptin neurons in the rat hypothalamus. Neurotoxicology 2013, 37:154-162. 10.1016/j.neuro.2013.04.012.
42. Palmer M.J., Moffat C., Saranzewa N., Harvey J., Wright G.A., Connolly C.N. Cholinergic pesticides cause mushroom body neuronal inactivation in honeybees. Nat. Commun. 2013, 4:1634. 10.1038/ncomms2648.
43. Rose P.H. Nicotine and the neonicotinoids. Mammalian toxicology of insecticides 2012, 184-220. The Royal Society of Chemistry, London. 10.1039/9781849733007-00184. T.C. Marrs (Ed.).
44. Sharp P.J. Strategies in avian breeding cycles. Anim. Reprod. Sci. 1996, 42:505-513. 10.1016/0378-4320(96)01556-4.
45. Wagner M.S., Wajner S.M., Maia A.L. The role of thyroid hormone in testicular development and function. J. Endocrinol. 2008, 199:351-365. 10.1677/JOE-08-0218.
46. World Health Organization, 1988. Dithiocarbamate pesticides, ethylenethiourea, and propylenethiourea: a general introduction. Environ. Health Criter. 78, WHO, Geneva. http://www.who.int/iris/handle/10665/39117.
47. Yoshimura T. Thyroid hormone and seasonal regulation of reproduction. Front. Neuroendocrinol. 2013, 34:157-166. 10.1016/j.yfrne.2013.04.002.
48. Yoshimura T., Yasuo S., Watanabe M., Iigo M., Yamamura T., Hirunagi K., Ebihara S. Light-induced hormone conversion of T4 to T3 regulates photoperiodic response of gonads in birds. Nature 2003, 426:178-181. 10.1038/nature02117.
49. Zaror C., Segura C., Mansilla H., Mondaca M.A., Gonzalez P. Kinetic study of Imidacloprid removal by advanced oxidation based on photo-fenton process. Environ. Tech. 2010, 31:1411-1416. 10.1080/09593331003680926.