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Changes in the structural and functional state of the thyroid gland of small mammals when exposed to low-intensity chronic radiation

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Abstract

The study gives a morphofunctional assessment of the state of the thyroid gland of tundra voles (Microtus oeconomus Pall.) in conditions of an increased radiation background (the Ukhta district of the Komi Republic (Russia) and the 30-km zone of the Chernobyl NPP), as well as in an experiment with chronic external gamma irradiation in the low dose range. The work summarizes the experience of more than 35 years of field and laboratory research. The authors have noted the high sensitivity of the thyroid gland to chronic radiation against the general irradiation of the organism both in natural conditions and in the experiment. The repeatability of the observed effects in voles from natural populations and the comparability of some effects with the morphological changes occurring in animals after exposure to ionizing radiation in the experiment indicates the radiation nature of these effects. The tundra voles living in conditions of increased radiation background have been identified for a greater variety of morphological rearrangements in the thyroid parenchyma than the experimental animals. The complex and ambiguous nature of the thyroid gland responses to radiation exposure indicates the possibility of a significant increase in the risk of negative effects of ionizing radiation in contrast with the expected results of biological effects’ extrapolation from high to low doses.

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References

  • Alexakhin RM, Arkhipov NP, Bardukharov RM, Vasilenko IYa, Drichko VF, Ivanov YuA, Maslov VI, Maslova KI, Nikiforov VS, Polikarpov GG, Popova ON, Sirotkin AI, Taskaev, AI, Testov BV, Titaeva NA, Fevraleva LT (1990). Heavy natural radionuclides biosphere: migration and biological effects on population and biogeocoenoses, Moscow. Nauka. 368 (in Russian)

  • Barescut J, Grigorkina E, Olenev G (2009) Radioadaptation of rodents in the zone of local radioactive contamination (Kyshtim Accident, Russia): 50 years on. Radioprotect 44:129–134. https://doi.org/10.1051/radiopro/20095028

    Article  Google Scholar 

  • Bashlykova LA, Raskosha OV (2023) Cytogenetic effects in the bone marrow of animals living in conditions of increased natural background radiation. Biol Bull 50(12):3261–3268. https://doi.org/10.1134/S1062359023120026

    Article  CAS  Google Scholar 

  • Beresford NA, Scott EM, Copplestone D (2020) Field effects studies in the Chernobyl exclusion zone: lessons to be learnt. J Environ Radioact 211:105893. https://doi.org/10.1016/j.jenvrad.2019.01.005

    Article  CAS  Google Scholar 

  • Beresford NA, Wright SM, Barnett CL, Hingston JL, Vives i Batlle J, Copplestone D, Kryshev II, Sazykina TG, Pröhl G, Arkhipov A, Howard BJ (2005) A case study in the Chernobyl zone Part 2: predicting radiation induced effects in biota. Radioprotection 40(1):299–305. https://doi.org/10.1051/radiopro:2005s1-045

    Article  Google Scholar 

  • Boiko YN, Cherevko AN, Petrova AM, Zubovich VK (1994) Thyroid and adrenal function in children born 5 years after the Chernobyl accident in economically unfavourable regions of Belarus. Problems Endocrino 40(5):22–24 (In Russ.)

    Article  Google Scholar 

  • Campbell M, Jialal I (2022) Physiology, endocrine hormones In: StatPearls [Internet]. StatPearls Publishing, Treasure Island (FL) https://www.ncbi.nlm.nih.gov/books/NBK538498

    Google Scholar 

  • Cox EM, Arai Y (2014) Environmental chemistry and toxicology of iodine. In Adv Agron 128:47–96. https://doi.org/10.1016/B978-0-12-802139-2.00002-0

    Article  Google Scholar 

  • Degosserie J, Heymans C, Spourquet C, Halbout M, D'Auria L, Van Der Smissen P, Vertommen D, Courtoy PJ, Tyteca D, Pierreux CE (2018) Extracellular vesicles from endothelial progenitor cells promote thyroid follicle formation. J Extracell Vesicles 7:1487250. https://doi.org/10.1080/20013078.2018.1487250

    Article  CAS  Google Scholar 

  • Drozdovitch V (2021) Radiation exposure to the thyroid after the Chernobyl accident. Front Endocrinol (Lausanne) 11:569041. https://doi.org/10.3389/fendo.2020.569041

    Article  Google Scholar 

  • Dubova O, Dubovyi A, Goralska I, Zaika S, Kovalova L (2023) Morphofunctional changes in the canine thyroid gland under low-intensity radiation exposure. Jpn J Vet Res 71:12–19. https://doi.org/10.57494/jjvr.71.1_12

    Article  Google Scholar 

  • El-Benhawy SA, Fahmy EI, Mahdy SM, Khedr GH, Sarhan AS, Nafady MH, Yousef Selim YA, Salem TM, Abu-Samra N, El Khadry HA (2022) Assessment of thyroid gland hormones and ultrasonographic abnormalities in medical staff occupationally exposed to ionizing radiation. BMC Endocr Disord 22(1):287. https://doi.org/10.1186/s12902-022-01196-z

    Article  CAS  Google Scholar 

  • Ermakova OV (2011) Comparative morphological analysis of peripheral endocrine glands of small mammals inhabiting areas with high levels of radioactivity and exposed to chronic irradiation in model experiments. Biophysics 56(1):135–139. https://doi.org/10.1134/S0006350911010088

    Article  Google Scholar 

  • Ermakova OV, Bashlykova LA, Raskosha OV, Starobor NN (2020) Effects of chronic low-intensity irradiation on reproductive parameters of the root vole (Alexandromys oeconomus): responses of parents and offspring. Russ J Ecol 51:242–249. https://doi.org/10.1134/S1067413620030066 (In Russian)

    Article  CAS  Google Scholar 

  • Ermakova OV, Raskosha OV (2005) Complex estimation of thyroid gland state in tundra voles inhabiting the natural radioactive polluted sites. Radiats Biol Radioecol 45:351–357 (in Russian)

    CAS  Google Scholar 

  • Ermakova OV, Raskosha OV (2019) Population characteristic of tundra vole in radioecological studies. Theor Appl Ecol 2:101–107. https://doi.org/10.25750/1995-4301-2019-2-101-107 (in Russian)

    Article  Google Scholar 

  • European Convention for the Protection of Vertebrate Animals used for Experimental and Other Scientific Purposes (1986). Strasburg. Europ. Treaty Series. 123. 48 pp

  • Faggiano A, Coulot J, Bellon N, Talbot M, Caillou B, Ricard M, Bidart JM, Schlumberger M (2004) Age-dependent variation of follicular size and expression of iodine transporters in human thyroid tissue. J Nucl Med 45:232–237

    CAS  Google Scholar 

  • Garnier-Laplace J, Della-Vedova C, Andersson P, Copplestone D, Cailes C, Beresford NA, Howard BJ, Howe P, Whitehouse P (2010) A multi-criteria weight of evidence approach for deriving ecological benchmarks for radioactive substances. J Radiol Prot 30(2):215–233. https://doi.org/10.1088/0952-4746/30/2/S02

    Article  CAS  Google Scholar 

  • Guo QS, Ruan P, Huang WX, Huang DZ, Qiu JC (2021) Occupational radiation exposure and changes in thyroid hormones in a cohort of Chinese medical radiation workers. Biomed Environ Sci 20:282–289. https://doi.org/10.3967/bes2021.037

    Article  CAS  Google Scholar 

  • Hosseini A, Brown JE, Evseeva TI, Sazykina TG (2011) Elaboration on a radiological environmental impact assessment methodology for Northern environments. Radioprotection. 46(6):765–770. https://doi.org/10.1051/radiopro/20116885s

    Article  Google Scholar 

  • Kesäniemi J, Jernfors T, Lavrinienko A, Kivisaari K, Kiljunen M, Mappes T, Watts PC (2019) Exposure to environmental radionuclides is associated with altered metabolic and immunity pathways in a wild rodent. Mol Ecol 28:4620–4635. https://doi.org/10.1111/mec.15241

    Article  CAS  Google Scholar 

  • Khmelnitsky ОК (2002) Cytological and histological diagnostics of thyroid gland diseases. Sankt-Petersbyrg, p 288 (in Russian)

    Google Scholar 

  • Kichigin AI, Taskaev AI (2004) “Water mining”: history of radium production in Republic of Komi (1931–1956). Vopr Istor Estestvozn Tekh 4:3–30 (in Russian)

    Google Scholar 

  • Kivisaari K, Boratyński Z, Lavrinienko A, Kesäniemi J, Lehmann P, Mappes T (2020) The effect of chronic low-dose environmental radiation on organ mass of bank voles in the Chernobyl exclusion zone. Int J Radiat Biol 96:1254–1262. https://doi.org/10.1080/09553002.2020.1793016

    Article  CAS  Google Scholar 

  • Korableva TV (2007) Study of cells with micronuclei in the assessment of age-related patterns of the thyroid gland: Avtoref. dis. ... сand. honey. Sciences Moscow

    Google Scholar 

  • Kudyasheva AG, Shishkina LN, Zagorskaya NG, Taskaev AI (2006) Biochemical consequences of radioactive contamination in the exclusion zone of the Chernobyl accident in populations of wild rodent. In the book: 25 Years after the Chernobyl accident: past, present and future. Editors: E. Burlakova and V. Naydich. USA. Nova Science Pub. Inc. (New York), pp. 303–329

  • Kuvenyova ON, Radionov SN (2013) The morphological changes of the thyroid gland under the effect of ionizing radiation. Tavricheskiy Mediko-Biologicheskiy vestn16:124–126

    Google Scholar 

  • Lyaginskaya AM, Osipov VA (2005) Short-lived isotopes of iodine (131–135) under conditions radiation accident: peculiarities of formation and distribution of absorbed doses in the thyroid gland, biological effects. Med Radiol Radiat Safety 50:18–26 (in Russian)

    Google Scholar 

  • Mariniello K, Ruiz-Babot G, McGaugh EC, Nicholson JG, Gualtieri A, Gaston-Massuet C, Nostro MC, Guasti L (2019) Stem cells, self-renewal, and lineage commitment in the endocrine system. Front Endocrinol (Lausanne) 10:772. https://doi.org/10.3389/fendo.2019.00772

    Article  Google Scholar 

  • Maslov VI, Maslova KI (1972) In: Verkhovskaya IN (ed) Radioecological research in natural biogeocenoses, Moscow, Nauka. pp 161–172 (in Russian)

  • Masson O, Steinhauser G, Wershofen H, Mietelski JW, Fischer HW, Pourcelot L, Saunier O, Bieringer J, Steinkopff T, Hýža M, Møller B, Bowyer TW, Dalaka E, Dalheimer A, de Vismes-Ott A, Eleftheriadis K, Forte M, Gasco Leonarte C, Gorzkiewicz K et al (2018) Potential source apportionment and meteorological conditions involved in airborne 131I detections in January/February 2017 in Europe. Environ Sci Technol 52(15):8488–8500. https://doi.org/10.1021/acs.est.8b01810

    Article  CAS  Google Scholar 

  • Materyi LD, Ermakova OV, Taskaev AI (2003) Morphofunctional assessment of the state of the organism of small mammals in radioecological research (on the example of tundra voles). Syktyvkar, Komi Branch of Academy Science of USSR, 164 (In Russian)

  • McBride WH, Schaue D (2020) Radiation-induced tissue damage and response. J Pathol 250:647–655. https://doi.org/10.1002/path.5389

    Article  Google Scholar 

  • Moiseev AA, Maslov VI, Testov BV, Ovchenkov Vya (1973) The dose loads on mouse-like rodents inhabiting the site of high level radioactivity. Moscow. State Committee on the Use of Nuclear Energy. 30 р. (in Russian)

  • Møller AP, Mousseau TA (2016) Are organisms adapting to ionizing radiation at Chernobyl? Trends Ecol Evol 31:281–289. https://doi.org/10.1016/j.tree.2016.01.005

    Article  Google Scholar 

  • Moskalev YuI (1991) Remote aftereffects of ionizing irradiation exposure, Moscow, Medicina, pp. 315–342 (in Russian).

  • Nadol’nik LI, Kardash NA, Martynchik DI, Kravchuk RI, Netsetskaia ZV, Basinskiĭ VA et al (2005) The effect of one-time external low- and high-dose gamma-irradiation on rat thyroid structure at the acute and remote periods. Radiats Biol Radioecol 45:433–441 (In Russian)

    Google Scholar 

  • Nadol'nik LI, Netsetskaia ZV, Vinogradov VV (2004) Effect of long-term exposure to low dose gamma-irradiation on the rat thyroid status. Radiats Biol Radioecol 44:76–80 (In Russian)

    CAS  Google Scholar 

  • Nagayama Y, Ichikawa T, Saitoh O, Abiru N (2009) Induction of late-onset spontaneous autoimmune thyroiditis by a single low-dose irradiation in thyroiditis-prone non-obese diabetic-H2h4 mice. J Radiat Res 50:573–577. https://doi.org/10.1269/jrr.09067

    Article  Google Scholar 

  • Orekhova NA (2020) Hepatic effects of low-dose rate radiation in natural mouse populations (Apodemus uralensis and Apodemus agrarius): comparative interspecific analysis. Int J Radiat Biol 96:1038–1050. https://doi.org/10.1080/09553002.2020.1770362

    Article  CAS  Google Scholar 

  • Pankaj G (2023) The genomic effects of radiation exposure: induction of cancers and genetic aberrations in mammalian cells. Res J Chem Environ 27:112–122. https://doi.org/10.25303/2709rjce1120122

    Article  CAS  Google Scholar 

  • Pavlov АV, Ermakova ОV, Korablyova TV, Raskosha OV (2013) Morphometric analysis of follicular structure of the thyroid gland after chronic low-dose gamma-irradiation. Morphol 143:43–46 (In Russian)

    CAS  Google Scholar 

  • Rasina LN, Grigorkina EB, Orekhova NA (2017) Adaptation of small mammals to radiocontaminated environment: oxidative metabolism and radioresistance. Dokl Biochem Biophys 476:340–343. https://doi.org/10.1134/S1607672917050143

    Article  CAS  Google Scholar 

  • Raskosha O, Bashlykova L, Starobor N (2023) Assessment of DNA damage in somatic and germ cells of animals living with increased radiation background and their offspring. Int J Radiat Biol 99:499–509. https://doi.org/10.1080/09553002.2022.2110327

    Article  CAS  Google Scholar 

  • Reynolds RM, Weir J, Stockton DL, Brewster DH, Sandeep TC, Strachan MW (2005) Changing trends in incidence and mortality of thyroid cancer in Scotland. Clin Endocrinol 62:156–162. https://doi.org/10.1111/j.1365-2265.2004.02187.x

    Article  Google Scholar 

  • Ross MH, Wojciech P (2016) Histology: a text and atlas: with correlated cell and molecular biology, 7th int. edn. Wolters Kluwer, Philadelphia, pp 758–766

    Google Scholar 

  • Saenko V, Ivanov V, Tsyb A, Bogdanova T, Tronko M, Demidchik Y, Yamashita S (2011) The Chernobyl accident and its consequences. Clin Oncol (R Coll Radiol) 23:234–243. https://doi.org/10.1016/j.clon.2011.01.502

    Article  CAS  Google Scholar 

  • Shaposhnikova LM, Raskosha OV, Rachkova NG (2023) Phytoremediation potential of willow herb and reed canary grass under conditions of polyelemental pollution. Theoretical and Applied. Ecology 1:162–169. https://doi.org/10.25750/1995-4301-2023-1-162-169 (in Russian)

    Article  Google Scholar 

  • Shaposhnikova LM, Shuktomova II (2015) Consequences of radioactive decontamination by earthfill method in a former radium production site. Russ J Ecol 46:299–302. https://doi.org/10.1134/S1067413615030108 (in Russian)

    Article  Google Scholar 

  • Shin E, Lee S, Kang H, Kim J, Kim K, Youn H, Jin YW, Seo S, Youn B (2020) Organ-specific effects of low dose radiation exposure: a comprehensive review. Front Genet 11:566244. https://doi.org/10.3389/fgene.2020.566244

    Article  CAS  Google Scholar 

  • Shinkarev SM, Samoylov AS, Granovskaya EO, Korneva EA, Kukhta BA, Androsova AA, Iatsenko VN (2017) Comparative analysis of the contribution of short-lived radioiodines to the thyroid radiation dose for the population after the Chernobyl and Fukushima accidents. Hygiene Sanit 96(9):827–832. https://doi.org/10.18821/0016-9900-2017-96-9-827-832 (in Russian)

    Article  Google Scholar 

  • Shishkina LN, Kudyasheva AG, Zagorskaya NG, Shevchenko OG, Taskaev AI (2012) Participation of the lipid peroxidation processes in mechanism of the wild rodent adaptation to radioactive contamination of the Chernobyl NPP zone. In: Burlakova EB, Naidich VI (eds) The lessons of Chernobyl: 25 years later. Nova Science Publishers, New York, pp 187–208

    Google Scholar 

  • Shuktomova II, Noskova LM (2006) Distribution of 226Ra and 232Th on the radium production waste repository site. Radiochemistry 48:593–596. https://doi.org/10.1134/S1066362206060105 (in Russian)

    Article  CAS  Google Scholar 

  • Shuryak I (2019) Review of resistance to chronic ionizing radiation exposure under environmental conditions in multicellular organisms. J Environ Radioact 212:106128. https://doi.org/10.1016/j.jenvrad.2019.106128

    Article  CAS  Google Scholar 

  • Sinnott B, Ron E, Schneider AB (2010) Exposing the thyroid to radiation: a review of its current extent, risks, and implications. Endocr Rev 31:756–773. https://doi.org/10.1210/er.2010-0003

    Article  Google Scholar 

  • Steinhauser G, Merz S, Kübber-Heiss A, Katzlberger C (2012) Using animal thyroids as ultra-sensitive biomonitors for environmental radioiodine. Environ Sci Technol 46(23):12890–12894. https://doi.org/10.1021/es303280g

    Article  CAS  Google Scholar 

  • Taskaev AI, Landa ER, Guryev DV, Butler NG, Kraemer TF (2003) Vodnyi: a long-term, low-level radiation exposure field site in Russia. Jpn J Health Phys 38:332–343. https://doi.org/10.5453/jhps.38.332

    Article  CAS  Google Scholar 

  • Tkachev AV (1970) Aspects of radiation affection of thyroid gland. Review of Doctor Biol. Sci. Degree Thesis. Leningrad, 30 pp. (in Russian)

  • UNSCEAR (United Nations Scientific Committee on the Effect of Atomic Radiation) (2010) Sources and Effects of Ionizing Radiation. Report to the General Assembly with Scientific Annexes. 1. United Nations, New York.

  • VanMiddlesworth L, Handl J (1997) 129I, 131I and 127I in animal thyroids after the Chernobyl nuclear accident. Health Phys 73(4):647–650. https://doi.org/10.1097/00004032-199710000-00010

    Article  CAS  Google Scholar 

  • Verger P, Catelinois O, Tirmarche M, Chérié-Challine L, Pirard P, Colonna M, Hubert P (2003) Thyroid cancers in France and the Chernobyl accident: risk assessment and recommendations for improving epidemiological knowledge. Health Phys 85:323–329. https://doi.org/10.1097/00004032-200309000-00008

    Article  CAS  Google Scholar 

  • Voitkevich АА (1967) Neuro-endocrine disintegration during the radiation sickness. Newsletter Acad Med USSR 12:5–14 (in Russian)

    Google Scholar 

  • Whitehead A (2014) Evolutionary genomics of environmental pollution. In: Landry C, Aubin-Horth N (eds) Ecological Genomics. Advances in Experimental Medicine and Biology, p 781. https://doi.org/10.1007/978-94-007-7347-9_16

    Chapter  Google Scholar 

  • Yarmonenko SP, Wainson AA (2004) Radiobiology of Humans and Animals, Moscow. Visshaya Shkola, 549 p (in Russian)

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Acknowledgements

We would like to express our sincere gratitude to Lyudmila Batura, laboratory assistant, Radioecology Department, Institute of Biology, Komi Science Center, Ural Branch, Russian Academy of Sciences, for her assistance in the preparation of histological drugs.

Funding

The study was carried out within the framework of the Ministry of Science and Higher Education project of the Institute of Biology of Komi Science Center of the Ural Branch of the Russian Academy of Science “The effect of ionizing radiation and factors of non-radiation nature on biological objects and biogenic migration of heavy natural radionuclides” (number 122040600024-5).

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All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Olga Еrmakova and Оksana Raskosha. Preparation of the initial draft was carried out by Olga Еrmakova. All authors read, edited, and agreed to the published version of the manuscript.

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Correspondence to Оksana Raskosha.

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All animals were kept in a vivarium in the scientific collection of experimental animals of the Institute of Biology of the Komi Scientific Center, the Ural Branch of the Russian Academy of Sciences (http://www.ckp-rf.ru/usu/471933/), in accordance with the “Regulations on the vivarium of experimental animals” (Protocol no. 1 dated January 24, 2017), complying sanitary-hygienic and bioethical requirements. The work with animals was carried out in accordance with the requirements of Directive 2010/63/EU of the European Parliament on Protection of Animals Used for Scientific Purposes.

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Еrmakova, O., Raskosha, О. Changes in the structural and functional state of the thyroid gland of small mammals when exposed to low-intensity chronic radiation. Environ Sci Pollut Res 31, 34170–34183 (2024). https://doi.org/10.1007/s11356-024-33504-6

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