{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,31]],"date-time":"2026-10-31T19:12:40Z","timestamp":1793473960284,"version":"4.5.0"},"reference-count":60,"publisher":"Radiation Research Society","issue":"3","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Radiation Research"],"published-print":{"date-parts":[[2020,12,21]]},"abstract":"<jats:p>The effects of radiation exposure on germ cells and the gonads have been well studied at acute high-dose exposures, but the effects of chronic low-dose-rate (LDR) irradiation, particularly relevant for radiation protection, on germ cells and the gonads are largely unknown. Our previous study revealed that chronic exposure of mice to medium-dose-rate (MDR, 200 or 400 mGy\/day) gamma-rays in utero for the entire gestation period (18 days) induced only a mild degree of general growth retardation, but with very drastic effects on the gonads and germ cells. In the current study, we further investigated the histomorphological changes in the gonads and the number of germ cells from gestation day (GD) 18 fetuses irradiated with MDR throughout the entire gestation period. The germ cells in the testes and ovaries of the MDR-irradiated fetuses were almost obliterated. Gestation day 18 fetuses exposed to LDR (20 mGy\/day) radiation for the entire gestation period showed decreases in the number of the germ cells, which were not statistically significant or only marginally significant at most. Further investigations on the effects of LDR irradiation in utero using more sensitive methods are necessary.<\/jats:p>","DOI":"10.1667\/rade-20-00093.1","type":"journal-article","created":{"date-parts":[[2021,2,19]],"date-time":"2021-02-19T14:47:29Z","timestamp":1613746049000},"page":"235-243","source":"Crossref","is-referenced-by-count":5,"title":["Effects of Continuous In Utero Low- and Medium-Dose-Rate Gamma-Ray Exposure on Fetal Germ Cells"],"prefix":"10.1667","volume":"195","author":[{"given":"Rei","family":"Nakahira","sequence":"first","affiliation":[{"name":"Departments of Radiobiology"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yoshiko","family":"Ayabe","sequence":"additional","affiliation":[{"name":"Departments of Radioecology, Institute for Environmental Sciences, 1-7, Ienomae, Obuchi, Rokkasho, Kamikita, Aomori, 039-3212, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ignacia","family":"Braga-Tanaka","sequence":"additional","affiliation":[{"name":"Departments of Radiobiology"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Satoshi","family":"Tanaka","sequence":"additional","affiliation":[{"name":"Departments of Radiobiology"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jun-Ichiro","family":"Komura","sequence":"additional","affiliation":[{"name":"Departments of Radiobiology"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1243","reference":[{"key":"34","doi-asserted-by":"crossref","unstructured":"IB Tanaka, S Tanaka, K Ichinohe, et al.  \"Radiat Res.\"  167, \"Cause of death and neoplasia in mice continuously exposed to very low dose rates of gamma rays.\" 417 (2007)","DOI":"10.1667\/RR0728.1"},{"key":"58","doi-asserted-by":"crossref","unstructured":"A Berger, A Ziv-Gal, J Cudiamat, et al.  \"Reprod Toxicol.\"  60, \"The effects of in utero bisphenol A exposure on the ovaries in multiple generations of mice.\" 39 (2016)","DOI":"10.1016\/j.reprotox.2015.12.004"},{"key":"25","doi-asserted-by":"crossref","unstructured":"HE Chemes, RA Rey, M Nistal, et al.  \"J Clin Endocrinol Metab.\"  93, \"Physiological androgen insensitivity of the fetal, neonatal, and early infantile testis is explained by the ontogeny of the androgen receptor expression in Sertoli cells.\" 4408 (2008)","DOI":"10.1210\/jc.2008-0915"},{"key":"39","unstructured":"et al.  \"R: A language and environment for statistical computing.\"  ,  (2019)"},{"key":"35","doi-asserted-by":"crossref","unstructured":"S Tanaka, IB Tanaka, S Sasagawa, et al.  \"Radiat Res.\"  160, \"No lengthening of life span in mice continuously exposed to gamma rays at very low dose rates.\" 376 (2003)","DOI":"10.1667\/RR3042"},{"key":"3","doi-asserted-by":"crossref","unstructured":"DL Preston, H Cullings, A Suyama, et al.  \"J Natl Cancer Inst.\"  100, \"Solid cancer incidence in atomic bomb survivors exposed in utero or as young children.\" 428 (2008)","DOI":"10.1093\/jnci\/djn045"},{"key":"8","doi-asserted-by":"crossref","unstructured":"S Sreetharan, C Thome, S Tharmalingam, et al.  \"Radiat Res.\"  187, \"Ionizing radiation exposure during pregnancy: Effects on postnatal development and life.\" 647 (2017)","DOI":"10.1667\/RR14657.1"},{"key":"31","doi-asserted-by":"crossref","unstructured":"I Adriaens, J Smitz, P Jacquet,  \"Hum Reprod Update.\"  15, \"The current knowledge on radiosensitivity of ovarian follicle development stages.\" 359 (2009)","DOI":"10.1093\/humupd\/dmn063"},{"key":"44","doi-asserted-by":"crossref","unstructured":"BF Kimler, SM Briley, BW Johnson, et al.  \"Reproduction.\"  155, \"Radiation-induced ovarian follicle loss occurs without overt stromal changes.\" 553 (2018)","DOI":"10.1530\/REP-18-0089"},{"key":"23","doi-asserted-by":"crossref","unstructured":"PJ O'Shaughnessy, L Willerton, PJ Baker,  \"Biol Reprod.\"  66, \"Changes in Leydig cell gene expression during development in the mouse.\" 966 (2002)","DOI":"10.1095\/biolreprod66.4.966"},{"key":"2","doi-asserted-by":"crossref","unstructured":"R Wakeford  and MP Little  \"Int J Radiat Biol.\"  79, \"Risk coefficients for childhood cancer after intrauterine irradiation: a review.\" 293 (2003)","DOI":"10.1080\/0955300031000114729"},{"key":"4","doi-asserted-by":"crossref","unstructured":"RE. Shore,  \"Int Congr Ser.\"  1236, \"Gaps in the epidemiology of in utero radiation-exposure effects.\" 13 (2002)","DOI":"10.1016\/S0531-5131(01)00782-8"},{"key":"5","doi-asserted-by":"crossref","unstructured":"T Verreet, M Verslegers, R Quintens, et al.  \"Neural Plast.\"  2016, \"Current evidence for developmental, structural, and functional brain defects following prenatal radiation exposure.\" 1243527 (2016)","DOI":"10.1155\/2016\/1243527"},{"key":"6","doi-asserted-by":"crossref","unstructured":"PU Devi  and R Baskar  \"Int J Radiat Biol.\"  70, \"Influence of gestational age at exposure on the prenatal effects of gamma-radiation.\" 45 (1996)","DOI":"10.1080\/095530096145319"},{"key":"7","doi-asserted-by":"crossref","unstructured":"SH Kim, SR Kim, YS Lee, et al.  \"J Vet Sci.\"  2, \"Influence of gestational age at exposure on the prenatal effects of gamma-radiation.\" 37 (2001)","DOI":"10.4142\/jvs.2001.2.1.37"},{"key":"9","doi-asserted-by":"crossref","unstructured":"S. Sasaki,  \"J Radiat Res.\"  32, \"Influence of the age of mice at exposure to radiation on life-shortening and carcinogenesis.\" S73 (1991)","DOI":"10.1269\/jrr.32.SUPPLEMENT2_73"},{"key":"10","doi-asserted-by":"crossref","unstructured":"CJ Coppenger  and SO Brown  \"Radiat Res.\"  31, \"The gross manifestations of continuous gamma irradiation on the prenatal rat.\" 230 (1967)","DOI":"10.2307\/3572323"},{"key":"11","doi-asserted-by":"crossref","unstructured":"KCM Gulay, IB Tanaka, J Komura, et al.  \"Radiat Res.\"  189, \"Effects of continuous gamma-ray exposure in utero in B6C3F1 mice on gestation day 18 and at 10 weeks of age.\" 425 (2018)","DOI":"10.1667\/RR14863.1"},{"key":"12","unstructured":"et al.  \"Summary of low-dose radiation effects on health, United Nations Scientific Committee on the Effects of Atomic Radiation. 2010 Report.\"  ,  (2011)"},{"key":"13","doi-asserted-by":"crossref","unstructured":"A Wdowiak, M Skrzypek, M Stec, et al.  \"Ann Agric Environ Med.\"  26, \"Effect of ionizing radiation on the male reproductive system.\" 210 (2019)","DOI":"10.26444\/aaem\/106085"},{"key":"14","doi-asserted-by":"crossref","unstructured":"M Skrzypek, A Wdowiak, L Panasiuk, et al.  \"Ann Agric Environ Med.\"  26, \"Effect of ionizing radiation on the female reproductive system.\" 606 (2019)","DOI":"10.26444\/aaem\/112837"},{"key":"15","doi-asserted-by":"crossref","unstructured":"EM Eddy, JM Clark, D Gong,  \"Gamate Res.\"  4, \"Origin and migration of primordial germ cells in mammals.\" 333 (1981)","DOI":"10.1002\/mrd.1120040407"},{"key":"17","doi-asserted-by":"crossref","unstructured":"A. McLaren,  \"Mol Cell Endocrinol.\"  163, \"Germ and somatic cell lineages in the developing gonad.\" 3 (2000)","DOI":"10.1016\/S0303-7207(99)00234-8"},{"key":"18","doi-asserted-by":"crossref","unstructured":"MS Mortensen, MG Gundgaard, G Daugaard,  \"Int J Androl.\"  34, \"Treatment options for carcinoma in situ testis.\" e32 (2011)","DOI":"10.1111\/j.1365-2605.2011.01178.x"},{"key":"19","doi-asserted-by":"crossref","unstructured":"JI Delic, JH Hendry, ID Morris, et al.  \"Radiother Oncol.\"  5, \"Leydig cell function in the pubertal rat following local testicular irradiation.\" 29 (1986)","DOI":"10.1016\/S0167-8140(86)80006-8"},{"key":"20","doi-asserted-by":"crossref","unstructured":"JI Delic, JH Hendry, ID Morris, et al.  \"J Androl.\"  7, \"Dose and time relationships in the endocrine response of the irradiated adult rat testis.\" 32 (1986)","DOI":"10.1002\/j.1939-4640.1986.tb00864.x"},{"key":"21","unstructured":"JI Delic, JH Hendry, ID Morris, et al.  \"Br J Cancer Suppl.\"  7, \"Serum androgen binding protein and follicle stimulating hormone as indices of Sertoli cell function in the irradiated testis.\" 105 (1986)"},{"key":"22","doi-asserted-by":"crossref","unstructured":"KC Belling, M Tanaka, MD Dalgaard, et al.  \"Reprod Biol Endocrinol.\"  11, \"Transcriptome profiling of mice testes following low dose irradiation.\" 50 (2013)","DOI":"10.1186\/1477-7827-11-50"},{"key":"24","doi-asserted-by":"crossref","unstructured":"PJ O'Shaughnessy, PJ Baker, H Johnston,  \"Int J Androl.\"  29, \"The foetal Leydig cell \u2013 differentiation, function and regulation.\" 90 (2006)","DOI":"10.1111\/j.1365-2605.2005.00555.x"},{"key":"26","doi-asserted-by":"crossref","unstructured":"C Ronnback, B Henricson, A Nilsson,  \"Acta Radiol Suppl.\"  310, \"Effect of different doses of 90Sr on the ovaries of the foetal mouse.\" 200 (1971)","DOI":"10.1080\/05678067109171805"},{"key":"27","doi-asserted-by":"crossref","unstructured":"RP Jensh  and RL Brent  \"Radiat Res.\"  116, \"The effects of prenatal X irradiation on the appearance of reflexes and physiologic markers in the neonatal rat.\" 416 (1988)","DOI":"10.2307\/3577385"},{"key":"28","doi-asserted-by":"crossref","unstructured":"HM. Beaumont,  \"Int J Radiat Biol Relat Stud Phys Chem Med.\"  3, \"Radiosensitivity of oogonia and oocytes in the foetal rat.\" 59 (1961)","DOI":"10.1080\/09553006114550071"},{"key":"29","doi-asserted-by":"crossref","unstructured":"HM. Beaumont,  \"Int J Radiat Biol Relat Stud Phys Chem Med.\"  4, \"The radiosensitivity of germ-cells at various stages of ovarian development.\" 581 (1962)","DOI":"10.1080\/09553006214550391"},{"key":"30","doi-asserted-by":"crossref","unstructured":"RP Vergouwen, R Huiskamp, RJ Bas, et al.  \"Radiat Res.\"  141, \"Radiosensitivity of testicular cells in the fetal mouse.\" 66 (1995)","DOI":"10.2307\/3579091"},{"key":"32","doi-asserted-by":"crossref","unstructured":"U Eichenlaub-Ritter, ID Adler, A Carere, et al.  \"Environ Res.\"  104, \"Gender differences in germ-cell mutagenesis and genetic risk.\" 22 (2007)","DOI":"10.1016\/j.envres.2006.10.002"},{"key":"33","doi-asserted-by":"crossref","unstructured":"RE. Shore,  \"Health Phys.\"  97, \"Low-dose radiation epidemiology studies: status and issues.\" 481 (2009)","DOI":"10.1097\/HP.0b013e3181ab98d9"},{"key":"36","doi-asserted-by":"crossref","unstructured":"T Yamada, M Hara, Y Ohba, et al.  \"Jikken Dobutsu.\"  34, \"Studies on implantation traces in rats. I. Size, observation period and staining. (Article in Japanese).\" 17 (1985)","DOI":"10.1538\/expanim1978.34.1_17"},{"key":"37","doi-asserted-by":"crossref","unstructured":"F Lopes, R Smith, S Nash, et al.  \"Mol Hum Reprod.\"  22, \"Irinotecan metabolite SN38 results in germ cell loss in the testis but not in the ovary of prepubertal mice.\" 745 (2016)","DOI":"10.1093\/molehr\/gaw051"},{"key":"38","doi-asserted-by":"crossref","unstructured":"E Smart, F Lopes, S Rice, et al.  \"Sci Rep.\"  8, \"Chemotherapy drugs cyclophosphamide, cisplatin and doxorubicin induce germ cell loss in an in vitro model of the prepubertal testis.\" 1773 (2018)","DOI":"10.1038\/s41598-018-19761-9"},{"key":"40","doi-asserted-by":"crossref","unstructured":"JJ. Chen,  \"Developmental and reproductive toxicity: A practical approach.\"  , \"Statistical analysis for developmental and reproductive toxicologists.\" 697 (2006)","DOI":"10.1201\/9781420040548.ch17"},{"key":"41","doi-asserted-by":"crossref","unstructured":"MS Golub  and CA Sobin  \"Neurotoxicol Teratol.\"  77, \"Statistical modeling with litter as a random effect in mixed models to manage \u201cintralitter likeness\u201d.\" 106841 (2020)","DOI":"10.1016\/j.ntt.2019.106841"},{"key":"42","doi-asserted-by":"crossref","unstructured":"G Liu, P Gong, H Zhao, et al.  \"Radiat Res.\"  165, \"Effect of low-level radiation on the death of male germ cells.\" 379 (2006)","DOI":"10.1667\/RR3528.1"},{"key":"43","doi-asserted-by":"crossref","unstructured":"JB Kerr, L Brogan, M Myers, et al.  \"Reproduction.\"  143, \"The primordial follicle reserve is not renewed after chemical or gamma-irradiation mediated depletion.\" 469 (2012)","DOI":"10.1530\/REP-11-0430"},{"key":"46","unstructured":"et al.  \"Annals of the International Commission on Radiological Protection. Publication 118: ICRP statement on tissue reactions\/early and late effects of radiation in normal tissues and organs\u2013threshold doses for tissue reactions in a radiation protection context.\"  ,  (2012)"},{"key":"47","doi-asserted-by":"crossref","unstructured":"G Pinon-Lataillade, MC Viguier-Martinez, AM Touzalin, et al.  \"Reprod Nutr Dev.\"  31, \"Effect of an acute exposure of rat testes to gamma rays on germ cells and on Sertoli and Leydig cell functions.\" 617 (1991)","DOI":"10.1051\/rnd:19910602"},{"key":"48","doi-asserted-by":"crossref","unstructured":"AN Viswanathan, LJ Lee, JR Eswara, et al.  \"Cancer.\"  120, \"Complications of pelvic radiation in patients treated for gynecologic malignancies.\" 3870 (2014)","DOI":"10.1002\/cncr.28849"},{"key":"49","doi-asserted-by":"crossref","unstructured":"W Wang, KS Hafner, JA Flaws,  \"Toxicol Appl Pharmacol.\"  276, \"In utero bisphenol A exposure disrupts germ cell nest breakdown and reduces fertility with age in the mouse.\" 157 (2014)","DOI":"10.1016\/j.taap.2014.02.009"},{"key":"52","doi-asserted-by":"crossref","unstructured":"U Luderer, MB Myers, M Banda, et al.  \"Reprod Toxicol.\"  69, \"Ovarian effects of prenatal exposure to benzo[a]pyrene: Roles of embryonic and maternal glutathione status.\" 187 (2017)","DOI":"10.1016\/j.reprotox.2017.03.001"},{"key":"53","doi-asserted-by":"crossref","unstructured":"NJ Camlin, AP Sobinoff, JM Sutherland, et al.  \"Biol Reprod.\"  94, \"Maternal smoke exposure impairs the long-term fertility of female offspring in a murine model.\" 39 (2016)","DOI":"10.1095\/biolreprod.115.135848"},{"key":"54","doi-asserted-by":"crossref","unstructured":"PB Comish, AL Drumond, HL Kinnell, et al.  \"PLoS One.\"  9, \"Fetal cyclophosphamide exposure induces testicular cancer and reduced spermatogenesis and ovarian follicle numbers in mice.\" e93311 (2014)","DOI":"10.1371\/journal.pone.0093311"},{"key":"55","doi-asserted-by":"crossref","unstructured":"M Rossitto, M Ollivier, S D\u00e9jardin, et al.  \"Commun Biol.\"  2, \"In utero exposure to acetaminophen and ibuprofen leads to intergenerational accelerated reproductive aging in female mice.\" 310 (2019)","DOI":"10.1038\/s42003-019-0552-x"},{"key":"56","doi-asserted-by":"crossref","unstructured":"PA Fowler, NJ Dora, H McFerran, et al.  \"Mol Hum Reprod.\"  14, \"In utero exposure to low doses of environmental pollutants disrupts fetal ovarian development in sheep.\" 269 (2008)","DOI":"10.1093\/molehr\/gan020"},{"key":"57","doi-asserted-by":"crossref","unstructured":"MC Lutterodt, KP Sorensen, KB Larsen, et al.  \"Hum Reprod.\"  24, \"The number of oogonia and somatic cells in the human female embryo and fetus in relation to whether or not exposed to maternal cigarette smoking.\" 2558 (2009)","DOI":"10.1093\/humrep\/dep226"},{"key":"60","doi-asserted-by":"crossref","unstructured":"Y Nitta, K Kamiya, K Yokoro,  \"J Radiat Res.\"  33, \"Carcinogenic effect of in utero 252Cf and 60Co irradiation in C57BL\/6N x C3H\/He F1 (B6C3F1) mice.\" 319 (1992)","DOI":"10.1269\/jrr.33.319"},{"key":"16","doi-asserted-by":"crossref","unstructured":"M Ginsburg, MH Snow, A McLaren,  \"Development.\"  110, \"Primordial germ cells in the mouse embryo during gastrulation.\" 521 (1990)","DOI":"10.1242\/dev.110.2.521"},{"key":"50","doi-asserted-by":"crossref","unstructured":"S Mahalingam, L Ther, L Gao, et al.  \"Reprod Toxicol.\"  74, \"The effects of in utero bisphenol A exposure on ovarian follicle numbers and steroidogenesis in the F1 and F2 generations of mice.\" 150 (2017)","DOI":"10.1016\/j.reprotox.2017.09.013"},{"key":"51","doi-asserted-by":"crossref","unstructured":"C Zhou, L Gao, JA Flaws,  \"Toxicol Appl Pharmacol.\"  318, \"Prenatal exposure to an environmentally relevant phthalate mixture disrupts reproduction in F1 female mice.\" 49 (2017)","DOI":"10.1016\/j.taap.2017.01.010"},{"key":"1","doi-asserted-by":"crossref","unstructured":"M Otake  and WJ Schull  \"Int J Radiat Biol.\"  74, \"Radiation-related brain damage and growth retardation among the prenatally exposed atomic bomb survivors.\" 159 (1998)","DOI":"10.1080\/095530098141555"},{"key":"45","doi-asserted-by":"crossref","unstructured":"M Saitou  and M Yamaji  \"Cold Spring Harb Perspect Biol.\"  4, \"Primordial germ cells in mice.\" a008375 (2012)","DOI":"10.1101\/cshperspect.a008375"},{"key":"59","doi-asserted-by":"crossref","unstructured":"N Narendran, L Luzhna, O Kovalchuk,  \"Front Genet.\"  10, \"Sex difference of radiation response in occupational and accidental exposure.\" 260 (2019)","DOI":"10.3389\/fgene.2019.00260"}],"container-title":["Radiation Research"],"original-title":[],"deposited":{"date-parts":[[2026,10,31]],"date-time":"2026-10-31T10:03:18Z","timestamp":1793440998000},"score":1,"resource":{"primary":{"URL":"https:\/\/bioone.org\/journals\/radiation-research\/volume-195\/issue-3\/RADE-20-00093.1\/Effects-of-Continuous-In-Utero-Low--and-Medium-Dose\/10.1667\/RADE-20-00093.1.full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,12,21]]},"references-count":60,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2021,3,1]]}},"URL":"https:\/\/doi.org\/10.1667\/rade-20-00093.1","relation":{},"ISSN":["0033-7587","1938-5404"],"issn-type":[{"value":"0033-7587","type":"print"},{"value":"1938-5404","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,12,21]]}}}