Effect of ionizing radiation on the female reproductive system
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Department of Clinical Dietetics, Faculty of Health Sciences, Medical University, Lublin, Poland
Diagnostic Techniques Unit, Faculty of Health Sciences, Medical University, Lublin, Poland
Institute of Rural Health, Lublin, Poland
Prof. W. Orłowski Independent Public Clinical Hospital / Medical Center for Postgraduate Education, Warsaw, Poland
Michal Skrzypek   

Department of Clinical Dietetics, Faculty of Health Sciences, Medical University of Lublin
Ann Agric Environ Med. 2019;26(4):606–616
Introduction and objective:
The tendency towards postponement of maternity implies a greater exposure of female germ cells to damaging environmental effects, including ionizing radiation (IR). Progress in paediatric oncology, based on the use of radiotherapy, also implies the occurrence of gonadal dysfunctions and subsequent female fertility disorders. Therefore, it seems justifiable to systematize the state of knowledge concerning the effect of IR on the female reproductive system.

Brief description of the state of knowledge:
A considerable part of studies concerning the effect of IR on female germ cells have been conducted on animals. Their extrapolation to humans is hindered because in animal studies high acute exposures are applied, which do not reflect human environmental exposures characterized by chronic low dose exposure. Studies on animals provide a heterogenous image, which hinders the formulation of unequivocal conclusions and indicates that radiosensitivity depends, i.a. on IR dose, stage of development of oocytes, the applied marker of the effects of IR, or on the species. LD50 of human oocytes is estimated to be below 2 Gy. The effect of IR depends, i.a. on the dose fractionation and the age (older women are more radiosensitive). In females, the effective sterilizing dose is: at birth 20.3 Gy, at 10 years 18.4 Gy, at 20 years 16.5 Gy, whereas at 30 years 14.3 Gy, which is associated with the available pool of ovarian follicles.

Within the range of low doses received as a result of environmental exposure to IR, there is no evidence for the occurrence of either adverse pregnancy outcomes, nor fertility disorders in females. These effects may be related to the cancer radiotherapy, or exposure to high IR doses during nuclear accidents.

Cadet J, Davies KJA. Oxidative DNA damage & repair: An introduction. Free Radic Biol Med. 2017; 107: 2–12. DOI: 10.1016/j.freeradbiomed.2017.03.030.
Sankaranarayanan K, Wassom JS. Ionizing radiation and genetic risks XIV. Potential research directions in the post-genome era based on knowledge of repair of radiation-induced DNA double-strand breaks in mammalian somatic cells and the origin of deletions associated with human genomic disorders. Mutat Res. 2005; 578(1–2): 333–370. DOI: 10.1016/j.mrfmmm.2005.06.020.
Agarwal A, Parekh N, Panner Selvam MK, Henkel R, Shah R, Homa ST, et al. Male Oxidative Stress Infertility (MOSI): Proposed Terminology and Clinical Practice Guidelines for Management of Idiopathic Male Infertility. World J Mens Health. 2019; 37(3): 396–312. DOI: 10.5534/wjmh.190055.
Wdowiak A, Bakalczuk G, Bakalczuk S. Evaluation of effect of selected trace elements on dynamics of sperm DNA fragmentation. Post Hig Med Dosw. 2015; 69: 1405–1410.
Wdowiak A, Wiktor H, Wdowiak L. Maternal passive smoking during pregnancy and neonatal health. Ann Agric Environ Med. 2009; 16(2): 309–312.
Wdowiak A, Lewicka M, Plewka K, Bakalczuk G. Nicotinism and quality of embryos obtained in in-vitro fertilization programmes. Ann Agric Environ Med. 2013; 20(1): 82–85. DOI: 10.26444/aaem/75422.
Michalak A, Krzeszowiak J, Markiewicz-Górka I. The correlations between aging of the human body, oxidative stress and reduced efficiency of repair systems. Post Hig Med Dosw. 2014; 68: 1483–1491.
Wdowiak A, Mazurek PA, Wdowiak A, Bojar I. Effect of electromagnetic waves on human reproduction. Ann Agric Environ Med. 2017: 24(1): 13–18. DOI: 10.5604/12321966.1228394.
Wdowiak A, Skrzypek M, Stec M, Panasiuk L. Effect of ionizing radiation on the male reproductive system. Ann Agric Environ Med. 2019; 26(2): 210–216. DOI: 10.26444/aaem/106085.
Skrzypek M, Wdowiak A, Marzec A. Application of dietetics in reproductive medicine. Ann Agric Environ Med. 2017; 24(4): 559–565. DOI: 10.26444/aaem/76997.
Stańczak J, Cierniak-Piotrowska M, Stelmach K, Znajewska A. [Demographic situation in Poland up to 2017. Births and fertility]. Warszawa: Zakład Wydawnictw Statystycznych; 2018. p. 12–13. [In Polish].
Stańczak J, Znajewska A. [Population. Size and structure and vital statistics in Poland by territorial division in 2018. As of December, 31]. Warszawa: Zakład Wydawnictw Statystycznych; 2019. p. 12. [In Polish].
Sawicka M. [Maternity is mostly associated with young women]. Rodzina w czasach szybkich przemian, Roczniki Socjologii Rodziny. Poznań: Adam Mickiewicz University Press; 2001. p. 245–257. [In Polish].
Szukalski P. [Demography and social gerontology – information bulletin]. 2012; 6: 1–4. Available fom: (access: 2019.07.07). [In Polish].
Dutreix J, Wambersie A. Introduction to radiobiology. Tailor&Praxis, London, New York, 1990.
Marci R, Mallozzi M, Di Benedetto L, Schimberni M, Mossa S, Soave I, et al. Radiations and female fertility. Reprod Biol Endocrinol. 2018; 16(1): 112. DOI: 10.1186/s12958-018-0432-0.
Shahbazi MN, Siggia ED, Zernicka-Goetz M. Self-organization of stem cells into embryos: A window on early mammalian development. Science. 2019; 364(6444): 948–951. DOI: 10.1126/science.aax0164.
Richardson BE, Lehmann R. Mechanisms guiding primordial germ cell migration: strategies from different organisms. Nat Rev Mol Cell Biol. 2010; 11(1): 37–49. DOI: 10.1038/nrm2815.
Grygoruk C, Sieczyński P, Ratomski K, Grusza M, Mrugacz G. [Select aspects of oogenesis and folliculogenesis]. Studia Medyczne. 2013; 29(2): 199–202. [In Polish].
Baker T.G. Comparative aspects of the effects of radiation during oogenesis. Mutat Res. 1971; 11: 9–22. DOI: 10.1016/0027-5107(71)90028-5.
Adler ID, Carere A, Eichenlaub-Ritter U, Pacchierotti F. Gender differences in the induction od chromosomal aberrations and gene mutations in rodent germ cells. Environ Res. 2007; 104: 37–45. DOI: 10.1016/j.envres.2006.10.002.
Krajewski P. [Biological effects of ionizing radiation]. Warsaw: Central Laboratory for Radiological Protection, Faculty of Physics, Warsaw University of Technology; 2009. Available from: (access: 2019.01.24). [In Polish].
Valerie K, Povirk LF. Regulation and mechanisms of mammalian double-strand break repair. Oncogene. 2003; 22(37): 5792–5812. DOI: 10.1038/sj.onc.1206679.
Pampfer S, Streffer C. Increased chromosome aberration levels in cells from mouse fetuses after zygote x-irradiation. Int J Radiat Biol. 1989; 55(1): 85–92.
Goedecke W, Eijpe M, Offenberg HH, van Aalderen M, Heyting C. Mre11 and Ku70 interact in somatic cells, but are differentially expressed in early meiosis. Nat Genet. 1999; 23(2): 194–198. DOI: 10.1038/13821.
Hamer G, Roepers-Gajadien HL, van Duyn-Goedhart A, Gademan IS, Kal HB, van Buul PP, et al. Function of DNA-protein kinase catalytic subunit during the early meiotic prophase without Ku70 and Ku86. Biol Reprod. 2003; 68(3): 717–721. DOI: 10.1095/biolreprod.102.008920.
Cox BD, Lyon MF. X-ray induced dominant lethal mutations in mature and immature oocytes of guinea-pigs and golden hamsters. Mutat Res. 1975; 28: 421–436. DOI: 10.1016/0027-5107(75)90236-5.
Tease C. Dose-related chromosome non-disjunction in female mice after x-irradiation of dictyate oocytes. Mutat Res. 1985; 151: 109–119. DOI: 10.1016/0027-5107(85)90189-7.
Caine A, Lyon MF. The induction of chromosome aberrations in mouse dictyate oocytes by X-rays and chemical mutagens. Mutat Res. 1977; 45, 325–331. DOI: 10.1016/0165-1110(92)90037-A.
Kirk M, Lyon MF. Induction of congenital anomalies in offspring of female mice exposed to varying doses of X-rays. Mutat Res. 1982; 106: 73–83. DOI: 10.1016/0027-5107(82)90191-9.
Griffin CS, Tease C, Fisher G. The effect of low-dose x-irradiation on numerical and structural chromosome anomaly induction in mouse immature oocytes. Mutat Res. 1990; 231: 137–142. DOI: 10.1016/0027-5107(90)90020-5.
Jacquet P, Buset J, Neefs M, Vankerkom J, Benotmane MA, Derradji H, et al. Transgenerational developmental effects and genomic instability after x-irradiation of preimplantation embryos: Studies on two mouse strains. Mutat Res. 2010; 687: 54–62. DOI: 10.1016/j.mrfmmm.2010.01.013.
Jacquet P, Buset J, Vankerkom J, Baatout S, de Saint-Georges L, Baugnet-Mahieu L, et al. Radiation-induced chromosome aberrations in guinea-pig growing oocytes, and their relation to follicular atresia. Mutat Res. 2001; 473: 249–254. DOI: 10.1016/S0027-5107(00)00153-6.
Johannisson R, Mormel R, Brandenburg B. Synaptonemal complex damage in fetal mouse oocytes induced by ionizing irradiation. Mutat Res. 1994; 311: 319–328. DOI: 10.1016/0027-5107(94)90190-2.
Mikamo K. Meiotic chromosomal radiosensitivity in primary oocytes of the Chinese hamster. Cytogenet Cell Genet. 1982; 33: 88–94. DOI: 10.1159/000131731.
Pan H, O’ Brien MJ, Wigglesworth K, Eppig JJ, Schultz RM. Transcription profiling during mouse oocyte development and the effect of gonadotropin priming and development in vitro. Dev Biol. 2005; 286: 493–506. DOI: 10.1016/j.ydbio.2005.08.023.
Tease C, Fisher G. The influence of maternal age on radiation-induced chromosome aberrations in mouse oocytes. Mutat Res. 1991; 262: 57–62. DOI: 10.1016/0165-7992(91)90107-f.
Tease C, Fisher G. X-ray-induced chromosome aberrations in immediately preovulatory oocytes. Mutat Res. 1986; 173: 211–215. DOI: 10.1016/0165-7992(86)90038-2.
Mavragani VI, Laskaratou DA, Frey B, Candéias SE, Gaip US, Lumniczky K, et al. Key mechanisms involved in ionizing radiation induced systemic effects. A current review. Toxicol Res. 2016; 5: 12. DOI: 10.1039/c5tx00222b.
Smith LE, Nagar S, Kim GJ, Morgan WF. Radiation-induced genomic instability: Radiation quality and dose response. Health Phys. 2003; 85: 23–29.
Camats N, Garcia F, Parrilla JJ, Calaf, Martin-Mateo M, Caldes MG. The GnRH analogue triptorelin confers ovarian radio-protection to adult female rats. Mutat Res. 2009; 669: 67–79. DOI: 10.1016/j.mrfmmm.2009.05.002.
Morgan WF. Is there a common mechanism underlying genomic instability, bystander effects and other nontargeted effects of exposure to ionizing radiation? Oncogene. 2003; 22: 7094–7099. DOI: 10.1038/sj.onc.1206992.
Nagasava H, Little JB. Induction of sister chromatid exchanges by extremely low doses of a-particles. Cancer Res. 1992; 52: 6394–6396.
Lorimore SA, Coates PJ, Wrihgt EG. Radiation-induced genomic instability and bystander effects: inter-related nontargeted effects of exposure to ionizing radiation. Oncogene. 2003; 22: 7058–7069. DOI: 10.1038/sj.onc.1207044.
Moens PB, Kolas NK, Tarsounas M, Marcon E, Cohen PE, Spyropoulos B. The time course and chromosomal localization of recombination-related proteins at meiosis in the mouse are compatible with models that can resolve the early DNA-DNA interactions without reciprocal recombination. J Cell Sci. 2002; 115: 1611–1622.
Baker SM, Plug AW, Prolla TA, Bronner CE, Harris AC, Yao X, et al. Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over. Nat Genet. 1996; 13: 336–342. DOI: 10.1038/ng0796-336.
Turner JM, Aprelikova O, Xu X, Wang R, Kim S, Chandramouli GV, et al. BRCA1, histone H2AX phosphorylation, and male meiotic sex chromosome inactivation. Curr Biol. 2004; 14: 2135–2142. DOI: 10.1016/j.cub.2004.11.032.
Wallace WH, Thomson AB, Kelsey TW. The radiosensitivity of the human oocyte. Hum Reprod. 2003: 18(1): 117–121. DOI: 10.1093/humrep/deg016.
Wallace WH, Thomson AB, Saran F, Kelsey TW. Predicting age of ovarian failure after radiation to a field that includes the ovaries. Int Radiat Oncol Biol Phys. 2005; 62: 738–744. DOI:10.1016/j.ijrobp.2004.11.038.
Diehn M, Cho RW, Clarke MF. Therapeutic implications of the cancer stem cell hypothesis. Semin Radiat Oncol. 2009; 19: 78–86. DOI: 10.1016/j.semradonc.2008.11.002.
Jacquet P, de Saint-Georges L, Vankerkom J, Baugnet-Mahieu L. Embryonic death, dwarfism and fetal malformations after irradiation of embryos at the zygote stage: Studies on two mouse strains. Mutat Res. 1995; 332: 73–87. DOI: 10.1016/0027-5107(95)00156-4.
Beaumont HM. The effects of acute x-irradiation on primordial germ-cells in the female rat. Int J Radiat Biol Relat Stud Phys Chem Med. 1966; 10: 17–28.
Pujol R, Cusido L, Rubio A, Egozcue J, Garcia M. Effect of X-rays on germ cells in female fetuses of Rattus norvegicus irradiated at three different times of gestation. Mutat Res. 1996: 356: 247–253. DOI: 10.1016/0027-5107(96)00067-X.
Pujol R, Cusido L, Rubio A, Egozcue J, Garcia M. X-ray-induced synaptonemal complex damage during meiotic prophase in female fetuses of Rattus norvegicus. Mutat Res. 1997; 379: 127–134. DOI: 10.1016/s0027-5107(97)00115-2.
Tateno H, Mikamo K. Effects of neonatal ovarian x-irradiation in the Chinese hamster. Correlation between the age of irradiation and the fertility span. J Radiat Res. 1989; 30: 185–190. DOI: 10.1269/jrr.30.209.
Tateno H, Mikamo K. Effects of neonatal ovarian x-irradiation in the Chinese hamster. II. Absence of chromosomal and developmental damages in surviving oocytes irradiated at the pachytene and resting dictyate stages. J Radiat Res. 1989; 30: 209–217. DOI: 10.1269/jrr.30.209.
Tateno H, Mikamo K. Neonatal oocyte development and selective oocyte-killing by X-rays in the Chinese hamster, Cricetulus griseus. Int J Radiat Biol Relat Stud Phys Chem Med. 1984; 45: 139–149.
Jacquet P, de Saint-Georges L, Buset J, Baatout S, Vankerkom J, Baugnet-Mahieu L. Cytogenetic effects of x-rays in the guinea pig female germ cells. II. The maturing oocyte. Mutat Res. 1997; 391: 193–199. DOI: 10.1016/s1383-5718(97)00068-5.
Jacquet P, Vankerkom J, Lambiet-Collier M. The female guinea pig, a useful model for the genetic hazard of radiation in man; preliminary results on germ cell radiosensitivity in foetal, neonatal and adult animals. Int J Radiat Biol. 1994; 65: 357–367. DOI: 10.1080/09553009414550421.
Pils S, Muller WU, Streffer C. Lethal and teratogenic effects in two successive generations of the hlg mouse strain after radiation exposure of zygotes- Association with genomic instability? Mutat Res. 1999; 429: 85–92. DOI: 10.1016/s0027-5107(99)00101-3.
Camats N, Garcia F, Parrilla JJ, Calaf J, Martin-Mateo M, Caldes MG. The GnRH analogue triptorelin confers ovarian radio-protection to adult female rats. Mutat Res. 2009; 669: 67–79. DOI: 10.1016/j.mrfmmm.2009.05.002.
Martinez-Flores I, Egozcue J, Garcia M. Effects on female fertility and germinal cells in prepubertal and adult rats (Rattus norvegicus) after X-ray irradiation. Adv Exp Med Biol. 1998; 444: 215–219. DOI: 10.1007/978-1-4899-0089-0_25.
Martinez-Flores I, Saez C, Egozcue J, Garcia M. Effects of ionizing radiation on oocytes of prepubertally irradiated rats. Int J Radiat Biol. 2000: 76: 1403–1407. DOI: 10.1080/09553000050151682.
Brewen JG, Payne HS, Preston RJ. X-ray-induced chromosome aberrations in mouse dictyate oocytes. I. Time and dose relationships. Mutat Res. 1976; 35: 111–120. DOI: 10.1016/0027-5107(76)90173-1.
Brewen JG, Payne HS. X-ray-induced chromosome aberrations in mouse dictyate oocytes. II. Fractionation and dose rate effects. Genetics. 1977; 87: 699–708.
Hansmann I, Jenderny J, Probeck HD. Nondisjunction and chromosome breakage in mouse oocytes after various X-ray doses. Hum Genet. 1982: 61: 190–192. DOI: 10.1007/bf00296439.
Reichert W, Buselmaier W, Vogel F. Elimination of X-ray-induced chromosomal aberrations in the progeny of female mice. Mutat Res. 1984; 139: 87–94. DOI: 10.1016/0165-7992(84)90109-x.
Reichert W, Hansmann I, Rohrborn G. Chromosome anomalies in mouse oocytes after irradiation. Humangenetik. 1975; 28: 25–38.
Yang F, Wang PJ. The mammalian synaptonemal complex: a scaffold and beyond. Genome Dyn. 2009; 5: 69–80. DOI: 10.1159/000166620.
Dobson MJ, Pearlman RE, Karaiskakis A, Spyropoulos B, Moens PB. Synaptonemal complex proteins: Occurrence, epitope mapping and chromosome disjunction. J Cell Sci. 1994; 107: 2749–2760.
Kouznetsova A, Benavente R, Pastink A, Hoog C. Meiosis in mice without a synaptonemal complex. PLoS One. 2011; 6(12): e2855. DOI: 10.1371/journal.pone.0028255.
Cusido L, Pujol R, Egozcue J, Garcia M. Cyclophosphamide-induced synaptonemal complex damage during meiotic prophase of female Rattus norvegicus. Mutat Res. 1995; 329: 131–141. DOI: 10.1016/0027-5107(95)00029-i.
Allen JW, de Weese GK, Gibson JB, Poorman PA, Moses MJ. Synaptonemal complex damage as a measure of chemical mutagen effects on mammalian germ cells. Mutat Res. 1987; 190: 19–24. DOI: 10.1016/0165-7992(87)90076-5.
Jacquet P, Adriaens I, Buset J, Neefs M, Vankerkom J. Cytogenetic studies in mouse oocytes irradiated in vitro at different stages of maturation, by use of an early preantral follicle culture system. Mutat Res. 2005; 583: 168–177. DOI: 10.1016/j.mrgentox.2005.03.008.
Russell LB, Russell WL. The Sensitivity of Different Stages in Oogenesis to the Radiation Induction of Dominant Lethals and other Changes in the Mouse. In: Mitchell JS, Holmes BE, Smith CC, editors. Progress in Radiobiology. Edinburgh, UK: Oliver and Boyd Ltd.; 1956. p. 187–192.
Russell WL. Effect of the interval between irradiation and conception on mutation frequency in female mice. Proc Natl Acad Sci USA. 1965; 54: 1552–1557. DOI: 10.1073/pnas.54.6.1552.
Kamiguchi Y, Mikamo K. Dose-response relationship for induction of structural chromosome aberrations in Chinese hamster oocytes after x-irradiation. Mutat Res. 1982; 103: 33–37. DOI: 10.1016/0165-7992(82)90083-5.
Edwards RG, Searle AG. Genetic radiosensitivity of specific post-dictyate stages in mouse oocytes. Genet Res. 1963; 4: 389–398. DOI: 10.1017/S0016672300003785.
Mandl AM. The radiosensitivity of oocytes at different stages of maturation. Proc R Soc Lond Ser. 1963; 158: 119–141. DOI: 10.1098/rspb.1963.0038.
Ashwood-Smith MJ, Edwards RG. DNA repair by oocytes. Mol Hum Reprod. 1996; 2: 46–51. DOI: 10.1093/molehr/2.1.46.
Hamatani T, Yamada M, Akutsu H, Kuji N, Mochimaru Y, Takano, M, et al. What can we learn from gene expression profiling of mouse oocytes? Reproduction. 2008; 135: 581–592. DOI: 10.1530/REP-07-0430.
Menezo Y, Russo G, Tosti E, El Mouatassim S, Benkhalifa M. Expression profile of genes coding for DNA repair in human oocytes using pangenomic microarrays, with a special focus on ROS linked decays. J Assist Reprod Genet. 2007; 24: 513–520. DOI: 10.1007/s10815-007-9167-0.
Su YQ, Sugiura K, Woo Y, Wigglesworth K, Kamdar S, Affourtit J, et al. Selective degradation of transcripts during meiotic maturation of mouse oocytes. Dev Biol. 2007; 302: 104–117. DOI: 10.1016/j.ydbio.2006.09.008.
Zheng P, Schramm RD, Latham KE. Developmental regulation and in vitro culture effects on expression of DNA repair and cell cycle checkpoint control genes in rhesus monkey oocytes and embryos. Biol Reprod. 2005; 72: 1359–1369. DOI: 10.1095/biolreprod.104.039073.
Wang S, Kou Z, Jing Z, Zhang Y, Guo X, Dong M, et al. Proteome of mouse oocytes at different developmental stages. Proc Nat Acad Sci USA. 2010; 107: 17639–17644. DOI: 10.1073/pnas.1013185107.
Barber RC, Dubrova YE. The offspring of irradiated parents, are they stable? Mutat Res. 2006; 598: 50–60. DOI: 10.1016/j.mrfmmm.2006.01.009.
Dubrowa YE. Genomic instability in the offspring of irradiated parents: facts and interpretations. Genetika. 2006; 42(10): 1116–1126.
Lűning KG, Frölen H, Nilsson A. Genetic effects of 239Pu salt injections in male mice. Mutat Res. 1976; 34: 539–542.
Morgan WF. Non-targeted and delayed effects of exposure to ionizing radiation: I. Radiation-induced genomic instability and bystander effects in vitro. Radiat Res. 2003; 159(5): 567–580. DOI: 10.1667/0033-7587(2003)159[0567:nadeoe];2.
Morgan WF. Non-targeted and delayed effects of exposure to ionizing radiation: II. Radiation-induced genomic instability and bystander effects in vivo, clastrogenic factors and transgeneratnal effects. Radiat Res. 2003;159(5): 581–596. DOI: 10.1667/0033-7587(2003)159[0581:nadeoe];2.
Dubrova YE, Plumb M, Brown J, Boulton E, Goodhead D, Jeffreys AJ. Induction of minisatellite mutations in the mouse germline by low-dose chronic exposure to gamma-radiation and fission neutrons. Mutat Res. 2000; 453: 17–24. DOI: 10.1016/s0027-5107(00)00068-3.
Shiraishi K, Shimura T, Taga M, Uematsu N, Gondo Y, Ohtaki M, et al. Persistent induction of somatic reversions of the pink-eyed unstable mutation in F1 mice born to fathers irradiated at the spermatozoa stage. Radiat Res. 2002; 157: 661–667. DOI: 10.1667/0033-7587(2002)157[0661:PIOSRO]2.0.CO;2.
Vorobtsova IE. Irradiation of male rats increases the chromosomal sensitivity of progeny to genotoxic agents. Mutagenesis. 2000; 15: 33–38. DOI: 10.1093/mutage/15.1.33.
Abouzeid Ali HE, Barber RC, Dubrova YE. The effects of maternal irradiation during adulthood on mutation induction and transgenerational instability in mice. Mutat Res. 2012; 732: 21–25. DOI: 10.1016/j.mrfmmm.2012.01.003.
Barber RC, Hardwick RJ, Shanks ME, Glen CD, Mughal SK, Voutounou M, et al. The effects of in utero irradiation on mutation induction and transgenerational instability in mice. Mutat Res. 2009; 664: 6–12. DOI: 10.1016/j.mrfmmm.2009.01.011.
Streffer C. Transgenerational transmission of radiation damage: Genomic instability and congenital malformation. J Radiat Res. 2006; 47: 19–24.
Jordan BR. The Hiroshima/Nagasaki survivor studies: discrepancies between results and general perception. Genetics. 2016; 203: 1505–1512. DOI: 10.1534/genetics.116.191759.
Radiation Effects Research Foundation. Birth defects among the children of atomic-bomb survivors (1948–1954) Available from: (access 2019.07.08).
Adriaens I, Smitz J, Jacquet P. The current knowledge on radiosensitivity of ovarian follicle development stages. Hum Reprod Update. 2009; 15: 359–377. DOI: 10.1093/humupd/dmn063.
Gao W, Liang JX, Yan Q. Exposure to radiation therapy is associated with female reproductive health among childhood cancer survivors: a meta-analysis study. J Assist Reprod Genet. 2015; 32(8): 1179–1186. DOI: 10.1007/s10815-015-0490-6.
Blot WJ, Sawada H. Fertility among female survivors of the atomic bombs of Hiroshima and Nagasaki. Am J Hum Genet. 1972; 24: 613–622.
Little J. The Chernobyl accident, congenital anomalies and other reproductive outcomes. Paed Per Epid. 1993; 7: 121–151. DOI: 10.1111/j.1365-3016.1993.tb00388.x.
Dubrova YE, Nesterov VN, Krouchinsky NG, Ostapenko VA, Neumann R, Neil DL, et al. Human minisatellite mutation rate after the Chernobyl accident. Nature. 1996; 380: 683–686. DOI: 10.1038/380683a0.
Wertelecki W, Yevtushok L, Zymak-Zakutnia N, Wang B, Sosyniuk Z, Lapchenko S, et al. Blastopathies and microcephaly in a Chernobyl impacted region of Ukraine. Con Anomalies. 2014; 54: 125–149. DOI: 10.1111/cga.12051.
Doyle P, Maconochie N, Roman E, Davies G, Smith PG, Beral V. Fetal death and congenital malformation in babies born to nuclear industry employees: report from the nuclear industry family study. Lancet. 2000; 356(9238): 1293–1299. DOI: 10.1016/S0140-6736(00)02812-9.