Academic Journal
Comparative cytogenetics of anembryonic pregnancies and missed abortions in human ; Сравнительная цитогенетика анэмбрионии и неразвивающейся беременности у человека
العنوان: | Comparative cytogenetics of anembryonic pregnancies and missed abortions in human ; Сравнительная цитогенетика анэмбрионии и неразвивающейся беременности у человека |
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المؤلفون: | T. V. Nikitina, E. A. Sazhenova, E. N. Tolmacheva, N. N. Sukhanova, S. A. Vasilyev, I. N. Lebedev, Т. В. Никитина, Е. А. Саженова, Е. Н. Толмачева, Н. Н. Суханова, С. А. Васильев, И. Н. Лебедев |
المساهمون: | The study was carried out as part of the state assignment No. 122020300041-7. |
المصدر: | Vavilov Journal of Genetics and Breeding; Том 27, № 1 (2023); 28-35 ; Вавиловский журнал генетики и селекции; Том 27, № 1 (2023); 28-35 ; 2500-3259 ; 2500-0462 ; 10.18699/VJGB-23-01 |
بيانات النشر: | Institute of Cytology and Genetics of Siberian Branch of the RAS |
سنة النشر: | 2023 |
المجموعة: | Vavilov Journal of Genetics and Breeding / Вавиловский журнал генетики и селекции |
مصطلحات موضوعية: | тетраплоидия, missed abortion, miscarriage, karyotype, chromosomal abnormalities, sex chromosomes, triploidy, tetraploidy, неразвивающаяся беременность, невынашивание беременности, кариотип, хромосомные аномалии, половые хромосомы, триплоидия |
الوصف: | Miscarriage is an important problem in human reproduction, affecting 10–15 % of clinically recognized pregnancies. The cases of embryonic death can be divided into missed abortion (MA), for which the ultrasound sign of the embryo death is the absence of cardiac activity, and anembryonic pregnancy (AP) without an embryo in the gestational sac. The aim of this study was to compare the frequency of chromosomal abnormalities in extraembryonic tissues detected by conventional cytogenetic analysis of spontaneous abortions depending on the presence or absence of an embryo. This is a retrospective study of 1551 spontaneous abortions analyzed using GTG-banding from 1990 to 2022 (266 cases of AP and 1285 cases of MA). A comparative analysis of the frequency of chromosomal abnormalities and the distribution of karyotype frequencies depending on the presence of an embryo in the gestational sac was carried out. Statistical analysis was performed using a chi-square test with a p < 0.05 significance level. The total frequency of chromosomal abnormalities in the study was 53.6 % (832/1551). The proportion of abnormal karyotypes in the AP and MA groups did not differ significantly and amounted to 57.1 % (152/266) and 52.9 % (680/1285) for AP and MA, respectively (p = 0.209). Sex chromosome aneuploidies and triploidies were significantly less common in the AP group than in the MA group (2.3 % (6/266) vs 6.8 % (88/1285), p = 0.005 and 4.9 % (13/266) vs 8.9 % (114/1285), p = 0.031, respectively). Tetraploidies were registered more frequently in AP compared to MA (12.4 % (33/266) vs. 8.2 % (106/1285), p = 0.031). The sex ratio among abortions with a normal karyotype was 0.54 and 0.74 for AP and MA, respectively. Thus, although the frequencies of some types of chromosomal pathology differ between AP and MA, the total frequency of chromosomal abnormalities in AP is not increased compared to MA, which indicates the need to search for the causes of AP at other levels of the genome organization, including microstructural chromosomal ... |
نوع الوثيقة: | article in journal/newspaper |
وصف الملف: | application/pdf |
اللغة: | English |
Relation: | https://vavilov.elpub.ru/jour/article/view/3629/1680; Ahern D.T., Bansal P., Faustino I., Kondaveeti Y., Glatt-Deeley H.R., Banda E.C., Pinter S.F. Monosomy X in isogenic human iPSCderived trophoblast model impacts expression modules preserved in human placenta. Proc. Natl. Acad. Sci. USA. 2022;119(40): e2211073119. DOI 10.1073/pnas.2211073119.; Angiolucci M., Murru R., Melis G., Carcassi C., Mais V. Association between different morphological types and abnormal karyotypes in early pregnancy loss. Ultrasound Obstet. Gynecol. 2011;37(2):219-225. DOI 10.1002/uog.7681.; Boss A.L., Chamley L.W., James J.L. Placental formation in early pregnancy: how is the centre of the placenta made? Hum. Reprod. Update. 2018;24(6):750-760. DOI 10.1093/humupd/dmy030.; Cheng H.H., Ou C.Y., Tsai C.C., Chang S.D., Hsiao P.Y., Lan K.C., Hsu T.Y. Chromosome distribution of early miscarriages with present or absent embryos: female predominance. J. Assist. Reprod. Genet. 2014;31(8):1059-1064. DOI 10.1007/s10815-014-0261-9.; Doubilet P.M., Benson C.B., Bourne T., Blaivas M., Society of Radiologists in Ultrasound Multispecialty Panel on Early First Trimester Diagnosis of Miscarriage and Exclusion of a Viable Intrauterine Pregnancy, Barnhart K.T., Benacerraf B.R., Brown D.L., Filly R.A., Fox J.C., Goldstein S.R., Kendall J.L., Lyons E.A., Porter M.B., Pretorius D.H., Timor-Tritsch I.E. Diagnostic criteria for nonviable pregnancy early in the first trimester. N. Engl. J. Med. 2013;369(15): 1443-1451. DOI 10.1056/NEJMra1302417.; Evdokimova V.N., Nikitina T.V., Lebedev I.N., Sukhanova N.N., Nazarenko S.A. About the sex ratio in connection with early embryonic mortality in man. Russ. J. Developmental Biology. 2000;31(4):251-257.; Fan L., Wu J., Wu Y., Shi X., Xin X., Li S., Zeng W., Deng D., Feng L., Chen S., Xiao J. Analysis of chromosomal copy number in first-trimester pregnancy loss using next-generation sequencing. Front. Genet. 2020;11:545856. DOI 10.3389/fgene.2020.545856.; Farquharson R.G., Jauniaux E., Exalto N., ESHRE Special Interest Group for Early Pregnancy (SIGEP). Updated and revised nomenclature for description of early pregnancy events. Hum. Reprod. 2005;20(11):3008-3011. DOI 10.1093/humrep/dei167.; Finley J., Hay S., Oldzej J., Meredith M.M., Dzidic N., Slim R., Aradhya S., Hovanes K., Sahoo T. The genomic basis of sporadic and recurrent pregnancy loss: a comprehensive in-depth analysis of 24,900 miscarriages. Reprod. Biomed. Online. 2022;45(1):125-134. DOI 10.1016/j.rbmo.2022.03.014.; Fu M., Mu S., Wen C., Jiang S., Li L., Meng Y., Peng H. Whole exome sequencing analysis of products of conception identifies novel mutations associated with missed abortion. Mol. Med. Rep. 2018;18(2): 2027-2032. DOI 10.3892/mmr.2018.9201.; Ginsberg N.A., Strom C., Verlinsky Y. Crown-rump lengths in missed miscarriages and trisomy 21. Ultrasound Obstet. Gynecol. 2001; 18(5):488-490. DOI 10.1046/j.0960-7692.2001.00571.x.; Gu C., Li K., Li R., Li L., Li X., Dai X., He Y. Chromosomal aneuploidy associated with clinical characteristics of pregnancy loss. Front. Genet. 2021;12:667697. DOI 10.3389/fgene.2021.667697.; Hardy K., Hardy P.J., Jacobs P.A., Lewallen K., Hassold T.J. Temporal changes in chromosome abnormalities in human spontaneous abortions: results of 40 years of analysis. Am. J. Med. Genet. A. 2016; 170(10):2671-2680. DOI 10.1002/ajmg.a.37795.; Hassold T., Benham F., Leppert M. Cytogenetic and molecular analysis of sex-chromosome monosomy. Am. J. Hum. Genet. 1988;42(4): 534-541.; Huang J., Zhu W., Tang J., Saravelos S.H., Poon L.C.Y., Li T.C. Do specific ultrasonography features identified at the time of early pregnancy loss predict fetal chromosomal abnormality? – A systematic review and meta-analysis. Genes Dis. 2019;6(2):129-137. DOI 10.1016/j.gendis.2018.10.001.; Kolte A.M., Bernardi L.A., Christiansen O.B., Quenby S., Farquharson R.G., Goddijn M., Stephenson M.D. ESHRE Special Interest Group, Early Pregnancy. Terminology for pregnancy loss prior to viability: a consensus statement from the ESHRE early pregnancy special interest group. Hum. Reprod. 2015;30(3):495-498. DOI 10.1093/humrep/deu299.; Larsen E.C., Christiansen O.B., Kolte A.M., Macklon N. New insights into mechanisms behind miscarriage. BMC Med. 2013;11:154. DOI 10.1186/1741-7015-11-154.; Lathi R.B., Mark S.D., Westphal L.M., Milki A.A. Cytogenetic testing of anembryonic pregnancies compared to embryonic missed abortions. J. Assist. Reprod. Genet. 2007;24(11):521-524. DOI 10.1007/s10815-007-9166-1.; Lebedev I.N., Kashevarova A.A., Skryabin N.A., Nikitina T.V., Lopatkina M.E., Melnikov A.A., Sazhenova E.A., Ivanova T.V., Evtushenko I.D. Array-based comparative genomic hybridization (array-CGH) in analysis of chromosomal aberrations and CNV in blighted ovum pregnancies. Zhurnal Akusherstva i Zhenskikh Bolezney = Journal of Obstetrics and Women’s Diseases. 2013;62(2):117-125. (in Russian); Lebedev I.N., Nikitina T.V. Cytogenetics of Human Embryonic Development Disorders (Heredity and Health). Tomsk: Pechatnaya Manufaktura Publ., 2013. (in Russian); Levy B., Sigurjonsson S., Pettersen B., Maisenbacher M.K., Hall M.P., Demko Z., Lathi R.B., Tao R., Aggarwal V., Rabinowitz M. Genomic imbalance in products of conception: single-nucleotide polymorphism chromosomal microarray analysis. Obstet. Gynecol. 2014; 124(2 Pt.1):202-209. DOI 10.1097/aog.0000000000000325.; Li X., Ouyang Y., Yi Y., Tan Y., Lu G. Correlation analysis between ultrasound findings and abnormal karyotypes in the embryos from early pregnancy loss after in vitro fertilization–embryo transfer. J. Assist. Reprod. Genet. 2017;34(1):43-50. DOI 10.1007/s10815-016-0821-2.; Liu Y., Liu Y., Chen H., Du T., Tan J., Zhang J. The frequencies of the presence of embryonic pole and cardiac activity in early miscarriages with abnormal karyotypes. Clin. Exp. Obstet. Gynecol. 2015; 42(4):490-494.; Ljunger E., Stavreus-Evers A., Cnattingius S., Ekbom A., Lundin C., Annéren G., Sundström-Poromaa I. Ultrasonographic findings in spontaneous miscarriage: relation to euploidy and aneuploidy. Fertil. Steril. 2011;95(1):221-224. DOI 10.1016/j.fertnstert.2010.06.018.; Long P., Liu Z., Wu B., Chen J., Sun C., Wang F., Huang Y., Chen H., Li Q., Ma Y. Generation of an induced pluripotent stem cell line from chorionic villi of a Patau syndrome spontaneous abortion. Stem Cell Res. 2020;45:101789. DOI 10.1016/j.scr.2020.101789.; Menasha J., Levy B., Hirschhorn K., Kardon N.B. Incidence and spectrum of chromosome abnormalities in spontaneous abortions: new insights from a 12-year study. Genet. Med. 2005;7(4):251-263. DOI 10.1097/01.gim.0000160075.96707.04.; Minelli E., Buchi C., Granata P., Meroni E., Righi R., Portentoso P., Giudici A., Ercoli A., Sartor M.G., Rossi A. Cytogenetic findings in echographically defined blighted ovum abortions. Ann. Genet. 1993;36(2):107-110.; Muñoz M., Arigita M., Bennasar M., Soler A., Sanchez A., Borrell A. Chromosomal anomaly spectrum in early pregnancy loss in relation to presence or absence of an embryonic pole. Fertil. Steril. 2010; 94(7):2564-2568. DOI 10.1016/j.fertnstert.2010.04.011.; Nikitina T.V., Lebedev I.N., Sukhanova N.N., Sazhenova E.A., Nazarenko S.A. A mathematical model for evaluation of maternal cell contamination in cultured cells from spontaneous abortions: significance for cytogenetic analysis of prenatal selection factors. Fertil. Steril. 2005;83(4):964-972. DOI 10.1016/j.fertnstert.2004.12.009.; Orzack S.H., Stubblefield J.W., Akmaev V.R., Colls P., Munné S., Scholl T., Steinsaltz D., Zuckerman J.E. The human sex ratio from conception to birth. Proc. Natl. Acad. Sci. USA. 2015;112(16): E2102-E2111. DOI 10.1073/pnas.1416546112.; Ouyang Y., Tan Y., Yi Y., Gong F., Lin G., Li X., Lu G. Correlation between chromosomal distribution and embryonic findings on ultrasound in early pregnancy loss after IVF-embryo transfer. Hum. Reprod. 2016;31(10):2212-2218. DOI 10.1093/humrep/dew201.; Ozawa N., Ogawa K., Sasaki A., Mitsui M., Wada S., Sago H. Maternal age, history of miscarriage, and embryonic/fetal size are associated with cytogenetic results of spontaneous early miscarriages. J. Assist. Reprod. Genet. 2019;36(4):749-757. DOI 10.1007/s10815-019-01415-y.; Parveen S., Panicker M.M., Gupta P.K. Generation of an induced pluripotent stem cell line from chorionic villi of a Turner syndrome spontaneous abortion. Stem Cell Res. 2017;19:12-16. DOI 10.1016/j.scr.2016.12.016.; Radzinsky V.E., Makletsova S.A., Aleev I.A., Rudneva O.D., Ryabinkina T.S. Missed miscarriage. Guidelines by MARS Reproductive Health Professional Medical Association. Moscow: StatusPraesens Editorial Office, 2015. (in Russian); Robinson H.P. The diagnosis of early pregnancy failure by sonar. Br. J. Obstet. Gynaecol. 1975;82(11):849-857. DOI 10.1111/j.1471-0528.1975.tb00588.x.; Romanova O.A. Endometrium immunoreactivity in missed miscarriage associated with chromosome aberrations in the chorion. Cand. Med. Sci. Diss. St. Petersburg, 2022. (in Russian); Savchenko R.R., Kashevarova A.A., Skryabin N.A., Zhigalina D.I., Lopatkina M.E., Nikitina T.V., Vasiliev S.A., Lebedev I.N. Analysis of CNVs in anembryonic pregnancy and missed abortions. Meditsinskaya Genetika = Medical Genetics. 2018;17(3):49-54. DOI 10.25557/2073-7998.2018.03.49-54. (in Russian); Segawa T., Kuroda T., Kato K., Kuroda M., Omi K., Miyauchi O., Watanabe Y., Okubo T., Osada H., Teramoto S. 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A yolk sac larger than 5 mm suggests an abnormal fetal karyotype, whereas an absent embryo indicates a normal fetal karyotype. J. Ultrasound Med. 2018;37(5):1233-1241. DOI 10.1002/jum.14467.; https://vavilov.elpub.ru/jour/article/view/3629 |
DOI: | 10.18699/VJGB-23-05 |
الاتاحة: | https://vavilov.elpub.ru/jour/article/view/3629 https://doi.org/10.18699/VJGB-23-05 |
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رقم الانضمام: | edsbas.541D14F1 |
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The cases of embryonic death can be divided into missed abortion (MA), for which the ultrasound sign of the embryo death is the absence of cardiac activity, and anembryonic pregnancy (AP) without an embryo in the gestational sac. The aim of this study was to compare the frequency of chromosomal abnormalities in extraembryonic tissues detected by conventional cytogenetic analysis of spontaneous abortions depending on the presence or absence of an embryo. This is a retrospective study of 1551 spontaneous abortions analyzed using GTG-banding from 1990 to 2022 (266 cases of AP and 1285 cases of MA). A comparative analysis of the frequency of chromosomal abnormalities and the distribution of karyotype frequencies depending on the presence of an embryo in the gestational sac was carried out. Statistical analysis was performed using a chi-square test with a p < 0.05 significance level. The total frequency of chromosomal abnormalities in the study was 53.6 % (832/1551). The proportion of abnormal karyotypes in the AP and MA groups did not differ significantly and amounted to 57.1 % (152/266) and 52.9 % (680/1285) for AP and MA, respectively (p = 0.209). Sex chromosome aneuploidies and triploidies were significantly less common in the AP group than in the MA group (2.3 % (6/266) vs 6.8 % (88/1285), p = 0.005 and 4.9 % (13/266) vs 8.9 % (114/1285), p = 0.031, respectively). Tetraploidies were registered more frequently in AP compared to MA (12.4 % (33/266) vs. 8.2 % (106/1285), p = 0.031). The sex ratio among abortions with a normal karyotype was 0.54 and 0.74 for AP and MA, respectively. Thus, although the frequencies of some types of chromosomal pathology differ between AP and MA, the total frequency of chromosomal abnormalities in AP is not increased compared to MA, which indicates the need to search for the causes of AP at other levels of the genome organization, including microstructural chromosomal ... ) Array ( [Name] => TypeDocument [Label] => Document Type [Group] => TypDoc [Data] => article in journal/newspaper ) Array ( [Name] => Format [Label] => File Description [Group] => SrcInfo [Data] => application/pdf ) Array ( [Name] => Language [Label] => Language [Group] => Lang [Data] => English ) Array ( [Name] => NoteTitleSource [Label] => Relation [Group] => SrcInfo [Data] => https://vavilov.elpub.ru/jour/article/view/3629/1680; Ahern D.T., Bansal P., Faustino I., Kondaveeti Y., Glatt-Deeley H.R., Banda E.C., Pinter S.F. Monosomy X in isogenic human iPSCderived trophoblast model impacts expression modules preserved in human placenta. Proc. Natl. Acad. Sci. USA. 2022;119(40): e2211073119. DOI 10.1073/pnas.2211073119.; Angiolucci M., Murru R., Melis G., Carcassi C., Mais V. Association between different morphological types and abnormal karyotypes in early pregnancy loss. Ultrasound Obstet. Gynecol. 2011;37(2):219-225. DOI 10.1002/uog.7681.; Boss A.L., Chamley L.W., James J.L. Placental formation in early pregnancy: how is the centre of the placenta made? Hum. Reprod. Update. 2018;24(6):750-760. DOI 10.1093/humupd/dmy030.; Cheng H.H., Ou C.Y., Tsai C.C., Chang S.D., Hsiao P.Y., Lan K.C., Hsu T.Y. Chromosome distribution of early miscarriages with present or absent embryos: female predominance. J. Assist. Reprod. Genet. 2014;31(8):1059-1064. DOI 10.1007/s10815-014-0261-9.; Doubilet P.M., Benson C.B., Bourne T., Blaivas M., Society of Radiologists in Ultrasound Multispecialty Panel on Early First Trimester Diagnosis of Miscarriage and Exclusion of a Viable Intrauterine Pregnancy, Barnhart K.T., Benacerraf B.R., Brown D.L., Filly R.A., Fox J.C., Goldstein S.R., Kendall J.L., Lyons E.A., Porter M.B., Pretorius D.H., Timor-Tritsch I.E. Diagnostic criteria for nonviable pregnancy early in the first trimester. N. Engl. J. Med. 2013;369(15): 1443-1451. DOI 10.1056/NEJMra1302417.; Evdokimova V.N., Nikitina T.V., Lebedev I.N., Sukhanova N.N., Nazarenko S.A. About the sex ratio in connection with early embryonic mortality in man. Russ. J. Developmental Biology. 2000;31(4):251-257.; Fan L., Wu J., Wu Y., Shi X., Xin X., Li S., Zeng W., Deng D., Feng L., Chen S., Xiao J. Analysis of chromosomal copy number in first-trimester pregnancy loss using next-generation sequencing. Front. Genet. 2020;11:545856. 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DOI 10.1046/j.0960-7692.2001.00571.x.; Gu C., Li K., Li R., Li L., Li X., Dai X., He Y. Chromosomal aneuploidy associated with clinical characteristics of pregnancy loss. Front. Genet. 2021;12:667697. DOI 10.3389/fgene.2021.667697.; Hardy K., Hardy P.J., Jacobs P.A., Lewallen K., Hassold T.J. Temporal changes in chromosome abnormalities in human spontaneous abortions: results of 40 years of analysis. Am. J. Med. Genet. A. 2016; 170(10):2671-2680. DOI 10.1002/ajmg.a.37795.; Hassold T., Benham F., Leppert M. Cytogenetic and molecular analysis of sex-chromosome monosomy. Am. J. Hum. Genet. 1988;42(4): 534-541.; Huang J., Zhu W., Tang J., Saravelos S.H., Poon L.C.Y., Li T.C. Do specific ultrasonography features identified at the time of early pregnancy loss predict fetal chromosomal abnormality? – A systematic review and meta-analysis. Genes Dis. 2019;6(2):129-137. DOI 10.1016/j.gendis.2018.10.001.; Kolte A.M., Bernardi L.A., Christiansen O.B., Quenby S., Farquharson R.G., Goddijn M., Stephenson M.D. ESHRE Special Interest Group, Early Pregnancy. Terminology for pregnancy loss prior to viability: a consensus statement from the ESHRE early pregnancy special interest group. Hum. Reprod. 2015;30(3):495-498. DOI 10.1093/humrep/deu299.; Larsen E.C., Christiansen O.B., Kolte A.M., Macklon N. New insights into mechanisms behind miscarriage. BMC Med. 2013;11:154. DOI 10.1186/1741-7015-11-154.; Lathi R.B., Mark S.D., Westphal L.M., Milki A.A. Cytogenetic testing of anembryonic pregnancies compared to embryonic missed abortions. J. Assist. Reprod. Genet. 2007;24(11):521-524. DOI 10.1007/s10815-007-9166-1.; Lebedev I.N., Kashevarova A.A., Skryabin N.A., Nikitina T.V., Lopatkina M.E., Melnikov A.A., Sazhenova E.A., Ivanova T.V., Evtushenko I.D. Array-based comparative genomic hybridization (array-CGH) in analysis of chromosomal aberrations and CNV in blighted ovum pregnancies. Zhurnal Akusherstva i Zhenskikh Bolezney = Journal of Obstetrics and Women’s Diseases. 2013;62(2):117-125. (in Russian); Lebedev I.N., Nikitina T.V. Cytogenetics of Human Embryonic Development Disorders (Heredity and Health). Tomsk: Pechatnaya Manufaktura Publ., 2013. (in Russian); Levy B., Sigurjonsson S., Pettersen B., Maisenbacher M.K., Hall M.P., Demko Z., Lathi R.B., Tao R., Aggarwal V., Rabinowitz M. Genomic imbalance in products of conception: single-nucleotide polymorphism chromosomal microarray analysis. Obstet. Gynecol. 2014; 124(2 Pt.1):202-209. DOI 10.1097/aog.0000000000000325.; Li X., Ouyang Y., Yi Y., Tan Y., Lu G. Correlation analysis between ultrasound findings and abnormal karyotypes in the embryos from early pregnancy loss after in vitro fertilization–embryo transfer. J. Assist. Reprod. Genet. 2017;34(1):43-50. DOI 10.1007/s10815-016-0821-2.; Liu Y., Liu Y., Chen H., Du T., Tan J., Zhang J. The frequencies of the presence of embryonic pole and cardiac activity in early miscarriages with abnormal karyotypes. Clin. Exp. Obstet. Gynecol. 2015; 42(4):490-494.; Ljunger E., Stavreus-Evers A., Cnattingius S., Ekbom A., Lundin C., Annéren G., Sundström-Poromaa I. Ultrasonographic findings in spontaneous miscarriage: relation to euploidy and aneuploidy. Fertil. Steril. 2011;95(1):221-224. DOI 10.1016/j.fertnstert.2010.06.018.; Long P., Liu Z., Wu B., Chen J., Sun C., Wang F., Huang Y., Chen H., Li Q., Ma Y. Generation of an induced pluripotent stem cell line from chorionic villi of a Patau syndrome spontaneous abortion. Stem Cell Res. 2020;45:101789. DOI 10.1016/j.scr.2020.101789.; Menasha J., Levy B., Hirschhorn K., Kardon N.B. Incidence and spectrum of chromosome abnormalities in spontaneous abortions: new insights from a 12-year study. Genet. Med. 2005;7(4):251-263. DOI 10.1097/01.gim.0000160075.96707.04.; Minelli E., Buchi C., Granata P., Meroni E., Righi R., Portentoso P., Giudici A., Ercoli A., Sartor M.G., Rossi A. Cytogenetic findings in echographically defined blighted ovum abortions. Ann. Genet. 1993;36(2):107-110.; Muñoz M., Arigita M., Bennasar M., Soler A., Sanchez A., Borrell A. Chromosomal anomaly spectrum in early pregnancy loss in relation to presence or absence of an embryonic pole. Fertil. Steril. 2010; 94(7):2564-2568. DOI 10.1016/j.fertnstert.2010.04.011.; Nikitina T.V., Lebedev I.N., Sukhanova N.N., Sazhenova E.A., Nazarenko S.A. A mathematical model for evaluation of maternal cell contamination in cultured cells from spontaneous abortions: significance for cytogenetic analysis of prenatal selection factors. Fertil. Steril. 2005;83(4):964-972. DOI 10.1016/j.fertnstert.2004.12.009.; Orzack S.H., Stubblefield J.W., Akmaev V.R., Colls P., Munné S., Scholl T., Steinsaltz D., Zuckerman J.E. 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The features ratio of chromosomal abnormalities and terms of persistence of gestational sacs among undeveloping pregnancies in cases without embryo (anembrioniya) and with the existing embryo: analysis of 1328 cases. Zdorov’e Zhenshchiny = Health of Woman. 2015;5(101):74-80. DOI 10.15574/HW.2015.101.74. (in Russian); Wang H., Yuan D., Wang S., Luo L., Zhang Y., Ye J., Zhu K. Cytogenetic and genetic investigation of miscarriage cases in Eastern China. J. Matern. Fetal. Neonatal. Med. 2020;33(20):3385-3390. DOI 10.1080/14767058.2019.1572738.; Wu X., Su L., Xie X., He D., Chen X., Wang M., Wang L., Zheng L., Xu L. Comprehensive analysis of early pregnancy loss based on cytogenetic findings from a tertiary referral center. Mol. Cytogenet. 2021;14(1):56. DOI 10.1186/s13039-021-00577-8.; Yoneda S., Shiozaki A., Yoneda N., Sameshima A., Ito M., Shima T., Nakashima A., Yoshino O., Kigawa M., Takamori R., Shinagawa Y., Saito S. 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