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Cited by 24Assisted Reproductive Technology and Twin PregnancyReproductive Biology and FertilityDevelopmental Biology and Gene Regulation

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Cellular mechanisms of monozygotic twinning: clues from assisted reproduction

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Jin, Hongbin, Han, Yang, Zenker, Jennifer·2024·Human Reproduction Update
DOI 10.1093/humupd/dmae022PMC PMC11532623
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Abstract

BACKGROUND: Monozygotic (MZ) twins are believed to arise from the fission of a single fertilized embryo at different stages. Monochorionic MZ twins, who share one chorion, originate from the splitting of the inner cell mass (ICM) within a single blastocyst. In the classic model for dichorionic MZ twins, the embryo splits before compaction, developing into two blastocysts. However, there are a growing number of ART cases where a single blastocyst transfer results in dichorionic MZ twins, indicating that embryo splitting may occur even after blastocyst formation. OBJECTIVE AND RATIONALE: For monochorionic MZ twins, we conducted a comprehensive analysis of the cellular mechanisms involved in ICM splitting, drawing from both ART cases and animal experiments. In addition, we critically re-examine the classic early splitting model for dichorionic MZ twins. We explore cellular mechanisms leading to two separated blastocysts in ART, potentially causing dichorionic MZ twins. SEARCH METHODS: Relevant studies including research articles, reviews, and conference papers were searched in the PubMed database. Cases of MZ twins from IVF clinics were found by using combinations of terms including ‘monozygotic twins’ with ‘IVF case report’, ‘ART’, ‘single embryo transfer’, or ‘dichorionic’. The papers retrieved were categorized based on the implicated mechanisms or as those with unexplained mechanisms. Animal experiments relating to MZ twins were found using ‘mouse embryo monozygotic twins’, ‘mouse 8-shaped hatching’, ‘zebrafish janus mutant’, and ‘nine-banded armadillo embryo’, along with literature collected through day-to-day reading. The search was limited to articles in English, with no restrictions on publication date or species. OUTCOMES: For monochorionic MZ twins, ART cases and mouse experiments demonstrate evidence that a looser ICM in blastocysts has an increased chance of ICM separation. Physical forces facilitated by blastocoel formation or 8-shaped hatching are exerted on the ICM, resulting in monochorionic MZ twins. For dichorionic MZ twins, the classic model resembles artificial cloning of mouse embryos in vitro, requiring strictly controlled splitting forces, re-joining prevention, and proper aggregation, which allows the formation of two separate human blastocysts under physiological circumstances. In contrast, ART procedures involving the transfer of a single blastocysts after atypical hatching or vitrified-warmed cycles might lead to blastocyst separation. Differences in morphology, molecular mechanisms, and timing across various animal model systems for MZ twinning can impede this research field. As discussed in future directions, recent developments of innovative in vitro models of human embryos may offer promising avenues for providing fundamental novel insights into the cellular mechanisms of MZ twinning during human embryogenesis. WIDER IMPLICATIONS: Twin pregnancies pose high risks to both the fetuses and the mother. While single embryo transfer is commonly employed to prevent dizygotic twin pregnancies in ART, it cannot prevent the occurrence of MZ twins. Drawing from our understanding of the cellular mechanisms underlying monochorionic and dichorionic MZ twinning, along with insights into the genetic mechanisms, could enable improved prediction, prevention, and even intervention strategies during ART procedures. REGISTRAITON NUMBER: N/A.

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  • Identical twins share identical genetic makeup and appear similar in physical appearance.

    “Identical twins share identical genetic makeup and appear similar in physical appearance (Jin et al., 2024).”

    From Seeing Double: A Case Study Examining Systemic Supervision and Therapy Conceptualization of Identical Twins (2026) · cites this paper as Jin et al., 2024

    The Introduction (page not available) describes monozygotic twins as “identical individuals originating from a single fertilized embryo,” supporting the claim about shared genetic makeup. Our copy does not specifically discuss their physical appearance, so that part of the sentence is not directly supported. (LLM, conf=0.82)

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Research works printed but not linked: 175

  1. Abdelilah, 1997, Pattern formation in janus-mutant zebrafish embryos, Dev Biol, 184, 70, 10.1006/dbio.1997.8517 · DOI
  2. Abdelilah, 1994, Implications for dorsoventral axis determination from the zebrafish mutation janus, Nature, 370, 468, 10.1038/370468a0 · DOI
  3. Alikani, 2003, Monozygotic twinning following assisted conception: an analysis of 81 consecutive cases, Hum Reprod, 18, 1937, 10.1093/humrep/deg369 · DOI
  4. Alikani, 1994, Monozygotic twinning in the human is associated with the zona pellucida architecture, Hum Reprod, 9, 1318, 10.1093/oxfordjournals.humrep.a138701 · DOI
  5. Astell, 2020, Zebrafish in vivo models of cancer and metastasis, Cold Spring Harb Perspect Med, 10, a037077, 10.1101/cshperspect.a037077 · DOI
  6. Aston, 2008, Monozygotic twinning associated with assisted reproductive technologies: a review, Reproduction, 136, 377, 10.1530/REP-08-0206 · DOI
  7. Bamforth, 2003, Mechanisms of monozygotic (MZ) twinning: a possible role for the cell adhesion molecule, E-cadherin, Am J Med Genet A, 120a, 59, 10.1002/ajmg.a.20076 · DOI
  8. Behr, 2000, Blastocyst-ET and monozygotic twinning, J Assist Reprod Genet, 17, 349, 10.1023/A:1009461213139 · DOI
  9. Behr, 2003, Visualization of atypical hatching of a human blastocyst in vitro forming two identical embryos, Fertil Steril, 80, 1502, 10.1016/j.fertnstert.2003.07.001 · DOI
  10. Bissiere, 2023, Updates on preimplantation embryo research, Fertil Steril, 120, 467, 10.1016/j.fertnstert.2023.04.039 · DOI
  11. Blickstein, 2007, On the possible cause of monozygotic twinning: lessons from the 9-banded armadillo and from assisted reproduction, Twin Res Hum Genet, 10, 394, 10.1375/twin.10.2.394 · DOI
  12. Brouillet, 2022, Molecular characterization of a rare case of monozygotic dichorionic diamniotic twin pregnancy after single blastocyst transfer in preimplantation genetic testing (PGT), Int J Mol Sci, 23, 10835, 10.3390/ijms231810835 · DOI
  13. Busnelli, 2019, Risk factors for monozygotic twinning after in vitro fertilization: a systematic review and meta-analysis, Fertil Steril, 111, 302, 10.1016/j.fertnstert.2018.10.025 · DOI
  14. Cao, 2020, Heterozygous mutations in ZP1 and ZP3 cause formation disorder of ZP and female infertility in human, J Cell Mol Med, 24, 8557, 10.1111/jcmm.15482 · DOI
  15. Cara, 2023, First case of dichorionic diamniotic triplet pregnancy after single blastocyst transfer, J Assist Reprod Genet, 41, 437, 10.1007/s10815-023-02989-4 · DOI
  16. Carter, 2018, Classics revisited: Miguel Fernández on germ layer inversion and specific polyembryony in armadillos, Placenta, 61, 55, 10.1016/j.placenta.2017.11.006 · DOI
  17. Casser, 2019, Multiplying embryos: experimental monozygotic polyembryony in mammals and its uses, Int J Dev Biol, 63, 143, 10.1387/ijdb.190016mb · DOI
  18. Casser, 2017, Totipotency segregates between the sister blastomeres of two-cell stage mouse embryos, Sci Rep, 7, 8299, 10.1038/s41598-017-08266-6 · DOI
  19. Chen, 2017, A recurrent missense mutation in ZP3 causes empty follicle syndrome and female infertility, Am J Hum Genet, 101, 459, 10.1016/j.ajhg.2017.08.001 · DOI
  20. Chida, 1990, Monozygous double inner cell masses in mouse blastocysts following fertilization in vitro and in vivo, J In Vitro Fert Embryo Transf, 7, 177, 10.1007/BF01135685 · DOI
  21. Cohen, 1991, Assisted hatching of human embryos, J In Vitro Fert Embryo Transf, 8, 179, 10.1007/BF01130802 · DOI
  22. Corner, 1922, The morphological theory of monochorionic twins as illustrated by a series of supposed early twin embryos of the pig, Bull Johns Hopkins Hosp, 33, 389
  23. Corner, 1955, The observed embryology of human single-ovum twins and other multiple births, Am J Obstet Gynecol, 70, 933, 10.1016/0002-9378(55)90001-6 · DOI
  24. Corsello, 2010, The world of twins: an update, J Matern Fetal Neonatal Med, 23(Suppl 3), 59, 10.3109/14767058.2010.508218 · DOI
  25. Cyranoski, 2009, Developmental biology: two by two, Nature, 458, 826, 10.1038/458826a · DOI
  26. Dai, 2019, ZP2 pathogenic variants cause in vitro fertilization failure and female infertility, Genet Med, 21, 431, 10.1038/s41436-018-0064-y · DOI
  27. De Neubourg, 2022, Single-embryo transfer implies quality of care in reproductive medicine, Reprod Biomed Online, 45, 899, 10.1016/j.rbmo.2022.04.001 · DOI
  28. De Sutter, 2006, Single embryo transfer (set) not only leads to a reduction in twinning rates after IVF/ICSI, but also improves obstetrical and perinatal outcome of singletons, Verh K Acad Geneeskd Belg, 68, 319
  29. Dessolle, 2010, Monozygotic triplet pregnancies after single blastocyst transfer: two cases and literature review, Reprod Biomed Online, 21, 283, 10.1016/j.rbmo.2010.04.011 · DOI
  30. Ding, 2018, The effect of blastocyst transfer on newborn sex ratio and monozygotic twinning rate: an updated systematic review and meta-analysis, Reprod Biomed Online, 37, 292, 10.1016/j.rbmo.2018.05.015 · DOI
  31. Dirican, 2021, On the origin of zygosity and chorionicity in twinning: evidence from human in vitro fertilization, J Assist Reprod Genet, 38, 2809, 10.1007/s10815-021-02294-y · DOI
  32. Dumortier, 2019, Hydraulic fracturing and active coarsening position the lumen of the mouse blastocyst, Science, 365, 465, 10.1126/science.aaw7709 · DOI
  33. Eliasen, 2021, Monochorionic twins after single blastocyst transfer: retrospective cohort and blinded time lapse annotation analysis, Reprod Biomed Online, 43, 62, 10.1016/j.rbmo.2021.04.001 · DOI
  34. Elizur, 2004, Monozygotic twinning is not associated with zona pellucida micromanipulation procedures but increases with high-order multiple pregnancies, Fertil Steril, 82, 500, 10.1016/j.fertnstert.2004.02.106 · DOI
  35. Enders, 2002, Implantation in the nine-banded armadillo: how does a single blastocyst form four embryos?, Placenta, 23, 71, 10.1053/plac.2001.0753 · DOI
  36. Faraj, 2008, Monozygotic triplet pregnancy following egg donation and transfer of single frozen-thawed embryo, Fertil Steril, 89, 1260.e9, 10.1016/j.fertnstert.2007.05.008 · DOI
  37. Fleming, 2001, Cell adhesion in the preimplantation mammalian embryo and its role in trophectoderm differentiation and blastocyst morphogenesis, Front Biosci, 6, D1000, 10.2741/Fleming · DOI
  38. Fouks, 2022, Twinning in ART: single embryo transfer policy, Best Pract Res Clin Obstet Gynaecol, 84, 88, 10.1016/j.bpobgyn.2022.03.010 · DOI
  39. Gardner, 2014, The timing of monozygotic twinning: a pro-life challenge to conventional scientific wisdom, Reprod Biomed Online, 28, 276, 10.1016/j.rbmo.2013.12.002 · DOI
  40. Gu, 2018, Inner cell mass incarceration in 8-shaped blastocysts does not increase monozygotic twinning in preimplantation genetic diagnosis and screening patients, PLoS One, 13, e0190776, 10.1371/journal.pone.0190776 · DOI
  41. Gurunath, 2015, Monochorionic triamniotic triplets following conventional in vitro fertilization and blastocyst transfer, J Hum Reprod Sci, 8, 54, 10.4103/0974-1208.153131 · DOI
  42. Hall, 2003, Twinning, Lancet, 362, 735, 10.1016/S0140-6736(03)14237-7 · DOI
  43. Hamamy, 2004, Familial monozygotic twinning: report of an extended multi-generation family, Twin Res, 7, 219, 10.1375/136905204774200479 · DOI
  44. Hammadeh, 2011, Assisted hatching in assisted reproduction: a state of the art, J Assist Reprod Genet, 28, 119, 10.1007/s10815-010-9495-3 · DOI
  45. Hawdon, 2023, Apicobasal RNA asymmetries regulate cell fate in the early mouse embryo, Nat Commun, 14, 2909, 10.1038/s41467-023-38436-2 · DOI
  46. Herranz, 2015, The timing of monozygotic twinning: a criticism of the common model, Zygote, 23, 27, 10.1017/S0967199413000257 · DOI
  47. Hisaki, 2014, Regulation of embryonic size in early mouse development in vitro culture system, Zygote, 22, 340, 10.1017/S0967199412000652 · DOI
  48. Hoekstra, 2008, Dizygotic twinning, Hum Reprod Update, 14, 37, 10.1093/humupd/dmm036 · DOI
  49. Hsu, 1980, Monozygotic twin formation in mouse embryos in vitro, Science, 209, 605, 10.1126/science.7190325 · DOI
  50. Huang, 2015, Microscale imaging of cilia-driven fluid flow, Cell Mol Life Sci, 72, 1095, 10.1007/s00018-014-1784-z · DOI
  51. Huang, 2014, Mutant ZP1 in familial infertility, N Engl J Med, 370, 1220, 10.1056/NEJMoa1308851 · DOI
  52. Hupalowska, 2018, CARM1 and paraspeckles regulate pre-implantation mouse embryo development, Cell, 175, 1902, 10.1016/j.cell.2018.11.027 · DOI
  53. Hviid, 2018, Determinants of monozygotic twinning in ART: a systematic review and a meta-analysis, Hum Reprod Update, 24, 468, 10.1093/humupd/dmy006 · DOI
  54. Illmensee, 2005, Efficient blastomere biopsy for mouse embryo splitting for future applications in human assisted reproduction, Reprod Biomed Online, 11, 716, 10.1016/S1472-6483(10)61690-2 · DOI
  55. Illmensee, 2010, Human embryo twinning with applications in reproductive medicine, Fertil Steril, 93, 423, 10.1016/j.fertnstert.2008.12.098 · DOI
  56. Imaizumi, 2003, A comparative study of zygotic twinning and triplet rates in eight countries, 1972-1999, J Biosoc Sci, 35, 287, 10.1017/S0021932003002876 · DOI
  57. Jain, 2004, Monozygotic twins and triplets in association with blastocyst transfer, J Assist Reprod Genet, 21, 103, 10.1023/B:JARG.0000029493.54929.be · DOI
  58. Jin, 2022, The second polar body contributes to the fate asymmetry in the mouse embryo, Natl Sci Rev, 9, nwac003, 10.1093/nsr/nwac003 · DOI
  59. Johnston, 2001, Conjoined twins, Lancet, 357, 149, 10.1016/S0140-6736(05)71191-0 · DOI
  60. Jundi, 2021, Monozygotic dichorionic-diamniotic twin pregnancy after single embryo transfer at blastocyst stage: a case report, JBRA Assist Reprod, 25, 168
  61. Juste-Lanas, 2023, Fluid flow to mimic organ function in 3D in vitro models, APL Bioeng, 7, 031501, 10.1063/5.0146000 · DOI
  62. Kaufman, 2004, The embryology of conjoined twins, Childs Nerv Syst, 20, 508, 10.1007/s00381-004-0985-4 · DOI
  63. Kawachiya, 2011, Blastocyst culture is associated with an elevated incidence of monozygotic twinning after single embryo transfer, Fertil Steril, 95, 2140, 10.1016/j.fertnstert.2010.12.018 · DOI
  64. Klein, 2005, Challenging traditional dogma: a report of two cases of late monozygotic splitting resulting in dichorionic twinning, Fertil Steril, 84, S238, 10.1016/j.fertnstert.2005.07.616 · DOI
  65. Klein, 2012, Eph/ephrin signalling during development, Development, 139, 4105, 10.1242/dev.074997 · DOI
  66. Knopman, 2010, Monozygotic twinning: an eight-year experience at a large IVF center, Fertil Steril, 94, 502, 10.1016/j.fertnstert.2009.03.064 · DOI
  67. Konno, 2020, The incidence of dichorionic diamniotic twin pregnancy after single blastocyst embryo transfer and zygosity: 8 years of single-center experience, Twin Res Hum Genet, 23, 51, 10.1017/thg.2020.5 · DOI
  68. Krawczyk, 2021, Developmental capacity is unevenly distributed among single blastomeres of 2-cell and 4-cell stage mouse embryos, Sci Rep, 11, 21422, 10.1038/s41598-021-00834-1 · DOI
  69. Krishnan, 2008, Monozygotic transplantation: concerns and opportunities, Am J Transplant, 8, 2343, 10.1111/j.1600-6143.2008.02378.x · DOI
  70. Kyono, 2013, The precise timing of embryo splitting for monozygotic dichorionic diamniotic twins: when does embryo splitting for monozygotic dichorionic diamniotic twins occur? Evidence for splitting at the morula/blastocyst stage from studies of in vitro fertilization, Twin Res Hum Genet, 16, 827, 10.1017/thg.2013.32 · DOI
  71. Landeira, 2015, Jarid2 coordinates nanog expression and PCP/Wnt signaling required for efficient ESC differentiation and early embryo development, Cell Rep, 12, 573, 10.1016/j.celrep.2015.06.060 · DOI
  72. Lee, 2008, Monozygotic triplets after single blastocyst transfer: case report and literature review, Aust N Z J Obstet Gynaecol, 48, 583, 10.1111/j.1479-828X.2008.00926.x · DOI
  73. Li, 2020, Monozygotic dichorionic-diamniotic pregnancies following single frozen-thawed blastocyst transfer: a retrospective case series, BMC Pregnancy Childbirth, 20, 768, 10.1186/s12884-020-03450-5 · DOI
  74. Lichtenstein, 1998, No paternal effect on monozygotic twinning in the Swedish Twin Registry, Twin Res, 1, 212, 10.1375/twin.1.4.212 · DOI
  75. Liu, 2018, Elevated incidence of monozygotic twinning is associated with extended embryo culture, but not with zona pellucida manipulation or freeze-thaw procedure, Fertil Steril, 109, 1044, 10.1016/j.fertnstert.2018.01.040 · DOI
  76. Liu, 2018, Four-generation pedigree of monozygotic female twins reveals genetic factors in twinning process by whole-genome sequencing, Twin Res Hum Genet, 21, 361, 10.1017/thg.2018.41 · DOI
  77. Liu, 2021, Modelling human blastocysts by reprogramming fibroblasts into iBlastoids, Nature, 591, 627, 10.1038/s41586-021-03372-y · DOI
  78. Luijkx, 2024, Monochorionic twinning in bioengineered human embryo models, Adv Mater, 36, e2313306, 10.1002/adma.202313306 · DOI
  79. Luke, 2014, Factors associated with monozygosity in assisted reproductive technology pregnancies and the risk of recurrence using linked cycles, Fertil Steril, 101, 683, 10.1016/j.fertnstert.2013.11.034 · DOI
  80. Luo, 2020, Novel mutations in ZP1 and ZP2 cause primary infertility due to empty follicle syndrome and abnormal zona pellucida, J Assist Reprod Genet, 37, 2853, 10.1007/s10815-020-01926-z · DOI
  81. Machin, 2009, Familial monozygotic twinning: a report of seven pedigrees, Am J Med Genet C Semin Med Genet, 151c, 152, 10.1002/ajmg.c.30211 · DOI
  82. Machin, 2009, Non-identical monozygotic twins, intermediate twin types, zygosity testing, and the non-random nature of monozygotic twinning: a review, Am J Med Genet C Semin Med Genet, 151c, 110, 10.1002/ajmg.c.30212 · DOI
  83. Mansour, 2000, Transfer of zona-free embryos improves outcome in poor prognosis patients: a prospective randomized controlled study, Hum Reprod, 15, 1061, 10.1093/humrep/15.5.1061 · DOI
  84. Martin, 2012, Three decades of twin births in the United States, 1980-2009, NCHS Data Brief, (80), 1
  85. Mateizel, 2016, Do ARTs affect the incidence of monozygotic twinning?, Hum Reprod, 31, 2435, 10.1093/humrep/dew216 · DOI
  86. Matorras, 2023, Early spontaneous twinning recorded by time-lapse, Twin Res Hum Genet, 26, 215, 10.1017/thg.2023.24 · DOI
  87. McLaren, 1995, Does monozygotic twinning occur in mice?, Genet Res, 66, 195, 10.1017/S0016672300034649 · DOI
  88. McNamara, 2016, A review of the mechanisms and evidence for typical and atypical twinning, Am J Obstet Gynecol, 214, 172, 10.1016/j.ajog.2015.10.930 · DOI
  89. Meintjes, 2001, Prospective identification of an in vitro-assisted monozygotic pregnancy based on a double-inner-cell-mass blastocyst, Fertil Steril, 76, S172, 10.1016/S0015-0282(01)02509-2 · DOI
  90. Ménézo, 2002, Monozygotic twinning: is it related to apoptosis in the embryo?, Hum Reprod, 17, 247, 10.1093/humrep/17.1.247 · DOI
  91. Mio, 2008, Time-lapse cinematography of dynamic changes occurring during in vitro development of human embryos, Am J Obstet Gynecol, 199, 660.e1, 10.1016/j.ajog.2008.07.023 · DOI
  92. Molè, 2020, Comparative analysis of human and mouse development: from zygote to pre-gastrulation, Curr Top Dev Biol, 136, 113, 10.1016/bs.ctdb.2019.10.002 · DOI
  93. Montag, 2000, Significance of the number of embryonic cells and the state of the zona pellucida for hatching of mouse blastocysts in vitro versus in vivo, Biol Reprod, 62, 1738, 10.1095/biolreprod62.6.1738 · DOI
  94. Morris, 2012, Developmental plasticity is bound by pluripotency and the Fgf and Wnt signaling pathways, Cell Rep, 2, 756, 10.1016/j.celrep.2012.08.029 · DOI
  95. Motosugi, 2005, Polarity of the mouse embryo is established at blastocyst and is not prepatterned, Genes Dev, 19, 1081, 10.1101/gad.1304805 · DOI
  96. Murphy, 1997, Twinning rates, Lancet, 349, 1398, 10.1016/S0140-6736(05)63241-2 · DOI
  97. Muter, 2023, Human embryo implantation, Development, 150, dev201507, 10.1242/dev.201507 · DOI
  98. Nagashima, 1989, Microsurgical bisection of porcine morulae and blastocysts to produce monozygotic twin pregnancy, Gamete Res, 23, 1, 10.1002/mrd.1120230102 · DOI
  99. Neumann, 2020, Dichorionic-diamniotic twin pregnancy after elective single-embryo transfer of a blastocyst, Dtsch Arztebl Int, 117, 716
  100. Noli, 2015, Discordant growth of monozygotic twins starts at the blastocyst stage: a case study, Stem Cell Reports, 5, 946, 10.1016/j.stemcr.2015.10.006 · DOI
  101. Noli, 2016, Potential of human twin embryos generated by embryo splitting in assisted reproduction and research, Hum Reprod Update, 23, 156
  102. O'Brien, 1984, Developmental potential of isolated blastomeres from early murine embryos, Theriogenology, 22, 601, 10.1016/0093-691X(84)90060-8 · DOI
  103. Onodera, 2017, The location of “8”-shaped hatching influences inner cell mass formation in mouse blastocysts, PLoS One, 12, e0175150, 10.1371/journal.pone.0175150 · DOI
  104. Osianlis, 2014, Incidence and zygosity of twin births following transfers using a single fresh or frozen embryo, Hum Reprod, 29, 1438, 10.1093/humrep/deu064 · DOI
  105. Otsuki, 2016, Grade and looseness of the inner cell mass may lead to the development of monochorionic diamniotic twins, Fertil Steril, 106, 640, 10.1016/j.fertnstert.2016.05.007 · DOI
  106. Papaioannou, 1989, Development and phenotypic variability of genetically identical half mouse embryos, Development, 106, 817, 10.1242/dev.106.4.817 · DOI
  107. Papanikolaou, 2010, Monozygotic twinning is not increased after single blastocyst transfer compared with single cleavage-stage embryo transfer, Fertil Steril, 93, 592, 10.1016/j.fertnstert.2008.12.088 · DOI
  108. Parazzini, 2016, Risk of monozygotic twins after assisted reproduction: a population-based approach, Twin Res Hum Genet, 19, 72, 10.1017/thg.2015.96 · DOI
  109. Pasquale, 2005, Eph receptor signalling casts a wide net on cell behaviour, Nat Rev Mol Cell Biol, 6, 462, 10.1038/nrm1662 · DOI
  110. Payne, 2007, Time-lapse recording identifies human blastocysts at risk of producing monozygotic twins, Hum Reprod, 22, i9
  111. Pedroza, 2023, Self-patterning of human stem cells into post-implantation lineages, Nature, 622, 574, 10.1038/s41586-023-06354-4 · DOI
  112. Peters, 2017, Unusual twinning resulting in chimerism: a systematic review on monochorionic dizygotic twins, Twin Res Hum Genet, 20, 161, 10.1017/thg.2017.4 · DOI
  113. Pinborg, 2005, IVF/ICSI twin pregnancies: risks and prevention, Hum Reprod Update, 11, 575, 10.1093/humupd/dmi027 · DOI
  114. Prodöhl, 1996, Molecular documentation of polyembryony and the micro-spatial dispersion of clonal sibships in the nine-banded armadillo, Dasypus novemcinctus, Proc Biol Sci, 263, 1643, 10.1098/rspb.1996.0240 · DOI
  115. Reimundo, 2021, Single-embryo transfer: a key strategy to reduce the risk for multiple pregnancy in assisted human reproduction, Adv Lab Med, 2, 179
  116. Roberts, 2011, Transcript profiling of individual twin blastomeres derived by splitting two-cell stage murine embryos, Biol Reprod, 84, 487, 10.1095/biolreprod.110.086884 · DOI
  117. Rossant, 2022, Early human embryonic development: blastocyst formation to gastrulation, Dev Cell, 57, 152, 10.1016/j.devcel.2021.12.022 · DOI
  118. Saito, 2000, Do assisted reproductive technologies have effects on the demography of monozygotic twinning?, Fertil Steril, 74, 178, 10.1016/S0015-0282(00)00557-4 · DOI
  119. Saravelos, 2016, Monochorionic quadramniotic and triamniotic pregnancies following single embryo transfers: two case reports and a review of the literature, J Assist Reprod Genet, 33, 27, 10.1007/s10815-015-0611-2 · DOI
  120. Schiewe, 2015, Potential risk of monochorionic dizygotic twin blastocyst formation associated with early laser zona dissection of group cultured embryos, Fertil Steril, 103, 417, 10.1016/j.fertnstert.2014.11.009 · DOI
  121. Schimmel, 2014, Laser-assisted zona pellucida thinning does not facilitate hatching and may disrupt the in vitro hatching process: a morphokinetic study in the mouse, Hum Reprod, 29, 2670, 10.1093/humrep/deu245 · DOI
  122. Sciorio, 2021, Focus on time-lapse analysis: blastocyst collapse and morphometric assessment as new features of embryo viability, Reprod Biomed Online, 43, 821, 10.1016/j.rbmo.2021.08.008 · DOI
  123. Semrl, 2023, Birth of monozygotic dichorionic twins after a single blastocyst embryo transfer: a case report of genetic determination of zygosity, F S Rep, 4, 231
  124. Seshagiri, 2009, Cellular and molecular regulation of mammalian blastocyst hatching, J Reprod Immunol, 83, 79, 10.1016/j.jri.2009.06.264 · DOI
  125. Sharara, 2010, Incidence of monozygotic twins in blastocyst and cleavage stage assisted reproductive technology cycles, Fertil Steril, 93, 642, 10.1016/j.fertnstert.2008.12.130 · DOI
  126. Shibuya, 2012, A successful birth of healthy monozygotic dichorionic diamniotic (DD) twins of the same gender following a single vitrified-warmed blastocyst transfer, J Assist Reprod Genet, 29, 255, 10.1007/s10815-011-9707-5 · DOI
  127. Sills, 2000, Human zona pellucida micromanipulation and monozygotic twinning frequency after IVF, Hum Reprod, 15, 890, 10.1093/humrep/15.4.890 · DOI
  128. Skiadas, 2008, Risk factors associated with pregnancies containing a monochorionic pair following assisted reproductive technologies, Hum Reprod, 23, 1366, 10.1093/humrep/den045 · DOI
  129. Sobek, 2015, High incidence of monozygotic twinning after assisted reproduction is related to genetic information, but not to assisted reproduction technology itself, Fertil Steril, 103, 756, 10.1016/j.fertnstert.2014.12.098 · DOI
  130. Song, 2022, Functional substitution of zona pellucida with modified sodium hyaluronate gel in human embryos, J Assist Reprod Genet, 39, 2669, 10.1007/s10815-022-02609-7 · DOI
  131. Steinman, 2001, Mechanisms of twinning. II. Laterality and intercellular bonding in monozygotic twinning, J Reprod Med, 46, 473
  132. Steinman, 2001, Mechanisms of twinning. IV. Sex preference and lactation, J Reprod Med, 46, 1003
  133. Steinman, 2003, Mechanisms of twinning. VI. Genetics and the etiology of monozygotic twinning in in vitro fertilization, J Reprod Med, 48, 583
  134. Steinman, 2001, Mechanisms of twinning. III. Placentation, calcium reduction and modified compaction, J Reprod Med, 46, 995
  135. Sun, 2021, A novel homozygous variant in ZP2 causes abnormal zona pellucida formation and female infertility, J Assist Reprod Genet, 38, 1239, 10.1007/s10815-021-02107-2 · DOI
  136. Sundaram, 2018, Multi-chorionic pregnancies following single embryo transfer at the blastocyst stage: a case series and review of the literature, J Assist Reprod Genet, 35, 2109, 10.1007/s10815-018-1329-8 · DOI
  137. Sutherland, 2019, Time-lapse imaging of inner cell mass splitting with monochorionic triamniotic triplets after elective single embryo transfer: a case report, Reprod Biomed Online, 38, 491, 10.1016/j.rbmo.2018.12.017 · DOI
  138. Swain, 2021, Fused blastocysts as a consequence of group embryo culture: observations, complications, and potential solutions, F S Rep, 2, 133
  139. Széll, 1991, Factors affecting the survival of bisected sheep embryos in vivo, Theriogenology, 36, 379, 10.1016/0093-691X(91)90466-Q · DOI
  140. Takehara, 2014, Dizygotic twin pregnancy after single embryo transfer: a case report and review of the literature, J Assist Reprod Genet, 31, 443, 10.1007/s10815-013-0170-3 · DOI
  141. Tandberg, 2007, Increasing twinning rates in Norway, 1967-2004: the influence of maternal age and assisted reproductive technology (ART), Acta Obstet Gynecol Scand, 86, 833, 10.1080/00016340701417323 · DOI
  142. Tang, 2012, Embryo splitting can increase the quantity but not the quality of blastocysts, Taiwan J Obstet Gynecol, 51, 236, 10.1016/j.tjog.2012.04.012 · DOI
  143. Tarkowski, 1982, A method for obtaining chimaeric mouse blastocysts with two separate inner cell masses: a preliminary report, Development, 71, 215, 10.1242/dev.71.1.215 · DOI
  144. Toledo, 2005, Is there increased monozygotic twinning after assisted reproductive technology?, Aust N Z J Obstet Gynaecol, 45, 360, 10.1111/j.1479-828X.2005.00451.x · DOI
  145. Tsunoda, 1985, Production of monozygotic twins following the transfer of bisected embryos in the goats, Theriogenology, 24, 337, 10.1016/0093-691X(85)90225-0 · DOI
  146. Ueno, 2014, Developmental potential of zona pellucida-free oocytes obtained following mild in vitro fertilization, Fertil Steril, 102, 1602, 10.1016/j.fertnstert.2014.08.025 · DOI
  147. Vajta, 2008, The Well-of-the-Well system: an efficient approach to improve embryo development, Reprod Biomed Online, 17, 73, 10.1016/S1472-6483(10)60296-9 · DOI
  148. Vajta, 2000, New method for culture of zona-included or zona-free embryos: the Well of the Well (WOW) system, Mol Reprod Dev, 55, 256, 10.1002/(SICI)1098-2795(200003)55:3<256::AID-MRD3>3.0.CO;2-7 · DOI
  149. Vajta, 2010, Zona-free embryo culture: is it a viable option to improve pregnancy rates?, Reprod Biomed Online, 21, 17, 10.1016/j.rbmo.2010.03.014 · DOI
  150. van der Hoorn, 2011, Dizygotic twin pregnancy after transfer of one embryo, Fertil Steril, 95, 805.e1, 10.1016/j.fertnstert.2010.08.026 · DOI
  151. van Dongen, 2021, Identical twins carry a persistent epigenetic signature of early genome programming, Nat Commun, 12, 5618, 10.1038/s41467-021-25583-7 · DOI
  152. van Dongen, 2024, New insights into the (epi)genetics of twinning, Hum Reprod, 39, 35, 10.1093/humrep/dead131 · DOI
  153. Van Langendonckt, 2000, Atypical hatching of a human blastocyst leading to monozygotic twinning: a case report, Fertil Steril, 74, 1047, 10.1016/S0015-0282(00)01554-5 · DOI
  154. Vela, 2011, Monozygotic pregnancies conceived by in vitro fertilization: understanding their prognosis, Fertil Steril, 95, 606, 10.1016/j.fertnstert.2010.04.001 · DOI
  155. Vitthala, 2009, The risk of monozygotic twins after assisted reproductive technology: a systematic review and meta-analysis, Hum Reprod Update, 15, 45, 10.1093/humupd/dmn045 · DOI
  156. Vitucci, 2020, Twin reversed arterial perfusion sequence: current treatment options, Int J Womens Health, 12, 435, 10.2147/IJWH.S214254 · DOI
  157. Waheed, 2009, Monozygotic twin formation in mouse embryos in vitro, J Duhok Univ, 12, 167
  158. Wang, 2018, Asymmetric expression of LincGET biases cell fate in two-cell mouse embryos, Cell, 175, 1887, 10.1016/j.cell.2018.11.039 · DOI
  159. Waszak, 2017, Effects of intrauterine environment on the magnitude of differences within the pairs of monozygotic and dizygotic twins, Twin Res Hum Genet, 20, 72, 10.1017/thg.2016.91 · DOI
  160. Watson, 2021, Live birth in a complete zona-free patient: a case report, J Assist Reprod Genet, 38, 1109, 10.1007/s10815-021-02114-3 · DOI
  161. Weatherbee, 2023, A model of the post-implantation human embryo derived from pluripotent stem cells, Nature, 622, 584, 10.1038/s41586-023-06368-y · DOI
  162. Willadsen, 1980, The viability of early cleavage stages containing half the normal number of blastomeres in the sheep, J Reprod Fertil, 59, 357, 10.1530/jrf.0.0590357 · DOI
  163. Willadsen, 1989, Cloning of sheep and cow embryos, Genome, 31, 956, 10.1139/g89-167 · DOI
  164. Willadsen, 1984, A simple procedure for the production of identical sheep twins, Vet Rec, 114, 240, 10.1136/vr.114.10.240 · DOI
  165. Willadsen, 1981, Attempts to produce monozygotic quadruplets in cattle by blastomere separation, Vet Rec, 108, 211, 10.1136/vr.108.10.211 · DOI
  166. Williams, 1984, Pregnancy rates with bisected bovine embryos, Theriogenology, 22, 521, 10.1016/0093-691X(84)90051-7 · DOI
  167. Wu, 2014, Monozygotic twinning after in vitro fertilization/intracytoplasmic sperm injection treatment is not related to advanced maternal age, intracytoplasmic sperm injection, assisted hatching, or blastocyst transfer, Taiwan J Obstet Gynecol, 53, 324, 10.1016/j.tjog.2014.07.001 · DOI
  168. Yan, 2015, Eight-shaped hatching increases the risk of inner cell mass splitting in extended mouse embryo culture, PLoS One, 10, e0145172, 10.1371/journal.pone.0145172 · DOI
  169. Yu, 2021, Blastocyst-like structures generated from human pluripotent stem cells, Nature, 591, 620, 10.1038/s41586-021-03356-y · DOI
  170. Zeng, 2023, Identification of zona pellucida defects revealed a novel loss-of-function mutation in ZP2 in humans and rats, Front Endocrinol (Lausanne), 14, 1169378, 10.3389/fendo.2023.1169378 · DOI
  171. Zenker, 2018, Expanding actin rings zipper the mouse embryo for blastocyst formation, Cell, 173, 776, 10.1016/j.cell.2018.02.035 · DOI
  172. Zenker, 2017, A microtubule-organizing center directing intracellular transport in the early mouse embryo, Science, 357, 925, 10.1126/science.aam9335 · DOI
  173. Zhang, 2016, Eph/ephrin signaling maintains the boundary of dorsal forerunner cell cluster during morphogenesis of the zebrafish embryonic left-right organizer, Development, 143, 2603
  174. Zhou, 2022, Can successful pregnancy be achieved and predicted from patients with identified ZP mutations? A literature review, Reprod Biol Endocrinol, 20, 166, 10.1186/s12958-022-01046-6 · DOI
  175. Zhou, 2019, Novel mutations in ZP1, ZP2, and ZP3 cause female infertility due to abnormal zona pellucida formation, Hum Genet, 138, 327, 10.1007/s00439-019-01990-1 · DOI

Cited by

Sorted by citations

Metadata

Authors
Jin, H., Han, Y., & Zenker, J.
Affiliations
  • Australian Regenerative Medicine Institute (AU)
  • University of California, Berkeley (US)
Corresponding author
Zenker, Jennifer
ORCID
Venue
Human Reproduction Update
Publisher
Oxford University Press (OUP)
Published
2024-07-12
Volume
30
Issue
6
Pages
692-705
ISSN
  • 1355-4786 (ISSN-L)
  • 1460-2369
DOI
10.1093/humupd/dmae022
PMC
PMC11532623
OpenAlex
W4400577917
Cited by
24
References
0
Citations by year
2026: 15 · 2025: 8 · 2024: 1
FWCI
2.24
Type
journal article
Language
en
Open access
Licence
Locations
  • Human Reproduction Update (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
  • National Health and Medical Research Council (APP2002507, APP2009409)
  • Sylvia & Charles Viertel Senior Medical
  • Canadian Institute for Advanced Research
  • The Australian Regenerative Medicine Institute
  • State Government of Victoria
  • Australian Government
Topics
  • Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Assisted Reproductive Technology and Twin Pregnancy
  • Health Sciences › Medicine › Reproductive Medicine › Reproductive Biology and Fertility
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Keywords
monozygotic twinning, monochorionic twins, dichorionic twins, embryo compaction, blastocoel formation, single blastocyst transfer, assisted reproduction, embryo aggregation, embryo cloning
MeSH terms
Animals, Blastocyst, Chorion, Embryo Transfer, Female, Humans, Pregnancy, Twins, Monozygotic, Reproductive Techniques, Assisted, Twinning, Monozygotic, Embryonic Development

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