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A Review of the Mechanisms and Evidence for Typical and Atypical Twinning Helen C

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A Review of the Mechanisms and Evidence for Typical and Atypical Twinning Helen C Expert Reviews ajog.org OBSTETRICS A review of the mechanisms and evidence for typical and atypical twinning Helen C. McNamara, MB, BS; Stefan C. Kane, MB, BS; Jeffrey M. Craig, PhD; Roger V. Short, ScD; Mark P. Umstad, MD mirror-image twins, polar body twins, The mechanisms responsible for twinning and disorders of twin gestations have been the complete hydatidiform mole with coex- subject of considerable interest by physicians and scientists, and cases of atypical istent twin, vanishing twins, fetus papy- twinning have called for a reexamination of the fundamental theories invoked to explain raceus, fetus in fetu, superfetation, and twin gestations. This article presents a review of the literature focusing on twinning and superfecundation. A detailed discussion atypical twinning with an emphasis on the phenomena of chimeric twins, phenotypically of monoamniotic twins, conjoined discordant monozygotic twins, mirror-image twins, polar body twins, complete hydati- twins, and twin-reversed arterial perfu- diform mole with a coexistent twin, vanishing twins, fetus papyraceus, fetus in fetu, sion sequence is beyond the scope of superfetation, and superfecundation. The traditional models attributing monozygotic this review and has been presented twinning to a fission event, and more recent models describing monozygotic twinning as elsewhere.1,2 a fusion event, are critically reviewed. Ethical restrictions on scientific experimentation with human embryos and the rarity of cases of atypical twinning have limited opportu- Traditional models of twinning nities to elucidate the exact mechanisms by which these phenomena occur. Refinements Traditionally it has been thought that in the modeling of early embryonic development in twin pregnancies may have significant dizygotic twins result from fertilization clinical implications. The article includes a series of figures to illustrate the phenomena of 2 distinct ova by 2 separate sperma- described. tozoa, whereas monozygotic twins are the product of a single ovum and sperm Key words: assisted reproductive technologies, chimeric twins, complete hydatidiform that subsequently divide to form 2 mole with coexistent twin, dizygotic, fetus in fetu, fetus papyraceus, mirror-image twins, embryos.1 monozygotic, twins, phenotypically discordant monozygotic twins, polar body twins, Widely accepted models of mono- superfecundation, superfetation, vanishing twin zygotic twinning are based on the un- proven hypothesis of postzygotic division of the conceptus (Figure 1). In this idespread use of assisted repro- Traditional models of twinning pertain- model, the number of fetuses, chorions, W ductive technologies (ART) in- ing to a fission event have been con- and amnions are determined by the volving the manipulation of the natural tested. New models involving fusion of timing of the embryo splitting (Table 1). mechanisms of fertilization and im- fetal membranes have been proposed. Proposed triggers for splitting include plantation has been accompanied by an This article presents a review of the postzygotic gene mutations, abnormal- increasing number of reports of atypical literature regarding the typical and ities in cell surface proteins, and abnor- twinning. Cases of atypical twinning atypical twinning, highlighting the phe- malities in the formation of the zona have inspired a reexamination of the nomena of chimeric twins, phenotypi- pellucida.3 The incidence of mono- fundamental theories of twinning. cally discordant monozygotic twins, zygotic twins is increased 2- to 5-fold in ART pregnancies,3 which might be pre- disposed to splitting because of From the Department of Maternal-Fetal Medicine (Dr McNamara, Dr Kane and Dr Umstad), Royal Womens Hospital, Department of Obstetrics and Gynaecology (Dr Kane and Dr Umstad), and handling, media, and microinjection or Faculty of Medicine, Dentistry and Health Sciences (Dr Short), University of Melbourne, and because of the intrinsic abnormalities Murdoch Childrens Research Institute (Dr Craig), Royal Children’s Hospital, Melbourne, Victoria, associated with infertility.4-6 Australia. It has conventionally been asserted Received March 2, 2015; revised Oct. 28, 2015; accepted Oct. 29, 2015. that monochorionicity confirms mono- J.M.C. is supported by grants from the Australian National Health and Medical Research Council zygosity, opposite-sex twins confirm (grants 1011070 and 1083779), the Financial Markets Foundation for Children (grant 032-2007), and dizygosity, and same-sex dichorionic ’ ’ the Murdoch Children s Research Institute, which is funded by the Victorian Government s twins remain of uncertain zygosity until Operational Infrastructure Support Program. S.C.K. is supported by a postgraduate scholarship from 7 the Australian National Health and Medical Research Council. postnatal evaluation occurs. The authors report no conflict of interest. New models of twinning Corresponding author: Mark P. Umstad, MD. [email protected] In 2013 Herranz8 argued that the 0002-9378/$36.00 ª 2016 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ajog.2015.10.930 hitherto-unchallenged hypothesis of 172 American Journal of Obstetrics & Gynecology FEBRUARY 2016 ajog.org Obstetrics Expert Reviews FIGURE 1 The traditional model of twinning Dizygotic twins are the product of 2 distinct fertilization events, resulting in dichorionic diamniotic twins with each conceptus developing to become a genetically distinct individual. Monozygotic twins result from postzygotic splitting of the product of a single fertilization event. Splitting on days 1e3 (up to the morula stage) results in dichorionic diamniotic twins, on days 3e8 (during which blastocyst hatching occurs) in monochorionic diamniotic twins, on days 8e13 in monochorionic monoamniotic twins, and if no split has occurred by day 13, in conjoined twins (not shown). In this diagram, 2 of the 3 oocyte-derived polar bodies are shown at the zygote stage. McNamara. Typical and atypical twinning. Am J Obstet Gynecol 2016. postzygotic splitting lacked scientific Herranz8 offered an alternative theory Denker9 opposed Herranz’s argu- proof. He argued that factors that initiate of twinning based on the following 2 ment, emphasizing that a lack of cleavage have not been specified, that principles: (1) monozygotic twinning oc- evidence may stem from ethical limita- coexistenceofseparateembryoswithina curs at the first cleavage division of the tions on scientific experimentation with single zona pellucida is unlikely, that zygote and (2) subsequent chorionicity human embryos. He highlighted that postzygotic splitting becomes more un- and amnionicity is determined by the data regarding twinning mechanisms in likely with the passage of time, and that degree offusion of embryonicmembranes animals, differences in the nature of the splitting has never been observed in vitro. within the zona pellucida (Figure 2). zona pellucida in vivo and in vitro, and FEBRUARY 2016 American Journal of Obstetrics & Gynecology 173 Expert Reviews Obstetrics ajog.org monochorionic twins may lead to erro- TABLE 1 neous conclusions.36 Chorionicity and amnionicity by time of zygote splitting Zygosity Twins Time of split Chorions Amnions Fetal mass Phenotypically discordant Dizygotic DC DA No split 2 2 2 monozygotic twins Phenotypic discordance in monozygotic Monozygotic DC DA Days 1e32 2 2 twins commonly occurs as a conse- Monozygotic MC DA Days 3e81 2 2 quence of epigenetic, mitochondrial, Monozygotic MC MA Days 8e13 1 1 2 and genetic discordance.1,37,38 Epige- Monozygotic Conjoined After day 13 1 1 1 netics has been implicated as a mediator of stochastic and twin-specific environ- DA, diamniotic; DC, dichorionic; MA, monoamniotic; MC, monochorionic. mental factors.39-41 Genetic differences McNamara. Typical and atypical twinning. Am J Obstet Gynecol 2016. within monozygotic pairs must arise de novo soon after zygotic cleavage if they are found in multiple somatic the developmental potential of cell line- twins with confined hematological and/ tissues and later in development if they ages after fertilization were not dis- or tissue chimerism have been reported are mosaic.42 Such differences can be cussed. Denker9 concluded that both the (Appendix 1).7,12,16-29 single base pair mutations42,43 or copy traditional fission model and Herranz’s Concerns have been raised that number variation44,45 or involve whole fusion model were unsubstantiated. chimeric twins might exhibit reproduc- chromosomes.46 Further examination of twinning tive dysfunction analogous to that of the On a genome-scale, the frequency of processes in typical and atypical twins bovine freemartin.30 Early follow-up epigenetic differences within mono- might confirm which, if either, of these studies described normal genitalia, go- zygotic pairs is likely to be high.39,40 Less models is more accurate. nads and endocrinological function in is known about the frequency of genetic gender-discordant chimeric twins to a discordance in monozygotic twins, Atypical twinning maximum of 18 months of age. How- although it is likely to be low.47,48 A review of the evidence for atypical ever, in 2013 Choi et al26 reported a case However, more genetic variation might twinning provides insights into the of MCDZ twins complicated by death in occur outside coding regions.49 Little is mechanisms of twinning and challenges utero of the female twin and severe known about the frequency of mito- aspects of traditional models of gonadal failure in the male cotwin. The chondrial discordance in twins.50 twinning.
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