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A review of the mechanisms and evidence for typical and atypical twinning

Published:November 05, 2015DOI:https://doi.org/10.1016/j.ajog.2015.10.930
      The mechanisms responsible for twinning and disorders of twin gestations have been the subject of considerable interest by physicians and scientists, and cases of atypical twinning have called for a reexamination of the fundamental theories invoked to explain twin gestations. This article presents a review of the literature focusing on twinning and atypical twinning with an emphasis on the phenomena of chimeric twins, phenotypically discordant monozygotic twins, mirror-image twins, polar body twins, complete hydatidiform mole with a coexistent twin, vanishing twins, fetus papyraceus, fetus in fetu, superfetation, and superfecundation. The traditional models attributing monozygotic twinning to a fission event, and more recent models describing monozygotic twinning as a fusion event, are critically reviewed. Ethical restrictions on scientific experimentation with human embryos and the rarity of cases of atypical twinning have limited opportunities to elucidate the exact mechanisms by which these phenomena occur. Refinements in the modeling of early embryonic development in twin pregnancies may have significant clinical implications. The article includes a series of figures to illustrate the phenomena described.

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      References

        • Hall J.
        Twinning.
        Lancet. 2003; 362: 735-743
        • Weber M.
        • Sebire N.
        Genetics and developmental pathology of twinning.
        Semin Fetal Neonatal Med. 2010; 15: 313-318
        • Kilby M.
        • Baker P.
        • Critchley H.
        • Field D.
        Consensus views arising from the 50th study group: multiple pregnancy.
        RCOG Press, London2006: 283-286
        • Derom C.
        • Vlietinck R.
        • Derom R.
        • Van den Berghe H.
        • Thiery M.
        Increased monozygotic twinning rate after ovulation induction.
        Lancet. 1987; 1: 1236-1238
        • Alikani M.
        • Noyes N.
        • Cohen J.
        • Rosenwaks Z.
        Monozygotic twinning in the human is associated with the zona pellucida architecture.
        Hum Reprod. 1994; 9: 1318-1321
        • Blickstein I.
        • Verhoeven H.C.
        • Keith L.G.
        Zygotic splitting after assisted reproduction.
        N Engl J Med. 1999; 340: 738-739
        • Umstad M.P.
        • Short R.V.
        • Wilson M.
        • Craig J.M.
        Chimaeric twins: why monochorionicity does not guarantee monozygosity.
        Aust N Z J Obstet Gynaecol. 2012; 52: 305-307
        • Herranz G.
        The timing of monozygotic twinning: a criticism of the common model.
        Zygote. 2013; : 1-14
        • Denker H.W.
        Comment on G. Herranz: The timing of monozygotic twinning: a criticism of the common model. Zygote (2013).
        Zygote. 2013; : 1-3
        • van Dijk B.A.
        • Boomsma D.I.
        • de Man A.J.M.
        Blood group chimerism in human multiple births is not rare.
        Am J Med Genet. 1996; 61: 264-268
        • Robinson E.
        • North D.
        • Horsfield G.
        • Kelly F.
        A case of twin chimerism.
        J Med Genet. 1976; 13: 528-530
        • Viëtor H.E.
        • Hamel B.C.
        • van Bree S.P.
        • et al.
        Immunological tolerance in an HLA non-identical chimeric twin.
        Hum Immunol. 2000; 61: 190-192
        • Sudik R.
        • Jakubiczka S.
        • Nawroth F.
        • Gilberg E.
        • Wieacker P.
        Chimerism in a fertile woman with 46,XY karyotype and female phenotype.
        Hum Reprod. 2001; 16: 56-58
        • Nylander P.P.
        • Osunkoya B.O.
        Unusual monochorionic placentation with heterosexual twins.
        Obstet Gynecol. 1970; 36: 621-625
        • Souter V.L.
        • Kapur R.P.
        • Nyholt D.R.
        • et al.
        A report of dizygous monochorionic twins.
        N Engl J Med. 2003; 349: 154-158
        • Quintero R.A.
        • Mueller O.
        • Martínez J.
        • et al.
        Twin-twin transfusion syndrome in a dizygotic monochorionic-diamniotic twin pregnancy.
        J Matern Fetal Neonatal Med. 2003; 14: 279-281
        • Williams C.A.
        • Wallace M.R.
        • Drury K.C.
        • et al.
        Blood lymphocyte chimerism associated with IVF and monochorionic dizygous twinning: case report.
        Hum Reprod. 2004; 19: 2816-2821
        • Ginsberg N.A.
        • Ginsberg S.
        • Rechitsky S.
        • Verlinsky Y.
        Fusion as the etiology of chimerism in monochorionic dizygotic twins.
        Fetal Diagn Ther. 2005; 20: 20-22
        • Miura K.
        • Niikawa N.
        Do monochorionic dizygotic twins increase after pregnancy by assisted reproductive technology?.
        J Hum Genet. 2005; 50: 1-6
        • Yoon G.
        • Beischel L.S.
        • Johnson J.P.
        • Jones M.C.
        Dizygotic twin pregnancy conceived with assisted reproductive technology associated with chromosomal anomaly, imprinting disorder, and monochorionic placentation.
        J Pediatr. 2005; 146: 565-567
        • Aoki R.
        • Honma Y.
        • Yada Y.
        • Momoi M.Y.
        • Iwamoto S.
        Blood chimerism in monochorionic twins conceived by induced ovulation: case report.
        Hum Reprod. 2005; 21: 735-737
        • Walker S.P.
        • Meagher S.
        • White S.M.
        Confined blood chimerism in monochorionic dizygous (MCDZ) twins.
        Prenat Diagn. 2007; 27: 369-372
        • Ekelund C.K.
        • Skibsted L.
        • Søgaard K.
        • et al.
        Dizygotic monochorionic twin pregnancy conceived following intracytoplasmic sperm injection treatment and complicated by twin-twin transfusion syndrome and blood chimerism.
        Ultrasound Obstet Gynecol. 2008; 32: 832-834
        • Hackmon R.
        • Jormark S.
        • Cheng V.
        • O'Reilly Green C.
        • Divon M.Y.
        Monochorionic dizygotic twins in a spontaneous pregnancy: a rare case report.
        J Matern Fetal Neonatal Med. 2009; 22: 708-710
        • Assaf S.A.
        • Randolph L.M.
        • Benirschke K.
        • Wu S.
        • Samadi R.
        • Chmait R.H.
        Discordant blood chimerism in dizygotic monochorionic laser-treated twin–twin transfusion syndrome.
        Obstet Gynecol. 2010; 116: 483-485
        • Choi D.H.
        • Kwon H.
        • Lee S.D.
        • et al.
        Testicular hypoplasia in monochorionic dizygous twin with confined blood chimerism.
        J Assist Reprod Genet. 2013; 30: 1487-1491
        • Fumoto S.
        • Hosoi K.
        • Ohnishi H.
        • et al.
        Chimerism of buccal membrane cells in a monochorionic dizygotic twin.
        Pediatrics. 2014; 133: e1097-e1100
        • Lee O.J.
        • Lee O.J.
        • Cho D.
        • et al.
        The first known case of blood group chimerism in monochorionic dizygotic twins in Korea.
        Ann Lab Med. 2014; 34: 259-262
        • Lee H.J.
        • Yoon S.C.
        • Ko J.M.
        • et al.
        Monochorionic dizygotic twins with discordant sex and confined blood chimerism.
        Eur J Pediatr. 2014; 173: 1249-1252
        • Short R.V.
        The bovine freemartin: a new look at an old problem.
        Philos Trans R Soc Lond B Biol Sci. 1970; 259: 141-147
        • Chen K.
        • Chmait R.H.
        • Vanderbilt D.
        • Wu S.
        • Randolph L.
        Chimerism in monochorionic dizygotic twins: case study and review.
        Am J Med Genet A. 2013; 161: 1817-1824
        • Hawcutt D.
        • Hammond B.
        • Sibbring J.
        • et al.
        Twin-twin confusion syndrome: blood chimerism in opposite sex dizygotic twins.
        J Obstet Gynaecol. 2011; 31: 446-448
        • Papadaki L.
        Binovular follicles in the adult human ovary.
        Fertil Steril. 1978; 29: 342-350
        • Tarkowski A.K.
        • Wojewodzka M.
        A method for obtaining chimaeric mouse blastocysts with two separate inner cell masses: a preliminary report.
        J Embryol Exp Morphol. 1982; 71: 215-221
        • La Sala G.B.
        • Villani M.T.
        • Nicoli A.
        • Gallinelli A.
        • Nucera G.
        • Blickstein I.
        Effect of the mode of assisted reproductive technology conception on obstetric outcomes for survivors of the vanishing twin syndrome.
        Fertil Steril. 2006; 86: 247-249
        • Ollikainen M.
        • Smith K.R.
        • Joo E.J.H.
        • et al.
        DNA methylation analysis of multiple tissues from newborn twins reveals both genetic and intrauterine components to variation in the human neonatal epigenome.
        Hum Mol Genet. 2010; 19: 4176-4188
        • Machin G.
        Some causes of genotypic and phenotypic discordance in monozygotic twin pairs.
        American journal of medical genetics. 1996; 61: 216-228
        • Czyz W.
        • Morahan J.M.
        • Ebers G.C.
        • Ramagopalan S.V.
        Genetic, environmental and stochastic factors in monozygotic twin discordance with a focus on epigenetic differences.
        BMC Med. 2012; 10: 93
        • Gordon L.
        • Joo J.E.
        • Powell J.E.
        • et al.
        Neonatal DNA methylation profile in human twins is specified by a complex interplay between intrauterine environmental and genetic factors, subject to tissue-specific influence.
        Genome Res. 2012; 22: 1395-1406
        • Loke Y.J.
        • Galati J.C.
        • Morley R.
        • et al.
        Association of maternal and nutrient supply line factors with DNA methylation at the imprinted IGF2/H19 locus in multiple tissues of newborn twins.
        Epigenetics. 2013; 8: 1069-1079
        • van Dongen J.
        • Ehli E.A.
        • Slieker R.C.
        • et al.
        Epigenetic variation in monozygotic twins: a genome-wide analysis of DNA methylation in buccal cells.
        Genes. 2014; 5: 347-365
        • Vadlamudi L.
        • Dibbens L.M.
        • Lawrence K.M.
        • et al.
        Timing of de novo mutagenesis–a twin study of sodium-channel mutations.
        N Engl J Med. 2010; 363: 1335-1340
        • Li R.
        • Montpetit A.
        • Rousseau M.
        • et al.
        Somatic point mutations occurring early in development: a monozygotic twin study.
        J Med Genet. 2014; 51: 28-34
        • Breckpot J.
        • Thienpont B.
        • Gewillig M.
        • Allegaert K.
        • Vermeesch J.R.
        • Devriendt K.
        Differences in copy number variation between discordant monozygotic twins as a model for exploring chromosomal mosaicism in congenital heart defects.
        Mol Syndromol. 2011; 2: 81-87
        • Ehli E.A.
        • Abdellaoui A.
        • Hu Y.
        • et al.
        De novo and inherited CNVs in MZ twin pairs selected for discordance and concordance on Attention Problems.
        Eur J Hum Genet. 2012; 20: 1037-1043
        • Edwards J.H.
        • Dent T.
        • Kahn J.
        Monozygotic twins of different sex.
        J Med Genet. 1966; 3: 117-123
        • Petersen B.-S.
        • Spehlmann M.
        • Raedler A.
        • et al.
        Whole genome and exome sequencing of monozygotic twins discordant for Crohn's disease.
        BMC Genomics. 2014; 15: 564
        • Abdellaoui A.
        • Ehli E.A.
        • Hottenga J.-J.
        • et al.
        CNV concordance in 1,097 MZ twin pairs.
        Twin Res Hum Genet. 2015; 18: 1-12
        • Yadav S.K.
        • Kumari A.
        • Javed S.
        • Ali S.
        DYZ1 arrays show sequence variation between the monozygotic males.
        BMC Genet. 2014; 15: 19
        • Detjen A.K.
        • Tinschert S.
        • Kaufmann D.
        • Algermissen B.
        • Nürnberg P.
        • Schuelke M.
        Analysis of mitochondrial DNA in discordant monozygotic twins with neurofibromatosis type 1.
        Twin Res Hum Genet. 2007; 10: 486-495
        • Springer S.P.
        • Searleman A.
        Laterality in twins: the relationship between handedness and hemispheric asymmetry for speech.
        Behav Genet. 1978; 8: 349-357
        • Rife D.C.
        Genetic studies of monozygotic twins: III. Mirror-imaging.
        J Hered. 1933; 24: 443-446
        • Sperber G.H.
        • Machin G.A.
        • J B.F.
        Mirror-image dental fusion and discordance in monozygotic twins.
        Am J Med Genet. 1994; 51: 41-45
        • Dirani M.
        • Chamberlain M.
        • Garoufalis P.
        • Chen C.Y.
        • Guymer R.H.
        • Baird P.N.
        Mirror-image congenital esotropia in monozygotic twins.
        J Pediatr Ophthalmol Strabismus. 2006; 43: 170-171
        • Hu J.T.
        • Liu T.
        • Qian J.
        • Zhang Y.B.
        • Zhou X.
        • Zhang Q.G.
        Occurrence of different external ear deformities in monozygotic twins: report of 2 cases.
        Plast Reconstr Surg Glob Open. 2014; 2: e206
        • Novak R.W.
        Laryngotracheoesophageal cleft and unilateral pulmonary hypoplasia in twins.
        Pediatrics. 1981; 67: 732-734
        • Karaca C.
        • Yilmaz M.
        • Karatas O.
        • Menderes A.
        • Karademir S.
        Mirror imaging cleft lip in monozygotic twins.
        Eur J Plast Surg. 1995; 18: 260-261
        • Satoh K.
        • Shibata Y.
        • Tokushige H.
        • Onizuka T.
        A mirror image of the first and second branchial arch syndrome associated with cleft lip and palate in monozygotic twins.
        Br J Plast Surg. 1995; 48: 601-605
        • Riess A.
        • Dufke A.
        • Riess O.
        • et al.
        Mirror-image asymmetry in monozygotic twins with kabuki syndrome.
        Mol Syndromol. 2012; 3: 94-97
        • Wang E.D.
        • Xu X.
        • Dagum A.B.
        Mirror-image trigger thumb in dichorionic identical twins.
        Orthopedics. 2012; 35: e981-e983
        • Goto T.
        • Nemoto T.
        • Okuma T.
        • Kobayashi H.
        • Funata N.
        Mirror-image solitary bone cyst of the humerus in a pair of mirror-image monozygotic twins.
        Arch Orthop Trauma Surg. 2008; 128: 1403-1406
        • Morison D.
        • Reyes C.V.
        • Skorodin M.S.
        Mirror-image tumors in mirror-image twins.
        Chest. 1994; 106: 608-610
        • Pascual-Castroviejo I.
        • Verdú A.
        • Román M.
        • De la Cruz-Medina M.
        • Villarejo F.
        Optic glioma with progressive occlusion of the aqueduct of sylvius in monozygotic twins with neurofibromatosis.
        Brain Dev. 1988; 10: 24-29
        • Nigro M.A.
        • Wishnow R.
        • Maher L.
        Colpocephaly in identical twins.
        Brain Dev. 1991; 13: 187-189
        • Helland C.A.
        • Wester K.
        Monozygotic twins with mirror image cysts: indication of a genetic mechanism in arachnoid cysts?.
        Neurology. 2007; 69: 110-111
        • Zhou J.Y.
        • Pu J.L.
        • Chen S.
        • Hong Y.
        • Ling C.H.
        • Zhang J.M.
        Mirror-image arachnoid cysts in a pair of monozygotic twins: a case report and review of the literature.
        Int J Med Sci. 2011; 8: 402-405
        • Thacker D.
        • Gruber P.J.
        • Weinberg P.M.
        • Cohen M.S.
        Heterotaxy syndrome with mirror image anomalies in identical twins.
        Congenit Heart Dis. 2009; 4: 50-53
        • Hwang M.S.
        • Su W.J.
        • Lin J.L.
        Asplenia syndrome in a pair of monozygotic twins.
        Acta Paediatr. 2006; 95: 500-501
        • Derom C.
        • Thiery E.
        • Vlietinck R.
        • Loos R.
        • Derom R.
        Handedness in twins according to zygosity and chorion type: A preliminary report.
        Behav Genet. 1996; 26: 407-408
        • Sommer I.E.
        • Ramsey N.F.
        • Bouma A.
        • Kahn R.S.
        Cerebral mirror-imaging in a monozygotic twin.
        Lancet. 1999; 354: 1445-1446
        • Medland S.E.
        • Wright M.J.
        • Geffen G.M.
        • et al.
        Special twin environments, genetic influences and their effects on the handedness of twins and their siblings.
        Twin Res. 2003; 6: 119-130
        • Medland S.E.
        • Duffy D.L.
        • Wright M.J.
        • et al.
        Genetic influences on handedness: data from 25,732 Australian and Dutch twin families.
        Neuropsychologia. 2009; 47: 330-337
        • Siebert J.R.
        • Machin G.A.
        • Sperber G.H.
        Anatomic findings in dicephalic conjoined twins: implications for morphogenesis.
        Teratology. 1989; 40: 305-310
        • Ooki S.
        An overview of human handedness in twins.
        Front Psychol. 2014; : 5
        • Schmerler S.
        • Wessel G.M.
        Polar bodies-more a lack of understanding than a lack of respect.
        Mol Reprod Dev. 2011; 78: 3-8
        • Bieber F.R.
        • Nance W.E.
        • Morton C.C.
        • et al.
        Genetic studies of an acardiac monster: evidence of polar body twinning in man.
        Science. 1981; 213: 775-777
        • Fisk N.M.
        • Ware M.
        • Stanier P.
        • Moore G.
        • Bennett P.
        Molecular genetic etiology of twin reversed arterial perfusion sequence.
        Am J Obstet Gynecol. 1996; 174: 891-894
        • Bristow R.E.
        • Shumway J.B.
        • Khouzami A.N.
        • Witter F.R.
        Complete hydatidiform mole and surviving coexistent twin.
        Obstet Gynecol Surv. 1996; 51: 705-709
        • Fishman D.A.
        • Padilla L.A.
        • Keh P.
        • Cohen L.
        • Frederiksen M.
        • Lurain J.R.
        Management of twin pregnancies consisting of a complete hydatidiform mole and normal fetus.
        Obstet Gynecol. 1998; 91: 546-550
        • Kutuk M.S.
        • Ozgun M.T.
        • Dolanbay M.
        • Batukan C.
        • Uludag S.
        • Basbug M.
        Sonographic findings and perinatal outcome of multiple pregnancies associating a complete hydatiform mole and a live fetus: a case series.
        J Clin Ultrasound. 2014; 42: 465-471
        • Massardier J.
        • Golfier F.
        • Journet D.
        • et al.
        Twin pregnancy with complete hydatidiform mole and coexistent fetus: obstetrical and oncological outcomes in a series of 14 cases.
        Eur J Obstet Gynecol Reprod Biol. 2009; 143: 84-87
        • Sebire N.J.
        • Foskett M.
        • Paradinas F.,J.
        • et al.
        Outcome of twin pregnancies with complete hydatidiform mole and healthy co-twin.
        Lancet. 2002; 359: 2165-2166
        • Sauerbrei E.E.
        • Salem S.
        • Fayle B.
        Coexistent hydatidiform mole and live fetus in the second trimester: an ultrasound study.
        Radiology. 1980; 135: 415-417
        • Chao A.S.
        • Tsai T.C.
        • Soong Y.K.
        Clinical management of a quadruplet pregnancy combining a triplet pregnancy with a classical hydatidiform mole: case report and review of literature.
        Prenat Diagn. 1999; 19: 1073-1076
        • Niemann I.
        • Sunde L.
        • Petersen L.K.
        Evaluation of the risk of persistent trophoblastic disease after twin pregnancy with diploid hydatidiform mole and coexisting normal fetus.
        Am J Obstet Gynecol. 2007; 197: 45.e1-45.e5
        • Levi S.
        Ultrasonic assessment of the high rate of human multiple pregnancy in the first trimester.
        J Clin Ultrasound. 1976; 4: 3-5
        • Robinson H.P.
        • Caines J.S.
        Sonar evidence of early pregnancy failure in patients with twin conceptions.
        Br J Obstet Gynaecol. 1977; 84: 22-25
        • Landy H.J.
        • Keith L.
        • Keith D.
        The vanishing twin.
        Acta Genet Med Gemellol (Roma). 1982; 31: 179-194
        • Landy H.J.
        • Weiner S.
        • Corson S.L.
        • Batzer F.R.
        • Bolognese R.J.
        The “vanishing twin”: ultrasonographic assessment of fetal disappearance in the first trimester.
        Am J Obstet Gynecol. 1986; 155: 14-19
        • Dickey R.P.
        • Olar T.T.
        • Curole D.N.
        • Taylor S.N.
        • Rye P.H.
        • Matulich E.M.
        The probability of multiple births when multiple gestational sacs of viable embryos are diagnosed at first trimester ultrasound.
        Hum Reprod. 1990; 5: 880-882
        • Spencer K.
        • Staboulidou I.
        • Nicolaides K.H.
        First trimester aneuploidy screening in the presence of a vanishing twin: implications for maternal serum markers.
        Prenat Diagn. 2010; 30: 235-240
        • Rodríguez-González M.
        • Serra V.
        • Garcia-Velasco J.A.
        • Pellicer A.
        • Remohí J.
        The 'vanishing embryo' phenomenon in an oocyte donation programme.
        Hum Reprod. 2002; 17: 798-802
        • Brady P.C.
        • Correia K.F.
        • Missmer S.A.
        • Hornstein M.D.
        • Barton S.E.
        Early beta-human chorionic gonadotropin trends in vanishing twin pregnancies.
        Fertil Steril. 2013; 100: 116-121
        • Pinborg A.
        • Lidegaard O.
        • la Cour Freiesleben N.I.
        • Andersen A.N.
        Consequences of vanishing twins in IVF/ICSI pregnancies.
        Hum Reprod. 2005; 20: 2821-2829
        • Pinborg A.
        • Lidegaard O.
        • la Cour Freiesleben N.I.
        • Andersen A.N.
        Vanishing twins: a predictor of small-for-gestational age in IVF singletons.
        Hum Reprod. 2007; 22: 2707-2714
        • Dickey R.P.
        • Taylor S.N.
        • Lu P.Y.
        • et al.
        Spontaneous reduction of multiple pregnancy: incidence and effect on outcome.
        Am J Obstet Gynecol. 2002; 186: 77-83
        • Chasen S.T.
        • Luo G.
        • Perni S.C.
        • Kalish R.B.
        Are in vitro fertilization pregnancies with early spontaneous reduction high risk?.
        Am J Obstet Gynecol. 2006; 195: 814-817
        • Shebl O.
        • Ebner T.
        • Sommergruber M.
        • Sir A.
        • Tews G.
        Birth weight is lower for survivors of the vanishing twin syndrome: a case-control study.
        Fertil Steril. 2008; 90: 310-314
        • Almog B.
        • Levin I.
        • Wagman I.
        • et al.
        Adverse obstetric outcome for the vanishing twin syndrome.
        Reprod Biomed Online. 2010; 20: 256-260
        • Anand D.
        • Platt M.J.
        • Pharoah P.O.
        Vanishing twin: a possible cause of cerebral impairment.
        Twin Res Hum Genet. 2007; 10: 202-209
        • Pharoah P.O.
        • Cooke R.W.
        A hypothesis for the aetiology of spastic cerebral palsy - the vanishing twin.
        Dev Med Child Neurol. 1997; 39: 292-296
        • Newton R.
        • Casabonne D.
        • Johnson A.
        • Pharoah P.
        A case-control study of vanishing twin as a risk factor for cerebral palsy.
        Twin Res. 2003; 6: 83-84
        • De Pascalis L.
        • Monti F.
        • Agostini F.
        • Fagandini P.
        • La Sala G.B.
        • Blickstein I.
        Psychological vulnerability of singleton children after the 'vanishing' of a co-twin following assisted reproduction.
        Twin Res Hum Genet. 2008; 11: 93-98
        • Huang T.
        • Boucher K.
        • Aul R.
        • Rashid S.
        • Meschino W.S.
        First and second trimester maternal serum markers in pregnancies with a vanishing twin.
        Prenat Diagn. 2015; 35: 90-96
        • Vlková B.
        • Hodosy J.
        Vanishing twin as a potential source of bias in non-invasive fetal sex determination: a case report.
        J Obstet Gynaecol Res. 2014; 40: 1128-1131
        • Masala M.
        • Saba L.
        • Zoppi M.A.
        • et al.
        Pitfalls in noninvasive fetal RhD and sex determination due to a vanishing twin.
        Prenat Diagn. 2014;
        • Curnow K.J.
        • Wilkins Haug L.
        • Ryan A.
        • et al.
        Detection of triploid, molar, and vanishing twin pregnancies by a single-nucleotide polymorphism–based noninvasive prenatal test.
        Am J Obstet Gynecol. 2015; 212: 79.e1-79.e9
        • Üstüner P.
        • Dilek N.
        • Saral Y.
        • Üstüner I.
        Coexistence of aplasia cutis congenita, faun tail nevus and fetus papyraceus.
        J Dermatol Case Rep. 2013; 7: 93-96
        • Daw E.
        Fetus papyraceus–11 cases.
        Postgrad Med J. 1983; 59: 598-600
        • Lagier L.
        • Maruani A.
        • Lardy H.
        • Gibertini I.
        • Lorette G.
        Fetus papyraceus: congenital pulmonary anomalies associated with congenital aplasia cutis on the surviving twin.
        Pediatr Dermatol. 2013; 30 (e143-e45)
        • Tempark T.
        • Shwayder T.A.
        Aplasia cutis congenita with fetus papyraceus: report and review of the literature.
        Int J Dermatol. 2012; 51: 1419-1426
        • Mazza J.M.
        • Klein J.F.
        • Christopher K.
        • Silverberg N.B.
        Aplasia cutis congenita in a setting of fetus papyraceus associated with small fetal abdominal circumference and high alpha-fetoprotein and amniotic acetylcholinesterase.
        Pediatr Dermatol. 2015; 32: 138-140
        • Lemke R.P.
        • Machin G.
        • Muttitt S.
        • Bamforth F.
        • Rao S.
        • Welch R.
        A case of aplasia cutis congenita in dizygotic twins.
        J Perinatol. 1993; 13: 22-27
        • Schaffer J.V.
        • Popiolek D.A.
        • Orlow S.J.
        Symmetric truncal aplasia cutis congenita following multifetal reduction of a sextuplet pregnancy.
        J Pediatr. 2008; 153: 860-863.e1
        • Lewis R.H.
        Foetus in foetu and the retroperitoneal teratoma.
        Arch Dis Child. 1961; 36: 220-226
        • Young G.W.
        Case of a foetus found in the abdomen of a boy.
        Med Chir Trans. 1809; 1: 236
        • Grant P.
        • Pearn J.H.
        Foetus-in-foetu.
        The Medical journal of Australia. 1969; 1: 1016-1019
        • Willis R.A.
        The structure of teratomata.
        J Pathol Bacteriol. 1935; 40: 1-36
        • Boyce M.J.
        • Lockyer J.W.
        • Wood C.B.S.
        Foetus in foetu: serological assessment of monozygotic origin by automated analysis.
        J Clin Pathol. 1972; 25: 793
        • Chen C.P.
        • Chern S.R.
        • Liu F.F.
        • et al.
        Prenatal diagnosis, pathology, and genetic study of fetus in fetu.
        Prenat Diagn. 1997; 17: 13-21
        • George V.
        • Khanna M.
        • Dutta T.
        Fetus in fetu.
        Journal of pediatric surgery. 1983; 18: 288-289
        • Ji Y.
        • Chen S.
        • Zhong L.
        • et al.
        Fetus in fetu: two case reports and literature review.
        BMC Pediatr. 2014; 14: 88
        • Hoeffel C.C.
        • Nguyen K.Q.
        • Phan H.T.
        • et al.
        Fetus in fetu: a case report and literature review.
        Pediatrics. 2000; 105: 1335-1344
        • Derniaux E.
        • Zachar D.
        • Bory J.P.
        • Gaillard D.
        • Favre R.
        • Graesslin O.
        Detection of a prenatal mature tumor arising from the external genitalia in a female fetus: fetus-in-fetu or teratoma?.
        Prenat Diagn. 2010; 30: 1110-1111
        • Du Plessis J.P.
        • Winship W.S.
        • Kirstein J.D.
        Fetus in fetu and teratoma. A case report and review.
        S Afr Med J. 1974; 48: 2119-2122
        • Hopkins K.L.
        • Dickson P.K.
        • Ball T.I.
        • Ricketts R.R.
        • O'Shea P.A.
        • Abramowsky C.R.
        Fetus-in-fetu with malignant recurrence.
        J Pediatr Surg. 1997; 32: 1476-1479
        • Spencer R.
        Parasitic conjoined twins: external, internal (fetuses in fetu and teratomas), and detached (acardiacs).
        Clinical anatomy (New York, NY). 2001; 14: 428-444
        • Brand A.
        • Alves M.C.
        • Saraiva C.
        • et al.
        Fetus in fetu–diagnostic criteria and differential diagnosis–a case report and literature review.
        J Pediatr Surg. 2004; 39: 616-618
        • Huddle L.N.
        • Fuller C.
        • Powell T.
        • et al.
        Intraventricular twin fetuses in fetu.
        J Neurosurg Pediatr. 2012; 9: 17-23
        • Gerber R.E.
        • Kamaya A.
        • Miller S.S.
        • et al.
        Fetus in fetu: 11 fetoid forms in a single fetus: review of the literature and imaging.
        Journal of ultrasound in medicine: official journal of the American Institute of Ultrasound in Medicine. 2008; 27: 1381-1387
        • Knox A.J.
        • Webb A.J.
        The clinical features and treatment of fetus in fetu: two case reports and a review of the literature.
        J Pediatr Surg. 1975; 10: 483-489
        • Has R.
        • Kalelioglu I.H.
        • Esmer A.C.
        • Demirbas R.
        • Yuksel A.
        • Yavuz E.
        Prenatal sonographic diagnosis of fetus in fetu.
        J Ultrasound Med. 2013; 32: 2212-2214
        • Song Q.Y.
        • Jiang X.P.
        • Jiang Y.
        • Ning G.
        • Yang T.Z.
        Fetus in fetu: from prenatal sonographic diagnosis to postnatal confirmation.
        Fetal Diagn Ther. 2014; (Epub ahead of print)
        • Escobar M.A.
        • Rossman J.E.
        • Caty M.G.
        Fetus-in-fetu: report of a case and a review of the literature.
        J Pediatr Surg. 2008; 43: 943-946
        • Bhat B.V.
        • Usha T.S.
        • Puri R.K.
        Superfoetation. Indian J Pediatr. 1989; 56: 291-293
        • James W.H.
        Gestational age in twins.
        Arch Dis Child. 1980; 55: 281-284
        • Singhal S.R.
        • Agarwal U.
        • Sharma D.
        • Sen J.
        Superfetation in uterus pseudo didelphys: an unreported event.
        Arch Gynecol Obstet. 2003; 268: 243-244
        • Roellig K.
        • Menzies B.R.
        • Hildebrandt T.B.
        • Goeritz F.
        The concept of superfetation: a critical review on a ‘myth’ in mammalian reproduction.
        Biol Rev Camb Philos Soc. 2011; 86: 77-95
        • Tarín J.J.
        • García-Pérez M.A.
        • Hermenegildo C.
        • Cano A.
        Unpredicted ovulations and conceptions during early pregnancy: an explanatory mechanism of human superfetation.
        Reprod Fertil Dev. 2013; 25: 1012-1019
        • Blickstein I.
        Superfecundation and superfetation: Lessons from the past on early human development.
        J Matern Fetal Neonatal Med. 2003; 14: 217-219
        • Harrison A.
        • Valenzuela A.
        • Gardiner J.
        • Sargent M.
        • Chessex P.
        Superfetation as a cause of growth discordance in a multiple pregnancy.
        J Pediatr. 2005; 147: 254-255
        • Amsalem H.
        • Tsvieli R.
        • Zentner B.S.
        • Yagel S.
        • Mitrani-Rosenbaum S.
        • Hurwitz A.
        Monopaternal superfecundation of quintuplets after transfer of two embryos in an in vitro fertilization cycle.
        Fertil Steril. 2001; 76: 621-623
        • Peigné M.
        • Andrieux J.
        • Deruelle P.
        • Vuillaume I.
        • Leroy M.
        Quintuplets after a transfer of two embryos following in vitro fertilization: a proved superfecundation.
        Fertil Steril. 2011; 95: 2124.e13-2124.e16
        • Terasaki P.I.
        • Gjertson D.
        • Bernoco D.
        • Perdue S.
        • Mickey M.R.
        • Bond J.
        Twins with two different fathers identified by HLA.
        N Engl J Med. 1978; 299: 590-592
        • Harris D.W.
        Superfecundation.
        J Reprod Med. 1982; 27: 39
        • Girela E.
        • Lorente J.A.
        • Alvarez J.C.
        • Rodrigo M.D.
        • Lorente M.
        • Villanueva E.
        Indisputable double paternity in dizygous twins.
        Fertil Steril. 1997; 67: 1159-1161
        • Wenk R.E.
        • Houtz T.
        • Chiafari F.
        • Brooks M.
        Superfecundation identified by HLA, protein, and VNTR DNA polymorphisms.
        Transfus Med. 1991; 1: 253-255
        • James W.H.
        The incidence of superfecundation and of double paternity in the general population.
        Acta Genet Med Gemellol (Roma). 1993; 42: 257-262
        • Hubinont C.
        • Lewi L.
        • Bernard P.
        • Marbaix E.
        • Debiève F.
        • Jauniaux E.
        Anomalies of the placenta and umbilical cord in twin gestations.
        Am J Obstet Gynecol. 2015; 213: S91-S102
        • Van de Leur S.J.
        • Zeilmaker G.H.
        Double fertilization in vitro and the origin of human chimerism.
        Fertil Steril. 1990; 54: 539-540
        • Safran A.
        • Reubinoff B.E.
        • Porat Katz A.
        • Werner M.
        • Friedler S.
        • Lewin A.
        Intracytoplasmic sperm injection allows fertilization and development of a chromosomally balanced embryo from a binovular zona pellucida.
        Hum Reprod. 1998; 13: 2575-2578
        • Vicdan K.
        • Işik A.Z.
        • Dagli H.G.
        • Kaba A.
        • Kişnişçi H.
        Fertilization and development of a blastocyst-stage embryo after selective intracytoplasmic sperm injection of a mature oocyte from a binovular zona pellucida: a case report.
        J Assist Reprod Genet. 1999; 16: 355-357
        • Letts R.M.
        • Shokeir M.H.
        Mirror-image coxa vara in identical twins.
        J Bone Joint Surg Am. 1975; 57: 117-118
        • Williams N.
        • Kapila L.
        Posterior urethral valves in twins with mirror image abnormalities.
        Br J Urol. 1993; 71: 615-616
        • Okamoto F.
        • Nonoyama T.
        • Hommura S.
        Mirror image myopic anisometropia in two pairs of monozygotic twins.
        Ophthalmologica. 2001; 215: 435-438
        • Morini F.
        • Ilari M.
        • Casati A.
        • Piserà A.
        • Oriolo L.
        • Cozzi D.A.
        Posterior urethral valves and mirror image anomalies in monozygotic twins.
        Am J Med Genet. 2002; 111: 210-212
        • Kobayashi F.
        • Sagawa N.
        • Konishi I.
        • Tsuruta Y.
        • Fujiwara H.
        • Mori F.
        Spontaneous conception and intrauterine pregnancy in a symptomatic missed abortion of ectopic pregnancy conceived in the previous cycle.
        Hum Reprod. 1996; 11: 1347-1349
        • Tuppen G.D.
        • Fairs C.
        • de-Chazal R.C.
        • Konje J.C.
        Spontaneous superfetation diagnosed in the first trimester with successful outcome.
        Ultrasound Obstet Gynecol. 1999; 14: 219-221
        • Archer J.
        Observations showing that a white woman, by intercourse with a white man and a Negro man, conceive twins, one of which shall be white and the other mulatto.
        Med Repository. 1810; 3d: 319
        • Verma R.S.
        • Luke S.
        • Dhawan P.
        Twins with different fathers.
        Lancet. 1992; 339: 63-64
        • Lu H.L.
        • Wang C.X.
        • Wu F.Q.
        • Li J.J.
        Paternity identification in twins with different fathers.
        J Forensic Sci. 1994; 39: 1100-1102