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The timing of monozygotic twinning: a criticism of the common model

Published online by Cambridge University Press:  05 June 2013

Gonzalo Herranz*
Affiliation:
Department of Medical Humanities, School of Medicine, University of Navarre, Pamplona, Spain
*
All correspondence to: Gonzalo Herranz. Department of Medical Humanities, School of Medicine, University of Navarre, Apartado 177, 31080 Pamplona, Spain. Tel: +34 948 425 600, ext. 6354. Fax: +34 948 425 630. e-mail: gherranz@unav.es

Summary

In the dominant model, monozygotic (MZ) twinning is universally accepted as a post-fertilization event resulting from splitting of the embryo along its first 2 weeks of development. The stage at which splitting occurs determines chorionicity and amnionicity. A short history on how the model was built is presented, stressing the role played by some embryologists, in particular George Corner, in its completion and final success. Strikingly, for more than 60 years no deep criticisms have been raised against the model, which, in virtue of its rational and plausible character, enjoys the status of undisputed truth. At close examination, the embryological support of the model shows some important weak points, particularly when dealing with late splitting. In the author's view, the model not only has contributed to ‘suspend’ our knowledge on the timing of MZ twinning, but seems indefensible and claims to be substituted. That factor could imply relevant consequences for embryology and bioethics. As an alternative to the model, a new theory to explain the timing of MZ twinning is proposed. It is based on two premises. First, MZ twinning would be a fertilization event. In that case, due to an alteration of the zygote–blastomere transition, the first zygotic division, instead of producing two blastomeres, generates twin zygotes. Second, monochorionicity and monoamnionicity would not depend on embryo splitting, but on fusion of membranes. Some support for this theory can be found in recent embryological advances and also in some explanations of old.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2013 

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References

Allen, F.D. (1969). Essentials of Human Embryology, 2 edn.New York: Oxford University Press, p. 34.Google Scholar
Anonymous Review of Current Literature (1956). J. Obstet. Gynaecol. Br Emp. 63, 459–79.Google Scholar
Arey, L.B. (1922). Direct proof of the monozygotic origin of human identical twins. Anat. Rec. 23, 245–8.Google Scholar
Assheton, R. (1893). An account of a blastodermic vesicle of the sheep of the seventh day, with twin germinal areas. J. Anat. Physiol. 32, 362–72.Google Scholar
Aston, K.I., Peterson, C.M. & Carrell, D.T. (2008). Monozygotic twinning associated with assisted reproductive technologies: a review. Reproduction 136, 377–86.Google Scholar
Bamforth, F., Brown, L., Senz, J. & Huntsman, D. (2003). Mechanisms of monozygotic (MA) twinning: a possible role for the cell adhesion molecule, E-cadherin. Am. J. Med. Genet. 120A, 5962.CrossRefGoogle Scholar
Beck, A.C. & Rosenthal, A.H. (1957). Obstetrical Practice, 7 edn.Baltimore: Williams & Wilkins, p. 546.Google Scholar
Behr, B. & Milki, A.A. (2003). Visualization of atypical hatching of a human blastocyst in vitro forming two identical embryos. Fertil. Steril. 80, 1502–3.Google Scholar
Benirschke, K. (1965). Major pathologic features of the placenta, cord and membranes. Birth Defects Original Article Series 1, 5263.Google Scholar
Benirschke, K. & Driscoll, S.G. (1967). The Pathology of the Human Placenta. New York: Springer–Verlag, p. 168.CrossRefGoogle Scholar
Benirschke, K. & Kim, C.K. (1973). Multiple pregnancy (first of two parts). New Engl. J. Med. 288, 1276–84.CrossRefGoogle Scholar
Blickstein, I. (2006). Monochorionicity in perspective. Ultrasound Obstet. Gynecol. 27, 235–8.CrossRefGoogle Scholar
Boklage, C.E. (2005). The biology of human twinning: a needed change of perspective. In Multiple Pregnancy. Epidemiology, Gestation and Perinatal Outcome, 2nd edn (eds Blickstein, I. & Keith, L.G.), London: Taylor & Francis. A Parthenon Book, p. 258Google Scholar
Boklage, C.E. (2010). How New Humans Are Made. Singapore: World Scientific Publishing, pp. 114–5.Google Scholar
Bompiani, A. (2006). Le Tecniche di Fecondazione Assistita: Una Rasegna Critica. Milano: Vita e Pensiero, p. 102Google Scholar
Boyd, J.D. & Hamilton, W.J. (1970). The Human Placenta. Cambridge: W. Heffer & Sons, p. 314.Google Scholar
Bulmer, M.G. (1970). The Biology of Twinning in Man. Oxford: Clarendon Press, p. 27.Google Scholar
Bumm, E. (1902). Grundriss zum Studium der Geburtshülfe. Wiesbaden: J.F. Bergmann, p. 282.Google Scholar
Conybeare, R.C. (1954). Monoamniotic twins. A review of the literature with case report. Obstet. Gynecol. 4, 444–7.Google Scholar
Corner, G.W. (1922). The morphological theory of monochorionic twins as illustrated by a series of supposed early twin embryos of the pig. Johns Hopkins Hosp. Bull. 33, 389–92.Google Scholar
Corner, G.W. (1955). The observed embryology of the human single-ovum twins and other multiple births. Am. J. Obstet. Gynecol. 70, 933–51.CrossRefGoogle ScholarPubMed
Corner, G.W. (1958). Anatomist at Large: An Autobiography and Selected Essays. New York: Basic Books.Google Scholar
Corner, G.W. (1981). The Seven Ages of a Medical Scientist. An Autobiography. Philadelphia: University of Pennsylvania Press.Google Scholar
Coulton, D., Hertig, A.T. & Long, W.N. (1947). Monoamniotic twins. Am. J. Obstet. Gynecol. 54, 119–23.Google Scholar
Craig, I.T. (1957). Monoamniotic twins with double survival. Am. J. Obstet. Gynecol. 73, 202–4.CrossRefGoogle ScholarPubMed
Derom, R. & Derom, C. (2005). Placentation. In Multiple Pregnancy. Epidemiology, Gestation & Perinatal Outcome, 2nd edn (eds Blickstein, I. & Keith, L.G.), London: Taylor & Francis: a Parthenon Book, p. 158.Google Scholar
Dollander, A.I. (1970). Embryologie générale comparée et humaine. In Éléments d'Embryologie (eds A. Dollander & R. Fenart), Paris: Flammarion, p. 328.Google Scholar
Downs, K.M. (2008). Embryological origins of the human individual. In Controversies in Science & Technology: From Climate to Chromosomes (eds Kleiman, D.L., Cloud-Hausen, K.A., Matta, C. & Handelsmaneds, J.), pp. 4668. New Rochelle, NY: Mary Ann Liebert.Google Scholar
Ebert, J.D. (1956). Department of Embryology. Carnegie Institution of Washington. Year Book, 1955–1956. Washington DC: Carnegie Institution of Washington, p. 290.Google Scholar
Edwards, R.G., Mettler, L. & Walters, D.E. (1986). Identical twins and in vitro fertilization. J. In Vitro Fertil. Embr. Transf. 3, 114–7.CrossRefGoogle ScholarPubMed
Greenhill, (1956). Year Book of Obstetrics and Gynecology. Chicago: Year Book Publishers, p. 258.Google Scholar
Grosser, O. (1927). Frühentwicklung, Eihautbildung und Placentation des Menschen und der Säugetiere. Deitsche Frauenheilkunde, Geburtshilfe, Gynäkologie und Nachbargebiete in Einzeldarstellungen. Band 5. München: J.F. Bergmann, p. 64.Google Scholar
Hall, J.G. (1996). Twins and twinning. Am. J. Med. Gen. 61, 202–4.Google Scholar
Hanes, M.V. (1954). Monoamniotic twins. Review of the literature with case report. Obstet. Gynecol. 4, 448–51.Google Scholar
Hartman, C.G. (1956). The scientific achievements of George Washington Corner, M.D. Am. J. Anat. 98, 519.Google Scholar
Hertig, A.T. (1945). On the development of the amnion and exocoelomic membrane in the pre-villous human ovum. Yale J. Biol. Med. 18, 107–15.Google Scholar
Hertig, A.T., Rock, J. & Adams, E.C. (1956). A description of 34 human ova within the first 17 days of development. Am. J. Anat. 98, 435–93.Google Scholar
Hertwig, R. (1906). Eireif, Befruchtung und Furchungsprozess. In Handbuch der Vergleichenden und Experimentellen Entwickelungslehre der Wirbeltiere, I. Band, I. Teil. Allgemeine Missbildungslehre. Jena: Gustav Fischer. Teil, I Hälfte (ed. Hertwig, O.) Jena: Verlag Gustav Fischer, p. 487.Google Scholar
Hughes, W. (1927). Sex-intergrades in foetal pigs. Biol. Bull. 52, 121–37.Google Scholar
Jones, H.W. Jr & Schrader, C. (1987). The process of human fertilization: implications for moral status. Fertil. Steril. 48, 189–92.Google Scholar
Kaufman, M.H. (2004). The embryology of conjoined twins. Childs Nerv. Syst. 20, 508525.Google Scholar
Klein, P. (1927). Zur Frage der Diagnose der Eineiigkeit bei Zwillingsschwangerschaft. Arch. Gynäk. 130, 788812.Google Scholar
Klein, J., Grunfeld, L., Duke, M., Mukherjee, T., Sandler, B. & Copperman, A.B. (2005). Challenging traditional dogma: a report of two cases of late monozygotic splitting resulting in dichorionic twinning. Fertil. Steril. 84(Suppl. 1), S2389.Google Scholar
Knopman, J., Kray, L.C., Lee, J., Fino, M.E., Novetsky, A.P. & Noyes, N. (2010). Monozygotic twinning: an eight-year experience at a large IVF center. Fertil. Steril. 94, 502–10.Google Scholar
Leroy, F. (1985). Early embryology and placentation of human twins. In Implantation of the Human Embryo. Proceedings of the Second Bourne Hall Meeting (eds Edwards, R.G., Purdy, J.M. & Steptoe, P.C.), pp. 396–8. London: Academic Press.Google Scholar
Lejeune, J. (1992). The Concentration Can: When does Human Life Begin. San Francisco: Ignatius Press, p. 197.Google Scholar
Leroy, F. (1985). Early embryology and placentation of human twins. In Implantation of the Human Embryo. Proceedings of the Second Bourne Hall Meeting (eds Edwards, R.G., Purdy, J.M. & Steptoe, P.C.), p. 395. London: Academic Press.Google Scholar
Librach, S. & Terrin, A.J. (1957). Monoamniotic twin pregnancy, with report of three cases of double survival, one of them with knotted cords. Am. J. Obstet. Gynecol. 74, 440–3.Google Scholar
López-Moratalla, N. & Cerezo, M. (2011). The self-construction of a living organism. In Information and Living Systems: Philosophical and Scientific Perspectives (eds Terzis, G. & Arp, R.), pp. 177204. Cambridge, MA: MIT Press.Google Scholar
Lord Zuckerman (1983). George Washington Corner. Biograph. Mem. Fell. Roy. Soc. 29, 92112.Google Scholar
Matias, A., Montenegro, N. & Blickstein, I. (2011). Monochorionicity: unveiling the black box. In Donald School Textbook of Ultrasound in Obstetrics and Gynecology, 3rd edn (eds Kurjak, A. & Chervenak, F.A.), p. 462. New Delhi: Jaypee Brothers Medical Publishers.Google Scholar
McGeady, T.A., Quinn, P.J., Fitzpatrick, E.S. & Ryan, M.T. (2006). Veterinary Embryology. Oxford: Blackwell Publishing Ltd, p. 39.Google Scholar
McLaren, A. (1982). The embryo. In Reproduction in Mammals. Book 2. Embryonic and Fetal Development (eds Austin, C.R. & Short, R.V.), p. 19. Cambridge: Cambridge University Press.Google Scholar
Meintjes, M., Guerami, A.R., Rodriguez, J.A., Crider-Pirkle, S.S. & Madden, J.D. (2001). Prospective identification of an in-vitro-assisted monozygotic pregnancy based on a double-inner-cell-mass blastocyst. Fertil. Steril. 76, S1723.Google Scholar
Ménézo, Y.J.R. & Sakkas, D. (2002). Monozygotic twinning: is it related to apoptosis in the embryo? Lett. Hum. Reprod. 17, 247–8.CrossRefGoogle ScholarPubMed
Mio, Y. & Maeda, K. (2008). Time-lapse cinematography of dynamic changes occurring during in vitro development of human embryos. Am. J. Obstet. Gynecol. 199, 660.e15.Google Scholar
Morton, W.R.M. (1957). Duplication of the pituitary and stomodeal structures in a 38-week male infant. Arch. Dis. Child. 32, 135–41.Google Scholar
Nance, W.E. (1990). Invited editorial: Do twin lions have larger spots? Am. J. Hum. Gen. 45, 646–8.Google Scholar
Newman, H.H. (1917). The Biology of Twins. Chicago: The University of Chicago Press, p. 13.Google Scholar
Niimura, S. (2003). Time-lapse videomicrographic analyses of contractions in mouse blastocysts. J. Reprod. Dev. 49, 413–23.Google Scholar
O'Rahilly, R. (1973). Developmental Stages in Human Embryos, including a survey of the Carnegie Collection. Part A. Embryos of the First Three Weeks (Stages 1–9). Carnegie Institution of Washington, p. 38.Google Scholar
O'Rahilly, R. & Müller, F. (1998). Embriología y Teratología Humanas. Barcelona: Masson.Google Scholar
Osborne, R.H. & de George, F.V. (1957). Selective survival in dizygotic twins in relation to the ABO blood groups. Am. J. Hum. Gen. 9, 321–30.Google Scholar
Patterson, J.T. (1913). Polyembryonic development in Tatusia novemcincta. J. Morphol. 24, 559682.Google Scholar
Payne, D., Okuda, A., Wakatsuki, Y., Takeshita, C., Iwata, K., Shimura, T., Yumoto, K., Ueno, Y., Flaherty, S. & Mio, Y. (2007). Time-lapse recording identifies human blastocysts at risk of producing monozygotic twins. Hum. Reprod. 22(Suppl. 1), i9.Google Scholar
Potter, J.C. (1927). Human monochorial twin embryos in separate amnions. Anat. Rec. 34, 253257.Google Scholar
Ramsey, E.M. (1994). George Washington Corner. Nat. Acad. Sci. Biograph. Mem. 65, 5693.Google Scholar
Redline, R.W. (2003). Nonidentical twins with a single placenta–disproving dogma in perinatal pathology. New Engl. J. Med. 349, 111–4.Google Scholar
Roberts, R.M. & Fisher, S.J. (2011). Trophoblast stem cells. Biol. Reprod. 84, 412–21.Google Scholar
Roode, M., Blair, K., Snell, P., Elder, K., Marchant, S., Smith, A. & Nichols, J. (2012). Human hypoblast formation is not dependent on FGF signalling. Dev. Biol. 361, 358–63Google Scholar
Salerno, L.J. (1959). Monoamniotic twinning. A survey of the American literature since 1935 with a report of four new cases. Obstet. Gynecol. 14, 205–13.Google Scholar
Schultze, O. (1897). Grundriss der Entwicklungsgeschichte des Menschen und der Säugethiere, für Studirende und Ärzte. Bearb. unter Zugrundelegung der 2. Aufl. des Grundrisses der Entwicklungsgeschichte von A. Koelliker. Leipzig: W. Engelmann, p. 176Google Scholar
Schwalbe, E. (1906). Die Morphologie der Missbildungen der Menschen und der Tiere. I. Teil. Allgemeine Missbildungslehre. Jena; Gustav Fischer.Google Scholar
Shibuya, Y. & Kyono, K. (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, 255–7.Google Scholar
Siemens, H.W. (1925). Die Diagnose der Eineiigkeit in geburtshilflicher und in dermatologischer Betrachtung. Arch. Gynäkol. 126, 625–45.Google Scholar
Sills, E.S, Tucker, M.J. & Palermo, G.D. (2000). Assisted reproductive technologies and monozygous twins: implications for future study and clinical practice. Twin Res. 3, 217–23.Google Scholar
Silver, L.M. (1987). Remaking Eden. Cloning and Beyond in a Brave New World. New York: Avon Books, p. 38;Google Scholar
Sobotta, J. (1901). Neuere Anschauungen über der Doppel(miss)bildungen mit besonderer Berücksichtigung der menschlichen Zwillingsgeburten. Würzb Abhand Gesamtgeb prakt Med. 4, 85105.Google Scholar
Spencer, R. (2000). Theoretical and analytical embryology of conjoined twins: Part I: Embryogenesis. Clin. Anat. 13, 3653.Google Scholar
Steinman, G. & Valderrama, E. (2001). Mechanisms of twinning. III. Placentation, calcium reduction and modified compaction. J. Reprod. Med. 46, 9951002.Google Scholar
Stern, K. (1960). Principles of Human Genetics. 2nd edn. San Francisco: WH Freeman, pp. 538–9.Google Scholar
Streeter, G.L. (1924). Carnegie Institution of Washington. Year Book No. 22. November 1, 1922, to October 31, 1923. Washington, Carnegie Institution of Washington; p. 85.Google Scholar
Strong, S.J. & Corney, G. (1967). The Placenta in Twin Pregnancy. Oxford:Pergamon Press, p. 17.Google Scholar
Tam, P.P.L. & Gad, J.M. (2004). Gastrulation in the mouse embryo. In Gastrulation. From Cells to Embryo (ed. Stern, C.D.), pp. 239–43. New York: SCHL Press.Google Scholar
Tarkowski, A.K. & Wojewodzka, M. (1982). A method for obtaining chimaeric mouse blastocysts with two separate inner cell masses: a preliminary report. J. Embryol. Exp. Morphol. 71, 215–21.Google Scholar
Van Langendonckt, A., Wyns, C., Godin, P.A., Toussaint-Demylle, D. & Donnez, J. (2000). Atypical hatching of a human blastocyst leading to monozygotic twinning: a case report. Fertil. Steril. 74, 1047–50.Google Scholar
Verpoest, W., Van Landuyt, L., Desmyttere, S., Cremers, A., Devroey, P. & Liebaers, I. (2009). The incidence of monozygotic twinning following PGD is not increased. Hum. Reprod. 24, 2945–50.Google Scholar
Verschuer, O. (1932). Die biologischen Grundlagen der menschlichen Mehrlingsforschung. Z. Indukt. Abstamm. Vererb. 61, 147207.Google Scholar
Wilder, H.H. (1904) Duplicate twins and double monsters. Am. J. Anat. 3, 387472, p. 391.Google Scholar