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Developmental Stages in Human Embryos

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Developmental Stages in Human Embryos DEVELOPMENTAL STAGES IN HUMAN EMBRYOS DEVELOPMENTAL STAGES IN HUMAN EMBRYOS Including a Revision of Streeter's ''Horizons" and a Survey of the Carnegie Collection RONAN O'RAHILLY and FABIOLA MULLER Carnegie Laboratories of Embryology, California Primate Research Center, and Departments of Human Anatomy and Neurolog}', University of California, Davis CARNEGIE INSTITUTION OF WASHINGTON PUBLICATION 63T 198"7 Library of Congress Catalog Card Number 87-070669 International Standard Book Number 0-87279-666-3 Composition by Harper Graphics, Waldorf, Maryland Printing by Meriden-Stinehour Press, Meriden, Connecticut Copyright © 1987, Carnegie Institution of Washington Dem Andenken von Wilhelm His, dem Alter en, der vor hundert Jahren die Embryologie des Menschen einfuhrte und dem seines Protege, Franklin P. Mall, dem Begrunder der Carnegie Collection. Wilhelm His, 1831-1904 Fr.mkhn P. Mall, 1862-191" George L Streeter, 1873-1948 PREFACE During the past one hundred years of human embryology, three land- marks have been published: the Anatomie der menschlichen Embryonen of His (1880-1885), the Manual of Human Embryology by Keibel and Mall (1910-1912), and Streeter's Developmental Horizons in Human Embryos (1942-1957, completed by Heuser and Corner). Now that all three milestone volumes are out of print as well as in need of revision, it seems opportune to issue an updated study of the staged human embryo. The objectives of this monograph are to provide a reasonably detailed morphological account of the human embryo (i.e., the first eight weeks of development), a formal classification into developmental stages, a catalogue of the preparations in the Carnegie Collection, and a reference guide to important specimens in other laboratories. The Carnegie staging system has now been accepted internationally and, when carefully ap- plied, allows detailed comparisons between the findings at one institution and those at another. The classifications and descriptions of stages 1-9 are based on light microscopy, and the criteria selected have stood the test of time. The present account is a revision of O'Rahilly's monograph of 1973. In stages 10-23, increasing attention is paid to external form, although internal structure is not, and should not be, neglected. Streeter's masterly account has been updated and is used here in treating stages 10-23. Many of Streeter's paragraphs have been left virtually unchanged (except for im- provements in terminology) but others have been altered considerably, and much new material has been added. Most of the drawings for stages 1-9 were prepared in the Department of Art as Applied to Medicine, the Johns Hopkins School of Medicine, under the direction of Ranice Crosby. Most of those for stages 10-23 are the work of James F. Didusch, although certain modifications in his terminology have been adopted. A major change made here from Streeter's account is in the systematic inclusion of standard references. It should be stressed, however, that no attempt has been made to provide a comprehensive bibliography. Many more references can be found in a series of articles on the timing and sequence of developmental events, beginning in Acta anatomica in 1971 and continuing in the Zeitschrift fur Anatomie und Entwicklungsge- schichte (now Anatomy and Embryology) from 1971 to 1983. For the nervous system, further references can be found in a continuing series of articles that began in 1981 in Anatomy and Embryology: stages 8-11 have already been published. Particular attention has been paid to nomenclature throughout. Most of the terms used are in agreement with the Nomina embryologica. The latter, however, unlike the Nomina anatomica, is not exclusively human, and hence certain inappropriate terms have been replaced here. It is appropriate to acknowledge here the great help provided by the National Institutes of Health, which have supported the writers' research (Grant No. HD-16702, Institute of Child Health and Human Develop- ment). It is a particular pleasure to acknowledge the enthusiasm and collab- oration of the late Dr. Ernest Gardner over many years, the friendship and assistance provided by Dr. Elizabeth M. Ramsey, and the continued encouragement of Dr. James D. Ebert, President of the Carnegie Insti- tution of Washington, whose invitation to establish the first nine stages was made twenty years ago. The authors wish to thank Mr. Ray Bowers and Miss Patricia Parratt of the Carnegie Institution's publications office for the exceptionally great care with which they brought this monograph to fruition. R. O'R. F. M. January 1987 INTRODUCTION The norm should be established; embryos should be arranged in stages. FRANKLIN P. MALL The combined use of fixation, sectioning with a mi- The Carnegie Collection crotome, and reconstruction from the resultant sec- tions first enabled Wilhelm His, Senior, to begin to Mall's collection of human embryos, begun in 1887, elucidate thoroughly the anatomy of individual human later became the basis of the Carnegie Collection (Mall embryos. Indeed, His may rightfully be called the "Ves- and Meyer, 1921). Mall (1913) stated his indebtedness alius of human embryology" (Muller and O'Rahilly, to His in the following terms: "We must thank His for 1986a). the first attempt to study carefully the anatomy of hu- Although fixatives other than spirits were introduced man embryos, but his work was planned on so large early in the nineteenth century, formalin was not em- a scale that he never completed it Thus we may ployed until the 1890s. His devised a microtome in trace back to him the incentive for Keibel's Nornien- about 1866. (A microtome had already been employed tafeln, Minot's great collection of vertebrate embryos as early as 1770.) The wax plate reconstruction tech- and mine of human embryos." nique of Born (1883), introduced in 1876, has under- In more recent years the Carnegie Collection has gone numerous modifications over the years. These, benefited enormously from the meticulous investiga- as well as graphic reconstruction, have been discussed tions of Bartelmez, the technical adroitness of Heuser, in a number of publications, e.g., by Gaunt and Gaunt and the donation of, as well as research on, remarkably (1978). Florian, who used graphic reconstruction of young specimens by Hertig and Rock. The microtomy the human embryo to great advantage, elaborated the of Charles H. Miller and William H. Duncan, the re- mathematical background in Czech in 1928. (See also constructions by Osborne O. Heard, the artwork by Fetzer and Florian, 1930.) James F. Didusch, and the photography of Chester F. It has been pointed out that "the idea of working Reather and Richard D. Grill, have each played a key out a complete account of the development of the role in the establishment of the superb embryological human body was always before the mind of His," and collection on which the present monograph is so largely his collaborator, Franz Keibel, proposed to provide based. In George W. Corner's apt comparison, the Col- "an account of the development of the human body, lection serves "as a kind of Bureau of Standards." based throughout on human material" (Keibel and Mall, 1910) rather than from the comparative stand- point. The result was the Manual of Human Embryol- Embryological Seriation ogy edited by Keibel and Mall (1910. 1912), which was His had made the first thorough arrangement of an important step in the goal of seeking precision in human embryos in the form of a series of selected human embryology. The hope was expressed that, sub- individual embryos, numbered in the presumed order sequently, a second attempt, 'whether made by us or of their development. The same principle was followed by others, will come so much nearer the goal (ibid.). in the published plates known as the Normentafeln, DEVELOPMENTAL STAGES IN HUMAN EMBRYOS edited by Franz Keibel from 1897 onward; the volume might be large enough to provide an adequate index on the human (by Keibel and Elze) appeared in 1908. of relative development. The limitations of the method are (l)that individual The original plan was "to cover as far as possible embryos cannot be arranged in a perfect series, be- the earliest specimens up to fetuses between 32 and cause any given specimen may be advanced in one 38 mm. long, the stage at which the eyelids have come respect while being retarded in another, and (2) that together," and "twenty-five age groups" were envi- it may prove impossible to match a new embryo exactly sioned (Streeter, 1942). Subsequently, Streeter (1951) with any one of the illustrated norms. The need for a decided that stage 23 "could be considered to mark more flexible procedure than a mere Entwicklungs- the ending of the embryonic period" proper. The on- reihe soon became apparent in experimental embryol- set of marrow formation in the humerus was "arbi- ogy. trarily adopted as the conclusion of the embryonic and the beginning of the fetal period of prenatal life. It occurs in specimens about 30 mm. in length" (Streeter, Embryonic Staging 1949). A scheme of the 23 stages, as modified and used In the words of Ross G. Harrison (Wilens, 1969), in the present monograph, is provided in Table 0-1. "the need for standardized stages in the embryonic The term "horizon" was borrowed from geology development of various organisms for the purpose of and archaeology by Streeter (1942) in order "to em- accurate description of normal development and for phasize the importance of thinking of the embryo as utilization in experimental work has long been rec- a living organism which in its time takes on many ognized." Because "development is a continuous pro- guises, always progressing from the smaller and sim- cess with an indefinite number of stages" (ibid), a pler to the larger and more complex." However, the certain number have to be chosen.
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