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Home , Aortic arches

The Human Embryonic in the Seventh Week'

DONALD G. VERNALL The Department of Anatomy, The University of Michigan, Ann Arbor, Michigan

Although cardiac development has in- Born's method of wax-plate reconstruc- terested investigators for more than 2,500 tion as modified by Kramer ('42) was years (see Kramer, '42 and Licata, '54 for employed. The model, reconstructed at a historical reviews) the discovery of many magnification of lOOX, is dissectable at of the details of cardiogenesis awaited the various levels in a plane coinciding with development of technics for the construc- the transverse plane in which the embryo tion of enlarged models of the embryonic was sectioned. Figure 3 illustrates the in- heart so that its anatomy could be seen ternal structure that is evident as several more easily. Such a technic was described succeeding segments of the model are re- by Born in 1883, but the method is so moved. The proximal portions of the ma- pains-taking and time-consuming that jor vessels entering or leaving the heart many gaps still exist in the available series have been included in the reconstruction of models illustrating the human heart at (figs. 1 and 2). various stages in its development. As Additional embryos of a comparable age these gaps become narrower, we are con- examined and compared with the model fronted with the problem of the individual are listed below: variability that occurs at each stage. The present paper, an attempt to fill u. of Crown-rump Streeter's Plane Mich. length horizon of one of the gaps in our knowledge of the Number mm number section of the human heart, is based ~~ EH286 14.5 XVIII Transverse on an enlarged model of the heart in the EH314 14.8 XVIII Transverse seventh week of its development. This is EH407 14.5 XVII Sagittal the period during which the coronary ves- EH568 14.0 XVIII Transverse sels and the secondary EH583 14.6 XVII Transverse appear. It is also a period in which many of the structures and relationships of the OBSERVATIONS adult heart are recognizable. External configuration MATERIALS AND METHODS The definitive positions and interrela- The model upon which the present study tionships of the four chambers of the is based was made from the heart of an heart and the associated major vessels embryo' with a crown-rump length of are externally apparent at this stage. 14.5 mm. The embryo was in Streeter's The pulmonary trunk crosses anterior Horizon early XVIII. Several factors led to the ascending trunk (fig. l), arches to the selection of this particular heart dorsad and to the left of it, and is con- for reconstruction: (1) it fits well into nected by the temporarily robust ductus the existing series of reported reconstruc- arteriosus (fig. 2) with the ventral sur- tions, (2) the crucial changes that are face of the left dorsal aortic root. occuring during this period have often The left fourth aortic arch and dorsal been described on the basis of interpola- aortic root are larger than their counter- tions between more carefully observed parts on the right side. earlier and later stages, and (3) the heart was particularly well preserved to demon- 1 This study was supported in part by a grant from the Michigan Heart Association. strate internal features to best advantage. 2 The University of Michigan Collection No. EH-841.

17 18 DONALD G. VERNALL

Fig. 1 Ventral view of a wax-plate reconstruction of the human embryonic heart in the seventh week of development. (Reconstruction X 100, illustration X 50.)

The continuity between the primordial distal portions of these can be pulmonary arteries (fig. 2) and the right seen projecting from this cut surface en- sixth aortic arch is obscured by the mass route to the developing . of tissue deep to the cut surface of the The four pulmonary veins converge into dorsal mesocardium, although the more a common trunk, the pulmonary inlet, be- EMBRYONIC HEART IN THE SEVENTH WEEK 19 fore entering the left atrium (fig. 3). Los of the right, narrow (fig. 3) as they be- ('58) refers to this dilated pulmonary in- come continuous with the horns of the let as the spatium pulmonale. (venous sinus). The wide lumen of the left common The left horn of the venous sinus has cardinal vein, and to a lesser extent that become more elongated than the right and

Fig. 2 Dorsal view of a wax-plate reconstruction of the human embryonic heart in the seventh week of development. (Reconstruction x 100, illustration X 50.) 20 DONALD G. VERNALL

passes diagonally across the dorsal wall of the inferior caval vein and from the left the heart in what approximates its ulti- and right horns of the venous sinus. mate position as the coronary sinus. In the floor of the sinal bay, a ridge is The anterior surface of the heart is visible between the orifices of the inferior devoid of attachment to the ventral body caval vein and the coronary sinus (fig. 3). wall. Ventral attachments are found on This ridge extends from the basal tip of the anterior surfaces of the ascending the left venous valve in a dorsolateral di- of the and inferior caval vein. rection toward the medial surface right venous valve. The originally continuous dorsal meso- The unguarded orifice of the pulmonary cardium has separated into a venous and inlet (spatium pulmonale) is located in an arterial segment. The cut surfaces of the floor of the left atrium in a bay which these dorsal attachments are indicated by is similar to the sinal bay of the right the light areas in figure 2. atrium (fig. 3). The medial wall of this The vessels of the coronary circulation bay is partly formed by the primary inter- are not apparent externally as yet although atrial septum. The atrial wall lateral to the proximal portions of the more major this pulmonary bay exhibits a local pro- channels can be found in sections of the liferation which Los ('58) refers to as the epicardium in the atrioventricular sulcus. crista pulmonalis sinistra (left pulmonary crest). This crest deepens the pulmonary Internal structure bay and marks the area where the left The most conspicuous structures within horn of the sinus venosus was absorbed the atrial chambers are the primary inter- into the atrial wall externally. The corre- atrial septum and the right and left venous sponding, but less clear, right pulmonary valves. There is no evidence of the sec- crest, which Los found at this stage is not ondary interatrial septum which if present recognizable in this model. would lie between the left venous valve The ventricles at this stage are of simi- and the primary interatrial septum in a lar size with walls that are richly trabecu- recess referred to by Tandler ('12) as the lated and of equal thickness. The conus interseptovalvular space. ridges have not fused and the ventricles The primary interatrial septum is dis- are in open continuity in this area. In the tinguished by the large secondary inter- region of the atrioventricular canals, how- atrial ostium which occupies almost the ever, the has met entire cephalic half of this partition. The the fused , and the primary interatrial ostium has been com- ventricles are separated from each other pletely obliterated by the fusion of the at this point. primary septum with the endocardial cush- DISCUSSION ion masses which have partitioned the atrioventricular canal. External configuration The left and right venous valves are The discrepant size relation between the both well developed, the left being almost left and right fourth aortic arches and as prominent as the right. The right ve- between the left and right dorsal aortic nous valve forms a baffle which directs roots heralds the development of the left the blood leaving the sinus venosus toward channel into the main systemic channel the interatrial orifice and away from the and the development of the right into the chamber of the right atrium. proximal portion of the right subclavian Both venous valves unite in the cephalo- . dorsal portion of the right atrium, above The convergence of the four pulmonary the level shown in figure 3, to form the veins into a common channel before en- prominent, but transitory, septum spur- tering the left atrium gives little indica- ium. From this ridge, the valves flare out tion that they will subsequently enter this (fig. 3) to enclose the deep sinal bay chamber separately after the common (Licata, '54) of the right atrium. Into trunk has been absorbed into the back of this chamber is discharged the blood from the heart at later stages of development. EMBRYONIC HEART IN THE SEVENTH WEEK 21

B Fig. 3 Internal structure revealed as succeeding segments of the model are removed. (Recon- struction X 100, illustration X 32.)

The lumina of the common cardial veins The position and the elongation of the are surprisingly wide relative to the caliber left sinus horn, as well as its point of of the anterior and posterior cardinal entry into the right atrium, graphically veins. The boundary between common illustrate the path followed by the venous cardinal vein and sinus horn is indicated sinus in its shift to the right of an original by the conspicuous narrowing of the chan- midline position. nel that has been described by Los ('58) The cut attachments to the ventral body in even younger embryos (4.4 mm cr wall that are visible on the anterior sur- length). faces of the ascending aorta and inferior 22 DONALD G. VERNALL caval vein are not, according to James (fig. 3). Licata ('54) reports that in the Baker (personal communication), rem- ninth week of development the area of the nants of a vanishing ventral mesocardium interatrial functional orifice is roughly that arose from the fusion of separate equal to the area of the inferior caval lateral primordia. Examination of earlier inlet, and Patten, Sommerfield, and Paff stages of development indicates that they ('29) describe this area at term as being are actually formed by the extension of only 40% of that of the inferior caval the pericardial cavity on each side of them. vein. Patten points out that this relative The relatively broad arterial and venous diminution in the size of the interatrial segments of the dorsal mesocardium give communication is correlated with the in- little indication of the further narrowing creasing pulmonary return to the left at- of these dorsal attachments of the heart rium as the lungs develop. that will later occur. Only in the portions The flow of blood from the right to the proximal to the cut surfaces of the right left atrium is further encouraged by the and left sinus horns is there some sug- position of the well-developed right venous gestion of this reduction. This is more valve. The effectiveness of this arrange- apparent in the mesocardium associated ment is demonstrated by the essentially with the distal portion of the left sinus similar size of the two atria in spite of the horn presaging the formation of the liga- striking differences in size of the venous mentous fold of Marshall in this area. channels discharging into them. Some in- vestigators were so intrigued with the effi- Internal structure ciency of this set-up that they felt little or The absence in the interseptovalvular none of the inferior caval stream could space of any evidence of the secondary escape being shunted into the left atrium. interatrial septum casts some doubt upon The various ingenious technics employed the validity of the predictions of some by Pohlman ('07, '09); Kellogg ('28, '30); investigators, such as Patten ('53), that Patten, Sommerfield, and Paff ('29); and this structure is always present at this Barclay, Franklin, and Prichard ('44) stage. Odgers ('35) and Los ('58) re- demonstrated conclusively, however, that ported that they were unable to find any not all of the inferior caval stream passes definite indication of this septum until into the left atrium. embryos had attained a crown-rump length The integrity of the right venous valve of 17.5 and 19.0 mm, respectively. The has not, as yet, been violated by the fact, however, that two of the five other thinned areas which will presage the subse- from 14.0 to 15.0 mm embryos ex- quent resorption of much of this structure amined in the current study did exhibit with the occasional persistence of strands recognizable secondary interatrial septa that make up Chiari's net. Of the six confirms, I feel, the prediction that this human hearts of this age that were ex- structure appears during the seventh amined. only one exhibited such thinned week; but suggests that it is not so well- areas. There is apparent in the model, developed as had previously been sup- however, a finger-like process which pro- posed. The discrepancies between the vari- jects from the dorsal wall of the right ous times at which the first appearance sinus horn into the lumen of the sinus of the secondary interatrial septum has venosus. Such a structure would perhaps been reported emphasizes the necessity account for those portions of Chiari's net for examining more specimens at each that are occasionally encountered in a stage of development in order to take position too medial to be considered a individual variability into fuller account. persistence of a portion of the right venous The extent of the foramen in the ceph- valve. alic half of the primary interatrial septum The left venous valve which Odgers would seem to permit the septum to offer ('35) described as being more prominent only minimal resistance to interatrial flow. than the right in the 5 mm embryo is The area of this orifice is many times still well-developed but is by this time greater than that of the inferior caval vein smaller than the right. Its position is such EMBRYONIC HEART IN THE SEVENTH WEEK 23 as to supplement the interatrial septum Sections of five other embryos, of a similar in forming a partial barrier to the flow of age, were examined and compared with blood from the inferior caval vein into the model. the left atrium. The ridge that is present in the floor of External configuration the sinal bay of the right atrium marks 2. The four chambers of the heart and the point where, in younger stages, the the associated major vessels are externally left and right sinal horns originally met. apparent in a close approximation to their This primordium of the venous sinus sep- adult positions. The pulmonary trunk tum will continue to develop until it com- arises anterior to the ascending aorta, pletely separates the inlets of the inferior arches around to the left of it, and con- vena cava and left sinus horn. In the nects with the anterior surface of the left course of this development it will meet dorsal aortic root via the large ductus and fuse with the medial surface of the arteriosus. The larger size of the left aortic right venous valve which is thereby sub- channel presages its persistence as the divided into the (Eustachian) valve of the dominant systemic channel accompanied inferior vena cava and the smaller, lower by a relative reduction of the right into (Thebesian) valve of the coronary sinus. the proximal part of the right subclavian This partition is the structure that has artery. The pulmonary arteries are small been named the venous sinus septum by but conspicuous channels which project Los ('58), the cavocoronary sinus septum into the dorsal body wall. The four pul- by Licata ('54), the sinus septum by Tand- monary veins enter the left atrium via a ler ('12), and the Querfalte by Born (1888). common trunk, the pulmonary inlet. The The medial wall of the pulmonary bay left horn of the sinus venosus is elongated. of the left atrium is formed by that por- Its diagonal position across the back of tion of the primary interatrial septum that the heart approximates the position it will has not been perforated by the interatrial occupy as the coronary sinus and reflects orifice. This arrangement serves to limit the path of the shift of the sinus venosus the flow of pulmonary blood across the to the right from an original midline posi- interatrial septum into the right atrium. tion. The proximal portions of the vessels A further functional significance to the of the coronary circulation are visible in relationship between the orifice of the pul- sections of the epicardium in the atrioven- monary inlet and the primary interatrial tricular sulcus. septum is pointed out by Licata ('54) who 3. The dorsal mesocardium has sepa- suggests that, at later stages, the mounting rated into a venous and an arterial seg- return of blood entering the heart at this ment, while the ventral mesocardium is point from the rapidly developing lungs absent. Ventral attachments are present would tend to crowd the primary inter- on the anterior surfaces of the aortic trunk atrial septum against the secondary inter- and inferior caval vein. atrial septum and encourage fusion. The lateral wall of the pulmonary bay Internal features is formed by the left pulmonary crest. The 4. The atrial chambers conspicuously gully-like channel between this pulmonary exhibit a primary interatrial septum, left crest and the primary interatrial septum and right venous valves, and septum extends in the floor of the left atrium from spurium. The secondary interatrial septum the pulmonary inlet to the left atrioven- is absent from the model although two of tricular canal. the five other hearts examined did demon- strate a recognizable secondary interatrial SUMMARY septum. A large secondary interatrial for- 1. A wax-plate reconstruction of a heart amen occupies, almost completely, the from a human embryo in its seventh week cephalic half of the primary septum. The of development with a crown-rump length well-developed right venous valve is 10- of 14.5 mm and in Streeter's Develop- cated so as to direct the blood entering mental Horizon early XVIII is described. from the inferior caval vein toward the 24 DONALD G. VERNALL

interatrial orifice. The left venous valve 1930 Studies on the of mammals. Am. J. Physiol., 91: 637-648. is also well developed but is somewhat Kramer, T. C. 1942 The partitioning of the smaller than the right. truncus and conus and the formation of the 5. The sinal bay of the right atrium is membranous portion of the interventricular septum in the human heart. Am. J. Anat., deep and sheltered by the venous valves. 71: 343-370. The primordium of the cavocoronary sinus Licata, R. H. 1954 The human embryonic septum is present as a ridge in the floor heart in the ninth week. Ibid., 94: 73-125. Los, J. A. 1958 De Embryonale Ontwikkeling of the sinal bay between the orifices of the van der Venae Pulmonales en de Sinus Coro- inferior caval vein and the left sinal horn. narius Bij de Mens. Doctoral Dissertation, Rijks- 6. The inlet (spatium pulmonale) of the universiteit te Leiden, Drukkerij “Luctor et pulmonary veins opens into a conspicuous Emergo’’-Leiden. 131 pp. + 56 figs. Odgers, P. N. B. 1935 The formation of the channel (pulmonary bay) in the floor of venous valves, the and the the left atrium. in the human heart. J. Anat., 7. The ventricles are in open continuity 69: 412422. Patten, B. M., A. Sommerfield and G. H. Paff in the region of the unfused conus ridges 1929 Functional limitations of the foramen but are separated in the area where the ovale in the human foetal heart. Anat. Rec., interventricular septum has become at- 44: 165-178. tached to the fused endocardia1 cushion Patten, B. M. 1953 Human Embryology. The Blakiston Division, McGraw-Hill Book Co., Inc., masses of the atrioventricular canal. There New York, 2nd ed., XVII + 798 pp. is, as yet, no distinction between what will 1960 The Development of the Heart. be the membranous and muscular portions Gould, The Pathology of the Heart. Charles C Thomas, Springfield, Ill., 2nd ed., Chap. 11: of the interventricular septum. Both ven- 24-92. tricles are similar in size, thickness of Pohlman, A. G. 1907 The fetal circulation walls, and amount of trabeculation. through the heart. A review of the more im- portant theories, together with a preliminary LITERATURE CITED report on personal findings. Johns Hopkins Hosp. Bull., 18: 409412. Barclay, F. P., K. J. Franklin and M. L. Prichard 1909 The course of the blood through 1944 The Foetal Circulation. Charles C the heart of the fetal mammal, with a note Thomas, Springfield, Ill., XVI + 275 pp. on the reptilian and amphibian circulations. Born, G. 1883 Die Plattenmodellirmethode. Anat. Rec., 3: 75-109. Arch f. mikr. Anat., 22: 584-599. Streeter, G. L. 1948 Developmental horizons in 1888 Uber die Bildung der Klappen, human embryos. Description of age groups Ostien, und Scheidewande im Saugetierherzen. XV, XVI, XVII, and XVIII, being the third Anat. Anz., I11 Jahrg., 3: 606612. issue of a survey of the Carnegie Collection. Chiari, H. 1897 Ueber Netzbildungen im rech- Contrib. to Embryol., Carnegie Inst. of Wash- ten Vorhofe des Herzens. Beitr. z. path. Anat. ington, 32: 133-203. U.Z. Allg. Path., 22: 1-10. Tandler, J. 1912 The development of the heart. Kellogg, H. B. 1928 The course of the blood In Keibel and Mall, Manual of Human Em- through the fetal mammalian heart. Anat. bryology. J. B. Lippincott Co., Philadelphia, Rec., 42: 443465. 2: 534-570.