The persisting right sixth aortic arch of mammals with a note on fetal coarctation.код для вставкиСкачать
THE PERSISTING RIGHT SIXTH AORTIC ARCH O F MAMMALS, WITH A NOTE ON FETAL COARCTATION RALPH F. SHANER Department of Anatomy, University of Alberta, Edmonton, Alberta, Canada SIXTEEN FIGURES Present day thoracic surgery is stimulating an interest in the right sixth or pulmonary aortic arch. Edwards ( '48a) has pointed out that this transient arch may persist as an impervious or slightly patent cord that may behave as a traction band and deform the aorta. I n addition, the right sixth arch may survive as a well developed functioning vessel and alter the postnatal arterial pattern. At least 16 instances of this sort have been recorded f o r man, not counting examples found with a right-sided aorta and in situs inversus. Such a right sixth arch recently turned up in the field of a heart operation (Blalock, '48). A persisting functioning right sixth aortic arch may be another of those rare anomalies that are not so rare, and which have practical significance. I n the course of an extensive study of abnormal embryonic pig hearts (Shaner, '54) I found 17 embryos with the right sixth aortic arch present after it should have disappeared. All but one were embryos of from 20 to 50 mm C. R. length roughly equivalent to the third imonth in human development. Many of the sixth arches in these embryos would doubtless have disappeared later, but a few had established themselves as vigorous vessels and had entered into unusual combinations with arteries derived from other arches ; combinations which foreshadow those already recorded in man. A discussion of such abnormal right sixth arches in the pig, of the 171 172 RALPH F. SHANER arterial arrangements they enter into, and of the factors involved is the subject of this paper. When is a right sixth arch abvzornzal.9 The kind of abnormal right sixth arch I am dealing with is not a vestigial cord, but a well developed vessel functioning after it should have disappeared. To distinguish such a vessel, one must review the normal transfiguration of the aortic arches. A good starting point is the arch system of a 13-mm pig embryo (fig. 1). At this stage there are four pairs of arches, pairs 111,IV, VT, and traces of V. From the roots of the third pair spring the external carotids; from the sixth sprout the tiny pulmonary arteries. The original symmetry of the arch system has already been altered. The truncus is divided into an aorta for the third and fourth pairs of arches, and a pulmonary trunk for the sixth pair. The left fourth and sixth arches are larger than the right ones. The left dorsal aorta is increasing at the expense of the right. I n both aortae the segment between the third and fourth arches is degenerating. The tiny pulmonary arteries are fused, preparatory to taking common origin from the left sixth arch - a peculiarity of the pig not found in man (Bremer, '01). The symmetrical arrangement of the arches is further altered by the descent of the heart into the chest and the dextral twist of the conus. I n a 16-mm embryo (fig. 2) the left sixth arch and the pu1,monary trunk are drawn out into a straight vessel, about which is wrapped a spiral vessel made up of the left fourth arch and the ventral aorta. The two ABBREVIATIONS (FOR ALL FIGURES) 111, IV, V, VI, Aortic arches A., Ventral aorta A.d.d., s., Right and left dorsal aorta B., Brachiocephalic artery C., Locus of fetal coarctation C.c.d., s., Right and left common carotid C.e.d., s., Riglit and left external carotid C.i.d., s., Right and left internal carotid D.a., Ductus arteriosus In., Innominate artery P., Pulmonary trunk P.d., s., Right and left pulmonary artery Sc.d., s., Right and left subclavian arterg T.,Truncus arteriosus RIGHT SIXTH AORTIC ARCH 173 Pd. s. J I? d.+v I 5 I Figures 1-5A Fig. 1 Aortic arches of a normal 13-mm pig embryo. The right third, fourth, and sixth arches are distinguished by crosses, circles, and striations, respectively. From a wax reconstruction of the vessel cavities. X 131.. Fig. 2 Aortic arches of a normal 16-mm pig embryo. The right third, fourth, and sixth arches are distinguished as in figure 1. From a wax reconstruction of the vessel cavities. X 134. Fig. 3 Aortic arches of a slightly abnormal 22-mm pig embryo, A.E.C. 927. The right third, fourth, and sixth arches distinguished as in figure 1. From a wax reconstruction of the vessel cavities. X 204. Fig. 4, 4 A Persisting right sixth arch in a 10-month infant. 4 is from Kelsey et al. ('53). 4 A is a diagram to explain the Kelsey ewe. Arches are marked as in figure 1. Fig. 5 , 5 A Distal segment of a right sixth arch forming the root of the right pulmonary artery in a &day infant, after Ambrus ( '36). 5 A is a diagram to explain the Ambrus case. Arches distinguished as in figure 1. 174 RALPH F. SHANER vessels are now the main outlets of the heart, are much enlarged, and pour blood into an enlarged left dorsal aorta. The other parts of the arch system are reformed around these two master vessels. The two third arches are now the first parts of the internal carotids. Their roots proximal to the external carotids are drawn out into common carotid arteries, as Heuser ('23) has so well illustrated. The segments of the dorsal aortae between the third and fourth arches are further attenuated preparatory to atrophy. The remaining vessels -the right fourth and sixth arches and the distal part of the right dorsal aorta -are reduced to the status of competing sources for the right subclavian artery. I n normal pig embryos the right sixth arch drops out after the 16-mm stage and the distal segment of the right dorsal aorta at the 20.7-mm stage (Heuser, 23) ; thereafter the reduced and-foreshortened right fourth arch alone supplies the right subclavian. The same arrangement is reached in an 18-mm human embryo ( Congdon, '22). A right sixth arch may therefore be considered abnormal when it occurs in an embryo much over 20 mrn in length. Additional anomalies within the heart would confirm such a conclusion. Simple rete.vltion of t h e right sixth arch. An example of an early abnormal right sixth arch is shown in figure 3, from a 22-mm pig embryo. The sixth arch can be recognized by its course and a peculiar covering of light staining tissue which it shares with the ductus arteriosus. This right sixth arch is admittedly a borderline case mhich may he either abnormal or just delayed normal. There are, however, other slight anomalies : incomplete rotation of the conus, rather late persistence of the distal part of the right dorsal aorta, and a left subclavian that arises farther down the aorta than it should. Such a functioning right sixth arch is one of the anomalies found in a 10-month human infant by Kelsey et al. ('53), whose figure is reproduced in figure 4. The heart of the Kelsey case suffered from complete transposition of the aorta, open interventricular foramen, and basal pulmonary stenosis. The R I G H T S I X T H AORTIC ARCH 175 human right sixth arch gives rise to the right pulmonary artery; it does not lose the artery as does the pig. The arch became indispensible with the closure of the ductus arteriosus. Nature performed a Blalock operation, using the right sixth arch instead of the usual subclavian. The vessel encountered by Rlalock ( '48)is probably another functioning right sixth arch, although its origin could not be observed. It was large enough to graft into the right pulmonary and to reproduce the Kelsey heart arrangement. Another instance of a functioning right sixth arch has been reported by McCullough and Wilbur ('44). Here the ductus arteriosus was also patent. Several older examples with and without a patent ductus arteriosus have been recorded by Poynter ( '16). ContiinuiNg right sixth arch with atrophy of its prox;imal segmeNt. In man the retention of the entire right sixth arch provides a double origin for the right pulmonary artery (fig. 4,4 A). Should the proximal segment of the sixth arch secondarily disappear, the right pulmonary artery would be supplied from the innominate artery through the iourth arch and distal remnant of the sixth arch, and the condition found in the Ambrus ( '36) case would result (figs. 5, 5 A). Similar right pulmonary arteries arising from the distal segment of the right sixth arch in man are recorded by Doering ( '14), Miiller ( '27), and Jew and Gross ( '52). I n each instance there are additional defects in other great vessels or in the heart valves. ContiNuing right sisth arch with loss of the innominate. When the right sixth arch persists as a functioning vessel, as in the pig embryo 'shown in figure 3, the arch forms a vascular loop with the aid of the innominate artery and right fourth arch. The loop supplies the right subclavian and right common carotid arteries. Such an arrangement of embryonic vessels is unstable; some part of the loop tends to becotme a stagnant vessel and drop out. I n the abnormal 35-mm pig embryo whose vessels are shown in figure 6, the innominate artery has disappeared. A vigorous 176 RALPH F. SHANBR right sixth arch (identified by its course and relations) supplies the right subclavian through the usual segment of the right dorsal aorta. It also supplies the internal and external carotids through a long vessel that must be a right fourth arch (with reversed flow) and a common carotid. A blind remnant of the vanished innominate is preserved in the wall of the ascending aorta. The heart of this 35-mm pig embryo has extensive defects: half-completed rotation of the conus, rudimentary semilunar cusps, nonfusion of proximal and distal conus ridges, aorta from the right ventricle, and patent interventricular foramen. A rather similar arrangement of the great vessels occurs in the 14-month infant described by Shapiro ( ’30). The heart was very abnormal. The only vessel leaving it was a “solitary truncus arteriosus” with three cusps and two reversed coronary arteries. A sketch of the great vessels, based upon Shapiro’s photographs and text, is shown in figures 7, 7 A. ‘Two centimeters above the cusps,” writes Shapiro, “two vessels were given off. One directly supplied the left lung. The other promptly divided into an innominate artery and a vessel led to the right lung. The left common carotid and subclavian arteries arose at a slightly higher level.” A comparison of figure 6 with figure 7 will bring out that a true innominate artery is missing in the Shapiro case. What Shapiro calls the “innominate” is really a persisting right sixth aortic arch. Continuing right sixth arch with loss of the right fourth arch. Should the right sixth arch in figure 3 be a strong vessel-stronger than it really is in this particular pig embryo-then the short fourth arch may become a stagnant link between two vessels: one made up of the right sixth arch and the right subclavian and the other of the innominate and the right common carotid. Under such conditions the right fourth arch might atrophy. I have found just this condition in a 100-mm pig embryo (fig. 8). The heart of this pig embryo is much deformed. The aorta arises from the right ventricle, which is nearly divided Cc.d. C.C.S.s c-.s. Sc.d. ’ In.= VI d i p S 7 T . 5. Figures 6-10 A Fig. 6 Persisting right sixth arch in an abnormal 35-mm pig embryo, A.E.C. 1004. The right third, fourth, and sixth arches distinguished as in figure 1. From a wax reconstruction of the vessel cavities. x 9 K,. Fig. 7, 7 A “Innominate” artery from right pulmonary in a 14-month infant, from Shapiro (’30). Sketch based upon photographs and text. 7 A is a diagram to explain the Shapiro case. Arches distinguished as in figure 1. Fig. 8 Persisting right sixth arch in an abnormal pig embryo, A.E.C. 832. The sixth arch is distinguished as in figure 1. Wax reconstruction of the vessel cavities. X 5 %. Fig. 9, 9 A Right subclavian artery from the pulmonary i n a fetal pig. After %egg (’46). 9 A is a diagram t o explain the Gregg case. The arches are distinguished as in figure 1. Fig. 10, 10 A Persisting right sixth arch and retroesophageal right subclavian i n a 17-month infant. After Edwards ( ’48b). 10 A is a diagram to explain the Edwards case. The arches are distinguished as in figure 1. 177 175 R A L P H P. SHANER in two by an hypertrophied moderator band ; in addition there is a patent interventricular foramen. The right subclavian arises from the pulmonary trunk through what is clearly a persisting right sixth arch. Such an anomalous right-sixth-arch-subclavian seems to be a favorite with pigs. I have found a second case in a 254mm embryo, and possibly two more of 35 and 40 mm, but the vessels were trimmed too closely for certain identification. Gregg ( '46) has described the same arrangement in a 21-ern pig. His figure is reproduced in figure 9. The heart in Gregg's case is normal. Another example from a new-born pig is given by Kitchell and Stevens ( ' 5 3 ) ; the condition of the heart is not mentioned. No human case is known to me. The closest parallel in man are three cases of a left subelavian arising from the left pulmonary artery, cited by Ghon ('08). As is well known, the most distal part of the right dorsal aorta - the part distal to the right subclavian in figure 3 may survive and act as the first part of a retroesophageal right subclavian. Should this be added to the Gregg scheme, then the vascular arrangement found in a 17-month infant by Edwards ('48b) results. Edwards' figure is reproduced in figure 10. The vessel linking the right pulmonary with the subclavian is a persisting sixth arch and a length of right dorsal aorta. The retroesophageal root of the right subclavian is very short. The heart is normal; the only other recorded anomaly is an imperforate anus. DISCUSSION The cause of the unusual vessel arrangements I have described seems to be the abnormal retention of the transient right sixth arch followed by secondary changes in other vessels. The retention of the arch was probably the consequence of a general slowing down in embryonic growth when the arch was flourishing. That some general disturbance in growth did take place, the anomalies in the heart of nearly every embryo testify. Under these conditions, the right sixth arch RIGHT S I X T H AORTIC ARCH 1.79 would tend to persist. When growth is resumed after a stoppage, the normal sequence of events is not necessarily followed ; disappearing structures 'may acquire unnatural dominance and survive, as Stockard ( ,Zl) pointed out long ago. Once established, the right sixth arch together with the anomalies within the heart must upset the hemodynamic forces within the arch system. Normally important vessels, such as the right fourth arch and the innominate artery, might become stagnant vessels and disappear. Such degeneration would be the passive result of disuse ; no active obstruction is needed. Fetal coarctatio9z. Nevertheless, a reading of the stimulating paper by Bremer ('48) led me to some observations on norlmal pig embryos which suggest that an active obstructive growth into the riglit dorsal aorta between the fourth and sixth arches - at the point C in figures 9 9and 10 A -might be accessory to the obliteration of the fourth arch in the Gregg and Edwards cases. Bremer, following Bonnet ( '03), distinguished between adult coarctation of the aorta opposite the mouth of the ductus arteriosus, and fetal coarctation situated a bit upstream. Both writers thought that fetal coarctation required some definite growth into the aorta. Bonnet suggested that the degeneration of the transient fifth arch extended into the aorta -at the point x in figure 11. Bremer found in rat embryos some indication of a growth into the aorta from the degenerating segment of the dorsal aorta between the third and fourth arches-at the point y in figure 11. I n addition, Bremer found the ingrowth on both sides of the embryo, and affecting both dorsal aortae. So far as pig embryos are concerned, I find some evidence that the distal end of the fifth arch is the site of such a growth into the dorsal aorta - as Bonnet thought -and further that the growth occurs into both dorsal aortae, as Bremer found in rat embryos. To begin with, pig embryos show considerable traces of a transient fifth arch. A complete arch is rare, but an ephemeral vessel arising from the fourth arch and ending in the dorsal aorta between the fourth and sixth arches 180 RALPH F. SHANER is common (fig. 11). Similar traces of a fifth arch appear in human embryos. A section through the distal ends of the last three arches on the left side of a 13-mm pig embryo (fig. 11L) shows a peculiar creasing of the aortic wall around the mouth of the degenerating fifth arch. The lateral crease, marked by an arrow, becomes an indentation in a 16-mm eimbryo (fig. 12 L), and then a well marked fold in older embryos (fig. 13). The fold becomes a pseudovalve over the outlet of the ductus arteriosus as the ductus enters the aorta obliquely on its lateral aspect. A similar structure has been found in the fetal guinea pig by Kennedy and Clark ( '41), and in the rabbit and dog by Hamilton et al. ( '37). Fetal coarctation appears early. I have found it in a 25-mm abnormal pig embryo. An example from an abnormal 35-mm pig is shown in figure 14. The narrowing develops just proximal to the fold just described. It seems reasonable that the fold has solmething to do with the fetal narrowing of the left dorsal aorta. Furthermore - and this is of immediate concern -the same creasing and indentation appears on the right side of the same embryos (figs. 11R, 12 R). I n normal embryos, where the sixth arch is disappearing at the same time, a true fold cannot develop. Rut in abnormal embryos with a persisting right sixth arch the fold could grow, block the aorta and obliterate the very short right fourth arch. Such a right sided coarctation combined with a persisting sixth arch would explain the vessel pattern found in the Gregg case (fig. 9 A ) , and in the Edwards case (fig. 10 A). The segment of the dorsal aorta between the fourth and sixth arches must be rather unstable on both sides of the embryo. The fifth arch drops off its ventral aspect. The nearby segment of the aorta between the third and fourth arches withers away. I n addition the left aorta suffers from a general colmpression (Barry, '51) and a migration of the left subclavian over it. Anomalies might be expected in a vessel undergoing such a transformation. RIGHT S I X T H AORTIC ARCH 181 A simple narrowing of the right dorsal aorta where the fourth and sixth arches join it would produce the peculiar isthmus in the right subclavian described by Love and Holms ( '39). The figure of Love and Holms is reproduced in figure i II R Figures 11-16 Fig. 11 Sections through the distal ends of the fourth, fifth, and sixth arches of a 13-mm normal pig embryo. Arrows point to lateral indentations. X 27. Fig. 12 Sections through the distal ends of the fourth and sixth arches of a normal 16-mm pig embryo. Arrows point t o lateral indentations. X 27. Fig. 13 Section through the distal ends of the left fourth and sixth arches of a normal 54-mm pig embryo. Arrow points to lateral fold. x 13%. Fig. 14 Fetal coarctation on the usual left side of a 35-mm a.bnorma1 pig embryo, A.E.C. 842. X 113. Fig. 15 Fetal coarctation on the right side of the embryo affecting the first part of the right subclavian artery. Adult form of coarctation also present on left side. Adult case, after Love and Holms ('39). Fig. 16 Diagram of aortic arches to show how fetal coarctation on the right side ooould prodGce retroefiophageal right subclavian artery. 182 RALPH F. S H A N E R 15. This constricted part of the right subclavian is derived from the old fourth arch and a bit of the dorsal aorta. A more severe coarctation of the right dorsal aorta might cut off the right subclavian from the fourth arch entirely and compel the artery to arise from a persisting distal segment of the right aorta, thus producing the well-known retroesophageal right subclavian (fig. 16). SUMMARY 1. The right sixth aortic arch may persist as a functioning vessel and enter into unusual combinations with the great vessels above the heart. Embryonic examples froim abnormal pig embryos are described and correlated with neonatal and adult examples in man and the pig. 2. Such abnormal vessel arrangements could be produced by an early developmental arrest leading to the retention of the right sixth arch, and followed by disuse atrophy of those parts of the aortic arch system that have become stagnant segments under the unusual hemodynamic conditions. 3. Normal fetal coarctation of the left aortic arch map arise from several causes ; in the pig it appears behind a fold in the dorsal aorta at the mouth of the transient fifth aortic arch. 4. A like fold begins on the right dorsal aorta. Either alone, or in co.mbination with a persisting right sixth arch, the fold may be a contributing cause for the unusual vessel arrangements of the region. LITERATURE CITED AMBRUS, G. 1936 Congenital absence of the right pulmonary artery with bleeding into the right lung. J. Tech. Meth. and Bull. Internat. Assn. Med. Mus., 2 5 : 103-109. BARRY, A. 1951 The aortic arch derivatives in the human adult. Anat. Rec., 111: 221-238. BLALOCK, A. 1948 Surgical procedures employed and anatomical variations encountered in the treatment of congenital pulmonic atenosis. Surg. Gyn. Obs., 87: 385409. RIGHT SIXTH AORTIC ARCH 183 BONNET,L. M. 1903 Sur la lesion dite s t h o s e congenitale de l’aorte. Rev. de med. Paris, I S : 255, 355, 419, and 481. BREMER,J. 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