Paper - An anatomical study of the closure of the ductus arteriosus (1942)
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Jager BV. and Wollenman OJ. An anatomical study of the closure of the ductus arteriosus. (1942) Am J Pathol. 18(4):595-613. PMID 19970645
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An Anatomical Study of the Closure of the Ductus Arteriosus
B. V. Jacer, M.D., and O. J. WoLLExan, je, M.D.
(From the Mallory Institute of Pathology, Boston City Hospital, Boston, Mass.)
- Received for publication, August 21, 1941.
The successful surgical ligation of a patent ductus arteriosus has aroused new interest in this structure. This report concerns an anatomical study of a series of ductus arteriosi in an attempt to determine the mechanism of closure.
The method of closure of the ductus arteriosus has long been a disputed point. The approach to this problem resolves itself into the factors concerned with the immediate physiological closure occurring shortly after birth and into the subsequent anatomical obliteration of the lumen.
The early concept that thrombosis was the immediate cause of closure has been discarded. Thrombi have been demonstrated rarely in the ductus arteriosi of infants** but are considered abnormal. Rauchfuss * found the ductus arteriosus thrombosed only four times in 1,400 infants. The ingenious theory of Strassmann* postulated that immediate closure of the ductus arteriosus is effected by means of a valvelike intimal fold situated at its aortic orifice. After birth the increased blood pressure in the aorta closes the valve, preventing reflux into the pulmonary artery. It has been well established that the ductus arteriosus enters the aorta at an acute angle and that the entrance into the pulmonary artery is less acute. Roeder * found that in newborn infants the angle of entrance of the ductus arteriosus into the aorta is always an acute angle of about 33 degrees. This has been confirmed by Graper.” Strassmann, and later Fromberg,® carried out a number of injection experiments in infants which purported to show that the ductus arteriosus could not be injected from the aortic side with greatly elevated pressure, although the injection from the pulmonary side allowed easy passage of fluid through the ductus arteriosus into the aorta. This work was regarded as proof of the effectiveness of the Strassmann valve. Fromberg pointed out the similarity of the entrance of the ductus arteriosus into the aorta with the entrance of the ureters into the bladder. The results of injection technic and the effectiveness of the Strassmann valve have been disputed by Graper, Linzenmeier® and others. Thus Graper believed the elevated intimal fold at the angulated junction of the ductus arteriosus with the aorta too small to be effective.
Schanz *° believed immediate closure of the ductus arteriosus resulted from stretching and knuckling of this structure produced by a change in position of the thoracic organs effective with the onset of respiration. Linzenmeier ® made careful comparative anatomical studies of stillborn fetuses and infants who had died after breathing and believed he could show a definite change in position of the heart and great vessels after respiration with resulting knuckling of the ductus arteriosus. In addition, he injected the ductus arteriosus of stillborn infants, then inflated the lungs and obtained moulds which demonstrated a knuckling of the ductus arteriosus following insufflation. This work was criticized by Graper,’ who made similar studies and concluded that while there was a knuckling of this structure with full inspiration, the knuckling was much less pronounced with expiration and therefore could not be the responsible factor in immediate closure.
A mechanism similar to that postulated by Schanz was that of Melka,” who presumed that at birth the pulmonary artery and aorta become distended with blood and compress the ductus arteriosus, producing immediate closure.
On the basis of the histological structure of the wall of the ductus arteriosus, effective closure by active muscular contraction has been a popular concept, supported by Graper,’ von Hayek,’ Swensson % and many others. Thus von Hayek was impressed by the similarity in structure of the muscle fibers of the umbilical artery and of the ductus arteriosus. Graper was of the opinion that the same stimulus which leads to contracture of the umbilical artery also leads to contracture of the ductus arteriosus. Recently new impetus has been given to this theory by the work of Barclay, Barcroft, Barron and Franklin.**** These workers used lamb fetuses delivered by cesarean section, leaving the maternal circulation intact and preventing respiration by holding a rubber bag containing amniotic fluid over the snouts of the fetuses. Radio-opaque dye was injected into the external jugular veins or the umbilical arteries of the fetuses and the outlines of the heart and great vessels were visualized and recorded with motion pictures. It was found that the ductus arteriosus of these fetuses became closed soon after birth (in one case, in 5 minutes) and that this closure occurred even in the absence of respiration and without interruption of the maternal circulation. In several instances they were able to force the dye into the femoral arteries of moribund fetuses in which the maternal circulation had been interrupted. The dye extended in a retrograde fashion into the aorta, ductus arteriosus and coronary arteries. From their studies they concluded that the pulmonary end of the ductus arteriosus is the first portion to close.
Confusion exists as to the histological structure of the ductus arteriosus in the newborn infant and in the subsequent anatomical changes leading to closure of the lumen. Rokitansky ** thought there was no difference in the histological structure between the ductus arteriosus and the aorta. Subsequent investigators (Graper,’ Linzenmeier,? Melka," von Hayek,’? Swensson** and many others) have shown this to be incorrect. There is general agreement that the ductus arteriosus of the newborn is looser in structure than the great vessels, that it has a well defined internal elastic lamina, has less elastic tissue than the great vessels, and that it has no external elastic lamina. There are conflicting views as well. Thus the direction of the muscle fibers in the media of the ductus arteriosus was described by von Hayek as running in spiral lines. Graper described an inner longitudinal layer of muscle fibers and an outer circular layer with interspersed longitudinal bundles. Melka found an inner and outer longitudinal layer and a central circular layer.
Swensson 7* made a careful histological study of a series of ductus arteriosi taken from human fetuses ranging from 3.5 to 47 cm. in length. Even in a 4.5 cm. fetus he observed that the ductus arteriosus had less elastic tissue and was looser in structure than the aorta and pulmonary arteries} In a 10 cm. fetus there was a well defined internal elastic lamina. In this fetus there was abundant collagen in the media of the pulmonary artery and aorta, yet there were only a few collagen strands in the media of the ductus arteriosus and these lay in the outer portion of the media. In a 23 cm. fetus he noted intimal pillows, ¢.e., eccentrically thickened intimal mounds composed of smooth muscle and elastic tissue. Beneath these mounds the internal elastic lamina was frequently fragmented and split. The pillows persisted in progressively older fetuses. From the 23 cm. fetus to the full-term infant there was no significant change in the structure of the ductus arteriosus. Graper 7 found that the ductus arteriosus of the newborn infant possesses thick intimal mounds. He pomted out the presence of holes in the loose inner portion of the media. These holes are situated most frequently near the bases of the intimal mounds and often contain precipitated plasma and cellular elements of the blood. Graper showed that with progressing age there are changes in the structure of the ductus arteriosus. The intimal pillows become thicker, with resulting narrowing of the lumen. The media becomes thicker and more compact and the holes in the media vanish. As early as 8 days after birth there is evidence of ischemic degeneration in the inner portion of the media with subsequent progression to include the intima and its mounds. There is a relative increase in elastic tissue due to degeneration of other structures. The lumen is visible for a period of 1% years but is occluded at each end. Throughout life the characteristics of a vessel are maintained. Melka ™ explained the closure as follows: Obliteration is a proliferative process, which he observed beginning as early as in a 5.5 cm. fetus. The internal elastic membrane proliferates in an asymmetrical fashion, forming mounds which project into the lumen. Gradually collagen grows from the mounds out into the lumen, effecting complete closure. Weizmann ™’ stated that in old age, calcification, cartilage and fat frequently appear in the course of the ductus arteriosus. Benninghoff ** observed that in the proliferating process, elastic fibers and connective tissue participate. In the scar of the ductus arteriosus in old age there is frequently calcium deposition. A stellate-shaped lumen most frequently remains in the central portion. Finally the structure is converted into a connective tissue strand in which elastic fibers and smooth muscle persist.
The time required for complete closure of the ductus arteriosus is variable. Monckeberg ** stated that any ductus arteriosus which remains open longer than 3 months should be regarded as patent, but added that occasional cases occur in which closure is effected in the second and third year. Christie,” in a series of 558 autopsied infants, found that at 2 weeks, 64 per cent of the ductus arteriosi were still patent; at 6 weeks, 20 per cent; at 12 weeks, only 5 per cent, and by the end of a year, only 1.2 per cent were still patent. Vierordt 7’ considered the ductus arteriosus obliterated at the end of 20 days. Théremin * found that the ductus arteriosus was open in 23 per cent of 144 infants varying from 134 to 4 months of age. Théremin observed that the obliterative process begins in the middle of the ductus arteriosus, progresses next to the pulmonic end and finally to the aortic end. According to Rokitansky,’* the pulmonic end narrows first.
Gerhardt * classified patent ductus arteriosus in adults into four types: (1) cylindrical type, (2) funnel-shaped type with the dilated portion at the aortic orifice, (3) window type with little or no separation between the aortic and pulmonary orifices, and (4) an aneurysmal dilatation of any portion. In addition there is a fifth type in which there is incomplete patency with closure occurring only at the pulmonic end. This type has been described by Hebb, Monckeberg ” and Altschule.”*
Material and Methods
Our material is composed of a series of 71 ductus arteriosi representing a range from 28 cm. fetuses to adults 80 years of age. The specimens were fixed in Zenker’s solution. The loose connective tissue was then removed from the vessel wall, measurements made and sections CLOSURE OF THE DUCTUS ARTERIOSUS 599
taken. The usual procedure was to take transverse sections at the aortic and pulmonic ends of the structure and also a transverse section of the central portion. Frequently, however, longitudinal sections of the pulmonic and aortic ends of the ductus arteriosus and transverse sections of the central portion were taken. The longitudinal sections included portions of the adjacent pulmonary artery and aorta. Sections were stained with phloxine and methylene blue and with Verhoeff’s elastic tissue stain, using the van Gieson counterstain.
All except 5 in this series of 71 ductus arteriosi were cylindrical in type. The acute angulation at the junction with the aorta was a constant occurrence. The ductus arteriosus varied from 0.5 to 1.3 cm. in. length and from o.1 to 0.8 cm. in diameter, after fixation. The average measurements in this series were 0.8 cm. in length and 0.3 cm. in width. Anatomical closure usually occurred by the end of the third week of life. An occasional vessel was found to be patent as late as the end of the second year. Three ductus arteriosi of the window type were observed in which the aortic and pulmonic orifices were closely approximated without any demonstrable intervening structure which could be identified as a vessel. All specimens of the window type were widely patent. These were obtained from infants of 3 days, 4 days and 3% months of age. In addition there were two adults with a ductus arteriosus of the cylindrical type closed only at the pulmonic end.
The ductus arteriosus presents a histological appearance similar to that of any systemic artery of equal size, with an intima, well defined internal lamina, media and adventitia. By intima is designated the portion of vessel wall lying internal to the internal elastic lamina. The intima is peculiar in that there are mounds which project into the lumen. These mounds, which contain fine elastic fibers, smooth muscle and later collagen, are an integral part of the mechanism of closure. They vary in number, width and length in a given cross section and in different portions of the same vessel. The media, in contrast to that of the aorta and pulmonary artery, is loose in structure and contains fine, wavy elastic fibers rather than coarse longitudinal bundles. No external elastic lamina is present in the ductus arteriosus. The adventitia, poorly delimited from the outer portion of the media, contains collagen, elastic fibers, smooth muscle and small blood vessels.
The peculiar elastic structure of the ductus arteriosus in contrast to that of the aorta and pulmonary artery is effectively shown in longitudinal sections of this vessel and the adjacent great vessels. The elastic fibers of the aorta and pulmonary artery condense into a coarse elastic band at the orifice of the ductus arteriosus. The major portion of the elastic fibers traverses obliquely to the adventitia at each end of the ductus arteriosus and terminates. A small portion forms the internal elastic lamina of the ductus arteriosus and the loose, fine meshwork of elastic fibers of the media.
Two 28 cm. fetuses were sources of the earliest specimens in this series. In these the lumina were widely patent. The thick internal elastic lamina was subendothelial except in several areas where low mounds projected slightly into the lumen. These mounds, which were composed of smooth muscle and moderate numbers of fine, wavy elastic fibers, appeared to arise from a splitting and reduplication of the underlying internal elastic lamina. The media was loose, thin, and consisted of smooth muscle and fine, wavy elastic fibers. Just beneath the internal elastic lamina the muscle fibers of the media had an oblique or radial arrangement which was most marked beneath the intimal mounds. Longitudinal muscle fibers flanked the radial fibers. The muscle fibers in the outer portion of the media were circular with a few interspersed longitudinal fibers. There was no collagen in the intima and the small amount which was present in the media lay near the adventitial border.
The ductus arteriosi of seven fetuses varying from 33 to 45 cm. in length showed slight changes from the 28 cm. fetuses. The lumina remained widely patent. The intimal mounds, which continued to be composed of elastic fibers and smooth muscle, showed a definite but variable degree of enlargement in respect to their height and width. Beneath the intimal mounds the tendency to fragmentation of the internal elastic lamina was more marked. The media showed no structural change from the previous specimens.
Five ductus arteriosi taken from full-term infants, ranging from a stillborn infant to those living 3 days, showed very little change. The intimal mounds were slightly larger, contained a moderate amount of elastic tissue and in several instances contained also a slight amount of collagen. The media remained loose and thin, with the muscle fibers coursing in the fashion previously described. In the midportion of the media of several of these specimens there were cellular whorls which were composed predominantly of concentric layers of smooth muscle fibers.
Four specimens obtained from infants living 4 days showed minor changes from those previously mentioned and in addition showed variations among themselves. The lumina of three were widely patent, whereas the lumen of the fourth was completely occluded by an early organizing thrombus. The intimal mounds were variable in size but seemed slightly larger than in younger specimens and in three instances contained small amounts of collagen. Two of these ductus arteriosi were striking in that there were“caps of cellular connective tissue projecting into the lumen from the surfaces of the mounds. These caps, which were subendothelial, apparently arise from an outgrowth of the connective tissue of the intimal mounds and can be differentiated readily from the intimal mounds because of the absence of elastic fibers in the caps. No changes in the structure of the media were observed.
The ductus arteriosi of six infants varying from 13 to 21 days of age showed progressive changes toward obliteration of the lumen. The lumen of one was occluded by an organizing thrombus. In this same specimen there was hemorrhage into the intima with extension into the media. In an infant, 21 days old, the lumen of the ductus arteriosus was occluded by vascular connective tissue, suggesting fusion of expanding connective tissue caps, although a revascularized organized thrombus could not be excluded. In three cases the lumina were markedly narrow and in one the lumen was widely patent. The intimal mounds present in this group were rich in elastic tissue and contained an increasing amount of collagen. The internal elastic lamina was maintained except at the mounds where it was fragmented. The media was more cellular, slightly thicker and more compact with an increase in elastic tissue and collagen. .
There was anatomical closure of four ductus arteriosi taken from infants varying from 22 to 30 days of age. In several, a slitlike orifice persisted in the central portion while one or both ends were occluded by expansion of the intimal mounds. In two the central portion was occluded by organizing thrombi. In all the intimal mounds were large, containing variable amounts of collagen and elastic tissue. Degenerative changes, as evidenced by acellular pink-staining material rich in elastic fibers, were present in the intimal mounds of two specimens. The media was similar to that of the previous group.
From the period of 1 to 3 months of age, six ductus arteriosi were studied. In five the lumina were occluded. This occlusion was effected largely by a proliferation of the intimal mounds with or without overlying caps of loose connective tissue. In one instance the lumen was occluded by an organized thrombus, while another had an unorganized thrombus in the lumen with hemorrhage into an intimal mound. In an infant, 3 months old, the lumen of the ductus arteriosus was patent but narrowed to a small slit throughout its course. The intimal mounds in all were increasingly rich in elastic tissue and contained variable, often large, amounts of collagen. Smooth muscle fibers became less conspicuous in the intimal mounds. No degenerative changes were present in the specimens in this group. The internal elastic lamina was frequently obscured by the abundance of elastic fibers in the intima and media. The media was dense, thick and rich in elastic fibers. With the increased thickness of the media the muscle fibers were almost entirely circular, with disappearance of the abundant longitudinal and radial fibers which were observed in earlier groups.
The ductus arteriosi of ten infants from 312 months to 1 year of age were examined. In every instance the lumen was occluded. The obliterated lumen contained a sparsely cellular tissue rich in collagen and elastic fibers. At 5 months of age degenerative changes were observed in the intima. By 7 months of age the lumen of the ductus arteriosus was occluded by acellular hyalinized material rich in elastic tissue. There was a variable degree of vascularization in the obliterated lumina. The ductus arteriosus of one infant, 6 months old, showed degenerative changes below the internal elastic lamina or in the inner portion of the media. The media otherwise showed no significant change from the previous group.
In a series of eight specimens taken from children varying from 1 to 7 years of age the lumina were occluded in five. In one child, 14 months old, and in another, 2 years old, the lumina of the ductus arteriosi were patent but persisted only as narrow slits. The lumen of a specimen obtained from a child of 4 years contained an unorganized thrombus. Degenerative changes in the vessel wall were more marked than previously. The media was dense and rich in collagen and elastic tissue. In this group, as in some of the older groups, there was occasionally a dense, thick elastic membrane lining a slitlike lumen. Further from the central axis there was often a second incomplete elastic lamina which probably represented the remaining fragments of the original internal elastic lamina.
Sixteen ductus arteriosi were obtained from adults varying from 16 to 80 years of age. The central portion of a specimen from a young adult, 16 years old, was occluded by an organizing thrombus while the pulmonic and aortic portions were completely obliterated. In two adults, 18 and 20 years old, small slitlike lumina persisted throughout the course of the ductus. The remaining specimens were closed completely, or only at the pulmonic end as observed in two adults of 20 and 48 years of age. Degenerative changes were more marked, especially in elderly people where calcification, bone formation and cartilage were occasionally observed. The borderline between intima and media became lost and the entire structure was usually represented by a mass of dense elastic tissue, collagen, hyaline material and a small amount of smooth muscle which lay toward the outer portion of the vessel wall. In longitudinal sections the intima of the pulmonary artery and aorta became thickened over the obliterated ends of the ductus arteriosus. This thickening, although less pronounced, was also present in younger age groups. It is at this site that atheromatous plaques are a common occurrence in the aortas of adults, even in the absence of marked atheromatous lesions elsewhere in the aorta.
Several unusual histological changes were observed in this whole series of ductus arteriosi. In the three patent ductus of the window type, there was, at the site of junction of the pulmonary artery and aorta, a slight thickening of the adjoining intimas, and a contrasting looseness of the media, with elastic tissue streaming from each major vessel toward the adventitial surface. The thickened intima contained elastic tissue, smooth muscle and, in one instance, collagen. There was no internal elastic lamina at the site of junction.
In four instances dissecting aneurysms were observed in the midportions of the cylindrical ductus arteriosus. Two specimens, which were from twins, 45 cm. in length and living 12 and 14 hours respectively, showed fresh hemorrhage in the inner and midportion of the media with elevation of the intima. The pulmonic and aortic ends were not involved. Vascular structure was otherwise similar to that previously described in this age group. One specimen from a full-term infant surviving for 12 hours showed mucinous degeneration with cyst formation in the midportion and outer portion of the media with recent hemorrhage involving half the circumference of the vessel. In an infant, 15 days old, the ductus arteriosus showed a hemorrhage extending directly from the lumen into the outer half of the media. In none of these four was there any evidence of rupture into the adventitia or any evidence of extension into the adjoining great vessels.
Summary and Conclusions
From a series of ductus arteriosi obtained from 71 autopsies, giving a range from 28 cm. fetuses to individuals 80 years of age, the mechanism of closure was studied. In a 28 cm. fetus the ductus arteriosus has a well defined internal elastic lamina which is subendothelial, except in several areas where there are low intimal mounds projecting into the lumen, rendering it eccentric. The mounds, which are composed of smooth muscle and fine elastic fibers, appear to arise from the internal elastic lamina which has a tendency to fragment beneath them. The media is loose in structure and is composed of fine, wavy elastic frbers and smooth muscle fibers. This affords a striking contrast to the aorta and pulmonary artery where the media is compact and composed of laminated bundles of dense elastic fibers. In the ductus arteriosi of full-term infants the only variation from this pattern lies in the slight increase in size and number of the intimal mounds.
Anatomical closure is effected largely by an increase in size and perhaps in number of these intimal mounds, which gradually become infiltrated with collagen. Frequently, subendothelial caps of loose connective tissue grow from the surfaces of the intimal mounds and assist in the obliterative process.
During, and subsequent to, the process of obliteration of the lumen the intima gradually becomes more rich in elastic tissue. The media becomes denser, thicker, and richer in collagen and elastic tissue. The internal elastic lamina usually becomes obscured by the dense elastic tissue of the intima and media. Degenerative changes appear in the vessel wall and in the obliterated lumen as early as 5 months of age. Anatomical closure of the lumen of at least a portion of the course of the vessel is usually effected by the third or fourth week of life. A small, slitlike, microscopical lumen may persist for several menths or occasionally longer. It appears that the central portion of the ductus arteriosus remains histologically patent longer than the aortic and pulmonic ends. In a few instances the pulmonic end is the first portion to become occluded. Thrombosis may occur in the lumen at any time from 4 to 30 days of age but has been observed as late as 4 years of age in this series. This is not a constant finding. In older age groups the ductus arteriosus consists of a dense mass of collagen and elastic tissue with only a few remaining muscle fibers. Hyalinization, calcification and even cartilage formation occur in this group.
It is apparent from this series of ductus arteriosi that many variations in histological structure from this described pattern may occur. These variations may in part account for the seemingly contradictory observations of other investigators.
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Description of Plates
Fig. 1. Fetus 28 cm. in length. Low intimal mounds with fragmentation of the internal elastic lamina. Media loose, and poor in elastic tissue. Elastic tissue stain. X 105.
Fig. 2. Full-term fetus. Fragmentation of elastic lamina at base of intimal mound. Loose structure of media. Elastic tissue stain. X 185.
Fig. 3. Infant, 13 days of age. Intimal mounds of increased size crowned by connective tissue cap. The media is less loose in structure. Elastic tissue stain. X 35 Fic. 4. Infant, 21 days of age. Lumen obstructed by connective tissue, suggesting an organized, recanalized thrombus. Increase in amount of elastic tissue of media. Elastic tissue stain. X 80.
Fig. 5. Infant, 22 days of age. Longitudinal section of obliterating aortic orifice of the ductus arteriosus showing aortic wall rich in elastic tissue while the ductus arteriosus is comparatively poor in elastic tissue and of looser structure. The streaming-in of elastic tissue, chiefly to the outer portion of the media. may be seen, but a slight amount is divided toward the intima to form the internal elastic lamina. Elastic tissue stam. X 25.
Fig.6. Infant, 2 months of age. Longitudinal section of the obliterated aortic orifice of the ductus arteriosus with intimal connective tissue thickening at the site. X 35.
Fig. 7. Infant, 6 months of age. Marked degenerative changes. The internal elastic lamina remains distinct. The intimal mounds are now composed of collagen. connective and elastic tissue. Elastic tissue stain. X 35.
Fig. 8. Newborn infant. Dissecting aneurysm of the ductus arteriosus. Intimal mounds present, but not prominent. Hematoxylin and eosin stain. X 30. S g, eo b
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