Talk:Paper - The nerve supply of the mammalian ductus arteriosus (1941)
THE NERVE SUPPLY OF THE MAMMALIAN DUCTUS ARTERIOSUS
By J. D. BOYD Anatomy Department, London Hospital Medical College
Kocs (1931) was the first to suggest, on theoretical grounds, that specialized pressor-receptor nerve-endings are found on those arteries of the adult mammal which are persistent portions of the embryonic branchial arch arterial pattern. The work of Ask-Upmark (1985) and observations published by the writer (Boyd, 1984, 1987a) support, in a general way, Koch’s suggestion, and the studies of Tello (1924), de Castro (1928), Nonidez (1935), Muratori (1987) and , Tschernjachiwsky (1938) have shown that there is an ample histological basis for the conclusion that the persistent portions of the third and fourth branchial arch arteries are provided with a special and characteristic afferent innervation. This innervation forms the receptor element in the aortic and carotid sinus proprioceptive reflex arcs. The presence of such specialized pressor-receptor regions in those arteries of the adult mammal which are derived from the third and fourth arch vessels has caused several investigators to postulate the presence of equivalent receptors in the pulmonary trunk and its main branches but the evidence for such a pulmonary arterial pressor-receptor mechanism is still inconclusive.
Koch (1931) quotes the observation of v. Schumacher (1902), Perman (1924) and Tello (1924) as evidence for a specialized nerve supply to the pulmonary arteries. These. investigators, however, were concerned only with the general relations of the nerves to the pulmonary vessels and none of them described nerve endings in the pulmonary artery of the type now recognized as specifically pressor-receptor in function. Takino (1933), and more recently, Takino & Watanabe (1938), as a result of extensive investigations of the nerve-endings in the pulmonary arteries of a number of mammalian types, conclude that. these vessels, and especially their extra-pulmonary portions, do receive a rich supply from sensory nerves. Indeed, they state that this supply is richer than that obtained from the vaso-motor nerves. Nonidez (1935), on the other hand, has stated that there is a complete and uniform absence of pressor-receptors from the wall of the pulmonary trunk and the proximal portions of the pulmonary arteries. ‘This point’, he writes, ‘can be established beyond reasonable doubt through the study of well impregnated sections of the hearts of new-born animals. When the size and characteristics of the pressor-receptors are considered it seems highly improbable that they would escape notice or that they failed to be impregnated.’
The physiological evidence is also inconclusive. Schwiegk (1935) has described slowing of the heart and a fall in the systemic blood pressure in the 458 J.D. Boyd
dog when the pressure within a perfused pulmonary artery is raised. Schweitzer (1936), who made similar experiments in the cat, obtained mainly negative results. He writes: ‘in the cat, pressure changes in the pulmonary circulation are only rarely associated with changes of systemic arterial pressure and heart rate. This is in marked contrast to the regularity of response obtained from the carotid sinus.’ To explain this difference Schweitzer suggested that destruction of the afferent nerves in the adventitia of the pulmonary artery during insertion of the cannula was responsible for the negative findings. In view of the difficulty presented by denervation of the carotid sinus or aorta, however, this explanation does not seem easily acceptable.
Takino & Watanabe (1988) have also described slowing of the heart and a marked fall in blood pressure following mechanical or electrical: stimulation of the pulmonary artery in the region of attachment of the ligamentum arteriosum of adult rabbits. The bradycardia and fall in blood pressure were not obtained when the stimulation had been preceded by sectioning of the left: aortic (depressor) nerve and the left vagus. As these workers also identified pressor-receptor nerve-endings in the walls of the pulmonary artery their contribution lends considerable support to those who hold the opinion that the pulmonary arteries possess a nervous mechanism similar to that found in the carotid sinus and the aorta.
In addition to portions of the pulmonary arteries the ductus arteriosus is also generally regarded as being derived from: the sixth branchial arch arteries of the embryo. Consequently a number of investigators (Watanabe, 1938; Muratori, 1937; Boyd, 1937 b; Takino & Watanabe, 1938; and Tschernjachiwsky, 1938) have examined the nerve supply of the ductus arteriosus, and the results obtained by: all these workers indicate that there is a sufficient histological basis for the assumption that, at any rate in foetal life, the ductus possesses a pressor-receptor apparatus similar to that found in the carotid sinus, the aortic arch and the innominate-subclavian arch of the right side.
_ Since publishing a note (1937 5) indicating that the ductus arteriosus of the rabbit possesses a specialized innervation I have collected material bearing on the subject from a number of mammalian species (pig, cat, dog, rat, mouse and man), and the purpose of this paper is to describe the results of a study of this material. As the material includes in many cases portions of the pulmonary arteries, some comment will be made on the nerve-endings found in these vessels, but the main object in view is a description of the nerve supply to the mammalian ductus arteriosus.
MATERIAL AND METHODS
The available material included transverse, sagittal and coronal serial sections through the thorax and root of the neck of rabbit embryos and foetuses of various developmental stages up to, and including, new-born specimens. A number of series of sections through the ligamentum arteriosum and adjacent portions of the aorta and main pulmonary arteries of adult Nerve supply of ductus arteriosus
rabbits have also been used. Some of this adult material was derived from rabbits on whom the operations described in an earlier publication (Boyd & McCullagh, 1938) had been performed, and included specimens from animals in which either the left vagus nerve, or the left aortic (‘depressor’) nerve, or both, had been sectioned a considerable time before the death of the animal.
In addition to this rabbit material, sections are available through the ductus arteriosus of various developmental stages of pig, mouse and human embryos and foetuses, and of new born and adult specimens of these mammals and of cat, dog and rat. Most of the sections are from series stained en bloc with one or other of the Cajal techniques, the younger embryos with the pyridine method, the older embryos and full-time foetuses with the de Castro (1925) modification: A few series were stained by the Bielschowsky or Bodian techniques.
Most of the available material was obtained from the rabbit and, consequently, this mammal will be used as the basis for the description. The variations found in the nerve supply to the ductus arteriosus in the other mammals will be referred to at the end of this description.
Text-fig. 1, which is a schematic reconstruction of the region of the
ductus arteriosus in a rabbit foetus.
nearly at full term gestation, shows the relationships between the ductus arteriosus and the nerves found in all the specimens from the 22 mm. stage of development. In all the embryonic and foetal rabbit material
Text-fig. 1. Schematic reconstruction of nerve supply to the ductus arteriosus in rabbit. 8, Sympathetic trunk; a, left aortic nerve; 1.s.a. left subclavian artery; a.s. ansa subclavia; v, left vagus nerve; r, recurrent nerve; d.a. ductus arteriosus.
branches of the left aortic (‘depressor’) nerve can be traced beyond the aortic arch to the ductus. Some of these fibres reach the ductus along the wall of the aorta so that the appearance is as if the aortic pressor-receptor area had spread on to the attached ductus arteriosus. Other fibres, however, and for the most part from the division of the left aortic nerve which is 460 J. D. Boyd
supplying the dorsal aspect of the aorta, leave the aorta and pass away from its wall to reach the ductus at some distance from the point at which it enters the former vessel (PI. 1, fig. 2). The aortic nerve itself usually -bifurcates a short distance above the aortic arch and, at the point of bifurcation, is related to the collection of cells similar to those of the carotid body, which Nonidez (1935) has called the aortic glomus. The bifurcation results usually in a larger anterior and a smaller posterior division which are distributed to the corresponding surfaces of the aortic arch in a limited area to the right of the origin of the left subclavian artery but not quite reaching the commencement of the brachiocephalic trunk. In most of the embryonic and foetal material the supply from the aortic nerve to the ductus arteriosus is distinctly greater from the posterior division, but in several embryos the anterior division appears to be the sole contributor. In many specimens it is possible to trace fibres from the sympathetic cord to the depressor nerve in the lower part of its course, or to one or both of its divisions. Some of these sympathetic fibres appear to be terminating in relation to the cells of the aortic glomus; others seem to continue in the aortic nerve bundle to the wall of the aorta, but the material does not permit of comment on their ultimate distribution. .
In addition to this supply from the left aortic nerve the ductus arteriosus receives a supply from the left vagus trunk as it crosses the vessel (P. 1, fig. 1). Once the fibres have entered the adventitia of the ductus it is impossible to separate those of aortic nerve origin from those of vagal origin, but my impression is that the vagus contributes chiefly to the antero-inferior aspect of the vessel while the aortic nerve is concerned mainly with the innervation of its postero-superior surface. In a few specimens the inferior aspect of the ductus arteriosus receives some fibres from the recurrent laryngeal nerve as this nerve hooks under it (Pl. 1, fig. 3). These fibres may be presumed to be vagal fibres which are leaving the nerve at a lower level than is usual and _ which accompany the recurrent nerve for a short distance. Finally, some fibres appear to reach the ductus arteriosus from the lower cervical and upper thoracic sympathetic cord of the left side. Certainly fibres of sympathetic origin are closely related to the terminal ramifications of the aortic nerve and, in some specimens, it has been possible to trace distinct bundles from the sympathetic trunk into the vagus nerve and, more rarely, to the ductus itself. In serial sections, however, it is impossible to be definite, and as the experimental results on adult rabbits made no contribution to this aspect of the problem, the relationship of the sympathetic fibres to the ductus is left undecided by the material available.
On reaching the ductus arteriosus, the fibres from the aortic nerve and the vagus trunk course for a variable distance in the adventitia and eventually terminate in endings which are very similar to those found in the carotid sinus and the aortic arch. In the younger embryos (see Text-fig. 2) the fibres tend to penetrate further into the wall of the ductus, approaching, and sometimes reaching, the intima. The fibres which reach the intima usually bend back Nerve supply of ductus arteriosus 461
into the muscular coat of the ductus and they represent the ‘fibres égarés’ described by Tschernjachiwsky (1929) in the carotid sinus of the human embryo. In the older embryos and new-born foetuses (see Text-fig. 2) the fibres are for the most part restricted to the outer third of the media and to the adventitia, but a few fibres can always be traced more deeply into the wall of the ductus.
The fibres which pass into the wall of the ductus are for the most part thick and possess a well-marked medullary sheath. These fibres terminate in endings
Text-fig. 2. Camera lucida drawings of nerve fibres in the wall of the ductus arteriosus of the rabbit. a, Full term foetus; 6, 32 mm. embryo.
(Text-fig. 8; Pl. 1, fig. 4) which are markedly branching and which possess small thickenings and rings on the branches very similar to those found on the nerve terminations of the other pressor-receptor areas. The endings in the ductus, however, are not as extensively ramified as are the better known ones. and occasionally are very circumscribed. Endings of these thick fibres other than of the branching variety have not been found and none of the endings are encapsulated.
In addition to these thick fibres, and their endings, which constitute the major nerve supply to the ductus arteriosus, other and much finer fibres can
Anatomy 75 ‘ 30 462 ~ «SD. Boyd
be found to enter it (Pl. 2, fig. 1). These fibres are very finely myelinated, and they terminate in relation to the muscle fibres of the wall of the ductus by simple endings which resemble the endings of vaso-motor fibres in other blood vessels. They appear, then, to be motor fibres. They may be of sympathetic origin, but some of them could be traced directly from the left vagus nerve to the ductus. This fact, however, does not preclude their ultimate origin from the sympathetic trunk. As has already been stated, my material is not suitable for determining the real nature of the relationship of the sympathetic nervous system to the ductus arteriosus. Nonidez (1939) has recently described a marked difference in the capacity for silver reduction of sympathetic and parasympathetic post-ganglionic fibres in material stained by the Cajal technique, the former fibres staining much more faintly. Unfortunately my material does not show this differentiation clearly enough to allow a decision to be made on this basis alone although it does give grounds for support of Nonidez’s contention.
After birth the ductus closes and eventually is represented by the tough fibrous band which is called the ligaméntum arteriosum. In the earlier stages of this investigation this embryonic vestige was ignored, but the work of Takino & Watanabe (1938) directed attention to it and its nerve supply has
‘now been studied in six normal adult specimens. In all of these specimens
the statement of these workers that the ligamentum arteriosum retains part of the nerve supply which it possesses in foetal life could be verified, but my material shows fewer endings in the ligamentum than they appear, from their account, to have found. In the adult rabbit material examined in this investigation the sensory endings are sparse in comparison with the embryonic and foetal ductus but they are unmistakeable and, like the foetal endings, show a close resemblance to those found in the other arterial pressor-receptor areas (see Pl. 2, fig. 7). As sections of the aorta and adjacent vessels from the rabbits which had been .used for investigations on the results of chronic. denervation of the pressor-receptor areas (Boyd & McCullagh, 1988) are available, it has been possible to study the changes in the nerve-endings in animals in which the left vagus and left aortic nerves had been sectioned. In rabbits
’ with both of these nerves cut, endings are completely absent from the liga mentum arteriosum. This finding corroborates the description which has been given for the embryonic and foetal ductus and demonstrates that this portion of the sixth branchial arch artery receives a nerve supply from both the left aortic nerve and the left vagus trunk. Further, in those rabbits in which only _ the left vagus or left aortic nerve had been sectioned endings could always be found (eight specimens) in the ligamentum arteriosum. This finding again supports the conclusion arrived at from a study of the embryonic and foetal material that there is a double origin of the fibres supplying the afferent innervation to the ductus. The material, however, does not permit of a statement on the relative contributions from these two sources to the ductus. In rabbits in which the right aortic and right vagus nerves had been sectioned no Nerve supply of ductus arteriosus 463
change was found in the sensory endings of ths ligamentum arteriosum. This is in agreement with results obtained by Takino & Watanabe.and strongly suggests that the nerve supply to the ductus is derived solely from the nerves of the left side. In none of the adult material have the finer fibres been found and it is, therefore, not possible to comment on the results of vagal’ section on them. .
The findings reported for the ductus arteriosus of the rabbit differ in no essential manner from those obtained in the other mammalian species which have been investigated. Examples of the sensory endings found in the different
Text-fig. 3. Sensory nerve-endings in the wall of the ductus arteriosus of A and B, rabbit; C, cat; D, dog; E, man.
species are shown in Text-fig. 3. The rabbit is a special case in that it possesses constantly a separate aortic (‘depressor’) nerve and, with the exception of the rat where the nervous relationships are very similar to those found in the rabbit, the sensory nerve supply of the ductus in all the other species investigated appears to be derived from the vagus nerve alone. The pig does possess a separate aortic nerve on the left side but this is distributed solely . to the aortic arch and could not be found to reach the ductus arteriosus. Watanabe (1938) reports that he was unable to find sensory endings in the ductus of young pigs. My embryonic pig material (18-100 mm. stages) shows a rich innervation of the ductus, but in the ductus of the only new-born pig
30-2 464 J. D. Boyd
investigated by me I was unable to find sensory endings. Whether this was due to faulty technique in staining or to a real absence of the endings in the new-born pig I am unable to state.
In none of the material from any of the mammals which have been studied has a rich afferent nerve supply been found in the walls of the distal part of the pulmonary arterial trunk or in its right and left branches. This is particularly true for the embryonic material where the absence of nerve fibres from the walls of these vessels contrasts markedly with the rich supply to the pressor-receptor areas of the aortic arch and the ductus arteriosus. Nevertheless, occasional ramified nerve-endings are to be found in the pulmonary vessels (Pl. 2, fig. 8). These endings, however, are never so richly branching as are those found in the other regions and they are much more scattered: It has not been found possible to identify in any of the material the area of © spread of nerve-endings from the ductus to the adjacent part of the pulmonary trunk as has been described by Takino & Watanabe in their rabbit sections. On the contrary, my material shows a marked diminution in the number of endings in the ductus arteriosus as one passes from the aorta to the pulmonary
_artery, and the pulmonary extremity of the ductus appears completely free from sensory endings. Further investigation with more adequate material has convinced me, however, that my earlier denial (1938) of a specialized afferent nerve supply to the pulmonary trunk was mistaken. But the supply of sensory endings to the pulmonary vessels in the portions examined is so sparse and their character so simple, in comparison with those in the aorta and ductus arteriosus, that it seems justifiable to conclude that the physiological significance of the former will be found to differ both quantitatively and qualitatively from that of the better known pressor-receptor areas.
Nonidez (1935), in his description of the aortic nerve and the glomus aorticum in the rabbit, briefly referred to a few nerve fibres terminating in the wall of the ductus arteriosus ‘by means of’arborizations of a much simpler type than those found in the aorta’. He stated that in no specimens were any fibres seen entering the pulmonary trunk itself and he suggested that the endings in the ductus might play a role during foetal life. My preparations, and the work of Takino & Watanabe, completely verify Nonidez’s description but show that the nerve supply is richer than he suspected. The recent work of Barcroft and his collaborators on the foetal circulation would seem to give a special significance to these histological findings. Their work has shown quite clearly (Barcroft, 1938; Barcroft et al. 1939) that the changes in: the ductus arteriosus at birth are abrupt and that functionally there is a rapid obliteration of its lumen. Anatomical obliteration of the lumen is not a sudden process and may take several weeks or months for its completion, so that ‘probe patency’ of the ductus will be present for some time after blood has ceased to flow through it. When a histological basis for the sudden closure of Nerve supply of ductus arteriosus 465
the ductus is looked for it can be found in the structure of its wall which has, when compared with the pulmonary trunk and the aorta, an increase in the amount of muscular tissue and a marked diminution in the number of elastic and collagenous fibres.
Through the kindness of Prof. Barcroft I have been able to examine the structure of the aorta, the pulmonary artery and the ductus arteriosus in a number of sheep foetuses before, at, and after full-term gestation. In sections stained with van Gieson the wall of the ductus in the sheep foetus takes up practically none of the acid fuchsin, resembling closely in tinge the staining of the heart musculature. On the other hand, the walls of the aorta and pulmonary arteries have a markedly reddish tinge. With slight differences in detail the results obtained on the ductus arteriosus of other mammals (dog, cat, rabbit, man) are similar, and in material stained for elastic tissue the ductus shows almost complete absence of elastic fibres in the media, a result
_Once again in marked contrast to the richness of the aorta and the pulmonary vessels in these fibres. The ductus arteriosus, then, is almost exclusively a ‘muscular’ artery while the pulmonary artery and the aorta are ‘elastic’ vessels, and it seems most probable that this difference in structure of the ductus from that of the adjacent segments of the pulmonary arteries and tlie aorta is associated with the peculiar behaviour of the ductus at birth.
The mechanism causing the contraction of the ductus arteriosus at birth and responsible for the maintenance of the contraction during the period necessary for anatomical obliteration of its lumen is not yet adequately understood. An explanation of the part played by the musculature of the wall of the vessel in the process has been given by Hayek (1985) who showed, by’ a geometrical analysis, that the peculiar obliquity of the muscle fibres in the wall of the human ductus arteriosus can greatly facilitate the physiological obliteration of its lumen at birth. His explanation seems acceptable as a statement of the functional significance of the musculature of the ductus in the mechanism of closure but it does not include an explanation of the factors involved in the control of the muscular contraction. Any explanation of the mechanism of closure of the ductus arteriosus at birth will have to take into consideration the nerve supply to this arterial segment, for physiological closure of the ductus must be the result of special muscular and nervous conditions obtaining in the wall of the vessel.
The finer fibres which have been described in the media of the foetal ductus are presumably the efferent fibres to its musculature and are probably concerned in the initiation and maintenance of the contraction of the sphincter-like muscle. Unfortunately the inherent difficulties of histological investigation on serial sections do not permit of a definite statement on the origin of these fibres. They appear, in foetal material, to be coming from the left vagus nerve, or its branches, but the connexions, at a higher level, between the vagus and the sympathetic trunk make it impossible to exclude a contribution from the latter source, and, indeed, some of the fibres appear to come to the ductus from 466 J. D. Boyd
the sympathetic trunk directly. As the finer fibres have not been found in the adult ligamentum arteriosum, the sections from those rabbits in which the left vagus and ‘aortic nerves had been cut can throw no light on the problem. Some results obtained by Barcroft and his co-workers (1988) in the guinea-pig foetus are suggestive, for they showed that stimulation of the left vagus nerve produced blanching of the ductus, presumably due to contraction of its musculature, but the possibility of sympathetic fibres being involved in the stimulation still holds for this experiment. These workers showed further, however, that the addition of pilocarpine to the Ringer’s solution being used to perfuse the ductus produced some degree of constriction of the vessel and in two out of three experiments atropine opened the ductus after the pilocarpine constriction. The experiments are not conclusive, and the investigators stressed their applicability only to the guinea-pig, but the results suggest a parasympathetic rather than a sympathetic supply to the musculature of the ductus.
It is difficult to assess the functional significance of the pressor-receptors found in the adventitia and outer portions of the media of the ductus arteriosus. The endings will be stimulated, mechanically, by changes in the pressure within the ductus or by contraction of the muscular coat of the ductus. During the — later part of foetal life, therefore, they may be concerned in reflexes which aid in the control of the foetal blood pressure, though the evidence for a control at this stage of development is poor. At birth, when. the circulation of blood through the ductus ceases, they may be concerned. in initiating reflexes which maintain the contraction of the musculature of the ductus until anatomical obliteration of the lumen is complete. After complete closure of the ductus and atrophy of its musculature some of the sensory endings may retrogress, but my material and the results obtained by Watanabe & Takino show that a number of the endings persist into adult life. Nonidez did not explicitly state that he found such endings in the ligamentum arteriosum of the adult rabbit but his statements suggest that he did for he writes ‘the possible function of nerve-endings in the wall of the obliterated duct (ligamentum arteriosum of the adult) can only be surmised’. Whatever the explanation may be it is quite definite that some, at least, of the sensory endings concerned in the supply of the foetal ductus do not retrogress when anatomical obliteration of its lumen occurs.
Finally it must be stressed that the sensory nerve supply to the ductus arteriosus (and possibly the sparser supply to the pulmonary trunk) fits in very well with the explanation suggested by Koch for the distribution of the | major arterial pressor-receptor areas. These areas are found on the portions of the branchial arch arteries which persist into adult life. Pressor-receptor endings of various sorts are found elsewhere in the vascular system, notably in the heart wall and in the great veins entering the right atrium (Nonidez, 1937). The wide distribution of such pressor-receptors, however, does not make less significant the striking fact of the concentration of specialized receptors Nerve supply of ductus arteriosus 467
in localized parts of the vascular system where they have apparently a special physiological significance. That one of the regions with this special significance is constituted by the branchial arch arteries of lower vertebrates is not surprising in view of the position of these vessels in relation to the outflow from the heart and the supply to the thin-walled vessels of the gills. In higher vertebrates the mechanism has been retained on the equivalent vessels and, whatever the ultimate explanation of this retention may be, the presence of an apparatus for recording the intravascular pressure on the. major arterial outflows from the heart has an obvious importance in the reflex control of the
The mammalian ductus arteriosus possesses a sensory innervation very similar to that possessed by the aorta and the carotid sinus. This nerve supply is derived from the left vagus nerve, and, when it is present, from the left aortic nerve. Fine nerve fibres, presumably motor, are also found terminating in relation to the muscular coat of the ductus, but the available material does not permit of a statement as to their origin. The distal portion of the pulmonary trunk and the proximal portions of the pulmonary arteries also possess a sparse affePent innervation.
The nerve supply of the ductus arteriosus is discussed in relation to the behaviour of the ductus at birth.
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EXPLANATION OF PLATES 1 AND 2
Fig. 1. Coronal section of the ductus arteriosus of a full-term rabbit foetus. The section is viewed ~ from behind. Branches of the left vagus nerve.can be seen in the wall of the ductus. de Castro technique. x 60. ,
Fig. 2. Transverse section of a portion of the wall of the ductus arteriosus of a full-term rabbit foetus. Fibres from the left aortic nerve are entering its wall. de Castro technique. x 60.
Fig. 3. Coronal section of the ductus arteriosus of a full-term rabbit foetus. The section is viewed from behind and fibres from the left recurrent nerve can 1 be seen entering it. de Castro technique. x60.
Fig. 4. Section of the wall of the ductus arteriosus of a full-term rabbit foetus to show pressorreceptor nerve-endings. de Castro technique. x 390.
Fig. 5. Nerve fibres and sensory endings in the wall of the ductus arteriosus of a full-term rabbit foetus. A fine fibre can be seen passing among the ramifications of a sensory ending. de Castro technique. x 390. .
Fig. 6. Fibres and nerve-endings in the wall of a human ductus arteriosus. Cajal technique. x 350.
Fig. 7. Sensory ending in the ligamentum arteriosum of an adult rabbit. Qajal technique. x 350.
Fig. 8. Portion of a sensory ending in the left pulmonary artery of a full-term rabbit foetus. de Castro technique. x 390.
‘ Journal of Anatomy, Vol. 75, Part 4 Plate 1
BOYD—NERVE SUPPLY OF DUCTUS ARTERIOSUS Journal of Anatomy, Vol. 75, Part 4 Plate 2
BOYD—NERVE SUPPLY OF DUCTUS ARTERIOSUS