Paper - On the time of the post-natal obliteration of the fetal blood-passages (1918)

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Scammon RE. and Norris EH. On the time of the post-natal obliteration of the fetal blood-passages (foramen ovale, ductus arteriosus, ductus venosus). (1918) Anat. Rec. 15(4): 166-180.

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This historic 1918 paper by Scammon and Norris ia an early description of the postnatal cardiovascular changes in human circulation.



Modern Notes: foramen ovale | ductus arteriosus | ductus venosus | heart | neonatal

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On The Time of the Post-Natal Obliteration of the Fetal Blood-Passages (Foramen Ovale, Ductus Arteriosus, Ductus Venosus)

Richard E. Scammon and Edgar H. Norris

Institute of Anatomy, University Of Minnesota

Three Plates

Introduction

It is gcnorally rocognized that two separate processes are involved in the occlusion of the fetal blood passages after birth. The first is the simple functional closure which takes place, in the great majority of cases, at or immediately following birth; the second is the permanent anatomic obliteration which occurs at a later period. The mechanics and histology of the latter process are generally discussed in our larger treatises on obstetrics and pediatrics, and in our major anatomical texts; but the thiie of postnatal obliteration is often unmentioned, although in a number the statement is made that the obliteration takes place in the first few days or, at most, weeks after birth.


The origin of the current concepts as expressed in these larger texts can be traced, we think, to the first statistical study on this subject, which was published ninety years ago by the French clinician Billard. This investigator collected data on the obliteration of the ductus venosus, ductus arteriosus, and foramen ovale in a series of one hundred and twenty-eight children who died in the first eight days of life. He found instances of the obliteration of ail these passages on the first day after birth. The foramen ovale and ductus arteriosus were closed in over fifty per cent of his cases on the eighth day while the ductus venosus was closed in a still larger number. He therefore concluded that the obliteration of the fetal blood-passages proceeded very rapidly - in the first few days of life - an opinion in accord with that held by a number of writers in the eighteenth century. The results of Billard's study were published in his 'Traits des maladies des enfants nouveau-n6s' in 1S2S. This work was extremely popular in its time; it passed through a number of French editions, was translated into Italian and German and twice app<>jired in American editions. In several publications of the middle of the last century Billard's figures are cited and his name is quoted in connection with them. In later works, however, the same opinion has been repeatedly expressed but its source apparently has been forgotten.


A large amount of data concerning the chronology of the postnatal obliteration of the fetal blood-passages has accumulated since the time of Billard. This material is scattered through the periodical literature of legal medicine, obstetrics, and pediatrics and is also uieluded in a number of rather inaccessible brochures. In the following pages we have collected as much as possible of these scattered data and have arranged them in tabular and graphic fonii. In so doing we have confined oiu-selves to those records in which series of consecutive cases have been assembled. These records include ob.serA^ations on children who were born at term, and also a few cases of children who were prematiu-ely born. In most instances, however, investigators have failed to separate these two groups. A comparison of the records of the few known cases of prematurity with those of children known to be born at term shows no appreciable difference in the time of obliteration of the fetal blood-passages. We hav(> therefore combined them in our tables. In all cases the patency of the fetal passages was te.sted either by injection or by probing, excepting those of Faber ('09) which were examined micro-scopically.


The results made apparent by this combined series of observations are at variance with the current concepts on the subject as expressed in most of our larger texts, and also with the results of Billard. Billard's observations were confirmed by Bernutz ('65) who found the ductus arteriosus closed in fourteen cases in a series of twenty-one children who died between the tenth and twentieth days, and in thirty-six out of thirty-eight children dying between the twentieth and sixtieth days. Since this time no observer has substunfiatod these findings. Although a number of series niueli larger than those of Billard and Bernutz' have been collected. Thus Elsasser ('52), in a series of nearly three hundred observations upon children of the first month, found obliteration of the ductus arteriosus in about two per cent and of the foramen ovale in about three per cent of his cases; and Alvannga ('69) found practical!}' no instances of obliteration of the foramen ovale or ductus arteriosus before sixty days. The findings of later obseivers (Alexeieff ('00), Theremin ('87-'95), KuchefT ('01) and others) agree essentially with those of Elsasser and Aharenga although they have noted some instances of earlier obliteration of the passages.

The Foramen Ovale

The compiled data on the obliteration of the foramen ovale are shown in extenso in table 1. Table 2 is a summary of these data giving by periods the total number of observations and the number and per cent of cases obliterated. Graphic representations of these data are shown in figure 1 curve A. and in figure 2. In the summary and curve the data of Billard are omitted because his findings are so directly opposed to those of all other investigators that we conclude that either his method of investigation was defective or that his definition of obliteration was entirely different.


As will be seen in table 2. less than one per cent of the foramina are completely closed in the first week of life, and less than two and one-half per cent in the second week. In the latter part of the first month the figures indicate that the obUterative process takes place more rapidly as the opening is impervious in about one-eighth of all cases of this period. The rapiditj' of this process mcreases during the second month, for the interatrial communication is obliterated in approximately one-sixth of all cases in the first half of this period and in about one-fourth in the latter half. During the third month somewhat less than ten per cent of the cases are obliterated so that by the end of the first trimester the foramen or {do is finally closed in about onethird of all cases. After the end of the third month the process again goes on more slowly and the average of obliteration in the second trimester is about forty per cent, that in the third trimester about forty-five per cent and that in the fourth trimester about fifty-five per cent. Our figures for the period between one and five years show an average obliteration of fifty-five per cent, which is five per cent less than that of the last trimester of the first year. This difference is due. no doubt, to the small number of cases tabulated in these two periods, and does not represent a real increase in the number of patent foramina. The figures of the .second five year interval indicate that two-thirds of the foramina are clo.sed: but the small amount of data for the period between the first and tenth years makes it impossible to say with certainty just when this increase in obliteration is bntuphf about. In the second drrado the percentage of open foramina is the same as in the period between five and ten years and the foramen ovale is found to be obliterated in about seventy two per cent of individuals of twenty years and over.


  • The cases reported by Bernutz were not examined by him personally but were oollected iit his instance by the interne of a colleague in the Hospice des EnfantsTrouv<5s.
  • Haberda ('96) studied the obliteration of the ductus venosus and ductus arteriosus in a considerable series of infants and children. As his data are not given in numerical form we are unable to include them in our summary. The general statements of this writer indicate that his findings were somewhat similar, as regards these two vessels, to our own.

Table 1 Data on the obliteration of the Foramen ovale

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Table 2 Obliteration of the Foramen ovale (5,858 cases)

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Curve A of figure 1 expresses graphically the frequency of obliteration of the foramen ovale during different periods in the first year of life. This curve is readily divisible into three parts. Tlie first portion, which extends from birth to the middle of the second week, is a short segment expressing the obliteration of a Uttle over two per cent of the ca.ses. It is followed by a longer segment rising abruptly and terminating in about the middle of the third month. Nearly half of the ca.ses which are finally closed are obliterated in the period represented by this segment (sixty- days), The third segment, extending from about the middle of the third month to the end of the year, shows a very slow but continuous rise and expresses the obliteration of about ten per cent of the total number of cases.


Fig. 1 Three curves representing the average percentages of obliterated fetal blood-passages at different periods in the first year of life. A, dotted line, foramen ovale, B, solid line, ductus arteriosus; C, broken line, ductus venosus. These curves are based upon the material summarized in tables 2, 4 and 5.


Figure 2 is a curve illustrating the froquoncy of tho oblitfration of the foraiiu'n ovale throughout life. The details of the obliteration during the first year, which have just been described, are masked in this figure by the diminution of the time unit. Here again three periods can be recognized which correspond roughly to infancy, childhood, and adolescence and maturity.


Fig. 2 A curve showing the average percentages of cases of oblit«rated foramen ovale at different periods throughout life. Based upon the material summarizcd in table 2.


During the first period the curve rises with extreme abruptness to a point at which fifty per cent of the cases are obliterated. The rise is continued but is much less rapid during the second period which extends from infancy well into childhood. In the third period, which extends to extreme old age, the curve rises very slowly to about seventy-two per cent. In all probability this final percentage of obliteration is reached in early maturity although the character of our data does not permit a graphic representation of this point.

The Ductus Arteriosus

Table 3 shows tho compiled ihxta. upon the post-natal obliteration of the ductus arteriosus, and table 4 summarizes these data by periods. The graphic presentation of this material is shown in figure 1, curve B. As in the ca.se of (he foramen ovale, and for the same reasons, we have omitted Billard's data and also those of Bernutz from the summarized table and from the curve.

Table 3 Data on the frequency of post-natal obliteration of the Ductus arteriosus

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Table 4 Obliteration of the Ductus arteriosus (1095 cases)

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During the first week of life the percentage of obliteration of the ductus arterio.sus is even less than that of the foramen ovale (three-tenths of one per cent). In the second week the percentage rises to an average of two and in the third and fourth weeks to an average of a little over eleven. From this tune on to the end of the third month the process of obliteration is e.\tremely rapid; in the first part of the second month it averages over thirty-seven per cent, in the latter part over forty-seven, and in the third month seventy-six per cent. During the fourth month the average obliteration is eighty-two per cent. Thereafter the percentage increases quite slowly until the end of the year. The average percentage of obliteration in the last three-quarters of the first year is nearly ninety-five.


The data available for the period after one year are small in amount and, with the exception of certain instances in Faber's series, all cases of this period were obliterated. It is quite possible that Faber's material included several specimens which, while containing remnants of the original lumen, were obliterated at other points. His method of examination might easily classify such cases iis patent. It is probable, therefore, that table 3 shows a much lower per cent of obliteration for this period than is actually the case.


Curve B of figure 1 is the graphic presentation of the data summarizes above. Like the curve for the foramen ovale already doserihod and represented in the same figure, this graph is readily divisible into three portions. The first segment extends from birth to the middle of the second week and shows a temunal obliteration of two per cent of the cases. The second segment rises abruptly, crosses that of the foramen ovale, and teniiiimted at about seventy-five per cent in the middle of the third month. The third segment, which extends from the middle of the third month to the end of the first year, shows a continuously decreasing rate of obliteration and terminates at nearly one hundred per cent. Probably all normal cases are closed shortly after the first year, although there are numerous records of individual cases of the anomalous persistence of the lumen of the ductus arteriosus in later life.


  • For the literature on the subject of persistent patency of the ductus arteriosus the reader is referred to the papers of Poynter ('16), Wells ('08) and Gerard ('00').

The Ductus Venosus

The material compiled upon the obliteration of the ductus venosus is shown in table 5 and is represented graphically in curve A of figure 1.


Table 5 Obliteration of the Ductus Venosus (1,761 cases)

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The process of oblilcnitidn is much more rapid in the ductus venosus than in the other fetal passiiges. During the first week the average is two and three-tenths per cent, in the second week it is eighteen per cent, in the third thirty-seven and one-half per cent, and in the last ten days of the first month about seventy six per cent: During the second month the percentage rises to nearly one hundred and thereafter all cases are obliterated.

The curve shown in figure I, while nuich more abrupt than that of the foramen ovale and the ductus arteriosus, is of the same general character and shows three segments. The first segment corresponds to the first few days after birth, and terminates between two and three per cent. The second segment rises with extreme abruptness to ninety-seven per cent in the middle of the second month. The third segment, which is very short, rises gradually to a full hundred per cent by the end of this month.

The Rate of the Obliterative Process in the Several Passages

In order to study the activity of the obliterative process in the various fetal blood-passages we have calculated from the graphs shown in figure 1 the average daily rate of obliteration for a series of periods in early life. This was done by determining from the graphs the initial and terminal percentages of obliteration for each given period. The initial percentage was then subtracted from the terminal one and the figure thus obtained divided by the number of dajs in the period. For example, in the case of the ductus arteriosus the percentage of obliteration at the beginning of the second month was fifty-seven and at the close wjvs seventy-nine and one-half. Thus twenty-two and one-half per cent of all cases were obUterated in this period of thirtA' days and the average daily rate of obliteration was seventy-five hundredths per cent. Table (5 shows the results of these calculations for the three passages and the curves in figure 3 express them graphically.


It will be seen by the examination of these curves that they have certain characters in common. Each starts with a low rate of obliteration, rises rapidly to a peak or niaxinium, and then declines to the base-line which represents the cessation of obliterative activity. In all cases the portion of the curve representing the decline in activity is less abrupt than is the initial rise.

Table 6 Approximate rate of daily and full obliteration of the Ductus venosus, Ductus arteriosus, Foramen ovale in early childhood

Table 6 to be formatted - unformatted table 6


Considering the curves individually, it will be noted that in the case of the ductus venosus both the initial and maximal rate of obUteration is much greater than that of the other two passages and that consequently the entire obliterative process is completed much sooner. The curve expressing the rate of obliteration of the ductus arteriosus is very similjir to that of the ductus venosus although the initial and maximal rates are lower and the apex of the curve falls at a later period. While the curve of the rate of obliteration of the foramen ovale shows the three common characters indicated in the preceding paragraph it is markedly different from the curves of the \cs.sol.s. It rises less abruptly to a lower maximum rate of obliteration which is maintained with but little loss for a much longer period, so that the curve presents a plateau which is entirely absent from the curves of the vessels. Following this plateau, the curve falls at first rapidly and then gradually over a long interval to the base line.

The results of this study may be summarized as follows:



Fig. 3 Three curves showing the approximate average daily rate of obliteration of the fetal blood-passnges in early life. A, dotted line, foramen ovale, B, solid line, ductus arteriosus; C, broken line, ductus venosus. Based upon the data summarized in table 6.

Summary

The tinio of oblitoration of the three fetal blood-passages (the ductus venosiis, the ductus arteriosus, and the foramen ovale) is distinctly hittr than is cojnnionly assumed. The process of obliteration in each of these passages shows three fairly- distinct periods: an initial period with a low rate of obliteration, a middle period in which the rate of obliteration rises and the majority of cases are closed, ami atenninal period in which the rate of obliteration is again slower.


Obliteration is most rapid in the ductus venosus. Although slow in the first week, the process reaches its maxiniuni before the end of the first month and in the third month and thereafter all cases are closed.*


The ductus arteriosus closes more slowly. The obliterative proce-s-s, which is very slow during the first two weeks of life, does not n>ach its maxiiimm until the second month. Threefourths of all cases arc closed at the end of the first trimester and over ninety-five per cent by the end of the first j^ear.

The period of the obliterative process of the foramen ovale is a matter of years rather than months. Beginning ver)' slowly the process reaches its maximum activity near the close of the first nxmth and continues with a slightly diminishing rate during the remainder of the first trunester. At the end of this time approximately one-third of all cases are closed. During the second trimester the rate of obliteration declines rapidl}' and thereafter decreases verj- slowly for an indefinite period — probably until early maturity, although few cases are closed after childliood. At the end of the first year about one-half of all cases are closed, ill th«' second deccnnium about two-thirds, and in maturity about seventy-two per cent.

^ * It has been shown by the studies of Wertheimer ('86), Nitdtin COl), Fontan ClI) and others that the vein which sometimes occupies the center of the ligament of the ductus venoaus in older children and adults is a new vessel developed after the obliteration of the ductus venosus and is not derived from the remains of this trunk.


Postscript

After this paper was in press we secured a summary of onrhundn (1 ;ind eighty-*,'Veii obsavations by Parrot on the obliteration of the ductus arteriosus. Parrot's findings are in general agroeint nt with thos.^ of other observers which we have sununarized above. Fnfortunatt'ly his cases under one year are grouped in such a way that wc? eaiuujt include them in our table 4, but if this were possible they would evidently affect our averages very little. Parrot found the ductus arteriosus patent in four ca.ses in thirty-three of one year and in one in fifty-four of two years. In seventeen crises of tliree y<>ars and over the the <luctus wa.s always obliterated.


Bibliography

Alexeieff 1900 The foramen ovale in tlie child. Diss. St. Petersburg.

Alvarenga, p. F. DaC. 1869 Considi^rations et observations sur IV'poque de I'occlusion du trou ovale et du canal arti^riel. Lisbon. Berndtz 1865 Quoted from Gc/rard, (1. ('00«).l

BiLLARD, C. M. 1828 Traitd des maladies des enfants nouveau-n^s et k la mamelle, fondi^ sur de nouvelles observations cliniques et d'anatomie pathologique, faites & I'hopital des enfants trouvos de Paris. Paris.

BizoT, J. 1837 Hecherches sur le coeur et le systtoe art(?riel chez I'homme. Mem. Soc. Med. d'Observation, T. I. EL6A8SER 1852 t'ber den Zustand der Fotuskreislaufwcge bei neugeborenen Kindern. Zeitschr. f. Staatsarzneik., Bd. LXIV.

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