Paper - Functional limitations of the foramen ovale in the human foetal heart

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Patten BM. Sommepfield WA. and Paff GH. Functional limitations of the foramen ovale in the human foetal heart. (1929) Anat. Rec. 44(2): 165-

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This historic 1929 paper by Patten described development of the human heart foramen ovale.

Modern Notes: foramen ovale

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Functional Limitations of the Foramen Ovale in the Human Foetal Heart

Bradley M. Patten
Bradley Patten ( -1971)

Bradley M. Patten, William A. Sommerfield, And George H. Paff

Laboratory Of Histology And Embryology, Western Reserve University School Of Medicine, And The Pathological Institute Of Vienna.

Three Figures

In examining an extensive series of foetal and infant hearts for congenital defects, we became convinced that the size of the foramen ovale was a misleading index of the capacity of the interatrial communication. The valvular fora- minis ova.lis seemed, with striking regularity, to be attached to the septum in such a manner that it would considerably restrict blood flow through the septal orifice. We were unable to find in the literature any reference to this functionally significant condition, except the passing comment of Rucd— inger ("[1, p. 404):

Die Valvfila foraminis ovalis fiir den Blutstrom aus dem rechten in den linken Vorhof in gewisser Hinsicht ein Hindernis abgibt, indem diese Klappe sich Von allen iibrigen Herzklappen dadurch unterscheidet, das sie an der eirunden Oeffnung unter allen Um- standen eine ziemlich strafi:'e'Spa.nnung zeigt.

As this observation of Ruedinger was not followed up by measurements of any sort or by further comment on the significance of such a condition, it has seemed worth while to make measurements designed to determine quantitatively the functional limitations imposed on the foramen ovale by its valvular mechanism.

  • It is a pleasure thus to acknowledge the fact that much of the material on which this work is based was procured through the cooperation of Herr Professor Doktor Rudolph M-aresch and his colleagues, of the Pathologisch-anatomisches Institut of Vienna. During the senior author’s stay there as a visiting worker the facilities of the institute and material from its unusually large autopsy service were placed at his disposal with unstinted generosity.

Fig. 1. Interior of the left atrium of the human heart at birth (X 131-); based on a photograph of a scale model retouched from direct study of :1 group of normal specimens. The valvula foraminis ovalis is shown in the position assumed when :1 stream of fluid is forced through the inferior vena cava.

The general structural conditions in the region of the foramen ovale at the time of birth are so familiar that they call merely for a word of comment to make clear where our measurements were taken. The valvula foraminis ovalis is attached to the left side of the interatrial septum, leaving between itself and the septum an elliptical space which is much the narrowest portion of the passage through which blood must How in reaching the left atrium from the right. This restricted outlet we shall refer to as the ‘functional orifice’ (fig. 1). because it is obviously the part of the pas- sage significant with reference to Volume of blood flow. t\Ieasurements of this functional orifice were made by means of a brass cone which we termed a Vessel gauge. The gauge was turned to such a taper that for a progression of 5 mm. along its axis there was an increase of 1 mm. in its diameter. Its calibration gave us an instrument capable of measuring a rigid orifice with reasonable accuracy to 0.1 mm. No practi- cal purpose Would be served by a more refined type of instru- ment, because the dilatability of the orifices to be measured introduced a possibility of error well beyond the 0.1—mm. limitations of the gauge. But we found that using an inser- tion pressure just suflicient to cause the walls to cling to the gauge when it was gently oscillated gave a method by which measurements made independently by different observers rarely varied over 0.2 of a millimeter. For tabulation and comparison, diameters thus obtained were converted mathe- matically to cross—sectional area in square millimeters. The method of measuring with a conical gauge an opening which, in fixed material, is somewhat elliptical does 11ot ap- pear, from a mathematical standpoint, all that might be desired. Nevertheless, fresh hearts opened under Water and observed while a stream of fluid is directed through this orifice show its plastic boundaries taking on a practically circular shape. Assuming that in the living heart this orifice can be regarded as potentially circular when dilated by the passage of a blood current seemed to entail less likelihood of error than any method of computing its size on the basis of the Variable elliptical shapes shown in dead material.

Fig. 2. Right atrial aspect of the same model shown in figure 1. similarly retouched (X 1%). Note that the oval forameu in the septum is of approximately the same size as the inferior cavul inlet, whereas the functional opening into the left atrium (compare fig. 1) is much restricted by the Way in which valvula foraminis ovalis is attached to the septum.

The oval foramen in the septum itself (fig. 2) with its wide individual Variability in shape and its muscular margins too heavy to be deformed by the passage of a blood current could not be measured accurately with a conical gauge. To deter- mine its cr0ss—seetional area, a modification of Nafiagas’ method was used. Two or more diameters were measured with dividers and pricked into millimeter eross—seetion paper. With these points for guides, a piece of the paper was trimmed down by repeated trials until it exactly fitted into the limbus fossae ovalis. A count of the squares in this paper then gave the area of the foramen ovale directly in square millimeters.

In the course of the work over one hundred hearts were studied. But since We felt that exclusion of material not in first—elass condition was more important for reliable results than a few additional measurements, only seventy-four speci- mens Were finally used. It should perhaps be emphasized that this selection was made entirely on the basis of whether or not a given heart appeared damaged, either by an autopsy incision so located that it interfered with making accurate measurements or by postmortem degeneration. No material passed as being in proper condition was excluded after it had been measured.

Table 1 shows the individual measurements in ten cases selected as being as near normal as possible in autopsy ma- terial. The infants were all Well nourished and near the average birth weight. None of them, as far as was known, had died because of cardiovascular conditions.

Table 1 Individual measurements of ten formalin-fixed hearts from well-developed new-born infants

As far as was ascertainable, no cardiovascular disturbance was involved in any of these cases

WEIGHT AREA cnoss-sncrrow FUNC'[‘1()NAL mmcrronar. rormunx ‘““‘=“" N°~ IN “SSA °VA“S élgfifiléiiffgf .~o§f§11}I§Fb3§L.: °l§¥l§£l)§Ec'iu°v§tW GRAMS IN SQMM‘ IN SQ.MM. IN SQ.MM. entries

.144 18.6 70.0 75.4 21.2 28

75 18.7 25.5 58.1 22.9 39 164 19.0 39.0 52.5 24.6 46 170 20.5 66.0 87.9 24.6 28 143 20.9 92.0 69.4 28.3 41 162 21.5 75.0 78.5 34.2 44 159 21.8 59.0 69.4 28.3 41

14 21.9 26.0 45.4 24.6 54 160 22.0 59.5 95.0 24.6 26 139 22.3 46.0 63.6 24.6 39

Averages 20.7 58.8 69.5 25.8 38.6

Table 2 Average dimensions for various groups of cases

All the measurements from which these averages were compiled were made on formalin-fixed hearts

, , AREA CRO S-SECTION FUNCTIONAL FUNCTIONAL , GROUPS “ EI‘;;HT FOSSA ARE: INFERIOR ommcn on F(;R}}A:,‘1§,NC(:;‘I;‘i:I,I‘l‘ ems .§:a%:.:.. °A:.a.°.*;:%.;%°E ‘°“1‘;“§i§3?.li‘“ ORIFICE Prematures (5 cases) 7.9 30.6 30.6 15.6 54.4 Normal group at term (unselected) (34 cases) 19.5 53.9 63.1 26.8 42.5 10 selected well- developed normals at term 20.7 58.8 69.5 25.8 38.6 Slight valvular defects (12 cases) 20.5 73.8 67.5 31.3 46.4 Extensive valvular defects (13 cases) 20.1 77.0 68.2 36.7 59.9

Table 2 gives average measurements from other groups. It is apparent at a glance that in the entire series the functional interatrial orifice is less than 50 per cent of the oval foramen in the septum. These results are the more striking because of the inclusion of a group of hearts from premature infants and of a group in which the valvula foraminis ovalis was de- fective. In the premature infants the valvula (septum I) and the main portion of the interatrial partition (septum II) have been less long associated than would have been the case had they gone to full term. In other words, the hearts of premature babies are further removed developmentally from the time (on the average, nine to twelve months after birth) whe11 complete fusion of septum I with septum II obliterates tl1e interatrial opening. VVe might, therefore, expect the functional orifice between these septa to be larger in pre- mature infants than it is at full term. Such, indeed, is the case (table 2). But even in the premature group the func- tional orifice proved to be but little more than half (54.4 per cent) the size of the septal opening.

The cases in which there was a definite deficiency of the valvular mechanism at the foramen ovale tell a similar story. By deficiency we mean any condition in which the valvula does not completely cover the septal opening. The imperfect closure may be due to abnormally extensive resorption of septum I in the formation of ostium secundum (fig. 3, A); to underdevelopment of septum II, leaving an abnormally large foramcn ovale (fig. 3, B); to a cribriform valvula (fig. 3, C); or to combinations of these primary types (fig. 3, D). The first two types of defects are fairly common. The rare cases of cribriform valvulae represent a reversion to condi- tions not appearing normally in the development of the human heart, but characteristic of the embryonic bird heart (Patten, ’25), and normally present in modified form in the foetal heart of certain ungulates (Bruch, ’63). Regardless of cause or type, all these valvular defects are functionally similar in that they abnormally increase the size of the effective orifice between the two atria. Yet a group of thirteen such cases (table 2) shows an average functional orifice which is but half of the size of the oval foramen in the septum.

As soon as it became evident that the true functional orifice between the atria was so much smaller than inspection of the foramen ovale would lead one to believe, we extended our observations to include the inferior caval inlet. For the most interesting thing about the interatrial communication is its significance with reference to the course of blood through the foetal heart, concerning which controversies have been smol- dering with periodic outbreaks ever since the time of Harvey.

Fig.3 Types of defects in the valvular mechanism of the foramen ovale. (Drawn direct from fresh specimens, reproduced % natural size.) A. Defect due to overresorption of septum primum (stillborn 3‘, autopsy 110. 176,204, Path. Inst, Vienna). B. Defect due to underdevelopment of septum secuntlum, leaving an abnormally large foramen ovale (9, lived 16 hours, autopsy no. 176,346, Path. Inst, Vienna). C. Perforated valvula, a reversion to primitive type of septum primum ((3‘, age 3 months, autopsy no. 176,312, Path. Inst., Vienna). D. Ex- tensive valvular defect involving a combination of all three of the above factors (specimen no. 4093, Rokitanski Museum, Vienna, from coroner’s autopsy of child aged about 5 months). It should be emphasized that, with the possible exception of the last case on which no clinical history was available, death was not attributable to cardiovascular disturbances. Much more extensive defects than any of these illustrated are not infrequently carried into maturity without producing any recognizable symptoms unless there is an intercurrent disturbance elsewhere in the cardiovascular mechanism or in the lungs.

The historical phases of the subject have been thoroughly covered by Pohlman (’O9) and more recently again by Kel- logg (’28), so they need not be gone into here. The striking thing is the persistence of the Sabatier (1791) doctrine that the entire inferior caval blood stream passes directly through the foramen ovale to the left atrium, while the superior caval blood passes with little or no mingling into the right ventricle. Possibly there exists, because of greater familiarity with the adult circulation where separation of pulmonary from sys- temic blood is so strikingly maintained, an unconscious bias toward interpreting the foetal circulation in terms of blood currents which maintain their identity. There is undeniably something intriguing about routing blood currents through the heart in such a manner that an immediate cause can be assigned for such a striking feature of development as the precocity of the head. VVhatever the underlying reasons may be, current text—book illustrations bear eloquent testimony as to the tenacity of the Sabatier conception in the face of an increasing accumulation of evidence against it.

The obviously important relation between the size of the postcaval inlet and the size of the interatrial communication, surprisingly enough, never seems to have been considered in this connection. This is probably attributable to the fact that, when viewed from the right, the foramen ovale appears ap- proximately the same size as the inferior caval orifice (fig. 2). It is only when a freshly opened heart is examined under water with especial reference to conditions on the left of the septum that the significance of the valvula foraminis ovalis in restricting interatrial blood flow becomes apparent.

Measurements of the postcaval inlet with the calibrated cone offered no difiiculties. The average relation found to exist between its size and that of the interatrial communication was, to us at least, startling. In the entire group of normal cases the functional orifice in the interatrial septum averaged but 42.5 per cent of the inferior caval orifice. There was, of course, quite a Wide range of individual variability (table 1), but in only three or four scattered cases in the entire series was the effective opening in the septum as much as 60 per cent of the caval orifice, and these instances were more than offset by hearts showing a functional orifice which was less than 30 per cent of the caval inlet.

There seems no rea.son to doubt the essential accuracy of these measurements. If the difference between the caval inlet and the functional interatrial opening had proved to be small, the significance of the findings might be questioned, because of possible differential shrinkage caused by preser- vation or because the methods of measurement were not more refined. But there seems no possibility that such sources of error could be of any import when one of the orifices con- sistently measured more than twice the size of the other. Furthermore, if it had been found possible to eliminate the most serious source of possible error——stretching the flexible and somewhat elliptical functional orifice to circular shape in measuring it with a conical gauge——the size difference be- tween the two orifices would have been increased rather than decreased. With reference to the effects of shrinkage, the limited number of hearts we were able to secure promptly after death and measure both before and after fixation showed the error again on the conservative side; for the inferior caval orifice exhibited more shrinkage in fixation than did the functional orifice (table 3). A greater number of cases might well show a. slight change in the average values obtained from our series, but any such change would not affect the essential findings of a functional interatrial orifice less than half the size of the inferior caval inlet.

We are acutely aware that the size of a vascular orifice is not the only factor which determines the volume of blood it can handle. When the technical difliculties of making pres- sure determinations for the foetal circulation have once been surmounted, we shall be on much surer ground. But the abundant experimental data available from animals studied after birth indicate that no great difference between the pressure iii the terminal portions of the cavae and the average intra—atrial pressure is to be expected in the foetal heart.

The size relations of the inferior caval inlet and the inter- atrial opening would, therefore, seem to afford a reasonable working approximation of the relative amounts of blood that would pass through them in a given time.

In the absence of exact knowledge, we may make two dif— ferent assumptions as to the force with which blood enters the right atrium. lf we assume the a.trium is filled by the slow Welling of blood into it from the great Veins, crossing of blood currents which maintain their integrity is obviously impossible, regardless of the size of the openings concerned. If We make the alternative assumption that the blood from inferior and superior cavae enters rapidly enough to produce definite currents, then the small size of the interatrial open- ing must force us to the same conclusion with regard to mix- ing of blood in the right atrium. The simple fact that the functional opening in the interatrial septum is less than half the inferior caval inlet makes it inconceivable that the entire posteaval blood current could enter the left atrium. The part of the postcaval current that cannot pass through the interatrial opening must eddy back into the right atrium and there be thoroughly mixed with the precaval blood.

Table 3 Individual measurements made on fresh hearts compared with measurements on the same hearts following fiation in 10 per cent formalin

WEIGHT IN , “REA OF . AREA OF FU())i1(i§igiiAL

..~...... N0. ems ‘ ".?‘;$’.l.“.$.‘S ”c‘ZfvT.f“.‘%.°§..7.’§‘.i’.f‘ F0§;>;:j;iM<;§;“«E Fresh Fixed Fresh Fixed Fresh Fixed Fresh Fixed -

153 22.7 18.2 34.5 30.0 78.5 63.6 28.3 28.3

176 25.2 23.7 ‘ 31.5 39.0 78.5 55.4 30.2 26.4

177 19.5 18.8 1 46.0 39.5 63.6 66.5 38.5 34.2

178 25.1 23.0 6 36.0 32.0 78.5 60.8 38.5 26.4

180 20.1 19.0 47.0 55.0 78.5 69.4 50.3 50.3

181 30.9 27.6 72.0 58.5 84.8 75.4 47.8 45.4 Totals 143.3 130.3 267.0 254.0 462.4 391.1 233.6 211.0 Averages 23.9 21.7 44.5 i 42.3 77.1 65.2 38.9 35.2

Fixed per cent’ of fresh 90 95 84.6 90.4

That mixing thus occurs in the hearts of mammals other than man has already been clearly indicated by the injection experiments of both Pohlman and Kellogg? But a concep- tion that has been as long promulgated and as widely accepted as the Sabatier doctrine is relinquished with reluctance. Even though it would seem that mixing of blood in the right atrium must be admitted to occur, it will still be argued that the foramen ovale could, by reason of its positional relation to the postcaval orifice, receive pure postcaval blood——as much of it as the valvula foraminis ovalis would permit to pass? The mixture in the right atrium seen in injection experiments could be accounted for as due to mingling of the superior caval blood with that portion of the inferior eaval blood which could not be accommodated by the foramen ovale. On this basis, too, colored particles injected into the inferior cava would, as reported by Pohlman and Kellogg, arrive simultane- ously in the two ventricles. Of course, if unmixed postcaval blood passed through the foramen ovale, the injected particles would be, for the short period of one blood circuit, relati.vely more numerous in the left than in the right ventricle. Such a condition is exceedingly difficult to demonstrate convincingly one way or the other. It must be admitted, therefore, that simultaneous coloration of the two ventricles following post- caval injections proves only what the size of the functional interatrial communication makes inevitable~—that not all the postca.val blood goes directly to the left atrium. But Kellogg’s experiments, which show simultaneous coloration of the ven- tricles following a precaval injection, do indicate unequivo- cally that even the postcaval blood which passes through the foramen ovale is mingled with precaval blood before it arrives in the left atrium. Naturally, such experiments as Kellogg’s cannot be carried out on human material, but the evidence here presented indicates that conditions must be similar in the human heart. For the impossibility of all the postcaval blood passing through an interatrial orifice less than half the size of the caval inlet entails as a direct conse- quence the eddying back into the right atrium of the blood that cannot pass by this route to the left atrium. An inspec- tion of figure 2 with this fact in mind makes it apparent that this back current would be strongest just where the blood from the superior vena cava enters, thereby establishing a series of eddies which would tend to mix the blood in the right atrium.

  • It should perhaps be commented on that some of the earlier injection experiments, such as those of Reid (’35), seemed to support the Sabatier theory. These experiments made with heavy starch masses in dead material cannot be considered seriously in comparison with those of Pohlman and Kellogg, who observed the course of minute colored particles suspended in the circulation of living foetuses.

3 It is of interest to note how close such a hypothetical argument brings us to the Wolff (l778)— Ruedinger (’71)-Ziegenspcek (’82, ’02, ’10) interpretation. According to their views, the inferior caval blood stream was supposed to be split against the margin of the foramen ovale, half going directly into each atrium. This conclusion they based on the positional relations of the caval entrance in hardened specimens. While Ziegenspeck did make some measure- ments of the main vessels entering and leaving the heart, which he uses in support of his contentions as to the course of the foetal circulation as a whole, he seems to have overlooked altogether the small size of the functional outlet of the foramen ovale.

Compared with conditions in adult mammals, the mixing of oxygenated blood freshly returned from the placenta with depleted blood returning from a circuit of the body may seem inefiicient. But this is a one-sided comparison. The foetus is an organism in transition. Starting with a simple ancestral plan of structure and living an aquatic life, it attains its full heritage but slowly. It must be viewed as much in the light of the primitive conditions from which it is emerging as in comparison with the definitive conditions toward which it is progressing. Below the bird-mammal level circulatory mechanisms with partially divided and undivided hearts and correspondingly unseparated blood streams meet all the needs of metabolism and growth. Maintenance of food, oxygen, and waste products at an average level which successfully supports life does not depend on ‘pure currents,’ although such separated currents undoubtedly make for higher efficiency in the rate of interchange of materials. From a comparative viewpoint, the fact that the mammalian foetus is supported by a mixed systemic circulation seems but natu- ral. Moreover, if the fundamental competence of such a circulation is emphasized rather than the respects in which it falls short of the perfected adult mechanism, we are much better able to understand such things as the abrupt and profound changes in the circulation at the time of birth and the seemingly impossible size of septal defects such as are not infrequently carried without serious handicap into maturity and even old age. There is no call for forced explanations as to how the door of the interatrial foramen is slammed shut and locked at the instant of birth; nor is there any necessity of regarding an uncomplicated defect in one of the partitions of the heart as an insurmountable obstacle to a fairly normal life. Open communication between the right and left sides of the heart after birth undeniably does reduce the efficiency of the cardiovascular mechanism; but the mechanism is flexible and has a large factor of safety. That it can and in many cases does function fairly successfully in spite of imperfect separation of pulmonary and systemic circuits is far easier to realize if the importance of separate blood streams is held in its proper perspective.

Literature Cited

BRUC-H, C. 1863 Uehcr den Schliessungsprocess des Foramcn ovale bei Menschen und Séiugethieren. Abhandlungen Senckenbergischen Naturf. Gesell— sclmft, Frankfurt a.M., Bd. 4, S. 46-62.

KELLOGG, 11. B. 1928 The course of the blood flow through the fetal mammalian Heart. Am. Jour. Anat., vol. 42, pp. 443-465.

NA:§'AGAs, J. C. 1921 On the patency of the foramen ovale in Filipino newborn children. Anat. Rec., vol. 21, pp. 339-352.

PATTEN, B. M. 1925 The interatrial septum of the chick heart. Anat. Rec., vol. 30, pp. 53-60.

Pohlman AG. The course of the blood through the heart of the fetal mammal, with a note on the reptilian and amphibian circulations. (1909) Anat. Rec. 3: 75-109.

PREYER, NV. 1885 Speoielle Physiologic dos Embryo. Leipzig, Th. Grieben.

R311), J. 1835a Injection of the vessels of the foetus to show some of the peculiarities of its circulation. Edin. Med. and Surg. Jour., vol. 43, pp. 11-13.

1835b Additional observations on the foetal (',iI‘(‘.ul211’iO11. Edin. Med. and Surg. Jour., vol. 43, pp. 3084310.

]?UI<:D1:\'G1~:1<. N. 1871 Ueber die Topographie der beiden Vorhiife und die Ein~ striimung des Blutes in dieselben bei dem Foetus. Jour. f. Kinder krankheiten, yd. 56, S. 402-407.

SABATIER, R. B. 1791 Traité complet d’n11aton1i(=, T. 2, p. 493. (Cited by Pohlman.)

VVOLFF, C. F. 1778 De foramine ()V:Ll1 ejusque in dirigendo sunguinis motu. Observ. Novas. Nov. Comment. Scient. Petropolit XX. (Cited by Ziegenspeck.)

ZIEGE_\'SPE(‘,K, R. 1882 Wc-lche Vefzindcrnngen erffiihrt die foetale Horzth£itig~ keit regelniiissig durcli die Geburt. Inaug. Diss. Jena. Drnck V011 Oetling.

1885 Uber don Blutkreislauf dos S£iugethiere— und Menschen-Fiitus. In I’reye1"s Physiol. dos Embryo, S. 596-607.
1902 Uober Foetal Kreislauf. Verlag Aertztlichen Rundschau. Munchen.

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