Nashville, TN

Definition: This is a very rare cardiovascular anomaly that occurs during intrauterine life and was first described in 1715 by Vieussens⁵ and again in 1875 ^[1] . It may occur at any moment in pregnancy, due to multiple causes (some unknown), with resulting arrhythmias, right heart failure and congestion, pericardial effusion, pleural effusion, ascites and/or nonimmune hydrops. If an accurate diagnosis is not made on time in the preterm or term fetus, or if the problem occurs in early pregnancy, intrauterine demise may occur ^{[2] , [3]} .

Case report:A 32-year-old woman, primigravida, in her third trimester pregnancy with an unremarkable history, who comes into our ultrasound department referred by her obstetrician because the fetus was not moving during the last 48 hours. At ultrasound the following findings were present: a 38 week pregnancy with a female fetus with normal growth curve, normal placenta and amniotic fluid index, rhythmic normal heart rate, discrete pericardial effusion, increased size of the right chambers with left bulging of the right atrial and ventricular septal walls, left bulging of the foramen ovale without an evident flap, absent forward doppler flow from the right to the left atrium and normal color doppler flow within the rest of heart.

The diagnosis of premature closure of the foramen ovale of unknown etiology was made. An induction of labor of this term pregnancy was planned and accomplished during the next few hours under strict fetal-maternal surveillance. The patient went through a normal labor and delivery. A follow up ultrasound scanning of the baby's heart was done one week later and a normal heart without pericardial effusion was found.

No more follow up was required from then on.

Synonyms: None.

Incidence: Unknown but very rare. Present at the autopsy in 60:10.000 of neonatal deaths⁵ and 90:10.000 of neonatal death with congenital heart disease. The isolated form is 10 times less common than the associated form⁵ .

Etiology: Several cardiac defects, mainly left hypoplastic heart and left obstructions, have been described as being potential causes/consequences of premature closure of the foramen ovale. While left hypoplastic heart is thought to be an early cause/consequence, obstructive processes are thought to be a late cause, with left side heart enlargement7 .  Aortic and mitral valve stenoses or atresias as well as parachute mitral valve and aortic coarctation, have been found by several authors as the leading cause of premature closure of the foramen ovale. In several unexplained and isolated cases other authors have hypothesized that this disorder may be caused by failure of development of the ostium secundum, excessive growth of the ostium secundum, endocarditis (such as those due to cytomegalovirus) or premature fusion of the ostium primum and the ostium secundum (due to an accelerated physiological process)^{1 ,2 ,3 , [4] ,5} . Very few cases have been found in association with transposition of the great arteries, Ebstein’s anomaly and anomalous pulmonary venous return^{8 ,9 , 12 ,14}.

Genetic anomalies: Unknown, but several cases has been described in females with gonadal dysgenesis³ .

Pathogenesis: When aortic or mitral valves are stenotic or atresic, or if there is an important aortic coarctation, a left heart overload causing increased left-sided pressure. This increased left atrial pressure enlarges the left cavities and press the septum secundum against the septum primum favoring the foramen ovale’s closure. If this happens, or if developmental disorders occur within the tissues of the septum primum and septum secundum, more of the right heart blood flow will be directed towards the pulmonary artery. The fetal pulmonary artery is not prepared for this event and an increase in the muscular layers of the main pulmonary vessels and arteriolar branches will eventually develop a pulmonary hypertension, which in turn produces retrograde right ventricular and atrial enlargement with left deviation of the septal walls. Cardiac failure will eventually overcome and may persist over the neonatal period if the fetus survives. This is due to the pulmonary hypertension. When the closure of the foramen ovale occurs very early in pregnancy a left hypoplastic heart will be the typical finding due to the decreased blood flow through the left heart ^{1 ,2 ,3 ,4 , [5] , [6]} .

Prenatal ultrasound diagnosis:  The appearance of the condition will depend on the time of onset. In early lesions enlarged heart with left bulging of the septal walls, discrete pericardial effusion, enlarged liver, decreased fetal movements with altered biophysical profile and thick interatrial septum without a foramen ovale flap can be seen. In late lesions skin edema, pericardial effusion, pleural effusion, ascites and hydrops, irregular heart rhythm with bradyarrhythmias or tachyarrhythmias and limited mitral or aortic valve movements are the mayor findings.^{1 ,2 ,4 ,5 ,7,8,9,10} According to the cause of the premature closure of the foramen ovale, other related findings such as those seen in aortic atresia with insufficiency of the mitral valve would be demonstrated by the application of color doppler mapping: absence of forward flow in the hypoplastic ascending aorta, reverse flow of blood from the ductus arteriosus into the severely hypoplastic aorta in the late systole, pansystolic mitral valve regurgitation, and absent flow across the foramen ovale as a result of the premature closure^11,12.

Differential diagnosis: All other causes of heart enlargement, pericardial effusion, ascites, pleural effusion, and hydrops should be considered.^{1 ,13,14,15,16,17,18,19}

Discussion: This particular case of isolated premature closure of the foramen ovale at term was probably due to a premature “physiologic” process (that to our belief ends up not being physiologic) in which the septum primum comes in apposition to the septum secundum and its foramen ovale, closing the communication between the foramen ovale and the ostium secundum (right atrium and left atrium). We assume, based on the ultrasonographic findings, that they corresponded to a recent event, which was seen as a mild pathologic process in the spectrum of findings normally encountered in these cases. Pericardial effusion, right heart enlargement with left bulging of the septal walls and absent foramen ovale’s flap with left bulging are well described ultrasonographic findings in late premature closures of the foramen ovale. It is well known that the foramen ovale is the shortcut through which the fetal heart provides oxygenated blood to preferential organs, mainly the brain and the heart itself. The decreased fetal movements also decrease oxygen consumption, which in turn prevents, at least temporarily, from fetal asphyxia and heart failure.

Reviewer: Ann Kavanaugh, MD

References

[1] Coulson CC, Kuller JA. Nonimmune hydrops fetalis secondary to premature closure of the foramen ovale. Am J Perinatol. 1994 Nov;11(6):439-40.

[2] Pesonen E, Haavisto H, Ammala P, Teramo K. Intrauterine hydrops caused by premature closure of the foramen ovale. Arch Dis Child. 1983 Dec;58(12):1015-6.

[3] Wigglesworth JS., Singer DB. Textbook of Fetal and Perinatal Pathology. Blackwell Scientific Publications. 1991

[4] Polin RA, Fox WW.  Fetal and Neonatal Phisiology. Saunders.  Philadelphia. 1992

[5] Pernot C, Marchal C, Ravault MC, Cloez JL, Lambert A. [Premature closure of the foramen ovale] Arch Fr Pediatr. 1979 Nov;36(9):949-58.

[6] Adams FH,Emmanouilides GC, Riemenschneider TA. Heart Disease in Infants, Children, and Adolescents. Fourth Ed. Williams & Willkins, Baltimore Maryland. 1989

7 Nowlen TT, Ayres NA, Kearney DL, Nihill MR, Grifka RG. Premature closure of the foramen ovale associated with aortic stenosis, left ventricular dilation with thrombus, and early mortality. Am J Cardiol. 2000 May 1;85(9):1159-61, A9.

8 Donofrio MT. Images in cardiovascular medicine. Premature closure of the foramen ovale andductus arteriosus in a fetus with transposition of the great arteries.Circulation. 2002 Mar 19;105(11):e65-6.

9 Berry LM, Padbury J, Novoa-Takara L, Emmanouilides GC. Premature "closing" of the foramen ovale in transposition of the great arteries with intact ventricular septum: rare cause of sudden neonatal death. Pediatr Cardiol. 1998 May-Jun;19(3):246-8.

10 Bharati S, Patel AG, Varga P, Husain AN, Lev M. In utero echocardiographic diagnosis of premature closure of the foramen ovale with mitral regurgitation and large left atrium. Am Heart J. 1991 Aug;122(2):597-600.

11 Gembruch U, Chatterjee M, Bald R, Eldering G, Gocke H, Urban AE, Hansmann M. Prenatal diagnosis of aortic atresia by colour Doppler flow mapping. Prenat Diagn. 1990 Apr;10(4):211-7.

12 Suzuki K, Doi S, Oku K, Murakami Y, Mori K, Mimori S, Ando M. Hypoplastic left heart syndrome with premature closure of foramen ovale: report of an unusual type of totally anomalous pulmonary venous return. Heart Vessels. 1990;5(2):117-9.

13 Harlass FE, Duff P, Brady K, Read J. Hydrops fetalis and premature closure of the ductus arteriosus: a review. Obstet Gynecol Surv. 1989 Jul;44(7):541-3. Review.

14 Arad P, Degani S. [Premature foramen ovale closure in newborn of a mother with Ebstein"s anomaly] Harefuah. 1988 Jun 15;114(12):589-92.

15 Moerman PL, Van Dijck H, Lauweryns JM, Eggermont E, Van der Hauwaert LG. Premature closure of the foramen ovale and congenital pulmonary cystic lymphangiectasis in aortic valve atresia or in severe aortic valve stenosis. Am J Cardiol. 1986 Mar 1;57(8):703-5.

16 Schall SA, Dalldorf FG. Premature closure of the foramen ovale and hypoplasia of the left heart. Int J Cardiol. 1984 Jan;5(1):103-7.

17 Pesonen E, Haavisto H, Ammala P, Teramo K. Intrauterine hydrops caused by premature closure of the foramen ovale. Arch Dis Child. 1983 Dec;58(12):1015-6.

18 Bhatt DR, Jue KL. Prenatal closure of the foramen ovale in complete transposition of great vessels. Observations in a case with intact ventricular septum and normally developed left heart chambers. Am J Cardiol. 1979 Sep;44(3):563-5.

19 Arger PH, Moranz J, Mennuti MT, Devenney JE. Premature closure of the foramen ovale as a cause of intrauterine fetal ascites. Rev Interam Radiol. 1979 Apr;4(2):93-4.