Mixed partial anomalous pulmonary venous drainage coexistent with an aortic valve abnormality - analysis of ultrasound diagnostics in a 10-year-old girl with Turner syndrome.

The authors present a case of echocardiographic diagnosis of a rare congenital cardiovascular anomaly in the form of mixed partial anomalous pulmonary veins connection in a 10-year-old girl with Turner syndrome and congenital mild stenosis of insufficient bicuspid aortic valve, made while diagnosing the causes of intestinal tract bleeding. The article presents various diagnostic difficulties leading to the delayed determination of a correct diagnosis, resulting from the absence of symptoms of circulatory failure in the early stage of the disease and the occurrence of severe and dominant auscultatory phenomena typical for congenital aortic valve defect which effectively masked the syndromes of increased pulmonary flow. The authors discuss the role of the impact of phenotypic characteristics of the Turner syndrome, in particular a short webbed neck restricting the suprasternal echocardiographic access and the presence of psychological factors associated with a long-term illness. The importance of indirect echocardiographic symptoms suggesting partial anomalous pulmonary veins connection in the presence of bicuspid aortic valve, e.g. enlargement of the right atrium and right ventricle, and paradoxical interventricular septum motion were emphasized in patients lacking ASD, pulmonary hypertension or tricupid and pulmonary valve abnormalities. The methodology of echocardiographic examination enabling direct visualization of the abnormal vascular structures was presented. Special attention was paid to the significance of highly sensitive echocardiographic projections: high right and left parasternal views in sagittal and transverse planes with patient lying on the side, with the use of two-dimensional imaging and color Doppler. Finally, the limitations of echocardiography resulting from the visualization and tracking of abnormal vascular structures hidden behind ultrasound non-conductive tissues were indicated, as was the role of other diagnostic modalities, such as angio-CT and/or nuclear magnetic resonance.

Introduction

Partial anomalous pulmonary venous drainage (PAPVD) is a developmental anomaly of the cardiovascular system, the cause of which can be sought both in the abnormal gene structure, as well as in environmental factors. The essence of the defect seems to be the persistence of the early-stage embryo connections between the systemic venous circulation (major celiac venous plexus) and pulmonary circulation( in the absence of a proper connection between the pulmonary veins and the left atrium of the heart, probably as a result of abnormal growth process of mesenchymal tissue located behind the heart (dorsal mesocardial protrusion, DMP), in the area of so-called second heart field (rear field) toward the venous/alluvial pole of the heart(. The lack of blood inflow from one or more pulmonary veins into the short, single common pulmonary vein which leads blood to the left atrium is visible at approximately the 8th week of the embr yo's age; this results in excessive angiogenesis of the celiac plexus and the emergence of their numerous connections with the cardinal venous system and lung parenchyma(. As a result, during the diagnosis of PAPVD a correct connection of two or three pulmonary veins with the left atrium is found, while the other pulmonary veins lack internal lumen (no lumenization) or undergo atresia(. The part of pulmonary parenchyma affected by the vascular anomaly drains venous blood to the venous system drainage area via the system of main and vertical veins or through the coronary sinus. The aim of this paper is to trace the applied strategy and diagnostic test technique on the example of a patient with Turner syndrome, concomitant aortic valve anomaly and a very rare form of mixed partial abnormal pulmonary venous connection.

Case report

A 10-year-old girl with Turner syndrome, remaining under observation since infancy due to moderate insufficiency and mild stenosis of bicuspid aortic valve, was admitted to the Clinic of Gastroenterology owing to recurrent gastrointestinal bleeding, and then referred to a follow-up echocardiography examination to the echocardiographic laboratory at the Department of Children's Cardiac Surgery of the Medical University of Warsaw before a scheduled colonoscopy under general anesthesia.

Transthoracic echocardiography confirmed the aortic pathology described above and it was stated at the same time that the size of the cavities of the left atrium and the left ventricle as well as the thickness and contractility of the left ventricular free wall were within the normal range appropriate for the child's age. However, what attracted the examiner's (WM) attention was paradoxical motion of the interventricular septum and enlargement of the right ventricle. It's diameter measured in LV long axis view exceeded upper normal limits; the dimensions of the right atrium and the pulmonary trunk were also borderline, what prompted the examiner to attempt to identify the cause of this condition (fig. 1).

Fig. 1

Presentation M reveals the enlargement of the right ventricle (RV) and an abnormal motion of the ventricular septum (↑↑) – a phenomenon that indicated the possibility of a low-pressure systemic-pulmonary shunt despite the absence of the atrial septal defect. Additional marking: LV – left ventricle

Right ventricular enlargement accompanied by paradoxical motion of the inter ventricular septum is characteristic feature of the right ventricular volume and/or pressure overload but not the left ventricular one in the course of aortic defect. Today, in spite of the widespread echocardiography, the detection of right heart enlargement caused by atrial septal defects and/or partially abnor mal pulmonary venous drainage still may be delayed. Less common reasons include: hemodynamically significant tricuspid and/or pulmonary valve insufficiency (e.g., in milder forms of Ebstein's anomaly), pulmonary hypertension, etc.

Structural abnormalities of the right heart valves and the presence of atrial septal defects were excluded in the described case, including those located marginally (e.g. of sinus venosus type). Also no echocardiographic features of pulmonary hypertension were found (low tricuspid and pulmonary valve regurgitant flow velocities). The image analysis of a part of the atrial septum located in the vicinity of the mouth of the superior vena cava (normal, without a sinus venosus defect) revealed a widening of the paracardiac section of the vein and clearly turbulent flow of blood into the right atrium. No entry of the right upper pulmonary vein into the left atrium was visualized, but lower right and both left pulmonary veins joining the left atrium were shown (fig. 2). In a two-dimensional presentation the diameters of the left pulmonary veins were smaller than that of the right lower pulmonary vein. Lower saturation of the color inflow from these veins was noted. Precise visualization of pulmonary and systemic veins was hampered by adverse anatomical conditions in a child with Turner syndrome (short neck restricting suprasternal access, inspiratory position of the thorax, abdominal discomfort) who reluctantly engaged in the examination.

Fig. 2

Suprasternal transverse projection. Visible left atrium (LA) and three tributaries of the pulmonary veins: lower right vein (3) and two left veins (1, 2). The bloodstream flowing into the left atrium from the left upper pulmonary vein (1) is clearly narrower than the others. Additional markings: Ao – ascending aorta, SVC – superior vena cava

Satisfactory visualization of the superior vena cava was achieved by using right parasternal projections with the patient positioned laterally on the right side, especially during maximal exhalation. About 3 cm above the right atrium a rather wide, horizontally extending vein was revealed in the transverse plane. It emerged from the lung tissue and ran to the superior vena cava which expanded visibly at that level. Located in its close proximity was the opening of the azygos vein which ran in the sagittal plane (figs. 3–5). The examining physician's attention was drawn to the image of the left brachiocephalic vein, also enlarged and showing increased flow. During the search for the cause with the use of high left parasternal projections with the patient positioned laterally on the left side, a vertical vein of ca. 8 mm diameter and with a turbulent flow, running from the bottom to the left brachiocephalic vein was observed. The initial segment of the vessel not revealed due to being obstructed by pulmonary tissue (figs. 6, 7).

Fig. 3

High right transverse parasternal projection. Visible opening of a wide vein (RUPV) running to the enlarged superior vena cava (SVC) over the branch of the right pulmonary artery (RPA). Its horizontal course indicates the pulmonary origin of the vessel. Additional markings: AoAsc – ascending aorta, RBV – right brachiocephalic vein

Fig. 5

High right longitudinal parasternal projection. Superior vena cava visualized in the long axis. At a distance of about 3 cm from the exit to the right atrium (RA) superior vena cava (SVC) is significantly widened (#), and the section in the immediate vicinity of the exit to the right atrium has a normal diameter. Additional markings: LA – left atrium, RPA – right pulmonary artery

Fig. 6

High left parasternal projection. Blue color is used to mark the flow in the descending aorta (AoD), red color to mark the upward movement in the vein located leftward from the aorta which drains into the left venous angle (V). Additional markings: LB – left brachiocephalic vein

Fig. 7

A slight deviation of the transducer to the left reveals a more peripheral section of the vertical vein (V) which runs from the depths of the lung tissue, above the left pulmonary artery (LPA). Additional marking: LA – left atrium

Color Doppler facilitates the visualization of an abnormal, horizontally oriented (in the transverse plane) superior vena cava (SVC) tributary. Markings: RUPV – right upper pulmonary vein, RPA – right pulmonary artery, AoAsc – ascending aorta

The presumptive diagnosis of a rare variety of mixed partial abnormal pulmonary venous drainage was made: the right upper pulmonary vein into the superior vena cava, and the left upper pulmonary vein (LUPV) through persistent vertical vein to the left brachiocephalic vein. The right sided anomalies did not raise any doubts. However, what remained vague were anatomical details of left pulmonary veins, as in the first phase of the examination the opening of two veins to the left atrium was revealed, which suggested that the image of the left pulmonary veins was correct. The fact that the additional venous channel on the left side could be explained by an unusual drainage from the left lung (a greater number of pulmonary veins from which the upper ones exit incorrectly), the presence of an abnormally running and larger than usual systemic vein (for example, accessory azygos vein, top left intercostal vein) or the existence of a connection between the venous and pulmonary venous systems (levoatrial cardinal vein or venous vessel connecting LUPV with the left brachiocephalic vein). It was essential to dispel the doubts in order to determine further course of procedure, and, above all, to schedule surgical correction.

Partial anomalous pulmonary venous drainage, comprising a relatively small part of the lung parenchyma (usually one incorrectly connecting vein or a larger number of small veins) does not cause significant hemodynamic consequences that require surgery. In case of anomalous drainage from more extensive areas, the shunt becomes hemodynamically significant and requires a corrective surgery. Due to the abnormal function of the aortic valve it was impossible to carry out echocardiographic calculation of Qp:Qs flow ratio which is important in making indications for cardiac surgery. It should be emphasized that the implications of right ventricular volume overload may be partially masked by aortic regurgitation, resulting in an additional volume burden on the left ventricle. Thus, the severity of kinetic disorders of the interventricular septum could not be a sufficient indicator of the size of the leak.

Minimally invasive computed tomography angiography (angio-CT) and magnetic resonance (MR) of the cardiovascular system are free from the constraints associated with the presence of aerated lung tissue and bone structures reflecting ultrasound. Moreover, they allow precise three-dimensional reconstruction of the heart and vascular structures, and the calculation of the mutual relationship of pulmonary and systemic flows(.

In the described case, the angio-CT examination (figs. 8, 9) confirmed the abnormal connection of the right upper pulmonary vein to the superior vena cava. It also resolved the doubts concerning the anatomy of the left pulmonary veins(fig. 10). It turned out that the venous drainage from the left lung occurred through three veins: the bottom and middle ones running correctly into the left atrium while the upper, considerably smaller than the others, drained via a vertical vein into the left venous angle. It is worth noting that the review of the chest X-ray taken for the purpose of correct determination of the area to be examined, revealed both abnormal vascularity of the right lung, which suggested that the right upper pulmonary vein was connected to the superior vena cava. It also revealed a shade corresponding to the vertically extending vein that connected to the left brachiocephalic vein.

Fig. 8

3D reconstruction of CT angiography. Front view. The left upper pulmonary vein drains via the vertical vein (3) to the enlarged brachiocephalic vein (1). Highly situated right upper pulmonary vein (4) returns the blood to the wide superior vena cava (2). Other markings: Ao – a scending aorta

Fig. 9

3D reconstruction of CT angiography. Rear view showing the enlarged superior vena cava (1) with the exit to the right upper pulmonary vein (2). Three pulmonary veins connect with the left atrium: one on the left side (3) and two right ones (4, 5). The upper left pulmonary vein drains via the vertical vein (8) to the brachiocephalic vein. Additional markings: 7 – ascending aorta, 6 – right pulmonary artery

Fig. 10

A simplified diagram of the pulmonary veins anatomy (author: MAK). Markings: LA – left atrium, RA – right atrium, RIPV – right inferior pulmonary vein, RUPV – right upper pulmonary vein, LAPV – left additional pulmonary vein, V – vertical vein, VBC – brachiocephalic vein, SVC – superior vena cava upper, LUPV – left upper pulmonary vein, LIPV – left inferior pulmonary vein

It was estimated that the small size of the abnormally connecting left pulmonary vein classified the systemic-pulmonary shunt as hemodynamically insignificant and justified the adoption of the watchful waiting approach. Important arguments for relinquishing the surgery included also the awareness of major technical difficulties that would occur in any attempt to correct the defect, as well as a possibility of the deterioration of the aortic valve function in the future. A potential necessity for surgical treatment of the valve would be associated with reopening the chest in the future if the patient was operated on at present. In the absence of significant symptoms that could be attributed to abnormal drainage of pulmonary veins, the child was stated eligible for further observation.

Discussion

Partial anomalous pulmonary venous drainage is among rare congenital anomalies found in 0.2–0.7% of autopsy studies(. It affects the right lung (85–88%) rather than the left one (9–10%), and occasionally affects both lungs (2–2.5%). In the majority of cases the defect is accompanied by a sinus venosus defect of the septum (60–65%) or ASD2/ PFO (20%)(. 15–20% of patients show no evidence of interseptal communication. PAPVD is diagnosed in up to 13% of patients with Turner syndrome – most commonly it takes a mixed form without the atrial septal defect(.

The presented case is another( good example of many difficulties which may arise both in diagnostics and the management of patients diagnosed with pulmonary venous anomalies. In a situation where a relatively small part of the pulmonary connection drains abnormally, the circulatory symptoms are not intensified and therefore are hard to detect in a clinical examination. Typical auscultatory phenomena, such as overactive, deformed precordium, ejection murmur above the pulmonary artery, rigid split of the second heart sound above the pulmonary artery, are present only in case of the large shunt. In the examined patient the ejection murmur was diagnosed at the base of the heart and it was preceded by a protosystolic click and quiet diastolic murmur radiating towards the apex. The presence of these symptoms has been explained so far with the bicuspid aortic valve, diagnosed by echocardiography already in early childhood. Abnormalities revealed in the chest X-ray and electrocardiogram, which are associated with the right ventricular volume overload and increased pulmonary blood flow, also depend on the severity of the shunt and thus are not perceptible in benign forms. No information on a conducted radiological examination of the chest or electrocardiogram was found during the analysis of medical records.

Transthoracic echocardiography is a primary diagnostic method of structural heart defects, but the diagnosis of pulmonary vein anomalies in a young, uncooperative, often crying and agitated child is very difficult. The main obstacle is the presence of exceedingly aerated lung tissue, usually making it impossible to trace the superior vena cava throughout its entire course and impeding the visibility of the entries of the pulmonary veins into the left atrium. Moreover, in a child with Turner syndrome and a short, webbed neck, there is limited suprasternal access which normally enables a good insight into the vascular structures of the upper mediastinum. What is very useful in the assessment of the atrial septum, the superior vena cava and right pulmonary vein is the right parasternal access with the patient positioned on the right side and exhaling deeply, but such conditions can be obtained only in older patients, able to follow commands and accepting the inconvenience of the long duration of the examination. In the described case, it was difficult to establish the optimal cooperation with the suffering (because of abdominal pain) child, tired with successive burdensome examinations.

In most cases the abnormal flow of right upper pulmonary vein coexists with sinus venosus atrial septal defect. An isolated connection of the upper right pulmonary vein to the superior vena cava occurs much more rarely.

In the absence of significant features of right ventricular volume overload, a visualization of the normal morphology of the atrial septum and particularly its upper part may encourage the abandonment of direct visualization of the course and connection of each pulmonary vein. In the described case, an additional diagnostic trap was the presence of two left pulmonary veins running into the left atrium. Coming across such an image is usually an indication to identify a correct drainage of left pulmonary veins. This observation of a vertical venous channel directly adjacent to the left lung and running into the left venous angle usually requires an extremely careful analysis of the images obtained from the zygomatic indentation and/or high left parasternal accesses. In the described case, because of the patient's neck anatomy and her negative attitude towards the examination, the suprasternal access was greatly limited, which significantly reduced the chance to visualize abnormal veins.

A not her factor which may influence the delay in the PAPVD diagnosis is a gradual, slow build-up of the right ventricle volume overload symptoms. The authors did not have descriptions or pictorial documentation of the previously performed echocardiograms. The medical history revealed that no size abnormalities of the right atrium, right ventricle or pulmonary artery had been reported to date, and there were also no anomalies of the ventricular septum kinetics. It is highly probable that in the earlier period the severity of overload irregularities was much smaller, so they were not perceptible in echocardiography. It is worth noting that it was the finding of the features of anatomically unexplained volume overload of the pulmonary circulation that became the reason for a more indepth image analysis which determined the cause of this condition.

Finally, it should be noted that the correct interpretation of the echocardiographic image could be hindered by the examiner's focus on the previously identified irregularities associated with the bicuspid, non-closing aortic valve. Some features of this anomaly, such as the left ventricular volume overload associated with aortic regurgitation, which can prevent the paradoxical motion of the ventricular septum, and the widening of the ascending aorta, causing the displacement of the superior vena cava, could have a masking effect on the PAPVD symptoms.

In conclusion, the authors would like to emphasize that the currently widely available ultrasound diagnostics combined with the examining physician's thoroughness may be considered a valuable tool for the initial detection of systemic and pulmonary venous anomalies in the mediastinal area in children.