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Ann Thorac Surg 2002;74:58-62
© 2002 The Society of Thoracic Surgeons

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Original article: cardiovascular

Morphometric analysis of aortic media in patients with bicuspid and tricuspid aortic valve

^a Deutsches Herzzentrum Berlin, Berlin, Germany

Accepted for publication March 28, 2002.

* Address reprint requests to Dr Pasic, Deutsches Herzzentrum Berlin, Augustenburger Platz 1, Berlin D-13353, Germany
e-mail: pasic{at}dhzb.de

	Abstract

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Background. Patients with bicuspid aortic valves tend to develop dilatation of the ascending aorta. The aim of this study was to analyze whether or not there is any histologic difference in the aortic media of patients with a bicuspid aortic valve or a tricuspid aortic valve.

Methods. A morphometric analysis of the wall of the ascending aorta was performed in 107 patients with bicuspid aortic valves undergoing aortic valve operations. The thickness of the elastic lamellae of the aortic media and the distances between the elastic lamellae were measured with the use of an image analysis system. The histologic specimens of the ascending aorta from 61 surgical patients with tricuspid aortic valve disease served as a control.

Results. The patients with bicuspid aortic valves had thinner elastic lamellae of the aortic media (2.71 ± 0.23 µm) of the ascending aortic wall than the patients with tricuspid aortic valve disease (2.83 ± 0.23 µm) (p = 0.006). The patients with bicuspid aortic valves also had greater distances between the elastic lamellae (27.21 ± 8.69 µm) of the ascending aortic wall in comparison with the patients with tricuspid aortic valve disease (24.34 ± 5.32 µm) (p = 0.033). There was no difference in the total thickness of the aortic media between the groups (p = 0.62).

Conclusions. Patients with a bicuspid aortic valve had thinner elastic lamellae of the aortic media and greater distances between the elastic lamellae than patients with a tricuspid aortic valve.

	Introduction

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Bicuspid aortic valve is one of the most frequent congenital heart defects. Its prevalence in the general population is approximately 1% to 2% [1]. Bicuspid aortic valve also can occur in combination with other congenital heart defects [2]; individuals with these conditions tend to have aortic valve stenosis or regurgitation, or both, develop early in life [3]. A bicuspid aortic valve (even when it is functioning normally) is frequently associated with an enlargement of the ascending aorta. This aortic wall dilatation is typically located on the convexity of the ascending aorta, although diffuse aortic enlargement also can occur. The presence of a bicuspid aortic valve carries a risk of severe complications such as aortic rupture or dissection [4, 5]. It is unknown whether this abnormality is caused by altered hemodynamic stress or by a developmental defect. There are only few histologic data from patients with bicuspid aortic valve, and these are predominantly from patients with aortic dissection already present [5–9]. In some studies the number of patients included was very small [10].

The aim of our study was to analyze the morphometric features of the aortic wall in patients with bicuspid and tricuspid aortic valves undergoing open heart operations.

	Material and methods

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Study group
We investigated aortic wall segments of the ascending aorta of 107 patients with bicuspid aortic valves who were undergoing aortic valve operations. There were 31 females and 76 males with a mean age of 60.9 ± 12.8 years. Only patients with a clearly congenital bicuspid valve as assessed by both intraoperative anatomical examination and patient history were included. The patients whose aortic valves became functionally bicuspid during their lifetime were not included in this group. Patients with tricuspid aortic valve disease combined with a connective tissue disorder also were not considered for this group. The main indications for valve operation were aortic valve stenosis in 50 patients (47%), regurgitation in 28 (26%), and combined aortic valve disease in 25 (23%).

Control group
The aortic wall segments of the ascending aorta of 61 surgical patients with tricuspid aortic valve disease (24 females, 37 males; mean age 59.5 ± 14.3 years) served as the control group. Patients with tricuspid aortic valve disease combined with a connective tissue disorder were not considered for this group. The main indications for valve operation were aortic valve stenosis in 35 patients (57%), regurgitation in 18 (29.5%), and combined aortic valve disease in 8 (13%).

There were no statistically significant differences between the mean ages of the study patients and the control group (p = 0.141).

Preoperative and intraoperative examinations and aortic wall excision
The diagnosis of a bicuspid or tricuspid aortic valve was established by echocardiography and angiography and was confirmed intraoperatively. The surgical protocol consisted of aorta-atrial cannulation for extracorporeal circulation and the use of cold crystalloid cardioplegic solution and moderate hypothermia of 30°C. The aortic cannula was placed in the proximal transverse aortic arch. The aorta was opened with an incision directed along the anterior aortic aspect into the noncoronary sinus of Valsalva. The aortic wall specimen taken at this time point was removed. At least a 3 mm x 8 mm piece of the aortic wall was excised from the incision at the convexity of the ascending aorta 2 to 4 cm above the level of the aortic valve annulus. The excised parts of the aortic wall were fixed in 10% formalin in buffered saline and then transferred for further processing and histologic examinations. If the aortic diameter was enlarged, the reduction aortoplasty to normal diameter was performed by removal of an elliptical portion of aortic wall along the aortotomy incision [11]

According to the diameter of the ascending aorta the patients with bicuspid and tricuspid aortic valve were divided into three subgroups: (1) patients without dilatation of the ascending aorta (diameter less than 38 mm), (2) patients with moderate dilatation of the ascending aorta (diameter between 39 and 49 mm), or (3) patients with severe dilatation of the ascending aorta (diameter 50 mm and more).

A normal ascending aorta without dilatation (diameter less than 38 mm) was found in 34 patients with bicuspid aortic valves and 29 patients with tricuspid aortic valves. A moderate dilatation of the ascending aorta (diameter between 39 and 49 mm) was found in 43 patients with bicuspid aortic valves and 20 patients with tricuspid aortic valves. A severe dilatation of the ascending aorta (diameter of the ascending aorta equal to 50 mm and more) was found in 30 patients with bicuspid aortic valves and 12 patients with tricuspid aortic valves.

Histologic examinations
We measured the total thickness of the aortic media, the thickness of the elastic lamellae of the aortic media, and the distances between the elastic lamellae. After histologic preparation of the specimen, morphometric measurements were done using an automatic microscope image analysis system (KS 400, release 3.2, Vision; Carl Zeiss, Jena, Germany). The histologic specimens were prepared with elastica van Gieson’s stain (Fig 1a). The elastic lamellae of the aortic media was color-marked (Fig 1b) and selected (Fig 1c) by removing the thin supporting membranes. Then measurements of the thickness of elastic lamellae of the aortic media and the distances between the elastic lamellae were performed at multiple measuring points (about 200 measuring points) at 73 sites for each specimen (Fig 1d). The multiple values were recorded as one single average value for each patient.

View larger version (117K): [in this window] [in a new window]   Fig 1. Preparation process for measurements with the microscope picture analyzing system. The histologic specimens were prepared with elastica van Gieson’s stain (a). Then the elastic lamellae of the aortic media were color-marked (b) and selected (c) by removing the thin supporting membranes. The fine white lines were then set in the field for measurements (d). The measurements included the thickness of the elastic lamellae and the distances between the lamellae. The arrows indicate two elastic lamellae and the distance between them that was measured.

Statistics
The student’s t test was used for statistical analysis. A p value of less than 0.05 was considered significant.

	Results

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
Differences between the groups
Thicknesses of aortic media
There was no difference (p = 0.62) in the total thickness of the aortic media between the patients with bicuspid and tricuspid valves (Fig 2).

View larger version (10K): [in this window] [in a new window]   Fig 2. Thickness of the aortic media (mm) (± 95% confidence interval) in patients with bicuspid and tricuspid aortic valves.

View larger version (10K): [in this window] [in a new window]   Fig 3. Thickness (± 2 standard error) of the elastic lamellae (µm) of the aortic media in patients with bicuspid and tricuspid aortic valves. Patients with a bicuspid aortic valve had significantly thinner elastic lamellae of the aortic media than patients with a tricuspid aortic valve.

View larger version (10K): [in this window] [in a new window]   Fig 4. Distances (± 2 standard errors) between the elastic lamellae (µm) of the aortic media in patients with bicuspid and tricuspid aortic valves. The distances between the elastic lamellae of the aortic media of the ascending aortic wall were significantly greater in patients with bicuspid aortic valves than in patients with tricuspid aortic valve disease.

View larger version (19K): [in this window] [in a new window]   Fig 5. Thickness (± 2 standard error) of the elastic lamellae (µm) of the aortic media in patients with bicuspid and tricuspid aortic valves according to the ascending aortic diameter.

View larger version (24K): [in this window] [in a new window]   Fig 6. Distances (± 2 standard error) of the elastic lamellae (µm) of the aortic media in patients with bicuspid and tricuspid aortic valves according to the ascending aorta diameter.

	Comment

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
Our study showed differences in histologic findings of the ascending aortic wall between the patients with bicuspid and tricuspid aortic valves. Although there was no difference in the total thickness of the aortic media between the groups, patients with a bicuspid aortic valve had thinner elastic lamellae of the aortic media and greater distances between the elastic lamellae than patients with a tricuspid aortic valve. The second main finding of our study was an increase of the distances between elastic lamellae in correlation with increasing diameter of the ascending aorta in patients with both bicuspid and tricuspid aortic valves.

There has been controversial discussion concerning whether aortic wall alterations in patients with bicuspid aortic valves are caused by a congenital wall defect of the aorta [3, 12–15] or whether the alterations are due to the abnormal hemodynamic stresses on the aortic wall caused by valve malformation [6, 16, 17]. As early as 1928, Abbott [18] theorized that bicuspid aortic valve, coarctation of the aorta, and aortic wall thinning and rupture were related to a common developmental abnormality. Schievink and Mokri [19] assumed a connection between a bicuspid aortic valve and aorto-arterial abnormalities, because the semilunar valves and the medial layer of the aortic arch and its branches are embryologically derived from the cells of the neural crest. Therefore, bicuspid aortic valves are considered part of a common developmental defect that also causes coarctation and aortic wall abnormalities. On the other hand, it is presumed that if the pressure gradient across the aortic valve is significantly high, which is frequently observed in patients with bicuspid aortic valves, the resulting hemodynamic stress also may play an important role in bringing about the changes that we saw in the aortic wall.

Systematic histologic examinations of the aortic wall from patients with bicuspid aortic valve do not exist. With the recently available microscope picture analyzing system it was possible to make systematic measurements of the thickness of and distances between the elastic lamellae of the aortic media from the ascending aorta segments. Parai and colleagues [10], who used morphometry to analyze the proportional target area for elastic tissue in Movat stained histologic slides, also showed a significantly smaller area of elastic lamellae per microscopic field in patients with bicuspid aortic valves than in patients with tricuspid aortic valve disease. However, most of the reports are from patients in whom an aortic dissection had already occurred [5, 7–9] or the patient numbers were very small [10].

The results of our study cannot resolve the question of whether this abnormality is caused by altered hemodynamic stress or by a developmental defect. Further hemodynamic studies in combination with investigations that analyze the ultrastructure of the elastic lamellae of the aortic media and the other constituents of the aortic wall are necessary in patients with a bicuspid aortic valve to elucidate the specific underlying defect.

	Acknowledgments

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
We thank Ms Anne Gale for her editorial assistance and Ms Julia Stein for the statistical calculations.

	References

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 

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