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(Chest. 2003;123:1379-1385.)
© 2003 American College of Chest Physicians

Clinicopathologic Study and DNA Analysis of 37 Cardiac Myxomas*

A 28-Year Experience

Elvira Acebo, MD; J. Fernando Val-Bernal, MD, PhD; J. Javier Gómez-Román, MD and J. Manuel Revuelta, MD

* From the Department of Anatomical Pathology (Drs. Acebo, Val-Bernal, and Gómez-Román) and the Service of Cardiovascular Surgery (Dr. Revuelta), Marqués de Valdecilla University Hospital, Medical Faculty, University of Cantabria, Santander, Spain.

Correspondence to: J. Fernando Val-Bernal, MD, PhD, Departamento de Anatomía Patológica, Hospital Universitario Marqués de Valdecilla, Avda Valdecilla 1, E-39008 Santander, Spain; e-mail: apavbj{at}humv.es


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Conclusions
 References
 
Purpose: This study was performed to identify morphologic features of cardiac myxomas related to embolism and to provide a better understanding of the biology of these tumors, mainly in relation to their interleukin (IL)-6 expression and DNA content.

Patients and methods: A total of 37 cardiac myxomas were reviewed retrospectively in a clinicopathologic study that included the correlation of echocardiographic and pathologic findings in 25 cases, together with immunohistochemical evaluation of IL-6 expression and flow cytometric DNA analysis of 35 tumors.

Results: There were 24 female patients and 13 male patients. The mean (± SD) age was 52 ± 15 years. Fifty-four percent of patients presented with dyspnea, 51% presented with increased erythrocyte sedimentation rate (ESR), and 27% presented with embolic episodes, which were significantly associated with villous surface tumors. Atrial fibrillation was registered in 19% of patients and was significantly associated with large left atrial myxomas. Echocardiography proved to be a reliable method for preoperative diagnosis and for predicting tumor size and morphology. There was no perioperative mortality or long-term recurrences. The frequency of early surgical complications was associated with a longer mean ischemic time. Seventeen percent of tumors had abnormal DNA content, and 74% of tumors showed immunohistochemical expression of IL-6. Neither of these factors showed a significant association with embolism or constitutional illness.

Conclusions: Villous surface myxomas are related to embolism, and large left atrial tumors are related to atrial fibrillation. Echocardiography is a reliable method with which to predict tumor size and morphology. Myxoma cells usually express IL-6, and some tumors have abnormal cellular DNA content. Surgical excision of the tumor is a safe and effective treatment.

Key Words: cardiac myxoma • clinical characteristics • flow cytometry • histopathologic finding • immunohistochemistry • interleukin-6


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Conclusions
 References
 
Cardiac myxomas are the most common primary heart neoplasms and account for approximately 75 to 80% of cardiac tumors in surgical series.1 Their clinical features have been widely studied and are well-recognized. Most patients present with one or more of the triad of embolism, intracardiac obstruction, and constitutional symptoms, which have been correlated with increased plasma levels of interleukin (IL)-6.2 3 Nevertheless, a small number of clinicopathologic studies have been reported,4 5 6 7 and most of them have focused on gross tumor appearance and have disregarded echocardiographic features.

This kind of tumor is regarded as a benign neoplasm but can be lethal because of embolic complications or atrioventricular obstruction. Its neoplastic nature is supported by reports of chromosomal abnormalities8 and by the abnormal DNA content demonstrated in three flow cytometry studies.9 10 11 It also has been suggested that an aneuploid DNA content or a high proliferative cell cycle fraction (PF) could be associated with an aggressive biological behavior,9 but this has not been supported by other authors.11

The present article reports our clinical and surgical experience with the cardiac myxomas that have been diagnosed at our institution over a period of 28 years. This includes pathologic and echocardiographic findings, and their relationship to different clinical features. Also described are an immunohistochemical study with antihuman IL-6 and a flow cytometry analysis to determine the DNA content of the tumors. To the best of our knowledge, this is the largest series that has been studied for the last two purposes.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Conclusions
 References
 
A retrospective review of the archival material at our institution revealed 37 cases of cardiac myxomas between January 1973 and June 2000. The medical charts, surgical pathology reports, and microscopic slides were available in all cases. The clinical charts provided data related to age, sex, presenting symptoms, echocardiographic characteristics, and surgical procedures. Chest auscultatory data were available for 34 patients, chest roentgenogram findings were available for 27 patients, and ECG records were available for 36 patients. Follow-up data were collected from the clinical records and by a standardized telephone interview.

Tumor size and morphologic features were retrieved from the surgical pathology reports. All sections stained with hematoxylin-eosin were examined, and the presence of fibrosis, calcification, Gamna-Gandy bodies (ie, calciferruginous deposits), and ossification was assessed. Mitotic activity was evaluated by examining 50 random high-power fields (ie, original x400).

The clinical and pathologic features of cardiac myxomas were analyzed statistically in order to identify morphologic aspects related to embolism, atrial fibrillation, and patient age at diagnosis. Echocardiographic features (ie, size and morphology) also were compared with the same pathologic findings.

Paraffin blocks were available in 35 cases. We performed an immunohistochemical study with antihuman IL-6. Briefly, 5-µm sections were stained (EnVision+ method; Dako; Glostrup, Denmark; and TechMate 500 automated immunostainer; BioTek; Santa Barbara, CA). The primary antibody was (monoclonal) antihuman IL-6 (Genzyme; Cambridge, MA [1:100]). To evaluate the antibody specificity and sensitivity, positive and negative tissues were used as controls.

Flow cytometry was performed in the same 35 cases to determine the DNA content of the cardiac myxomas. Paraffin-embedded tissue was processed by the Hedley method12 and was analyzed in a flow cytometer (FACScan; Becton Dickinson; Sunnyvale, CA), and a histogram analysis was performed (Modfit LT, version 2.0.2 for Macintosh; Becton Dickinson). Guidelines for the implementation of clinical DNA cytometry were followed for the analysis.13 The PF (ie, the percentage of cells in G2 + M cell cycle phase) also was calculated.

Statistical comparisons were made using the Fisher exact test, Student t test for unpaired data, and the Pearson correlation.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Conclusions
 References
 
Clinical Findings
A total of 37 patients (24 women and 13 men) underwent evaluation and surgical treatment for atrial myxomas over the 27-year period. Patient age at diagnosis ranged from 12 to 73 years (mean [± SD] age, 52 ± 15 years). Except for one familial myxoma, all cases were sporadic myxomas. All the tumors were solitary and involved the atrial cavities. There were 30 left atrial myxomas (81%), 6 right atrial myxomas (16%), and 1 biatrial myxoma (3%). Most myxomas (70%) were attached to the atrial septum near the fossa ovalis.

The clinical presentation is summarized in Table 1 . Five patients (13%) were asymptomatic. In these cases, the myxoma was an incidental finding during echocardiography that had been performed for other reasons. Dyspnea was the most frequent symptom at diagnosis (54%). Arterial embolization occurred in 10 patients (27%). Eight patients had symptoms related to cerebral emboli, three patients had symptoms of acute arterial ischemia of the limbs, and one patient presented with a pulmonary embolus. Symptoms had been present for an average of 14 ± 14 months (range, 12 days to 72 months). Rare findings included polycythemia in one patient with a right atrial myxoma and systemic vasculitis in the patient with the biatrial myxoma. Both of these abnormalities disappeared after surgical excision of the cardiac tumors.


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  		Table 1. Clinical Presentation

 
Of the 34 patients whose auscultatory data were available, 29 (85%) had abnormal findings. The most common alteration was a systolic murmur (17 patients [50%]), followed by a loud first sound (11 patients [32%]), an opening snap (9 patients [26%]), and a diastolic murmur (5 patients [15%]). Sixteen of the 27 available chest roentgenograms (59%) showed abnormalities. These included pulmonary vascular congestion in 10 patients (37%), cardiomegaly in 7 patients (26%), and specific chamber enlargement in 6 patients (22%). Abnormal ECG reports were found in 20 of 36 patients (56%). Sinus rhythm was registered in 27 patients (75%), atrial fibrillation in 7 patients (19%), supraventricular tachycardia in 1 patient (3%), and sinus arrhythmia in 1 patient (3%). Signs of atrial hypertrophy were present in 13 patients (36%).

Preoperative diagnosis was achieved in all patients by transthoracic echocardiography (two-dimensional,34 patients; and M-mode, 3 patients). There were no false-positive diagnoses. In two cases, the diagnosis of cardiac myxoma was suggested after histopathologic examination of the tumor emboli.

Myxoma excisions were performed under cardiopulmonary bypass (CPB) in all cases. The mean CPB time was 56 ± 25 min (range, 23 to 139 min), and the mean ischemic time was 36 ± 17 min (range, 8 to 85 min). Tumors were excised with underlying endocardial tissue in 33 cases, and without it in 4 cases. In these cases, the tumor was shaved off the atrium. The surgical approach was by left atrial incisions, with the exception of four right atrial myxomas in which a right atrial approach was used. The biatrial myxoma was resected by biatriotomy. Two patients underwent concomitant surgery (aortic valve replacement, one patient; mitral valve repair, one patient).

There was no perioperative mortality. Fourteen of the 37 patients (38%) had early complications. Arrhythmias were the most common complication, occurring in six patients (16%; atrial fibrillation, three patients; flutter 2:1, two patients; and complete heart block requiring pacemaker insertion, one patient). Thromboembolic episodes were also frequent and affected four patients (10%; embolus to the right arteria cerebri media, one patient; embolus to the right arteria poplitea, one patient; pulmonary thromboembolism, one patient; and right upper limb thrombophlebitis episode, one patient). Other complications included constrictive pericarditis (one patient), postpericardiectomy syndrome (one patient), aortic valve insufficiency (one patient), and tricuspid valve insufficiency (one patient), which later required valve replacement. Patients with these complications had been exposed to a longer ischemic time (42 ± 19 vs 31 ± 15 min, respectively; p = 0.0457) and a longer CPB time (63 ± 28 vs 51 ± 21 min, respectively; p = 0.1461).

Two patients were lost to follow-up. The remainder were followed for an average of 90 ± 77 months (median, 69 months). One 73-year-old patient died of a biliary tract carcinoma 10 years after myxoma surgery. The remaining patients were free of symptoms at the time of this study. The conditions of two patients with residual tricuspid insufficiency and aortic valve insufficiency, respectively, worsened after surgery. Control echocardiography was available in 27 patients, with no evidence of recurrence after a mean follow-up time of 57 ± 65 months (median, 37 months). Eight of 10 patients with arterial embolization at presentation made a complete recovery. Two patients experienced permanent loss of vision and peripheral circulatory insufficiency. All patients with constitutional symptoms except one recovered after surgical excision of the myxoma.

Pathologic Findings
The mean tumor diameter was 57 ± 24 mm (range, 20 to 160 mm). On gross examination, 19 myxomas (51%) displayed a villous surface and a soft consistency (Fig 1 , bottom), and 18 tumors (49%) were smooth and compact (Fig 1 , top). The cut surface was gray or pink with frequent hemorrhagic foci. Cystic change was a striking feature in one case. Gross calcifications were evident in four tumors (11%).



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  		Figure 1. Top: smooth surface myxoma. Bottom: villous surface myxoma.

 
Microscopic examination showed the classic lepidic cells disposed singly or displaying cellular syncytia or cord-like structures. Characteristically, the cells formed concentric rings that were one or several layers thick surrounding a blood vessel. Neoplastic cells were set in a loose myxoid matrix with variable amounts of inflammatory cells (ie, lymphocytes, plasma cells, mast cells, and histiocytes). Hemosiderin-laden macrophages, hemorrhagic foci, and fibrotic areas (56%) were also frequent. Gamna-Gandy bodies (21%), calcification (16%), and ossification (10%) were occasionally present. Mitotic figures were observed in eight myxomas (21%), with a mitotic rate ranging from 0 to 3 mitoses per 50 high-power fields. Glandular structures were present in one case and hypercellular areas were present in another, which was classified as an atypical myxoma.

Clinicopathologic Correlation
The only pathologic feature that was significantly associated with embolic myxomas was a villous surface (Table 2 ). None of the tumors with calcifications embolized. Nevertheless, we failed to show a significant association between the gross villous surface and the presence of calcification (data not shown).


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  		Table 2. Morphologic Features of Myxomas Related to Embolism*

 
On the other hand, patients with left atrial myxomas and atrial fibrillation (six patients) had tumors the diameters of which were larger than those of patients with left atrial myxomas and sinus rhythm (21 patients) [75 ± 16 vs 50 ± 14 mm, respectively; p = 0.0009].

Myxomas with fibrotic areas affected older patients, although no significant difference was found (mean age, 55 ± 13 vs 46 ± 15 years, respectively; p = 0.054). The same is true for ossified myxomas (mean age, 63 ± 12 vs 50 ± 14 years, respectively; p = 0.103) and calcified myxomas (gross calcifications: mean age, 61 ± 6 vs 50 ± 14 years, respectively [p = 0.149]; microscopic calcifications: mean age, 58 ± 9 vs 50 ± 15 years, respectively [p = 0.209]).

The maximum diameter according to echocardiographic (two-dimensional) and pathologic reports was found to have a strong correlation (r = 0.917; p < 0.05) in the 25 cases analyzed. The echocardiographic features were recorded in 11 of 37 reports. The features in six cases were well-demarcated and homogeneous, and those in five cases were polylobulated and fringed. There was good agreement between the echocardiographic and pathologic records (Table 3 ). The only myxoma that was misclassified echocardiographically corresponded to a tumor with three small (ie, < 1 cm in length) papillary-like structures on the surface, which had not been noticed on echocardiography. An analysis of the relationship between surface on echocardiography and embolic phenomena showed that none of the six well-demarcated myxomas had given rise to emboli, but four of five polylobulated tumors had (p = 0.015).


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  		Table 3. Echocardiographic and Pathologic Correlation (n = 11)*

 
Immunohistochemistry
Immunoreactivity to IL-6 was assessed in 35 cases. Granular cytoplasmic positivity was observed in 26 myxomas (74%). In all positive cases, lepidic, endothelial, smooth muscle cells and cardiomyocytes reacted with the antibody. Most patients with an abnormal laboratory parameter (eg, anemia, hypergammaglobulinemia, or increased ESR) had myxomas that expressed IL-6, although statistically this relationship was not significant (Table 4 ).


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  		Table 4. Systemic Illness Manifestations and Immunohistochemical IL-6 Expression*

 
Flow Cytometry
Of the 35 tumors analyzed, 29 (83%) had normal DNA content (DNA diploid) and six (17%) had abnormal DNA content (DNA aneuploid). No significant associations were found between the DNA ploidy pattern and clinicopathologic features (Table 5 ). Interestingly, the only atypical (ie, very cellular) myxoma was DNA aneuploid. The mean PF was 8.9 ± 6.7%. Although mean PF was higher in DNA aneuploid myxomas than in DNA diploid myxomas, no significant difference was found (16 ± 11% vs 8 ± 5%, respectively; p = 0.274).


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  		Table 5. Ploidy Pattern vs Clinical and Pathologic Features*

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Conclusions
 References
 
Primary tumors of the heart are very rare, occurring in 0.0017% of collected autopsy series.14 Cardiac myxomas are the most common and usually arise on the left side of the atrial septum near the fossa ovalis.1

The clinical presentation of cardiac myxomas is not specific and depends on their size, location, and mobility. Patients usually present with one or more of the triad of intracardiac obstruction, embolism, and constitutional symptoms. Dyspnea is thought to occur as a consequence of atrioventricular valve obstruction. Its frequency in the English literature is between 24%5 and 89%,15 and in our series dyspnea affected 54% of patients. Atrial fibrillation, which also can contribute to dyspnea, occurred in 19% of our cases, compared with a reported prevalence of around 10%.5 16 17 However, some studies have found more variable frequencies, ranging from 2.5%18 to 36%,19 with this last figure reported in a series that only included patients who were > 75 years of age. Interestingly, we have demonstrated a significant association between larger left atrial myxomas and atrial fibrillation, something that, to the best of our knowledge, has not been reported previously. Nevertheless, left atrial size has been associated with an increased risk of this kind of arrhythmia.20 Therefore, it is reasonable to postulate that large left atrial myxomas are capable of expanding the left atria, which are prone to fibrillation.

Constitutional symptoms and related laboratory abnormalities were also frequent, and our results are consistent with those of other series.18 21 Most of our patients recovered once the tumor had been surgically removed. IL-6 has been detected in tissue cultures from cardiac myxoma cells,2 and several studies3 22 23 have shown a relationship between IL-6 plasma level and the occurrence of a constitutional syndrome that disappeared once the myxoma had been excised. There is only one extensive immunohistochemical study that has examined IL-6 expression.24 It was performed on 15 cardiac myxomas and showed that 80% of the tumors were immunoreactive for this cytokine, although a significant association between IL-6 expression and a constitutional syndrome was not demonstrated.24 In our series, 76% of tumors were positive for IL-6, and most patients with abnormal laboratory parameters had myxomas expressing IL-6. Nevertheless, we failed to find a significant association between IL-6 and the constitutional syndrome. This could be explained because the immunohistochemical expression of IL-6 in tissue does not always preclude an increased plasma level, which is more directly related to the syndrome.

Embolism is the other classic symptom of cardiac myxomas and is a cause of death in patients with unresected tumors. Published figures for embolism range from 6%21 to 43%.7 In our series, embolism occurred in 27% of patients, which is consistent with the results of other series.6 17 18 We have found a significant association between the occurrence of embolism and a villous tumor surface. This may be because of the ability of these friable myxomas to shed tumor fragments into the bloodstream. In fact, myxomas in two of our patients were diagnosed after histopathologic examination of surgically removed emboli. Hence, any surgically removed embolus should be histopathologically examined. A few previous clinicopathologic studies have reported the same statistical relationship.5 6 7 17

The proportion of aneuploid DNA tumors in our series was 17%, which is similar to that of other studies9 10 11 (Table 6 ). There are confusing reports9 11 about the relationship between aneuploid DNA content and aggressive biological behavior determined by embolism. On this matter, we agree with Seidman et al11 that aneuploid DNA content is not related to embolism. We believe that the identification of aneuploid DNA tumors favors the neoplastic nature of cardiac myxomas, although its biological significance remains largely unknown. The low PF is consistent with slow-growth tumors and scant mitotic activity.


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  		Table 6. Flow Cytometry in Sporadic Cardiac Myxomas*

 
Fibrotic, ossified, and calcified myxomas affected older patients, but the association was not statistically significant. This finding is in agreement with the only extensive clinicopathologic study published for cardiac myxomas5 and argues for degenerative phenomena occurring in the myxomas of older patients.

The abnormalities found on cardiac auscultation, ECG, and chest radiographs were nonspecific. Preoperative diagnosis was established in all patients by transthoracic echocardiography, which is widely recognized as an excellent diagnostic method.15 16 17 18 19 21 Another important and new aspect of our study was the comparison of echocardiographic and pathologic findings. We have demonstrated that echocardiography is an accurate and reliable method with which to predict the diameter and morphology of cardiac myxomas. A 1999 study25 reported that polypoid myxomas were the only independent predictor of systemic embolism. We have found that polylobulated myxomas diagnosed by echocardiography were significantly associated with embolic episodes. Therefore, echocardiography allowed us to identify those patients with tumors who were prone to embolization and in more urgent need for surgery.

Surgery-related mortality is reported to be < 5% for cardiac myxomas.17 26 In our series, there was no perioperative mortality, which has been equaled only in smaller case series.6 7 27 The early complication rate was 37%, which is similar to those of other studies.27 28 Reported values range from 46%20 down to 20%.16 Our patients with early complications were exposed to a longer mean ischemic time, which, as far as we know, has not been reported previously in cardiac myxoma series. Arrhythmias were the most common complication, and they affected 16% of patients. In one study,29 arrhythmias occurred in as many as 90% of patients after surgery for cardiac myxomas and were related to the number of left atrial incisions.

The frequency of recurrences in cardiac myxomas varies between 3% for sporadic cases and 22% for cases of Carney complex.30 Recurrence has been related to incomplete excision, multifocality, and shedding of tumor fragments. No recurrences have been documented among our patients. Four patients whose myxomas were removed without resection of the underlying myocardium were free of tumor. We agree with other authors7 21 27 28 that a simple excision of a small fragment of the normal atrium seems to be enough to prevent recurrence, which is more likely to be related to a predisposition for multifocality rather than to incomplete resection.30


   Conclusions
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusions
References
 
Cardiac myxomas are benign neoplasms that may have abnormal DNA content. They usually express IL-6 by immunohistochemical staining. Their morphology is related to different biological behavior. The irregular surface tumors are related to embolism, and large left atrial tumors are related to atrial fibrillation. Clinical diagnosis is best achieved by echocardiography, which is a reliable method to predict their size, morphology, and subsequent likelihood to embolize. Early surgical complications are linked with a longer ischemic time. Surgical excision is a safe and effective procedure.


   Acknowledgements
 
We are grateful to Ian Williams from the Department of Philology of the University of Cantabria for revising the final manuscript.


   Footnotes
 
Abbreviations: CPB = cardiopulmonary bypass; ESR = erythrocyte sedimentation rate; IL = interleukin; PF = proliferative cell cycle fraction

This study was supported by a grant from the Fundación Marqués de Valdecilla, Santander, Spain.

Received for publication December 14, 2001. Accepted for publication September 23, 2002.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusions
 References
 

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