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Cardiac encasement by metastatic myxoid liposarcoma
Cardiovascular Pathology 11 (2002) 322 – 325
Cardiac encasement by metastatic myxoid liposarcoma Douglas S. Leea, Maja Barnardb,*, Michael R. Freemana, Stuart J. Hutchisona, Anthony F. Grahama, Brian Chiub a Department of Cardiology, St. Michael’s Hospital, University of Toronto, Toronto, Ontario, Canada Department of Laboratory Medicine and Pathology, St. Michael’s Hospital, University of Toronto, Toronto, Ontario, Canada
b
Received 10 May 2002; received in revised form 7 August 2002; accepted 20 August 2002
Abstract Isolated cardiac metastasis from a primary liposarcoma of noncardiac origin is a rare occurrence. A patient who presented with biventricular failure and constrictive hemodynamics years after successful resection of a primary liposarcoma of the thigh is described. Extensive cardiac encasement by tumor was suspected on diagnostic imaging. Hemodynamic instability and multiorgan failure necessitated urgent exploratory sternotomy. The patient died intraoperatively. Extensive metastatic sarcoma limited to the heart was confirmed during surgical procedure. This case suggests that in clinical and pathological investigation of a cardiac mass, knowledge of previous extracardiac involvement with soft tissue sarcoma is essential. D 2002 Elsevier Science Inc. All rights reserved. Keywords: Sarcoma; Heart neoplasms; Metastasis
1. Summary A patient who presented with biventricular failure and constrictive hemodynamics years after successful resection of a primary liposarcoma of the thigh is described. Isolated cardiac involvement with extensive cardiac encasement by metastatic liposarcoma was subsequently confirmed by histopathologic evaluation of the surgical specimen.
found in up to 20% of patients who die with multiple organ involvement, isolated cardiac metastasis is rare and may be difficult to distinguish clinically from a primary cardiac tumor [5,6]. Symptoms are present in approximately 15% of patients with cardiac metastasis and more than 50% of cases with cardiac involvement are identified only at autopsy [5 –7]. Heightened awareness of the possibility of secondary cardiac involvement is warranted. We report a case of isolated cardiac involvement by metastatic myxoid liposarcoma and review the literature.
2. Introduction Primary tumors of the heart are rare occurrences with reported frequencies of 0.02% to 0.03% of autopsy series [1]. The most common primary cardiac tumor is a benign cardiac myxoma [2]. Malignant tumors comprise 25% of all primary cardiac tumors and are usually sarcomas [3]. Secondary cardiac tumors are 20 to 40 times more frequent than primary lesions [4]. Although cardiac metastases can be
* Corresponding author. Department of Pathology, Princess Margaret Hospital, University Health Network, 610 University Avenue, Room 4-302, Toronto, Ontario, Canada M5G 2M9. Tel.: +1-416-946-2104; fax: +1-416946-6579. E-mail address: [email protected] (M. Barnard).
3. Case report A 53-year-old woman presented with progressive dyspnea over a 2-month period. Five years prior to presentation, a biopsy-proven myxoid liposarcoma of the thigh was diagnosed and treated with radiation therapy, followed by surgical excision that demonstrated extensively necrotic tumor and clear resection margins. She was followed on a yearly basis and no recurrence was documented clinically. Initial investigations included complete hematologic and biochemical profile (including cardiac enzymes), which were normal. The only salient finding on electrocardiogram was diffuse low-voltage. Chest radiograph revealed bilateral pleural effusions and an enlarged cardiac shadow suggesting
1054-8807/02/$ – see front matter D 2002 Elsevier Science Inc. All rights reserved. PII: S 1 0 5 4 - 8 8 0 7 ( 0 2 ) 0 0 1 3 1 - X
D.S. Lee et al. / Cardiovascular Pathology 11 (2002) 322–325
the diagnosis of congestive heart failure. A ventilation – perfusion lung scan was of intermediate probability for pulmonary embolism and the patient was anticoagulated with intravenous heparin. Transthoracic echocardiogram suggested left ventricular dysfunction but the cardiac chambers were not adequately visualized. She was transferred to a tertiary care institution for further management and investigation. Examination revealed the following vital signs: heart rate of 80/min and blood pressure of 100/60 mmHg with no pulsus paradoxus. Cyanosis was not present. Jugular venous pressure was elevated and the carotid pulse was decreased in volume. Heart sounds were very distant and no murmurs, rubs or clicks were audible. The remainder of the examination revealed hepatomegaly and bilateral pitting edema to the knees. Chest computed tomography with 7 mm axial sections was performed, which revealed bilateral pleural effusions and a large loculated pericardial effusion located predominantly posterior and lateral to the heart causing cardiac compression (Fig. 1). No mediastinal lymphadenopathy was noted. The transthoracic echocardiogram revealed a soft tissue mass anterior, lateral and posterolateral to the heart. Cardiac chamber dimensions were small and the heart was shifted rightward within the thoracic cavity. Cardiac encasement by intrapericardial tumor was suspected and a surgical approach for diagnosis and palliation was undertaken. In-hospital course quickly became that of a progressive low-output state with evidence of end-organ compromise. Urine output decreased to anuria and shock liver ensued. Cardiac enzyme leak was not detected in the peripheral blood as evidenced by creatine kinase isoforms and troponin I. A pulmonary artery catheter was inserted because of worsening hemodynamic status. The cardiac filling pressures were elevated and equilibrated consistent with constrictive physiology, suggesting cardiac encasement. Inotropic support with dobutamine and dopamine was initiated and the patient was then taken to the operating room. At induction, the patient
Fig. 1. Computed tomographic image of cardiac mass. The region of interest (asterisk) is adjacent to the heart and has a CT density of 20 Hounsfield units suggesting fluid. Visually, the density was similar to that of a pleural effusion.
323
Fig. 2. Gross appearance of external surface of the cardiac tumor showing an area of attachment to the myocardium (arrows).
became asystolic and after multiple boluses of epinephrine and atropine, a wide-complex rhythm ensued. The patient underwent emergent exploratory sternotomy. Examination of the heart at surgery revealed a tumor of gelatinous consistency encasing the left ventricle with focal attachment to the heart. The tumor was partially excised, but the patient died intraoperatively after prolonged, open cardiac massage. No autopsy was performed. Gross examination of the surgical specimen revealed a fragmented tumor mass weighing 850 g and measuring in aggregate 14 12 6 cm. The external surface was smooth, except for a ragged, circular area of myocardial attachment measuring 4 cm in diameter (Fig. 2). On cut section, the tumor consisted of fairly homogeneous, tanpink soft gelatinous tissue. Microscopic examination revealed a focal infiltration of cardiac muscle by a tumor composed of small round or spindle-shaped cells in a myxoid background, surrounded by a plexiform network of thin-walled capillaries (Fig. 3). Frequent lipoblasts containing oil red O-positive intracytoplasmic lipid droplets were identified. Although areas of increased cellularity
324
D.S. Lee et al. / Cardiovascular Pathology 11 (2002) 322–325
Fig. 3. (A) Microscopically, tumor cells infiltrate in between myocardial cells as seen in the lower half of field (H&E, original magnification 100). (B) Cardiac tumor shows characteristic features of myxoid liposarcoma with frequent lipoblasts, myxoid background and a network of thin-walled capillaries (H&E, original magnification 400).
with occasional mitotic figures were present, suggestive of early transition, there was no fully developed round cell differentiation. The immunohistochemical studies were noncontributory with lipoblasts negative for S100 protein; however, the characteristic histologic appearance was diagnostic of myxoid liposarcoma and was identical to the tumor excised from the thigh 5 years previously.
4. Discussion Cardiac sarcomas are malignant neoplasms of mesenchymal cells, which may have fibrous, smooth muscle, skeletal muscle, vascular, fat or osteogenic differentiation, and up to 20% cannot be classified. The clinical presentation of cardiac sarcoma varies according to the chamber involved [8]. Right atrial or ventricular tumors may present as pulmonary disease with hemoptysis and dyspnea while left-sided tumors may initially present with a neurological constellation of visual loss, hemiparesis or seizures. However, the clinical presentations may be diverse and may mimic other common cardiovascular conditions such as heart failure, pericarditis or myocardial infarction. The site of involvement may also suggest the nature of the underlying disease process. Primary sarcomas are usually present in the atria or the right-sided chambers and are diffusely infiltrative. A recent series from a national referral centre for cancer pathology found that the left atrium was the most common site followed by the right ventricle and the right atrium [8]. In this series, however, referral bias due to difficulties in classification may have contributed to
the larger proportion of left atrial tumors. Rarely, primary sarcomas present at the pulmonic valve, pulmonary artery, interatrial septum and very rarely does sarcoma originate at the left ventricle [6]. In contrast to primary sarcomas, metastatic liposarcomas involve both the right and left ventricles with varying degrees of extension into the epicardium or pericardium. Sarcoma metastatic to the heart is a rare diagnosis, occurring at a frequency of 0.6% in one autopsy series of patients with malignancy [9]. There have been only two reported cases of isolated cardiac metastasis of myxoid liposarcoma [10,11]. Although not confirmed by autopsy, our patient had no clinical or radiological evidence of metastatic disease elsewhere. Patients with metastatic liposarcoma may present initially with a mass in a lower extremity followed by cardiac presentation 5 to 30 years after the primary tumor has been diagnosed. Liposarcomas are malignant neoplasms that contain lipoblasts and are extremely rare tumors in the heart. This category of neoplasms includes several distinct subtypes that show great diversity in terms of histology, clinical behavior and cytogenetic abnormalities, and range from localized well-differentiated tumors to metastatic high-grade sarcomas. An accurate subtyping of these tumors is essential, since it correlates with grade and prognosis. About half of all liposarcomas are of myxoid subtype. These tumors share clinical features and cytogenetic abnormalities with round cell liposarcomas, with many tumors showing transitional or mixed histologic features. Myxoid and round cell liposarcomas likely represent two ends of a spectrum, with increased amount of round cell differentiation indicative of higher grade and more aggressive behavior [12]. A unique cytogenetic feature seen in both subtypes is the reciprocal translocation t(12;16)(q13;p11), resulting in rearrangement of the DNA transcription factor gene CHOP. Clinically, myxoid liposarcomas have a predilection for the lower extremities and tend to recur locally. Distant metastases are rare, particularly after surgical resection, but may occur in the lungs, liver, pleura and lymph nodes. Surgical or medical therapy for isolated cardiac metastasis of sarcoma has not been rigorously studied because of the rarity of the condition. By extrapolation from studies of primary cardiac sarcomas, survival may be improved by chemotherapy or radiation [13,14]. Surgery may be considered when palliation is needed or complete resection of the tumor is possible [10]. Earlier diagnosis may improve surgical outcome [15,16]. Therefore, after detection of an intrapericardial or intracardiac mass, the possibility of cardiac metastasis from latent extracardiac tumor should be considered. In conclusion, we report a rare case of a patient with isolated cardiac encasement by metastatic liposarcoma who presented with a symptom complex suggesting biventricular congestive heart failure and a hemodynamic profile consistent with constriction. This case illustrates that increased awareness of the possibility of latent cardiac metastasis after
D.S. Lee et al. / Cardiovascular Pathology 11 (2002) 322–325
complete resection of a primary noncardiac sarcoma may aid in the diagnosis of a cardiac mass.
References [1] Reynen K. Frequency of primary tumors of the heart. Am J Cardiol 1996;77:107. [2] Silverman NA. Primary cardiac tumors. Ann Surg 1980;191:127 – 38. [3] McCallister HA. Primary tumors and cysts of the heart and pericardium. In: Harvey WP, editor. Current problems in cardiology. Chicago: Year Book Medical Publishers, 1979. pp. 8 – 51. [4] Prichard RW. Tumors of the heart: review of the subject and report of one hundred fifty cases. Arch Pathol 1951;51:98 – 128. [5] Smith LH. Secondary tumors of the heart. Rev Surg 1976;33:223 – 31. [6] Poole GV, Meredith JW, Breyer RH, Mills SA. Surgical implications in malignant cardiac disease. Ann Thorac Surg 1983;36: 484 – 91. [7] Malaret GE, Aliaga P. Metastatic disease of the heart. Cancer 1968; 457 – 66. [8] Veinot JP, Burns BF, Commons AS, Thomas J. Cardiac neoplasms at
[9]
[10]
[11] [12]
[13] [14] [15] [16]
325
the Canadian reference centre for cancer pathology. Can J Cardiol 1999;15:311 – 9. Burke A, Virmani R. Tumors metastatic to the heart and pericardium. In: Rosai J, editor. Atlas of tumor pathology: tumors of the heart and great vessels. Washington (DC): Armed Forces Institute of Pathology, 1995. p. 196. Lagrange J, Despins P, Spielman M, et al. Cardiac metastases: case report of an isolated cardiac metastasis of a myxoid liposarcoma. Cancer 1986;58:2333 – 7. Ravikumar TS, Topulos GP, Anderson RW, Grage TB. Surgical resection for isolated cardiac metastases. Arch Surg 1983;118:117 – 20. Weiss SW, Goldblum JR. Liposarcoma. In: Weiss SW, editor. Enzinger and Weiss’s soft tissue tumors. 4th ed. St. Louis: Mosby, 2001. pp. 641 – 93. Burke AP, Cowan D, Virmani R. Primary sarcomas of the heart. Cancer 1992;69:387 – 95. Perocchio M, Caponnetto S. Primary malignant cardiac tumors. Minerva Cardioangiol 1992;40:179 – 93. Perchinsky MJ, Lichtenstein SV, Tyers GF. Primary cardiac tumors: forty years’ experience with 71 patients. Cancer 1997;79:1809 – 15. Molina JE, Edwards JE, Ward HB. Primary cardiac tumors: experience at the University of Minnesota. Thorac Cardiovasc Surg 1990; 38(Suppl 2):183 – 91.
Cardiac encasement by metastatic myxoid liposarcoma Douglas S. Leea, Maja Barnardb,*, Michael R. Freemana, Stuart J. Hutchisona, Anthony F. Grahama, Brian Chiub a Department of Cardiology, St. Michael’s Hospital, University of Toronto, Toronto, Ontario, Canada Department of Laboratory Medicine and Pathology, St. Michael’s Hospital, University of Toronto, Toronto, Ontario, Canada
b
Received 10 May 2002; received in revised form 7 August 2002; accepted 20 August 2002
Abstract Isolated cardiac metastasis from a primary liposarcoma of noncardiac origin is a rare occurrence. A patient who presented with biventricular failure and constrictive hemodynamics years after successful resection of a primary liposarcoma of the thigh is described. Extensive cardiac encasement by tumor was suspected on diagnostic imaging. Hemodynamic instability and multiorgan failure necessitated urgent exploratory sternotomy. The patient died intraoperatively. Extensive metastatic sarcoma limited to the heart was confirmed during surgical procedure. This case suggests that in clinical and pathological investigation of a cardiac mass, knowledge of previous extracardiac involvement with soft tissue sarcoma is essential. D 2002 Elsevier Science Inc. All rights reserved. Keywords: Sarcoma; Heart neoplasms; Metastasis
1. Summary A patient who presented with biventricular failure and constrictive hemodynamics years after successful resection of a primary liposarcoma of the thigh is described. Isolated cardiac involvement with extensive cardiac encasement by metastatic liposarcoma was subsequently confirmed by histopathologic evaluation of the surgical specimen.
found in up to 20% of patients who die with multiple organ involvement, isolated cardiac metastasis is rare and may be difficult to distinguish clinically from a primary cardiac tumor [5,6]. Symptoms are present in approximately 15% of patients with cardiac metastasis and more than 50% of cases with cardiac involvement are identified only at autopsy [5 –7]. Heightened awareness of the possibility of secondary cardiac involvement is warranted. We report a case of isolated cardiac involvement by metastatic myxoid liposarcoma and review the literature.
2. Introduction Primary tumors of the heart are rare occurrences with reported frequencies of 0.02% to 0.03% of autopsy series [1]. The most common primary cardiac tumor is a benign cardiac myxoma [2]. Malignant tumors comprise 25% of all primary cardiac tumors and are usually sarcomas [3]. Secondary cardiac tumors are 20 to 40 times more frequent than primary lesions [4]. Although cardiac metastases can be
* Corresponding author. Department of Pathology, Princess Margaret Hospital, University Health Network, 610 University Avenue, Room 4-302, Toronto, Ontario, Canada M5G 2M9. Tel.: +1-416-946-2104; fax: +1-416946-6579. E-mail address: [email protected] (M. Barnard).
3. Case report A 53-year-old woman presented with progressive dyspnea over a 2-month period. Five years prior to presentation, a biopsy-proven myxoid liposarcoma of the thigh was diagnosed and treated with radiation therapy, followed by surgical excision that demonstrated extensively necrotic tumor and clear resection margins. She was followed on a yearly basis and no recurrence was documented clinically. Initial investigations included complete hematologic and biochemical profile (including cardiac enzymes), which were normal. The only salient finding on electrocardiogram was diffuse low-voltage. Chest radiograph revealed bilateral pleural effusions and an enlarged cardiac shadow suggesting
1054-8807/02/$ – see front matter D 2002 Elsevier Science Inc. All rights reserved. PII: S 1 0 5 4 - 8 8 0 7 ( 0 2 ) 0 0 1 3 1 - X
D.S. Lee et al. / Cardiovascular Pathology 11 (2002) 322–325
the diagnosis of congestive heart failure. A ventilation – perfusion lung scan was of intermediate probability for pulmonary embolism and the patient was anticoagulated with intravenous heparin. Transthoracic echocardiogram suggested left ventricular dysfunction but the cardiac chambers were not adequately visualized. She was transferred to a tertiary care institution for further management and investigation. Examination revealed the following vital signs: heart rate of 80/min and blood pressure of 100/60 mmHg with no pulsus paradoxus. Cyanosis was not present. Jugular venous pressure was elevated and the carotid pulse was decreased in volume. Heart sounds were very distant and no murmurs, rubs or clicks were audible. The remainder of the examination revealed hepatomegaly and bilateral pitting edema to the knees. Chest computed tomography with 7 mm axial sections was performed, which revealed bilateral pleural effusions and a large loculated pericardial effusion located predominantly posterior and lateral to the heart causing cardiac compression (Fig. 1). No mediastinal lymphadenopathy was noted. The transthoracic echocardiogram revealed a soft tissue mass anterior, lateral and posterolateral to the heart. Cardiac chamber dimensions were small and the heart was shifted rightward within the thoracic cavity. Cardiac encasement by intrapericardial tumor was suspected and a surgical approach for diagnosis and palliation was undertaken. In-hospital course quickly became that of a progressive low-output state with evidence of end-organ compromise. Urine output decreased to anuria and shock liver ensued. Cardiac enzyme leak was not detected in the peripheral blood as evidenced by creatine kinase isoforms and troponin I. A pulmonary artery catheter was inserted because of worsening hemodynamic status. The cardiac filling pressures were elevated and equilibrated consistent with constrictive physiology, suggesting cardiac encasement. Inotropic support with dobutamine and dopamine was initiated and the patient was then taken to the operating room. At induction, the patient
Fig. 1. Computed tomographic image of cardiac mass. The region of interest (asterisk) is adjacent to the heart and has a CT density of 20 Hounsfield units suggesting fluid. Visually, the density was similar to that of a pleural effusion.
323
Fig. 2. Gross appearance of external surface of the cardiac tumor showing an area of attachment to the myocardium (arrows).
became asystolic and after multiple boluses of epinephrine and atropine, a wide-complex rhythm ensued. The patient underwent emergent exploratory sternotomy. Examination of the heart at surgery revealed a tumor of gelatinous consistency encasing the left ventricle with focal attachment to the heart. The tumor was partially excised, but the patient died intraoperatively after prolonged, open cardiac massage. No autopsy was performed. Gross examination of the surgical specimen revealed a fragmented tumor mass weighing 850 g and measuring in aggregate 14 12 6 cm. The external surface was smooth, except for a ragged, circular area of myocardial attachment measuring 4 cm in diameter (Fig. 2). On cut section, the tumor consisted of fairly homogeneous, tanpink soft gelatinous tissue. Microscopic examination revealed a focal infiltration of cardiac muscle by a tumor composed of small round or spindle-shaped cells in a myxoid background, surrounded by a plexiform network of thin-walled capillaries (Fig. 3). Frequent lipoblasts containing oil red O-positive intracytoplasmic lipid droplets were identified. Although areas of increased cellularity
324
D.S. Lee et al. / Cardiovascular Pathology 11 (2002) 322–325
Fig. 3. (A) Microscopically, tumor cells infiltrate in between myocardial cells as seen in the lower half of field (H&E, original magnification 100). (B) Cardiac tumor shows characteristic features of myxoid liposarcoma with frequent lipoblasts, myxoid background and a network of thin-walled capillaries (H&E, original magnification 400).
with occasional mitotic figures were present, suggestive of early transition, there was no fully developed round cell differentiation. The immunohistochemical studies were noncontributory with lipoblasts negative for S100 protein; however, the characteristic histologic appearance was diagnostic of myxoid liposarcoma and was identical to the tumor excised from the thigh 5 years previously.
4. Discussion Cardiac sarcomas are malignant neoplasms of mesenchymal cells, which may have fibrous, smooth muscle, skeletal muscle, vascular, fat or osteogenic differentiation, and up to 20% cannot be classified. The clinical presentation of cardiac sarcoma varies according to the chamber involved [8]. Right atrial or ventricular tumors may present as pulmonary disease with hemoptysis and dyspnea while left-sided tumors may initially present with a neurological constellation of visual loss, hemiparesis or seizures. However, the clinical presentations may be diverse and may mimic other common cardiovascular conditions such as heart failure, pericarditis or myocardial infarction. The site of involvement may also suggest the nature of the underlying disease process. Primary sarcomas are usually present in the atria or the right-sided chambers and are diffusely infiltrative. A recent series from a national referral centre for cancer pathology found that the left atrium was the most common site followed by the right ventricle and the right atrium [8]. In this series, however, referral bias due to difficulties in classification may have contributed to
the larger proportion of left atrial tumors. Rarely, primary sarcomas present at the pulmonic valve, pulmonary artery, interatrial septum and very rarely does sarcoma originate at the left ventricle [6]. In contrast to primary sarcomas, metastatic liposarcomas involve both the right and left ventricles with varying degrees of extension into the epicardium or pericardium. Sarcoma metastatic to the heart is a rare diagnosis, occurring at a frequency of 0.6% in one autopsy series of patients with malignancy [9]. There have been only two reported cases of isolated cardiac metastasis of myxoid liposarcoma [10,11]. Although not confirmed by autopsy, our patient had no clinical or radiological evidence of metastatic disease elsewhere. Patients with metastatic liposarcoma may present initially with a mass in a lower extremity followed by cardiac presentation 5 to 30 years after the primary tumor has been diagnosed. Liposarcomas are malignant neoplasms that contain lipoblasts and are extremely rare tumors in the heart. This category of neoplasms includes several distinct subtypes that show great diversity in terms of histology, clinical behavior and cytogenetic abnormalities, and range from localized well-differentiated tumors to metastatic high-grade sarcomas. An accurate subtyping of these tumors is essential, since it correlates with grade and prognosis. About half of all liposarcomas are of myxoid subtype. These tumors share clinical features and cytogenetic abnormalities with round cell liposarcomas, with many tumors showing transitional or mixed histologic features. Myxoid and round cell liposarcomas likely represent two ends of a spectrum, with increased amount of round cell differentiation indicative of higher grade and more aggressive behavior [12]. A unique cytogenetic feature seen in both subtypes is the reciprocal translocation t(12;16)(q13;p11), resulting in rearrangement of the DNA transcription factor gene CHOP. Clinically, myxoid liposarcomas have a predilection for the lower extremities and tend to recur locally. Distant metastases are rare, particularly after surgical resection, but may occur in the lungs, liver, pleura and lymph nodes. Surgical or medical therapy for isolated cardiac metastasis of sarcoma has not been rigorously studied because of the rarity of the condition. By extrapolation from studies of primary cardiac sarcomas, survival may be improved by chemotherapy or radiation [13,14]. Surgery may be considered when palliation is needed or complete resection of the tumor is possible [10]. Earlier diagnosis may improve surgical outcome [15,16]. Therefore, after detection of an intrapericardial or intracardiac mass, the possibility of cardiac metastasis from latent extracardiac tumor should be considered. In conclusion, we report a rare case of a patient with isolated cardiac encasement by metastatic liposarcoma who presented with a symptom complex suggesting biventricular congestive heart failure and a hemodynamic profile consistent with constriction. This case illustrates that increased awareness of the possibility of latent cardiac metastasis after
D.S. Lee et al. / Cardiovascular Pathology 11 (2002) 322–325
complete resection of a primary noncardiac sarcoma may aid in the diagnosis of a cardiac mass.
References [1] Reynen K. Frequency of primary tumors of the heart. Am J Cardiol 1996;77:107. [2] Silverman NA. Primary cardiac tumors. Ann Surg 1980;191:127 – 38. [3] McCallister HA. Primary tumors and cysts of the heart and pericardium. In: Harvey WP, editor. Current problems in cardiology. Chicago: Year Book Medical Publishers, 1979. pp. 8 – 51. [4] Prichard RW. Tumors of the heart: review of the subject and report of one hundred fifty cases. Arch Pathol 1951;51:98 – 128. [5] Smith LH. Secondary tumors of the heart. Rev Surg 1976;33:223 – 31. [6] Poole GV, Meredith JW, Breyer RH, Mills SA. Surgical implications in malignant cardiac disease. Ann Thorac Surg 1983;36: 484 – 91. [7] Malaret GE, Aliaga P. Metastatic disease of the heart. Cancer 1968; 457 – 66. [8] Veinot JP, Burns BF, Commons AS, Thomas J. Cardiac neoplasms at
[9]
[10]
[11] [12]
[13] [14] [15] [16]
325
the Canadian reference centre for cancer pathology. Can J Cardiol 1999;15:311 – 9. Burke A, Virmani R. Tumors metastatic to the heart and pericardium. In: Rosai J, editor. Atlas of tumor pathology: tumors of the heart and great vessels. Washington (DC): Armed Forces Institute of Pathology, 1995. p. 196. Lagrange J, Despins P, Spielman M, et al. Cardiac metastases: case report of an isolated cardiac metastasis of a myxoid liposarcoma. Cancer 1986;58:2333 – 7. Ravikumar TS, Topulos GP, Anderson RW, Grage TB. Surgical resection for isolated cardiac metastases. Arch Surg 1983;118:117 – 20. Weiss SW, Goldblum JR. Liposarcoma. In: Weiss SW, editor. Enzinger and Weiss’s soft tissue tumors. 4th ed. St. Louis: Mosby, 2001. pp. 641 – 93. Burke AP, Cowan D, Virmani R. Primary sarcomas of the heart. Cancer 1992;69:387 – 95. Perocchio M, Caponnetto S. Primary malignant cardiac tumors. Minerva Cardioangiol 1992;40:179 – 93. Perchinsky MJ, Lichtenstein SV, Tyers GF. Primary cardiac tumors: forty years’ experience with 71 patients. Cancer 1997;79:1809 – 15. Molina JE, Edwards JE, Ward HB. Primary cardiac tumors: experience at the University of Minnesota. Thorac Cardiovasc Surg 1990; 38(Suppl 2):183 – 91.