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Triple valve replacement in a patient with severe carcinoid heart disease
PII: S0967-2109(01)00137-5
Cardiovascular Surgery, Vol. 10, No. 3, pp. 287–290, 2002 2002 The International Society for Cardiovascular Surgery Published by Elsevier Science Ltd. All rights reserved 0967-2109/02 $22.00
www.elsevier.com/locate/cardiosur
CASE REPORT Triple valve replacement in a patient with severe carcinoid heart disease M. Wilhelmi, M. K. H. Fritz, S. Fischer, A. Haverich and W. Harringer Division of Thoracic and Cardiovascular Surgery, Hanover Medical School, Carl Neuberg Straße 1, 30623 Hanover, Germany We report on the case of a 34-year-old male patient suffering from end-stage carcinoid heart disease with severe tricuspid, pulmonary and mitral valve regurgitation. In addition, a persisting foramen ovale was present. The primary carcinoid tumor was never discovered. However, urine 5-hydroxy-indole-acetic-acid (5-HIAA) were consistently elevated after the first diagnosis of carcinoid disease and after eight years of medication with Octreotide and Interferon α-2b our patient developed significant cardiac insufficiency mainly due to severe valvular dysfunction. Ultimately, mechanical tricuspid, mitral and pulmonary valve replacement was performed. Twelve hours following the operation the patient had to be returned to the operating room for persisting intrathoracic hemorrhage. He recovered uneventfully and was discharged from hospital on day 37. Twelve months following triple valve replacement the cardiac status recovered from preoperative NYHA-IV to NYHA-I. 2002 The International Society for Cardiovascular Surgery. Published by Elsevier Science Ltd. All rights reserved Keywords: carcinoid syndrome, cardiac tumor, Hedinger syndrome, cardial fibrosis
Introduction Carcinoid tumors arise in 1.5/100,000 people in the general population [1]. The carcinoid syndrome occurs in less than 4% of patients with carcinoid tumor [2]. Clinically, carcinoid syndrome is characterized by cutaneous flushing, watery diarrhea, bronchospasm, teleangiectasias and valvular heart disease. Carcinoid heart disease occurs in approximately 60% of patients with carcinoid syndrome and is characterized by plaque-like, fibrous endocardial thickening, which classically involves the right atrium and ventricle [3]. Valvular disease is the most common cardiac pathology and mainly affects the tricuspid valve. Pellikka et al. observed tricuspid valve damage in 97% of patients with carcinoid heart
Correspondence to: Dr M. Wilhelmi, Hanover Medical School, Division of Thoracic-Cardiovascular Surgery, Carl-Neubergstrasse 1, 30623 Hannover, Germany. Tel.: +49-511-532-2393; Fax: +49-511532-5404; e-mail: [email protected]
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JUNE 2002 VOL 10 NO 3
disease, whereas the pulmonary valve was involved in 88% of cases [4]. Involvement of the left atrium and ventricle does not occur usually, except in patients with bronchial carcinoids or right-to-left intracardiac shunts [5]. Although valvular replacement in patients with symptomatic carcinoid heart disease is associated with a high perioperative morbidity and mortality, it should be considered before significant right ventricular dysfunction develops [6,7].
Case presentation We report on a case of a 34-year-old male patient with carcinoid syndrome. The primary site of the carcinoid tumor was never found. However, during an eight years period of treatment with medication (Interferon α-2b (Intron A, Essex Pharma, Munich, Germany) 3 Mega s.c., 3x/week and an Octreotide alanolgon (Sandostatin, Sandoz, Nu¨rnberg, Germany) 200mg s.c., 3x/d), the patient developed multiple liver metastases with accompanying right cardial fibrosis (Hedinger-Syndrome) leading to sev287
Triple valve replacement in a patient with severe carcinoid heart disease: M. Wilhelmi et al.
ere secondary tricuspid, pulmonary and mitral valve dysfunction. Clinically our patient presented with severe peripheral cyanosis, recurrent episodes of skin flushing and dyspnea at rest, which required continuous oxygen insufflation through a nasal tube. Echocardiographic examinations and cardiac catheterization demonstrated severe heart failure with elevated systolic right ventricular pressures of approximately 60 mmHg, severe tricuspid regurgitation (grade III–IV) and a combined lesion of the pulmonary valve (regurgitation grade II–III/stenosis grade II). Additionally, the left ventricle was enlarged and showed compromised function with an ejection fraction of 40% and mitral valve dysfunction (regurgitation grade I/stenosis grade I–-II). In addition, a persisting foramen ovale (PFO) became evident. No relevant coronary artery stenosis was observed. Hepatic ultrasound and computed tomgraphic (CT) scan revealed an enlarged liver with diffuse metastases. Blood count, electrolytes and liver function tests were found to be within normal ranges, except a progressive thrombocytopenia (79,000/µl) and decreased serum levels of coagulation factors II and V (factor II: 45%, factor V: 65%). The preoperative chest X-ray is shown in Figure 1. Due to the severity of symptoms and significantly impaired cardiac function the patient underwent triple valve replacement. After median sternotomy standard cardiopulmonary bypass was established. For myocardial protection intermittent cold shot crystalloid cardioplegia was used. After left-sided transseptal atriotomy the fibrotic mitral valve with fused and shortened chordae tendineae became visible. The right atrial wall was thickened and the endocardial surfaces were covered with white pla-
ques typical for carcinoid heart disease. Furthermore, the tricuspid valve leaflets were thickened and shortened resulting in severe regurgitation. The annulus of the valve was 15 mm in diameter and the leaflets were retracted. An annuloplasty using autologous pericardial material was performed. For valve replacements St. Jude Medical (St. Jude Medical, Nu¨ rnberg, Germany) artificial bi-leaflet valves were used (mitral valve: 29 mm, tricuspid valve: 31 mm, pulmonary valve 23 mm). Finally, the PFO was closed by a single stitch closure. The patient was admitted to the ICU in hemodynamically stable conditions. However, 12 h following the operation he developed signs of intrathoracic hemorrhage and was returned to the operating theatre. Diffuse bleeding was found with no signs for surgical bleedings. It is likely that the accompanying hepatic dysfunction and secondarily impaired blood coagulation has caused the bleeding. The patient recovered uneventfully and was discharged from hospital on postoperative day 37. Echocardiographic controls revealed an enlarged right ventricle, but significantly improved left and right ventricular function. Figure 2 demonstrates the chest X-ray three months following triple valve replacement. The six months follow-up demonstrated further improvement in cardiac function with a left ventricular ejection fraction of 60%. One year after triple valve replacement the cardiac status is NYHA I. An ECG exercise test, which could not be performed preoperatively due to severely impaired cardiac function, revealed satisfying results with a maximum of 75W stress, which the patient handled successfully. During the 2 min exercise period, which had to be stopped because of muscular exhaustion, neither signs of dyspnea nor corresponding ECG changes
Figure 1 Preoperative chest X-ray
Figure 2 3 months postoperative chest X-ray
288
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Triple valve replacement in a patient with severe carcinoid heart disease: M. Wilhelmi et al.
occurred. During exercise the maximum blood pressure was 148/76 mmHg at a heart rate of 137 beats/min. One year after triple valve replacement the patient is in good physical condition. His sport activities include downhill skiing and soccer. The actual medication consists of an octreotide analogue (Sandostatin, Sandoz, Germany) 200 mg 3x/d s.c., interferon α-2b (Intron A, Essex Pharma, Germany) 3 Mega, 3x/week s.c., potassiumhydrogencarbonate (Nephrotrans, Medice, Iserlohn, Germany) 0.5 g 3x/d, and for routine coagulation phenprocoumon (Marcumar, Roche, GrenzachWyhlen, Germany) once a day. Ultrasound examinations revealed no increase in size and numbers of the liver metastases.
Conclusions Patients with carcinoid heart disease have a dismal prognosis. Right sided heart failure leads to increased morbidity and mortality. Valvular replacement in patients with symptomatic carcinoid heart disease is associated with increased numbers of perioperative complications, primarily due to postoperative bleeding and right ventricular failure. Although cardiac surgery for carcinoid heart disease carries a high risk for perioperative mortality, and despite the dictum that metastatic malignancy is a contradiction to open heart surgery, surgical intervention should be considered when cardiac symptoms become severe [3,6,8]. Since 1963 cardiac valve replacement has been performed in patients with carcinoid heart disease. However, it remains controversial whether biological valves are superior to artificial valves or vice versa [6,9-13]. Although comparative studies on artificial and biological valve replacement in tricuspid position did not show significant differences in the early postoperative outcome [9,10], hypothetical danger may exist regarding the affection of biological valves by the same process that initially affected the native valves. In addition, biological valve replacement is associated with accelerated degeneration leading to valvular dysfunction within 10–15 years after implantation. Connolly et al. speculated that somatostatin might have a positive effect on the outcome after bioprosthesis implantation due to its antagonistic mechanism against serotonin [6]. This hypothesis, however, is not supported by evidence in the literature. Moreover, biological valve prostheses are at risk of valve destruction by ongoing release of somatostation. McDonald et al. reported a case of biological tricuspid valve degeneration (Carpentier Edwards valve) four years after biological tricuspid valve replacement [8]. Ridker et al. reported on the implantation of a bioprosthesis in tricuspid position which showed leaflet thickening and typical carcinoid plaques after a eleven years period [11]. Ohri CARDIOVASCULAR SURGERY
JUNE 2002 VOL 10 NO 3
et al. reported on a case in which typical carcinoid plaques developed on the leaflets of a cryopreserved allograft three months after pulmonary valve replacement [12]. Controversially, Connolly et al. recommended the use of bioprostheses in the treatment of carcinoid heart disease in order to lower the risk ment [12]. Controversially, Connolly et al. recaddition to accompanying liver dysfunction [6]. This is indeed a reasonable argument for the use of biological heart valves. However, the frequent use of anticoagulation time determination by selftesting instruments helps to keep bleeding complications at a low risk after mechanical heart valve replacement. Based on our experience from this case and the sparse evidence from the literature we suggest heart valve replacement to be performed in patients with carcinoid heart disease at the onset of valvular dysfunction. Especially in young patients we believe the replacement of affected valves by artificial mechanical valves to be the treatment of choice. Warfarin intake increases the risk for acute hemorrhage, which can be minimized by frequently and accurately performed monitoring. To our knowledge this is the first report on a triple valve replacement involving the tricuspid, pulmonary and mitral valve in a patient suffering from carcinoid heart disease. Due to the short number of patients with carcinoid heart disease, clinical trails will be difficult to perform. Therefore, detailed singular reports on successful treatment strategies will help to successfully treat individual cases of carcinoid heart disease.
References 1. Basson, M. D., Ahlman, H. and Wangberg, B., Biology and management of the midgut carcinoid. Am J Surg, 1993, 165, 228–297. 2. Zeitels, J., Neunheim, K. and Kaplan, E. L., Carcinoid tumors: a 37-year experience. Arch Surg, 1982, 117, 732–737. 3. Kulke, M. H. and Mayer, R. J., Carcinoid tumors. N Engl J Med, 1999, 340(11), 858–868. 4. Pellikka, P. A., Tajik, A. J. and Khandheria, B. K., Carcinoid heart disease, Clinical and echocardiographic spectrum in 74 patients. Circulation, 1993, 87, 1188–1198. 5. Fischer, S., Kruger, M. and McRae, K., Giant bronchial carcinoid tumors: a multidisciplinary approach. Ann Thorac Surg, 2001, 71(1), 386–393. 6. Connolly, H. M., Nishimura, R. A. and Smith, H. C., Outcome of cardiac surgery for carcinoid heart disease. J Am Coll Cardiol, 1995, 25, 410–416. 7. Connolly, H. M., Schaff, H. V. and Nishimura, R. A., Cardiac surgery for carcinoid heart disease (abstract). Circulation, 1997, 96(Suppl I), I–507. 8. McDonald, M. L., Nagorney, D. M. and Connolly, H. M., Carcinoid and carcinoid syndrome: successful surgical treatment. Ann Thorac Surg, 199, 67, 537–539. 9. Lundin, L., Hansson, E. -E. and Landelius, J., Surgical treatment of carcinoid heart disease. J Thorac Cardiovasc Surg, 1990, 100, 552–561. 10. Knott-Craig, C. J., Schaff, H. V. and Mullany, C. J., Carcinoid disease of the heart, Surgical management of ten patients. J Thorac Cardiovasc Surg, 1992, 102, 475–481. 11. Ridker, P. M., Chertow, G. M. and Karlson, E. W., Biopros-
289
Triple valve replacement in a patient with severe carcinoid heart disease: M. Wilhelmi et al. thetic tricuspid valve stenosis associated with extensive plaque deposition in carcinoid heart disease. Am Heart J, 1991, 121, 1835–1838. 12. Ohri, S. K., Schofield, J. B. and Hodgson, H., Carcinoid heart disease: ealy failure of an allograft valve replacement. Ann Thorac Surg, 1994, 58, 1161–1163.
290
13. Ludin, L., Carcinoid heart disease. A cardiologist’s viewpoint. Acta Oncol, 1991, 30, 499–502. Paper accepted 14 November 2001
CARDIOVASCULAR SURGERY
JUNE 2002 VOL 10 NO 3
Cardiovascular Surgery, Vol. 10, No. 3, pp. 287–290, 2002 2002 The International Society for Cardiovascular Surgery Published by Elsevier Science Ltd. All rights reserved 0967-2109/02 $22.00
www.elsevier.com/locate/cardiosur
CASE REPORT Triple valve replacement in a patient with severe carcinoid heart disease M. Wilhelmi, M. K. H. Fritz, S. Fischer, A. Haverich and W. Harringer Division of Thoracic and Cardiovascular Surgery, Hanover Medical School, Carl Neuberg Straße 1, 30623 Hanover, Germany We report on the case of a 34-year-old male patient suffering from end-stage carcinoid heart disease with severe tricuspid, pulmonary and mitral valve regurgitation. In addition, a persisting foramen ovale was present. The primary carcinoid tumor was never discovered. However, urine 5-hydroxy-indole-acetic-acid (5-HIAA) were consistently elevated after the first diagnosis of carcinoid disease and after eight years of medication with Octreotide and Interferon α-2b our patient developed significant cardiac insufficiency mainly due to severe valvular dysfunction. Ultimately, mechanical tricuspid, mitral and pulmonary valve replacement was performed. Twelve hours following the operation the patient had to be returned to the operating room for persisting intrathoracic hemorrhage. He recovered uneventfully and was discharged from hospital on day 37. Twelve months following triple valve replacement the cardiac status recovered from preoperative NYHA-IV to NYHA-I. 2002 The International Society for Cardiovascular Surgery. Published by Elsevier Science Ltd. All rights reserved Keywords: carcinoid syndrome, cardiac tumor, Hedinger syndrome, cardial fibrosis
Introduction Carcinoid tumors arise in 1.5/100,000 people in the general population [1]. The carcinoid syndrome occurs in less than 4% of patients with carcinoid tumor [2]. Clinically, carcinoid syndrome is characterized by cutaneous flushing, watery diarrhea, bronchospasm, teleangiectasias and valvular heart disease. Carcinoid heart disease occurs in approximately 60% of patients with carcinoid syndrome and is characterized by plaque-like, fibrous endocardial thickening, which classically involves the right atrium and ventricle [3]. Valvular disease is the most common cardiac pathology and mainly affects the tricuspid valve. Pellikka et al. observed tricuspid valve damage in 97% of patients with carcinoid heart
Correspondence to: Dr M. Wilhelmi, Hanover Medical School, Division of Thoracic-Cardiovascular Surgery, Carl-Neubergstrasse 1, 30623 Hannover, Germany. Tel.: +49-511-532-2393; Fax: +49-511532-5404; e-mail: [email protected]
CARDIOVASCULAR SURGERY
JUNE 2002 VOL 10 NO 3
disease, whereas the pulmonary valve was involved in 88% of cases [4]. Involvement of the left atrium and ventricle does not occur usually, except in patients with bronchial carcinoids or right-to-left intracardiac shunts [5]. Although valvular replacement in patients with symptomatic carcinoid heart disease is associated with a high perioperative morbidity and mortality, it should be considered before significant right ventricular dysfunction develops [6,7].
Case presentation We report on a case of a 34-year-old male patient with carcinoid syndrome. The primary site of the carcinoid tumor was never found. However, during an eight years period of treatment with medication (Interferon α-2b (Intron A, Essex Pharma, Munich, Germany) 3 Mega s.c., 3x/week and an Octreotide alanolgon (Sandostatin, Sandoz, Nu¨rnberg, Germany) 200mg s.c., 3x/d), the patient developed multiple liver metastases with accompanying right cardial fibrosis (Hedinger-Syndrome) leading to sev287
Triple valve replacement in a patient with severe carcinoid heart disease: M. Wilhelmi et al.
ere secondary tricuspid, pulmonary and mitral valve dysfunction. Clinically our patient presented with severe peripheral cyanosis, recurrent episodes of skin flushing and dyspnea at rest, which required continuous oxygen insufflation through a nasal tube. Echocardiographic examinations and cardiac catheterization demonstrated severe heart failure with elevated systolic right ventricular pressures of approximately 60 mmHg, severe tricuspid regurgitation (grade III–IV) and a combined lesion of the pulmonary valve (regurgitation grade II–III/stenosis grade II). Additionally, the left ventricle was enlarged and showed compromised function with an ejection fraction of 40% and mitral valve dysfunction (regurgitation grade I/stenosis grade I–-II). In addition, a persisting foramen ovale (PFO) became evident. No relevant coronary artery stenosis was observed. Hepatic ultrasound and computed tomgraphic (CT) scan revealed an enlarged liver with diffuse metastases. Blood count, electrolytes and liver function tests were found to be within normal ranges, except a progressive thrombocytopenia (79,000/µl) and decreased serum levels of coagulation factors II and V (factor II: 45%, factor V: 65%). The preoperative chest X-ray is shown in Figure 1. Due to the severity of symptoms and significantly impaired cardiac function the patient underwent triple valve replacement. After median sternotomy standard cardiopulmonary bypass was established. For myocardial protection intermittent cold shot crystalloid cardioplegia was used. After left-sided transseptal atriotomy the fibrotic mitral valve with fused and shortened chordae tendineae became visible. The right atrial wall was thickened and the endocardial surfaces were covered with white pla-
ques typical for carcinoid heart disease. Furthermore, the tricuspid valve leaflets were thickened and shortened resulting in severe regurgitation. The annulus of the valve was 15 mm in diameter and the leaflets were retracted. An annuloplasty using autologous pericardial material was performed. For valve replacements St. Jude Medical (St. Jude Medical, Nu¨ rnberg, Germany) artificial bi-leaflet valves were used (mitral valve: 29 mm, tricuspid valve: 31 mm, pulmonary valve 23 mm). Finally, the PFO was closed by a single stitch closure. The patient was admitted to the ICU in hemodynamically stable conditions. However, 12 h following the operation he developed signs of intrathoracic hemorrhage and was returned to the operating theatre. Diffuse bleeding was found with no signs for surgical bleedings. It is likely that the accompanying hepatic dysfunction and secondarily impaired blood coagulation has caused the bleeding. The patient recovered uneventfully and was discharged from hospital on postoperative day 37. Echocardiographic controls revealed an enlarged right ventricle, but significantly improved left and right ventricular function. Figure 2 demonstrates the chest X-ray three months following triple valve replacement. The six months follow-up demonstrated further improvement in cardiac function with a left ventricular ejection fraction of 60%. One year after triple valve replacement the cardiac status is NYHA I. An ECG exercise test, which could not be performed preoperatively due to severely impaired cardiac function, revealed satisfying results with a maximum of 75W stress, which the patient handled successfully. During the 2 min exercise period, which had to be stopped because of muscular exhaustion, neither signs of dyspnea nor corresponding ECG changes
Figure 1 Preoperative chest X-ray
Figure 2 3 months postoperative chest X-ray
288
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Triple valve replacement in a patient with severe carcinoid heart disease: M. Wilhelmi et al.
occurred. During exercise the maximum blood pressure was 148/76 mmHg at a heart rate of 137 beats/min. One year after triple valve replacement the patient is in good physical condition. His sport activities include downhill skiing and soccer. The actual medication consists of an octreotide analogue (Sandostatin, Sandoz, Germany) 200 mg 3x/d s.c., interferon α-2b (Intron A, Essex Pharma, Germany) 3 Mega, 3x/week s.c., potassiumhydrogencarbonate (Nephrotrans, Medice, Iserlohn, Germany) 0.5 g 3x/d, and for routine coagulation phenprocoumon (Marcumar, Roche, GrenzachWyhlen, Germany) once a day. Ultrasound examinations revealed no increase in size and numbers of the liver metastases.
Conclusions Patients with carcinoid heart disease have a dismal prognosis. Right sided heart failure leads to increased morbidity and mortality. Valvular replacement in patients with symptomatic carcinoid heart disease is associated with increased numbers of perioperative complications, primarily due to postoperative bleeding and right ventricular failure. Although cardiac surgery for carcinoid heart disease carries a high risk for perioperative mortality, and despite the dictum that metastatic malignancy is a contradiction to open heart surgery, surgical intervention should be considered when cardiac symptoms become severe [3,6,8]. Since 1963 cardiac valve replacement has been performed in patients with carcinoid heart disease. However, it remains controversial whether biological valves are superior to artificial valves or vice versa [6,9-13]. Although comparative studies on artificial and biological valve replacement in tricuspid position did not show significant differences in the early postoperative outcome [9,10], hypothetical danger may exist regarding the affection of biological valves by the same process that initially affected the native valves. In addition, biological valve replacement is associated with accelerated degeneration leading to valvular dysfunction within 10–15 years after implantation. Connolly et al. speculated that somatostatin might have a positive effect on the outcome after bioprosthesis implantation due to its antagonistic mechanism against serotonin [6]. This hypothesis, however, is not supported by evidence in the literature. Moreover, biological valve prostheses are at risk of valve destruction by ongoing release of somatostation. McDonald et al. reported a case of biological tricuspid valve degeneration (Carpentier Edwards valve) four years after biological tricuspid valve replacement [8]. Ridker et al. reported on the implantation of a bioprosthesis in tricuspid position which showed leaflet thickening and typical carcinoid plaques after a eleven years period [11]. Ohri CARDIOVASCULAR SURGERY
JUNE 2002 VOL 10 NO 3
et al. reported on a case in which typical carcinoid plaques developed on the leaflets of a cryopreserved allograft three months after pulmonary valve replacement [12]. Controversially, Connolly et al. recommended the use of bioprostheses in the treatment of carcinoid heart disease in order to lower the risk ment [12]. Controversially, Connolly et al. recaddition to accompanying liver dysfunction [6]. This is indeed a reasonable argument for the use of biological heart valves. However, the frequent use of anticoagulation time determination by selftesting instruments helps to keep bleeding complications at a low risk after mechanical heart valve replacement. Based on our experience from this case and the sparse evidence from the literature we suggest heart valve replacement to be performed in patients with carcinoid heart disease at the onset of valvular dysfunction. Especially in young patients we believe the replacement of affected valves by artificial mechanical valves to be the treatment of choice. Warfarin intake increases the risk for acute hemorrhage, which can be minimized by frequently and accurately performed monitoring. To our knowledge this is the first report on a triple valve replacement involving the tricuspid, pulmonary and mitral valve in a patient suffering from carcinoid heart disease. Due to the short number of patients with carcinoid heart disease, clinical trails will be difficult to perform. Therefore, detailed singular reports on successful treatment strategies will help to successfully treat individual cases of carcinoid heart disease.
References 1. Basson, M. D., Ahlman, H. and Wangberg, B., Biology and management of the midgut carcinoid. Am J Surg, 1993, 165, 228–297. 2. Zeitels, J., Neunheim, K. and Kaplan, E. L., Carcinoid tumors: a 37-year experience. Arch Surg, 1982, 117, 732–737. 3. Kulke, M. H. and Mayer, R. J., Carcinoid tumors. N Engl J Med, 1999, 340(11), 858–868. 4. Pellikka, P. A., Tajik, A. J. and Khandheria, B. K., Carcinoid heart disease, Clinical and echocardiographic spectrum in 74 patients. Circulation, 1993, 87, 1188–1198. 5. Fischer, S., Kruger, M. and McRae, K., Giant bronchial carcinoid tumors: a multidisciplinary approach. Ann Thorac Surg, 2001, 71(1), 386–393. 6. Connolly, H. M., Nishimura, R. A. and Smith, H. C., Outcome of cardiac surgery for carcinoid heart disease. J Am Coll Cardiol, 1995, 25, 410–416. 7. Connolly, H. M., Schaff, H. V. and Nishimura, R. A., Cardiac surgery for carcinoid heart disease (abstract). Circulation, 1997, 96(Suppl I), I–507. 8. McDonald, M. L., Nagorney, D. M. and Connolly, H. M., Carcinoid and carcinoid syndrome: successful surgical treatment. Ann Thorac Surg, 199, 67, 537–539. 9. Lundin, L., Hansson, E. -E. and Landelius, J., Surgical treatment of carcinoid heart disease. J Thorac Cardiovasc Surg, 1990, 100, 552–561. 10. Knott-Craig, C. J., Schaff, H. V. and Mullany, C. J., Carcinoid disease of the heart, Surgical management of ten patients. J Thorac Cardiovasc Surg, 1992, 102, 475–481. 11. Ridker, P. M., Chertow, G. M. and Karlson, E. W., Biopros-
289
Triple valve replacement in a patient with severe carcinoid heart disease: M. Wilhelmi et al. thetic tricuspid valve stenosis associated with extensive plaque deposition in carcinoid heart disease. Am Heart J, 1991, 121, 1835–1838. 12. Ohri, S. K., Schofield, J. B. and Hodgson, H., Carcinoid heart disease: ealy failure of an allograft valve replacement. Ann Thorac Surg, 1994, 58, 1161–1163.
290
13. Ludin, L., Carcinoid heart disease. A cardiologist’s viewpoint. Acta Oncol, 1991, 30, 499–502. Paper accepted 14 November 2001
CARDIOVASCULAR SURGERY
JUNE 2002 VOL 10 NO 3