Abstract
Introduction
Primary benign right ventricular tumours are rare. They can cause significant mortality without appropriate and timely treatment. We investigated surgical treatment and survival characteristics for right ventricular tumours.
Materials and methods
From 2007 to 2017, 21 patients with primary benign right ventricular tumours who underwent tumour resection were retrospectively reviewed. Clinical findings and follow-up results were analysed.
Results
Thirteen men and eight women were enrolled, with a mean age of 42.3 ± 15.3 years. The most frequent histotypes were myxoma, haemangioma and papillary fibroelastoma. Eight patients underwent concomitant tricuspid valvuloplasty and one had tricuspid valve replacement. No major adverse events or death occurred during the perioperative period. One patient with haemangioma underwent partial tumour resection; however, the tumour regressed gradually during follow-up. Within the 10-year follow-up period (mean 4.8 ± 2.6 years), the recurrence-free and overall survival rates were 81.0% and 85.7%, respectively.
Conclusions
Tumour resection for primary benign right ventricular tumours is safe and effective, and has a good prognosis. Tricuspid valvuloplasty or tricuspid valve replacement may be necessary for the resection of right ventricular tumours to improve the haemodynamics. Haemangiomas naturally undergo spontaneous regression.
Keywords: Cardiac tumours, Surgery, Tricuspid valve, Follow-up
Introduction
Primary cardiac tumours are rare, and they have a high mortality.1,2 Surgical resection can lead to favourable results and long survival time. Cardiac tumours are mostly located in the left heart system, especially the left atrium; only 5% of tumours are located in the right ventricle.3,4 The few available papers on right ventricular tumours were mainly case reports. We therefore retrospectively analysed clinical data for 21 patients with primary benign right ventricular tumours in Fuwai Hospital, Beijing, to evaluate the surgical and prognostic characteristics.
Materials and methods
Patients
From 2007 to 2017, 30 patients underwent surgical resection of primary right ventricular tumours in Fuwai Hospital. Five paediatric patients and four patients with malignant or epicardial tumours were excluded, and the remaining 21 patients (13 men and 8 women) were enrolled. The study was approved by the Ethics Committee of Fuwai Hospital and the need for patient consent was waived.
Surgical methods
All tumour resections were performed via median sternotomy on cardiopulmonary bypass combined with anaesthesia, moderate (30–32 degrees C) systemic hypothermia and cardiac arrest. The details of the surgical technique were determined according to the location, size, mobility and myocardial infiltration of tumours. In this study, 11 patients (52.4%) were operated from the right atrium approach, with 7 (33.3%) from the right ventricular outflow tract; 2 patients from the right atrium plus pulmonary artery incisions and 1 from the right atrium, right ventricle plus pulmonary artery incisions. Heart tumours are so brittle that the manipulation should be as gentle as possible to avoid tumour ruptures and secondary embolic events. Patients were rewarmed and weaned from bypass without difficulty.
Data collection
Data were collected from the institutional database. Medical records were reviewed to obtain preoperative and postoperative variables, including the clinical complaints, New York Heart Association (NYHA) classification, cardiac imaging examination and operation time. After discharge, patients were followed up in clinic. Ischaemic events, recurrence, survival and other late complications from any cause were obtained. The end of follow-up was December 2018.
Statistical analysis
All data were stored using Microsoft Excel. Statistical analysis was performed using SPSS version 24. Continuous data were expressed as the mean plus or minus standard deviation. Categorical variables were expressed as numbers and percentages. Recurrence-free and overall survival rates were constructed according to the Kaplan–Meier method.
Results
Preoperative clinical features
Overall, the mean age at tumour diagnosis was 42.3 ± 15.3 years. The most common complaints were palpitations (n = 6, 28.6%), exertional dyspnoea (n = 5, 23.8%) and lower limb oedema (n = 4, 19.0%). However, six patients showed no obvious symptoms and were diagnosed by transthoracic echocardiography (TTE) due to auscultation findings when presenting for respiratory infection or during routine physical examination. Only one cerebral embolic event was present without peripheral or pulmonary embolism events, and approximately 71.4% (n = 15) of patients presented with NYHA I/II (Table 1).
Table 1.
Presenting characteristics of 21 patients
| Symptom | Patients | |
|---|---|---|
| (n) | (%) | |
| Asymptomatic | 6 | 28.6 |
| Obstruction cardiac: | ||
| Palpitations | 6 | 28.6 |
| Exertional dyspnoea | 5 | 23.8 |
| Lower limb oedema | 4 | 19.0 |
| Chest pain or discomfort | 2 | 9.5 |
| Dizziness/syncope | 1 | 4.8 |
| Constitutional: | ||
| Fever | 3 | 14.3 |
| Fatigue | 3 | 14.3 |
| Anaemia | 1 | 4.8 |
| Thromboembolism: | ||
| Cerebral | 1 | 4.8 |
| Pulmonary | 0 | |
| Peripheral | 0 | |
Preoperative examination
Patients underwent blood tests, electrocardiography and TTE, and results were within acceptable levels. The most common rhythm disturbance was right bundle branch block (n = 12, 57.1%), followed by ST segment changes in ten patients, and T wave changes in six patients. The majority of patients were diagnosed with TTE; however, computed tomography (CT; n =12, 57.1%) and magnetic resonance imaging (MRI; n = 12) were also used, with seven patients undergoing CT and MRI simultaneously to further distinguish benign and malignant neoplasms (Table 2).
Table 2.
Preoperative examination of 21 patients
| Examination | Patients | |
|---|---|---|
| (n) | (%) | |
| Electrocardiogram: | ||
| Right bundle branch block | 12 | 57.1 |
| ST segment change | 10 | 47.6 |
| T wave change | 6 | 28.6 |
| Tachycardia | 4 | 19.0 |
| Premature ventricular contraction | 2 | 9.5 |
| Atrial fibrillation | 2 | 9.5 |
| Bradycardia | 0 | |
| Transthoracic echocardiography: | ||
| Left ventricular ejection fraction | 65.6 ± 5.0 | |
| LVEDD (mm) | 44.5 ± 8.2 | |
| RVEDD (mm) | 24.7 ± 9.0 | |
| RVOTO | 11 | 52.4 |
| Tricuspid insufficiency | 8 | 38.1 |
| Aortic insufficiency | 1 | 4.8 |
| Mitral insufficiency | 0 | |
| Imaging: | ||
| Computed tomography | 12 | 57.1 |
| Magnetic resonance imaging | 12 | 57.1 |
LVEDD, left ventricular end diastolic dimension; RVEDD, right ventricular end diastolic dimension; RVOTO, right ventricular outflow tract obstruction
Intraoperative and postoperative conditions
Some 21 patients underwent cardiac tumour resection, including total tumour resection in 20 and partial resection in 1. Concomitant surgeries were present in 10 patients, including tricuspid valvuloplasty in 8, tricuspid valve replacement in 1 and coronary artery bypass grafting in 1. Four patients with moderate to severe tricuspid insufficiency underwent De Vega annuloplasty. In three other patients, the tricuspid valves were invaded by tumours, so the decision was made to resect the attachment of the tumour to the leaflet; the leaflet defects in two patients were sutured with 5–0 sutures, before the 32-mm Edwards MC3 tricuspid annuloplasty ring was inserted. The leaflet defect in another patient was closed with a patch of autologous pericardium and a subsequent De Vega annuloplasty was performed.
Reconstruction of the tricuspid valve with a bovine pericardial patch was performed in one patient. The tricuspid valve in another patient was extensively stretched and tethered by the tumour and was replaced by a 27-mm Medtronic MOSAIC III valve. Coronary artery bypass grafting was performed using left in-situ internal thoracic artery in a 67-year-old man because of an over 90% stenosis of the left anterior descending artery. The method of tricuspid valve surgery was comprehensively determined based on the tumour location, the degree of infiltration and damage to the tricuspid valve, and the structural change of the tricuspid annulus.
There were no early events, such as haemorrhage, acute kidney injury or cerebral stroke, and no deaths in the perioperative period. The mean time of surgery was 193.7 ± 54.0 minutes, with a cardiopulmonary bypass time of 85.5 ± 46.7 minutes and an aortic cross-clamp time of 56.6 ± 41.4 minutes (Table 3).
Table 3.
Operative characteristics of 21 patients
| Operative characteristics | Patients | |
|---|---|---|
| (n) | (%) | |
| Time: | ||
| Surgery (minutes) | 193.7 ± 54.0 | |
| CPB (minutes) | 85.5 ± 46.7 | |
| Cross-clamp (minutes) | 56.6 ± 41.4 | |
| Mechanical ventilation (hours) | 12.5 ± 4.6 | |
| Intensive care stay (hours) | 36.5 ± 23.6 | |
| Hospital stay (days) | 9.8 ± 3.4 | |
| Intraoperative blood loss (ml) | 537.6 ± 166.0 | |
| Resection: | ||
| Total | 20 | |
| Subtotal | 1 | |
| Concomitant surgery: | ||
| Tricuspid valvuloplasty | 8 | 38.1 |
| Tricuspid valve replacement | 1 | 4.8 |
| CABG | 1 | 4.8 |
| Surgical incision: | ||
| Right atrium | 11 | 52.4 |
| RVOT | 7 | 33.3 |
| RA + pulmonary artery | 2 | 9.5 |
| RA + RV + pulmonary artery | 1 | 4.8 |
CABG, coronary artery bypass grafting; RA, right atrium; RV, right ventricle; RVOT, right ventricular outflow tract; RV: Right ventricle
The common original positions were the right ventricular inflow tract (n = 6, 28.6%) and the right ventricular outflow tract (n = 6, 28.6%). Pathological examination of all specimens revealed that myxoma was the most frequent histotype (n = 10, 47.6%), followed by haemangioma (n = 4) and papillary fibroelastomas (n = 3; Table 4).
Table 4.
Tumour site and histotype of 21 patients
| Operative characteristics | Patients | |
|---|---|---|
| (n) | (%) | |
| Size (cm) | 6.0 ± 5.0 × 3.7 ± 3.2 | |
| Original site of tumour: | ||
| Right ventricular inflow tract | 6 | 28.6 |
| Right ventricular outflow tract | 6 | 28.6 |
| Right ventricular free wall | 2 | 9.5 |
| Tricuspid valve | 2 | 9.5 |
| Right ventricular septum | 1 | 4.8 |
| Right ventricular inflow tract + free wall | 1 | 4.8 |
| Right atrium + RVIT | 1 | 4.8 |
| Right atrium + RVIT + RVOT | 1 | 4.8 |
| Right atrium + Right ventricle + RVIT | 1 | 4.8 |
| Histotype: | ||
| Myxoma | 10 | 47.6 |
| Haemangioma | 4 | 19.0 |
| Papillary fibroelastoma | 3 | 14.3 |
| Fibroma | 2 | 9.5 |
| Rhabdomyoma | 1 | 4.8 |
| Lymphangioma | 1 | 4.8 |
RVIT, right ventricular inflow tract; RVOT, right ventricular outflow tract
Mild pleural and/or pericardial effusion occurred in 16 patients, while no patients required drainage. The pleural effusion disappeared, as confirmed by TTE and chest roentgenogram before discharge. No patients underwent low cardiac output syndrome, atrial fibrillation or wound infection after surgery.
Follow-up results
All patients were followed up by telephone or in clinic, with a mean follow-up time of 4.8 ± 2.6 years. No events, such as thromboembolism or pleural effusion, were found during follow-up. Furthermore, for a 21-year-old woman with haemangioma with partial tumour resection, the follow-up TTE showed that the tumour had gradually regressed. There were 18 patients who underwent TTE and electrocardiography at the most recent follow-up, which showed that the cardiac function and dimensions of patients were normal on discharge with no significant changes during follow-up. Over 50% of patients continued to have right bundle branch block; all had the condition before surgery and no new cases occurred. Two patients newly developed atrial fibrillation, with no new ST segment changes or T wave changes.
Survival analysis
Four patients who underwent complete resection showed recurrence during follow-up; one myxoma recurred at one year after surgery. A further myxoma recurred at 15 months after surgery. Two patients with fibromas had a recurrence at one month and two years after surgery, respectively (Supplementary Table 1, online only). The recurrence-free rate was 81.0% during long-term follow-up (Fig 1).
Figure 1.
Postoperative recurrence-free survival for resection of cardiac tumours
Three patients died during follow-up and all patients had tumour recurrence. One patient with myxoma died of tumour recurrence and low left ventricular ejection fraction related to left heart failure seven years after surgery. For two patients with fibroma, one died of tumour recurrence three years after resection and another died of sudden death at night six months after surgery, which indicated that patients with myxoma might have a better survival rate than non-myxoma patients. The overall survival rate was 85.7% during the 10-year follow-up (Fig 2). More details of the follow-up for 21 patients are shown in Supplementary Table 2 (online only).
Figure 2.
Kaplan–Meier post-surgery survival for resection of cardiac tumours
Discussion
Primary cardiac tumours are rare, with a reported prevalence of 1.38–30/100,000 people. Right ventricular tumours account for only approximately 5% of cardiac tumours.2,3,5 The current literature on treatment for right ventricular tumours is mostly case reports, so definitive statements are often inconclusive. We conducted this study to summarise surgical experience for primary benign right ventricular tumours.
The symptoms of primary cardiac tumours may vary according to tumour histotypes, location, size and haemodynamic conditions.6 Clinically, symptoms of cardiac tumours mainly involve three mechanisms: intracardiac obstruction, systemic embolisation of tumour fragments and constitutional symptoms by unclear mechanisms.5,7
In this study, 15 patients presented with fatigue, syncope and other right ventricular inflow or outflow tract symptoms, and four of them presented symptoms of right heart failure, such as lower limb oedema. However, only one patient presented with cerebral thromboembolism, which we thought might not be associated with the right-sided tumour. Compared with left heart system tumours, right heart system tumours are more likely to cause right bundle branch block, which may be related to tumour invasion and compression of the right bundle branch, as over 50% of patients presented with right bundle branch block in this study.
Haemangiomas are extremely rare benign cardiac tumours that occur most frequently in the ventricular septum and right ventricle; sometimes complete surgical excision may be difficult because of its vascular nature. In this report, a 21-year-old woman with haemangioma underwent subtotal tumour resection because of large volume (15×12cm) and massive infiltration of the myocardium, while a follow-up TTE showed that the tumour had gradually regressed.
TTE has a crucial role in achieving a proper diagnosis of cardiac tumours and mass characteristics, with the positive diagnosis rate reaching 77.78%. Thus, cardiac CT and MRI remain a second-level diagnostic examination to achieve a better definition of tumour location and relationship with surrounding structures, especially with the suspension of a malignant mass.8,9 In this study, patients were diagnosed with TTE, and 17 patients underwent CT or MRI to distinguish the benign and malignant tumours and to determine the invasion of surrounding structures. Compared with postoperative histopathological results, the combination of CT and MRI can lead to excellent accuracy in the distinction of benign or malignant neoplasms before surgery.10–13
Surgery can provide a good prognosis for benign cardiac tumours.14 In this study, we found that tumour resection could lead to a good prognosis, with no serious complications during the perioperative period and long-term follow-up. Within the 10-year follow-up period, four tumours recurred and the recurrence was all within two years, which means that patients with primary benign right ventricular tumours should be closely followed for a minimum of two years to evaluate tumour recurrence. The recurrence time is shorter than a previous study, which found tumour recurrence occurred mainly within four years after tumour resection.5 This may be a feature of primary benign right ventricular tumours or might be due to bias from limited cases.
There have been many hypotheses of the cause of tumour recurrence, mainly including tumour multifocality, intraoperative seeding, tumour cell polyploid mutation and malignancy transformation.15,16 In this series, all four recurrent tumours, including two myxomas and two fibromas, underwent total tumour resection and histological examination confirmed the tumour-free margin. Recurrence of two myxomas was potentially attributed to unrecognised multicentric origins of primary lesions or intraoperative dissemination of tumour cells. For two fibromas, it might have been very difficult not to leave small pieces of tumour behind because these tumours were integrated with and partly immersed in myocardia; however, recurrence is unusual, as has been reported by previous studies.17
Three patients died during the long-term follow-up; the recurrence-free and overall survival rates at 10 years were 81.0% and 85.7%, respectively, which indicates that positive surgical resection for primary benign ventricular tumours might be associated with excellent long-term survival.
Limitations
The limitations of this series include the retrospective nature of the analysis in a single institution with a limited number of cases. In addition, the long-term span, different surgeons and the progress of cardiopulmonary bypass techniques may have an impact on clinical outcomes. Despite these limitations, we believe this study provides insight into the surgical experience and long-term outcome of surgical resection.
Conclusions
Primary benign right ventricular tumours are rare, with no specific clinical features, and this study is a rare series report on this matter. TTE is the most commonly used imaging tool for evaluating cardiac tumours; the combination of CT and MRI can be helpful for the distinction of benign or malignant tumours. Tricuspid valvuloplasty or tricuspid valve replacement may be required for resection of right ventricular tumours to improve the haemodynamics. Haemangioma has a natural tendency of spontaneous regression or shrinkage. Surgical resection is safe and effective, and can provide excellent long-term survival for primary benign right ventricular tumours.
References
- 1.Burazor I, Aviel-Ronen S, Imazio M et al. Primary malignancies of the heart and pericardium. Clin Cardiol 2014; : 582–588. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Poterucha TJ, Kochav J, O’Connor DS, Rosner GF. Cardiac tumors: clinical presentation, diagnosis, and management. Curr Treat Options Oncol 2019; : 66. [DOI] [PubMed] [Google Scholar]
- 3.Lau C, Leonard JR, Schwann AN et al. A 20-year experience with resection of primary cardiac tumors and metastatic tumors of the heart. Ann Thorac Surg 2019; : 1126–1131. [DOI] [PubMed] [Google Scholar]
- 4.Habertheuer A, Andreas M, Wiedemann D et al. A rare case of obstructive right atrial lipoma. Ann R Coll Surg Engl 2014; : e39–e41. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Elbardissi A, Dearani J, Daly R et al. Survival after resection of primary cardiac tumors: a 48-year experience. Circulation 2008; : S7–15. [DOI] [PubMed] [Google Scholar]
- 6.Yanagawa B, Chan EY, Cusimano RJ, Reardon MJ. Approach to surgery for cardiac tumors: primary simple, primary complex, and secondary. Cardiol Clin 2019; : 525–531. [DOI] [PubMed] [Google Scholar]
- 7.Burke A, Jeudy J, Virmani R. Cardiac tumours: an update: cardiac tumours. Heart 2008; : 117–123. [DOI] [PubMed] [Google Scholar]
- 8.Kim EY, Choe YH, Sung K et al. Multidetector CT and MR imaging of cardiac tumors. Korean J Radiol 2009; : 164–175. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Lestuzzi C. Primary tumors of the heart. Curr Opin Cardiol 2016; : 593–598. [DOI] [PubMed] [Google Scholar]
- 10.Krumm P, Mangold S, Gatidis S et al. Clinical use of cardiac PET/MRI: current state-of-the-art and potential future applications. Jpn J Radiol 2018; : 313–323. [DOI] [PubMed] [Google Scholar]
- 11.Pazos-López P, Pozo E, Siqueira ME, et al. Value of CMR for the differential diagnosis of cardiac masses. JACC Cardiovasc Imaging 2014; : 896–905. [DOI] [PubMed] [Google Scholar]
- 12.Beroukhim RS, Prakash A, Buechel ER et al. Characterization of cardiac tumors in children by cardiovascular magnetic resonance imaging: a multicenter experience. J Am Coll Cardiol 2011; : 1044–1054. [DOI] [PubMed] [Google Scholar]
- 13.Yanagawa B, Mazine A, Chan EY et al. Surgery for tumors of the heart. Semin Thorac Cardiovasc Surg 2018; : 385–397. [DOI] [PubMed] [Google Scholar]
- 14.Li S, Gao C. Surgical experience of primary cardiac tumor: single-institution 23-year report. Med Sci Monit 2017; : 2111–2117. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Shinfeld A, Katsumata T, Westaby S. Recurrent cardiac myxoma: seeding or multifocal disease?. Ann Thorac Surg 1998; : 285–288. [DOI] [PubMed] [Google Scholar]
- 16.McCarthy PM, Schaff HV, Winkler HZ et al. Deoxyribonucleic acid ploidy pattern of cardiac myxomas: another predictor of biologically unusual myxomas. J Thorac Cardiovasc Surg 1989; : 1083–1086. [PubMed] [Google Scholar]
- 17.Karabinis A, Samanidis G, Khoury M et al. Clinical presentation and treatment of cardiac myxoma in 153 patients. Medicine 2018; : e12397. [DOI] [PMC free article] [PubMed] [Google Scholar]