Right Atrium Tumor Extension Through the Inferior Vena Cava. Considerations About Nine Cases Operated Under Cardiopulmonary Bypass

Introduction Adrenocortical and renal cell carcinomas rarely invade the right atrium (RA). These neoplasms need surgical treatment, are very aggressive and have poor prognostic and surgical outcomes. Case series We present a retrospective cohort of nine cases of RA invasion through the inferior vena cava (four adrenocortical carcinomas and five renal cell carcinomas). Over 13 years (2002-2014), nine patients were operated in collaboration with the team of urologists. Surgery was possible in all patients with different degrees of technical difficulty. All patients were operated considering the imaging examinations with the aid of CPB. In all reported cases (renal or suprarenal), the decision to use CPB with deep hypothermic circulatory arrest (DHCA) on surgical strategy was decided by the team of urological and cardiac surgeons. Conclusion Data retrospectively collected from patients of public hospitals reaffirm: 1) Low incidence with small published series; 2) The selected cases did not represent the whole historical casuistry of the hospital, since they were selected after the adoption of electronic documentation; 3) Demographic data and references reported in the literature were presented as tables to avoid wordiness; 4) The series highlights the propensity to invade the venous system; 5) Possible surgical treatment with the aid of CPB in collaboration with the urology team; 6) CPB with DHCA is a safe and reliable option; 7) Poor prognosis with disappointing late results, even considering the adverse effects of CPB on cancer prognosis are expected but not confirmed.


INTRODUCTION
Adrenocortical carcinoma (ACC) and renal cell carcinoma (RCC) are aware malignancies that occasionally present extending into the right atrium (RA) through the inferior vena cava. Patients can present with a variety of signs and symptoms, depending on the extent of the tumor. These neoplasms demand surgical treatment, are very aggressive and have poor prognosis and surgical outcomes. Therefore, this unusual pathological situation has to be in mind of the "heart team". The discovery of a mass in the right atrium obliges the clinician to perform a broad differential diagnosis between a primary cardiac tumor (myxoma being the most frequent), invasion of an extracardiac tumor, vegetations on the tricuspid valve and atrial thrombus. Tumor extension with vena cava thrombosis is a relatively frequent complication of renal carcinoma, but only exceptionally reaches the right atrium. It is also exceptional that this was a chance finding in an asymptomatic patient [1] .
As an overview, Castro-Dominguez et al. [2] stated that ACC is a highly aggressive malignant neoplasm with an incidence rate of 1 to 2 cases per million people per year. Overall 5-year survival is poor, ranging from 15 to 44% in reported series. Multimodality imaging with echocardiogram, computed tomography (CT), positron emission tomography (PET) and magnetic resonance imaging (MRI) aids not only in establishing the diagnosis but also in anatomic evaluation to determine the best surgical approach [2] .
According to Locali et al., based on a series of 14 cases, these tumors are routine in urological surgery. But they are important in the context of cardiovascular surgery due to possible complications with intracaval and/or intracardiac thrombi. Studies in this area, however, are mostly case reports or case series with small sample numbers. Due mainly to the rarity of this complication, few studies have been performed with larger case numbers, providing reliable conclusions [3] .
Therefore, the objective of this presentation was based on the relative scarcity of reported cases, presenting nine cases of RA invasion through the inferior vena cava (four adrenocortical and five renal tumors) performed over 13 years.

Cases Series
Over 13 years (2002-2014), nine patients were operated in collaboration with the team of urologists. The patients were allocated into 2 groups presented in Table 1.
Patients were operated on mainly considering imaging CT scans that were good enough for tumor observations ( Figure 3).
In all reported cases (renal or suprarenal), the use of CPB with deep hypothermic circulatory arrest (DHCA) and the surgical strategy were decided by the team of urological and cardiac surgeons. In summary, through a modified chevron incision, starting two fingerbreadths below the right costal margin and extending laterally to the midaxillary line, the kidney was exposed and mobilized laterally and posteriorly, the perirenal collateral circulation and the renal artery were ligated. Infrarenal inferior vena cava (IVC) and the contralateral renal vein were dissected. Liver mobilization, when necessary, was performed. After the abdominal step, a median sternotomy was performed, the pericardium was opened, CPB was installed and DHCA was carried out (Figure 1).
Only once the aorta was clamped for infusion of cardioplegia in a patient who had a mild coronary lesion. In other cases, induced ventricular fibrillation was expected, always maintaining good drainage of the left chambers. After CPB, the IVC was   incised from the liver border to the renal vein and the tumor was removed in block. After tumor removal, saline was injected to wash the proximal region of the IVC, low flow CPB was carried out, and body rewarming according to the total circulatory arrest protocol. When necessary, polytetrafluoroethylene (PTFE) or bovine pericardium patches were used for the IVC reconstruction. Histological samples are presented in Figure 4, confirming the diagnosis.  [8] presented a case that seems to be the 8 th case report of left adrenocortical cancer with tumor thrombus extension into IVC and right atrium. More recently, Castro-Dominguez et al. [2] reported one case of a large ACC with extension to the IVC and right atrium (RA). Our nine cases will be added to the medical literature without changing the low incidence paradigm with small published series, because they do not represent the whole historical casuistry of the hospital, since they are chosen after the adoption of electronic documentation.
DHCA is the most commonly used method and allows complete tumor resection without increasing operative risk. The cardiothoracic team, considering the unusual situation, opted for routine cardiac surgeries (median sternotomy, careful venae

DISCUSSION
As already mentioned, adrenocortical carcinomas and renal cell carcinomas (RCC) are rare malignancies. According to Spanish data, collected between early 1975 and April 1997, among 212 patients who underwent surgery for RCC, only 2 cases showed right atrial extension [5] . Among the metastatic tumors of the heart, those arising from the genitourinary system are amongst the most common [6] . Most of the case reports references were presented in Table 2.
Patients can present with a variety of signs and symptoms, depending on the extent of the tumor. CT scan of chest and abdomen represents the gold standard in ACC staging, while magnetic resonance imaging (MRI) is preferred for tumor thrombus characterization. Complete surgical resection is the only curative option for localized disease. Kidney-sparing surgery should be performed when possible. Hedican and Marshall [7]

A B
About the possible influence of the type of neoplasia, we did not find any publications directly correlating the type of neoplasia with possible dissemination caused or favored by CPB. In other words, it cannot be said that a particular kind of cancer is more susceptible to propagation by CPB. The application of CPB in oncologic patients is still controversial, with the possible disadvantages of hematogenous dissemination of tumor cells. There are two possible mechanisms through which CPB might contribute to the hematogenous dissemination of tumor cells. First, tumor cells contaminated in the blood reservoir might spread through the arterial cannula. Second, the CPB homeostasis imbalance may contribute to the dissemination of neoplastic cells preoperatively suppressed by the host defense system. Finally, further research is needed to know whether the transient immunosuppression associated with CPB can promote the spread and growth of pre- Table 2. Selected references. existing cancer cells. However, adverse effects of CPB on cancer prognosis are expected but have not been confirmed [11,12] .

CONCLUSION
The present data retrospectively collected from public hospital patients reaffirm: 1) Low incidence with small published series; 2) The selected cases did not represent the whole historical casuistry of the hospital, since they are selected after the adoption of electronic documentation; 3) Demographic data and references reported in the literature were presented as tables to avoid wordiness; 4) The series highlights the propensity to invade the venous system; 5) Possible surgical treatment with the aid of CPB in collaboration with the urology team; 6) CPB with DHCA is a safe and reliable option; 7) Poor prognosis with disappointing late results, even considering that adverse effects of CPB on cancer prognosis are expected but have not been confirmed.

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FC STJ SB RBR AJR WVAV PRBE Acquisition, analysis, or interpretation of data for the work; final approval of the version to be published Acquisition, analysis, or interpretation of data for the work; final approval of the version to be published Acquisition, analysis, or interpretation of data for the work; final approval of the version to be published Acquisition, analysis, or interpretation of data for the work; final approval of the version to be published Substantial contributions to the conception or design of the work; final approval of the version to be published Substantial contributions to the conception or design of the work; final approval of the version to be published Substantial contributions to the conception or design of the work; or the acquisition, analysis, or interpretation of data for the work; drafting the work or revising it critically for important intellectual contente; final approval of the version to be published