Right atrial metastasis after renal cell carcinoma operation: a case report

Introduction

Clear cell renal cell carcinoma (ccRCC) is a heterogeneous malignancy derived from renal tubular epithelial cells, accounting for 60–75% of all renal cell carcinomas. In recent years, the incidence of ccRCC has increased significantly. At the time of first clinical diagnosis, about 15% of patients are found to have distant metastases. Treatment options for patients with high-risk metastatic clear cell renal cell carcinoma (mccRCC) mainly include immune checkpoint inhibitors and tyrosine kinase inhibitors (TKIs) (1). Common metastases include the lungs, bones, and liver, whereas cardiac metastases are rare, there are no precise guidelines to follow, and the presentation and treatment of these patients are rarely reported. In this study, we report the case of a patient with ccRCC that had metastasized to the lungs, right thigh muscle, and heart who was treated in our department. The clinical features, related characteristics, pathogenesis, and treatment strategies were analyzed to provide a reference for the diagnosis and treatment of cardiac metastatic tumors. We present this case in accordance with the CARE reporting checklist (available at https://acr.amegroups.com/article/view/10.21037/acr-24-258/rc).

Case presentation

The patient was a 51-year-old woman who underwent right laparoscopic radical nephrectomy under general anesthesia at Northern Jiangsu People’s Hospital Affiliated to Yangzhou University in 2018. The operation was uneventful. The postoperative pathology report showed that ccRCC (grades I–II) was found in the right kidney. No adjuvant treatment was utilized. The patient was followed with surveillance imaging postoperatively. In January 2022, the patient developed symptoms including loss of appetite, fatigue, and weight loss. A chest computed tomography (CT) examination on 26 January 2022 showed multiple nodules in both lungs, raising the possibility of tumor metastasis. A positron emission tomography (PET)-CT scan showed the following: After the operation for right renal carcinoma, the soft tissue mass in the intermuscular space of the right thigh presented an abnormal increase in fluorodeoxyglucose (FDG) metabolism, multiple pulmonary nodules with slight abnormal increases in FDG metabolism, bilateral pleural effusion, and pericardial effusion. The possibility of malignant lesions was considered. Magnetic resonance imaging (MRI) of the lower extremities showed enhancing nodules in the bone marrow cavity of the upper femur on the right, and a mass in the muscle and soft tissue of the medial thigh was also observed on the right side. A clinical diagnosis was made of multiple metastases of kidney cancer.

Since January 29, the patient received immunotherapy with sintilimab (200 mg IVGTT. q3w, d1) in combination with sunitinib-targeted therapy (50 mg qd, p.o. take the drug for 4 weeks and stop the drug for 2 weeks) for a cycle, and an ultrasound-guided biopsy was performed on February 7, 2022. Based on the pathological results of the right thigh combined with hematoxylin and eosin (HE), immunohistochemistry, and previous medical history, a diagnosis of metastatic ccRCC was made (Figure 1). The patient had no family history of tumor-related genetics, and had no history of diabetes, coronary artery diseases, hypertension, hepatitis, drug allergy, previous trauma, or operation (2).

Figure 1 Immunohistochemistry and pathology: tumor cells cKpan (focal area +), Vimentin (+), Smae 100 (−), CK7 (−), EMA (+), E-cadherin (focal area +), CD10 (+), CD117 (−), Ki67 (about 50% +), RCC (−). Diagnostic conclusion: (right thigh) combined with HE, immunohistochemistry, and the previous medical history, a diagnosis of metastatic clear cell renal cell carcinoma was made. Magnification (from left to right): 200×, 200×. RCC, renal cell carcinoma; HE, hematoxylin and eosin.

In February 2022, the patient experienced sudden neck swelling with purple lips. Pulmonary artery computed tomography angiography (CTA) revealed a filling defect in the right atrium, suggestive of an embolism. Cardiac color Doppler ultrasound revealed a 40 mm × 48 mm solid medium echo in the right atrium, which was relatively fixed and blocked the entrance of the superior vena cava. The right atrium was found to house a mass pending further investigation (Figure 2A,2B). A surgical biopsy was performed to determine whether the mass was a secondary tumor or a kidney cancer metastasis. The patient was transferred to the Cardiovascular Center on the same day for cardiac tumor resection and atrial reconstruction. The patient’s cardiopulmonary function was poor, and the operation was difficult; it was necessary to establish a cardiopulmonary bypass and closely monitor the patient’s blood pressure and heart rhythm. Through the median incision of the sternum into the chest, the “human” shape cuts the heart bag, revealing the heart. During intracardiac exploration, a 5 cm × 6 cm × 8 cm solid mass was observed in the right atrium that invaded the atrial septum, left atrial roof, atrial septum, and superior vena cava, and blocked the superior vena cava. Further, the tricuspid annulus was enlarged by greater than three fingers width, with moderate-to-severe insufficiency. Cardiopulmonary bypass was rotated for 77 minutes, and the ascending aorta was blocked for 59 minutes. The results of postoperative pathology and immunohistochemistry indicated mccRCC in the heart (Figure 3). The patient’s tumor stage was rTxN0M1, stage IV. The patient’s superior vena cava occlusion was relieved, and she recovered well after surgery. After the operation, the patient was discharged on the 10^th day after surgery. Follow-up examination showed that the patient developed lung infection 2 weeks later, and the symptoms improved after treatment with antibiotics, anticoagulation, and nutritional support in the local hospital. The results of follow-up showed that the patient survived for 6 months after surgery (Figure 4).

Figure 2 Cardiac color Doppler ultrasound revealed a 40 mm × 48 mm solid moderate echo in the right atrium, and the position was relatively fixed and blocked the entrance of the superior vena cava. The thicknesses of the interventricular septum and ventricular wall were normal, and the activity of each segment of the interventricular septum and left ventricular wall was not coordinated. The echo and shape of each valve were normal, and the activity was normal.

Figure 3 Postoperative pathological and immunohistochemical considerations: (heart) HE combined with immunohistochemical results, medical history, diagnosis, and metastatic clear cell renal cells. Postoperative pathology: tumor cells cKpan (partial area +), S100 (−), P16 (−), Desmin (soil), SMA (−), Myogenin (−), MyoD1 (−), H-caldesmon (−), SOX10 (−), Ki67 (about 80% +), Vimentin (+), CD68 (+), CDB4 (−), Pax-8 (+), CA9 (±), RCC (−), CD10 (+). Magnification (from left to right): 200×, 200×. HE, hematoxylin and eosin; SMA, smooth muscle actin; RCC, renal cell carcinoma.

Figure 4 Timeline. PET, positron emission tomography; CT, computed tomography; CTA, computed tomography angiography.

All procedures performed in this study were in accordance with the ethical standards of the institutional and/or national research committee(s) and with the Helsinki Declaration (as revised in 2013). Written informed consent for publication of this case report and accompanying images was not obtained from the patient or the relatives after all possible attempts were made.

International Multidisciplinary Team (iMDT) discussion

Opinions from Department of Oncology, Northern Jiangsu People’s Hospital Affiliated to Yangzhou University

Most cardiac metastases occur in patients aged 50–70 years and are not significantly related to gender (3). The most common origin of cardiac metastases are primary cancers of the lungs, breast, and lymph glands, whereas cardiac metastases originating from renal cell carcinoma are rare (4). Although 10–25% of patients with renal cell carcinoma may have metastases, the symptoms of cardiac metastases are less pronounced than those of other distant organs, and clinical diagnosis remains difficult (5). It is important to note that single cardiac metastases of the primary tumor are rare and usually occur after multiple metastases. The main routes of cardiac metastasis include the following: (I) hematogenous dissemination, often involving myocardium and endocardium, seen in the metastasis of malignant melanoma, lymphoma, and sarcoma; (II) lymphatic metastasis, often involving the pericardium and epicardium, commonly seen in lung cancer metastasis; (III) spread along the vein to the heart chamber, commonly found in renal cell carcinoma, hepatocellular carcinoma, uterine leiomyoma and pheochromocytoma; (IV) direct invasion: seen in mediastinum, pleural tumors, and breast cancer (6).

Regular postoperative follow-up is necessary for patients with cancer, and for patients with suspected cardiac metastases, echocardiogram can be used to determine whether patients with malignant tumors have cardiac metastases (7). When it comes to imaging, color Doppler echocardiography can quickly and easily show the location, size, and shape of heart tumors. Echocardiography in this patient clearly showed the space occupied by the superior vena cava and right atrial inflow tract. In this case, the patient with heart metastasis of kidney cancer was in an advanced stage and had a strong desire for treatment, but it still progressed after immunotherapy (8), the patient’s vital signs are unstable at the time of onset, so she was treated with cardiac surgery. There have been cases showing an association between cardiac metastasis and VHL V165G mutation, and further genomic mutation screening of cardiac metastasis cases may provide new findings (9).

In cardiac metastases, although endocardial and intracardiac involvement is rare and accounts for only 5% of cardiac metastases, it can have serious consequences due to obstruction or embolism. Right atrial tumors have a variety of clinical manifestations, such as syncope, pulmonary embolism, and even acute heart failure, mainly due to tumor size and obstruction (10). In this case, after multiple tumor metastases, the tumor cells were located in the inferior vena cava and extended to the right atrium, resulting in circulatory obstruction with corresponding signs of ischemia and hypoxia (11).

Surgery remains the most common treatment for patients with primary tumors and heart metastases. Surgery can reduce tumor burden, alleviate tumor mass effect, alleviate symptoms, and improve quality of life (12). Cardiac tumor resection, cardiopulmonary bypass, and complete resection of the tumor are required during left and right atrial reconstruction, including invasion of the right atrium, atrial septum, left roof, and superior vena cava, and reconstruction of the left atrium, atrial septum, and right side with bovine pericardium. After surgery, the patient’s fluid and electrolyte balance should be ensured, and the patient should be extubated as soon as possible after the vital signs stabilize. Various antiarrhythmic drugs are routinely used after surgery. In some cases, for patients that are stable from a cardiovascular standpoint, patients can be managed with systemic therapy alone (2).

The postoperative survival of cardiac metastatic malignancy is affected by various factors such as the patient’s age, tumor source, tumor burden, and underlying diseases. Complications that may occur after cardiac tumor surgery include: sudden death, infection, arrhythmia, pericardial effusion, heart failure, recurrence of embolism, tumor recurrence, etc., pulmonary infection occurs after cardiac surgery, considering that it is related to the patient’s advanced lung metastasis, and the patient’s postoperative immune function is poor, B-type natriuretic peptide (BNP), myocardial injury markers, infection markers, coagulation and bedside electrocardiogram, chest CT and other related examinations should be regularly reviewed after surgery, and the patient’s vital signs and mediastinum and pericardial drainage tube drainage should be closely monitored, and anti-infection and anticoagulation should be continued, nutritional support and other treatments, maintain fluid and electrolyte balance, and strengthen postoperative management.

The disadvantages of this case are that the patient did not undergo genetic testing, regular follow-up examinations were not timely, the disease progressed suddenly, and the postoperative evaluation was insufficient.

Opinions from the international experts on questions related to the diagnosis and treatment of this patient

What are the best prevention for cardiac metastases?

Expert opinion 1: cardiac metastases from renal cell carcinoma represent a rare clinical entity (13). Cardiac tumors originating from renal cell carcinoma may present as synchronous or metachronous disease. While there is not much that can prevent synchronous cardiac metastasis, adjuvant therapy following primary tumor resection could presumably prevent the development of metachronous cardiac metastasis following surgical resection of renal cell carcinoma.

KEYNOTE-564 involved (14,15) administering pembrolizumab or placebo to patients with clear-cell renal-cell carcinoma who were at high risk for recurrence after surgery. Patients were randomly assigned in a 1:1 ratio to receive either pembrolizumab at a dose of 200 mg or a placebo. These treatments were given intravenously every 3 weeks for up to 17 cycles (approximately 1 year), or until disease recurrence, unacceptable toxicity, or withdrawal of consent. The study aimed to assess the efficacy of pembrolizumab in improving disease-free survival and overall survival compared to the placebo.

KEYNOTE-564 trial demonstrated that pembrolizumab provided a significant improvement in survival outcomes for renal-cell carcinoma patients. The hazard ratio (HR) for recurrence or death was 0.72 [95% confidence interval (CI): 0.59 to 0.87], indicating a 28% reduction in the risk of recurrence or death compared to placebo. Additionally, the hazard ratio for death was 0.62 (95% CI: 0.44 to 0.87), showing a 38% reduction in the risk of death with pembrolizumab compared to placebo. These hazard ratios underline the strong survival benefits of pembrolizumab in this setting.

In the KEYNOTE-564 trial, pembrolizumab was associated with a higher incidence of toxicities compared to placebo. Serious adverse events of any cause occurred in 20.7% of patients in the pembrolizumab group, compared to 11.5% in the placebo group. Grade 3 or 4 adverse events related to treatment were significantly higher in the pembrolizumab group, affecting 18.6% of patients, compared to just 1.2% in the placebo group.

The most common immune-mediated adverse events and infusion reactions in the pembrolizumab group included hypothyroidism, pneumonitis, and colitis, among others, and these occurred in 36.5% of patients compared to 7.3% in the placebo group. Despite the higher incidence of toxicities, there were no treatment-related deaths in the pembrolizumab group, indicating a manageable safety profile for most patients.

Expert opinion 2: an evaluation of changes at the molecular level can be derived by comparing preoperative immunohistochemistry of the primary RCC tumor and pathological immunohistochemistry after cardiac metastasis. First, an understanding of the most relevant markers present in the immunohistochemistry of the primary RCC tumor is important. These include PAX2 and PAX8, which are renal transcription factors that are present in both normal renal parenchyma and neoplasms. As a result, these markers are usually the standard determinant of metastasis stemming from renal lineage. For determination of specific RCC subtype, carbonic anhydrase IX (CA9), a transmembrane protein, is often identified on immunohistochemistry as it is usually only positive in ccRCC. Vimentin, CD10 glycoprotein and epithelial membrane antigen (EMA) will also stain positive in cases of ccRCC (16). When compared to primary tumor immunohistochemistry, pathological immunohistochemistry of cardiac metastasis may overall demonstrate relative de-differentiation. Specifically, PAX8 and CD10 expression can be decreased in metastatic disease compared to primary RCC. Furthermore, pathological immunohistochemistry after cardiac metastasis may demonstrate increased expression of EZH2 and programmed death-ligand 1 (PD-L1) that allow for tumor adaptation and proliferation in the metastatic microenvironment (17).

This case involved a patient whose initial disease was suspected to be a localized renal mass consistent with RCC, which typically holds favorable prognosis after radical nephrectomy—especially with negative ureteral margins. While it is difficult to predict metastasis of RCC, especially to less common locations such as the heart or thigh muscle, the optimal prevention strategy to detect potential disease recurrence is consistent surveillance imaging after initial radical nephrectomy. For this patient who was determined to have grade II ccRCC, National Comprehensive Cancer Network (NCCN) guidelines recommend surveillance imaging with either abdominal CT or MRI every 6 months for the first 2 years postoperatively then annually for at least 5 years (18). Ideally, following this guideline will identify recurrence prior to life-threatening clinical presentations, however, patient-based circumstances could always prevent adherence to optimal follow-up.

If the tumor metastasizes to the heart, what is the best treatment strategy?

Expert opinion 1: treatment for cardiac metastasis from renal cell carcinoma (RCC) is complex and not well-established due to the rarity of the condition (14,19). Some key points include:

Systemic therapy: immunotherapy using agents like nivolumab (anti-PD-1) and ipilimumab (anti-CTLA-4) has shown promise, although these therapies have not been specifically tested in cardiac metastases. A combination of immunotherapy and targeted therapy with TKIs can also be effective, though TKIs pose risks of cardiotoxicity, complicating treatment decisions.

Metastasectomy: surgical resection of cardiac metastasis may be an option if the metastasis is isolated and surgically accessible. However, many patients are not candidates for surgery due to the tumor’s location or underlying conditions. Metastasectomy may be more appealing in the setting of hemodynamic sequelae from a cardiac metastasis.

Angiointerventional techniques: limited reports on the utility of angiointerventional techniques for cardiac tumors exist and can be utilized in selected settings, particularly with hemodynamic compromise in patients that are not good candidates for surgery (19).

Radiation therapy: while the data surrounding the use of radiation therapy for cardiac metastases is unavailable, stereotactic ablative radiotherapy could also be an option in an effort to avoid progression when other options are not available (20).

Expert opinion 2: as cardiac involvement is a rare presentation of metastatic RCC, there does not currently exist a universally standardized treatment approach. With a 1-year survival rate estimated below 30%, metastatic RCC has shown resistance to several modalities of systemic therapy (21). Certain tyrosine kinase inhibitors such as sunitinib have demonstrated potential efficacy in prevention of progression of RCC metastasis to the heart (22). More recent investigation has also outlined a role for immunotherapy, specifically a combination of nivolumab (targeting PD-1) and ipilimumab (targeting CTLA-4), as demonstrating long-term disease response (23). This patient was initially managed with sunitinib and PD-1 immunotherapy (sintilimab) after right thigh biopsy confirmed metastatic RCC. The role of surgery in this treatment pathway depends on the patient’s clinical condition. If the patient is otherwise stable and asymptomatic, then likely neoadjuvant treatment with systemic therapies should precede cardiac surgery. However, if the patient is clinically unstable, as in this case, cardiac surgery may need to be performed upfront to provide the best outcome, if technically feasible.

How should the patient be managed after surgery?

Expert opinion 1: systemic therapy with an immune checkpoint inhibitor +/− targeted therapy would be appropriate for this patient after surgery.

Expert opinion 2: if cardiac surgery is performed for cardiac metastasis from primary RCC, their management after surgery must be multidisciplinary. This should involve a collaborative follow-up plan involving medical oncology, urology, cardiology, and cardiovascular surgery, as there is no standardized algorithm for patients in these clinical situations (24). From an oncologic perspective, the patient should be evaluated as to whether they are a candidate for adjuvant therapy with one of the systemic agents to prevent further recurrence. From a urologic perspective, surveillance abdominopelvic imaging should likely be continued at least every 6 months following surgical intervention for cardiac metastasis. From a cardiac perspective, the patient should likely be followed with close monitoring of cardiac function as deemed appropriate with serial electrocardiograms and transthoracic echocardiography. Again, post-surgical management for patients with these novel presentations of metastatic RCC must be individually catered on a case-by-case basis.

Conclusions

This case study shows the rare clinical manifestations of cardiac metastasis from ccRCC. The tumor may metastasize to the heart through blood circulation, lymphatic metastasis, and venous spread, causing serious consequences. Doppler echocardiography is an effective means of detecting cardiac metastasis at an early stage. For patients who have hemodynamic sequelae of their cardiac metastases, surgical treatment is favored. Early detection and treatment are the key to prolonging the survival of patients with cardiac metastasis from tumors.

Acknowledgments

Funding: None.

Footnote

Reporting Checklist: The authors have completed the CARE reporting checklist. Available at https://acr.amegroups.com/article/view/10.21037/acr-24-258/rc

Peer Review File: Available at https://acr.amegroups.com/article/view/10.21037/acr-24-258/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://acr.amegroups.com/article/view/10.21037/acr-24-258/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. All procedures performed in this study were in accordance with the ethical standards of the institutional and/or national research committee(s) and with the Helsinki Declaration (as revised in 2013). Written informed consent for publication of this case report and accompanying images was not obtained from the patient or the relatives after all possible attempts were made.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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