The 10 Commandments for Minimally Invasive Removal of Nonmalignant Intracardiac Tumors

Introduction

Intracardiac tumors, although rare,^1,2 represent a distinctive subset of cardiac pathology. These tumors are observed at a rate of 0.001% to 0.03%^1,2 at autopsy, and about 80% of them are benign tumors with myxomas, accounting for more than 50% of this group. Nonmalignant intracardiac tumors, such as myxomas, lipomas, fibromas, and papillary fibroelastomas, are often discovered incidentally during cardiac imaging or due to related nonspecific symptoms. These tumors, although typically benign, can have adverse secondary effects on cardiac function or downstream consequences such as stroke or limb ischemia. Therefore, surgical removal is often warranted. Traditionally, a full sternotomy approach has been the standard method for intracardiac tumor removal. However, it is invasive and associated with considerable increased invasiveness and morbidity for what is usually a low-risk procedure in relatively young patients. Removal of benign intracardiac tumors is ideally suited for a minimally invasive approach due to their potential for reduced morbidity, shorter hospital lengths of stay, improved cosmetic outcomes, and earlier return to work. This article aims to provide a comprehensive overview of minimally invasive removal of nonmalignant intracardiac tumors, covering the entire spectrum from diagnosis to a comprehensive review of various minimally invasive surgical techniques. In this article, we review the minimally invasive approaches to intracardiac tumors.

Commandment 1: Comprehensive Preoperative Planning

A comprehensive medical history and physical examination is paramount to determine the diagnosis, approach, and overall patient risk. Patients often present with symptoms such as chest pain, dyspnea, or palpitations, which can be attributed to the tumor’s effect on cardiac function and in more ominous cases with syncope or stroke. A thorough history is important as it may help in narrowing the differential diagnosis of a recently found intracardiac mass. A history of malignancies or family history of intracardiac tumors may hint at either a malignant process or the possibility of Carney syndrome. Physical examination looking for evidence of changes in skin pigmentation or skin myxomas should be performed on all patients found to have an intracardiac mass.

Diagnostic testing includes transthoracic echocardiography (TTE), transesophageal echocardiogram (TEE), cardiac computed tomography (CT) scan, cardiac magnetic resonance imaging (MRI), and potentially a positron emission tomography (PET) scan, to determine the size, location, and characteristics of the tumor. More importantly, it can determine if the intracardiac tumor is as a result of an extracardiac mass with cardiac extension. Examples of such tumors include lung cancer, hepatic cancers, caval tumors, and uterine tumors. The management of these lesions differs from that of nonmalignant intracardiac tumors and will not be discussed in this article.

It is critical to determine tumor characterization. Determining if the tumor is benign or malignant, its exact location, and whether it has invaded nearby structures is important as these factors will determine treatment strategies and surgical approach. TTE is often the first-line imaging modality for diagnosing intracardiac masses. It provides the surgical team with important tumor characteristics and helps guide the surgical procedure required, including the surgical approach.

Cardiac CT and MRI are valuable imaging modalities for diagnosing intracardiac tumors. They are particularly helpful for detecting the extent of tumor invasion and its relationship to other cardiac structures. Surgical approach may vary depending on CT findings. The values of a CT scan extend beyond tumor characteristics, but it is required for preoperative planning for minimally invasive approaches. The surgical team needs to assess arterial and venous access as well as the pleural space for a safe entry. PET scan, although rarely needed, may be useful for differentiating between benign and malignant intracardiac tumors in those cases in which the diagnosis remains uncertain.

Multidisciplinary consultation may go beyond the customary cardiothoracic surgeon and cardiologist interaction and may necessitate the collaboration of oncology and radiology to further understand the nature of the lesion and the treatment plan, which may also help determine the appropriate surgical approach.

The most common benign intracardiac mass is a myxoma. Although histologically benign, it may be lethal in some cases due to embolization or valve obstruction. Patients with smooth tumors without obstructive symptoms may wait for elective surgery, whereas villous myxomas entail a high embolic risk and require prompt surgical treatment. Although this fact should not affect the surgical approach, it is possible due to lack of robotic platform availability that a nonrobotic approach may be required. The team should never delay care for a surgical approach and add potential risk of complication to our patients.

While most benign tumors are not infiltrative, invasive cardiac lipomas can invade adjacent structures. The diagnosis of invasive cardiac lipomas is challenging, and a high degree of suspicion is required. In some cases, a biopsy may be necessary to confirm the diagnosis. Invasive cardiac lipoma is a rare, benign tumor that originates from adipose tissue and can develop within the heart. Imaging is crucial, with CT and MRI helping establish the diagnosis.^3–5 The density of the cardiac lipomas is similar to that of subcutaneous fat, although unlikely, and liposarcoma must be ruled out. In some cases, a biopsy may be necessary to confirm the diagnosis. Although benign, these tumors can pose significant clinical challenges due to their infiltration to adjacent structures.

Intracardiac tumor biopsy may be required in some elective cases to rule out malignancy prior to operative planning. The extent of resection may change upon histopathological result of the tumor. Biopsy should be performed on most undetermined tumors of the right cardiac chambers and very selectively for left chamber masses.

The significance of diagnostic modalities cannot be understated, as they guide the selection of treatment strategies and surgical approach and provide valuable insight about the nature and extent of intracardiac tumors.

Commandment 2: Choosing the Right Approach

Today, patient and referring physician preferences for less invasive approaches drive where patients are referred and who performs the surgical resection. The approaches available for intracardiac tumor resection include the partial sternotomy/ministernotomy whether upper or lower, the minithoracotomy, video-assisted thoracotomy (VATS), and the robotic approach (minithoracotomy or total endoscopic; Fig. 1). ⁶

Fig. 1.

Minimally invasive approaches to intracardiac tumor resection. (a) Full sternotomy, (b) partial upper sternotomy, (c) right minithoracotomy, (d) robotically assisted approach. Reprinted under the STM Permissions Guidelines from Innovations, Volume 15, Issue 1, Gillinov et al., “The 10 Commandments for Mitral Valve Repair,” Copyright 2019. ⁶

Choosing which approach will come down to the tumor characteristics and patient anatomy/physiology. Another important factor is surgeon and operative team comfort level and experience. While many of these intracardiac tumor cases are technically less challenging than other cardiac procedure such as mitral valve repair, surgeons must not venture past their and their team’s comfort zone. We do not agree with making your usual approach even less invasive because intracardiac tumor resection may be a less complex case than your usual practice. This is not the time, for example, to embark on a first-time robotic or VATS rather than the team’s usual ministernotomy experience.

Perioperative imaging with TTE/TEE and CT chest, abdomen, and pelvis is of critical importance before embarking on a minimally invasive approach. There are several key factors that must be assessed prior to determining the approach.

TTE/TEE

Key assessments must be made prior to determining the patient’s candidacy for minimally invasive surgery and for which approach. Does the patient have aortic regurgitation (AR) that may impede the delivery of adequate cardioplegia and limit myocardial protection? This may prevent the robotic approach from being a viable option. Depending on the severity of the AR, the only minimally invasive option may be a ministernotomy.

Is the patient’s ejection fraction (EF) acceptable for a minimally invasive procedure? Patients with lower EF may not tolerate a longer ischemic time. During preoperative planning, the surgical team needs to take into account their previous experience and operative timing with minimally invasive approaches.

Does the patient require extensive reconstruction, and is it feasible via the surgical approach with which the surgical team is familiar?

CT Scan

This is a crucial tool in determining the surgical approach and the safety of such an approach. The key aspects that require analysis are as follows:

1. Assessment for vascular abnormalities

2. Discontinuous inferior vena cava

3. Type B dissection

4. Unreported inferior vena cava filter

5. Small or occluded femoral arteries

Fused right or left chest preventing entry

Large hiatal hernias

Other unsuspected finding such as malignancies

Pulmonary Assessment

Pulmonary assessment is a component of all cardiac surgical cases but is even more crucial for nonsternotomy approaches as they often require selective single-lung ventilation. The surgical team must assess the patient’s ability to tolerate single-lung ventilation and maybe consider preoperative anesthesiology clearance in some complex or marginal cases.

Lower and upper ministernotomy is an approach that is an option for virtually any patient and surgical team. A thorough review of the preoperative TTE and operative TEE can help determine which approach to use. It is recommended to use the upper ministernotomy approach when dealing with superior vena cava (SVC) or aortic/aortic valve tumors as exposure of these structures is most visualized, whereas a lower ministernotomy can be used for right atrial or left atrial tumors. For tumors of the left ventricle or right ventricle, either approach can be used depending on the tumor’s exact location and the surgeon’s experience with their approach.

With increased experience, the surgeon can perform the same operation through a minithoracotomy, VATS, or robotically. These approaches offer a less invasive surgery compared with partial sternotomy and in some cases even better visualization. The main factor in determining these approaches is surgeon and team expertise and comfort as well as the thorough assessment of the preoperative echocardiogram and CT scan.

Finally, we would be remiss not to mention the following: “Do not be afraid to convert.” The surgeon must at all times conduct a safe and appropriate operation; compromising on safety and the surgical goals would offer the patient no favors.

Commandment 3: Cannulation, Perfusion, and Myocardial Protection

Understanding our cannulation strategies is crucial for all intracardiac tumor resection. Every one of these cases will be performed while on the heart-lung machine, and determining the cannulation approach and alternatives preoperatively is critical. The options are central versus peripheral or a combination of the two. The ministernotomy approach can often be cannulated centrally. The central approach has the advantage of increased user familiarity and reduced stroke rate. At times, patient anatomy, such as the location of the right atrium, can make venous cannulation difficult and may require peripheral cannulation. Furthermore, the ascending aortic length may be too short to be able to cannulate centrally and may also require peripheral cannulation. An important aspect of central cannulation during minimally invasive surgery is to be able to decannulate safely and to be able to repair the cannulation site if necessary. If control and repair of central cannulation sites are not possible or very difficult, peripheral cannulation should be performed.

For nonsternotomy approaches, peripheral cannulation is the best strategy. Peripheral cannulation can be done open or percutaneously. Regardless of the approach, a thorough examination of the preoperative imaging should be performed. Cannulation should be performed via Selinger technique under both ultrasound and TEE guidance. If a percutaneous approach is being used, then a Perclose ProGlide™ (Abbott, Chicago, IL, USA) can be inserted prior to vessel dilation or the MANTA system (Teleflex, Wayne, PA, USA) can be used after decannulation. If the patient’s peripheral vascular disease contraindicates peripheral cannulation, axillary cannulation can be used. Cannulating using an 8 or 10 mm graft is the preferred approach to minimize the risk of vessel narrowing.

Myocardial protection strategy is paramount for a successful procedure. The first strategic question is whether the operation will be performed with a beating or arrested heart. On-pump beating-heart surgery is a safe option for right-sided lesions that do not require entry to any left-sided structure. When considering beating-heart surgery, the team must assess their ability to perform a complete margin-free resection on the moving heart and be prepare to arrest the heart if the surgical goals cannot be met because of the technical difficulty of working on the beating heart. Another option would be to perform the case on a fibrillating heart, which would facilitate the surgical procedure; however, the team needs to ensure that no AR is present to avoid left ventricular distention and myocardial injury. In cases in which the resection will involve entry to the left side of the heart, such as intra-atrial septum resection and reconstruction, care must be taken to avoid air embolization such as performing the case under fibrillatory arrest, the placement of a root vent, or arresting the heart.

Most surgical procedures will be performed on the arrested heart. This can be achieved via a direct root vent placement and direct cross-clamping or by endoballoon placement. Either approach is acceptable and has its own pros and cons. The endoballoon is not an option for any transaortic approach procedures. Del Nido or Custodial cardioplegia are great options for these cases as they can eliminate the need for cardioplegic redosing.

Commandment 4: Margins—Do Not Accept a Substandard Resection and Reconstruction

Complete resection of the intracardiac tumor with a negative margin is paramount. The nonmalignant nature of these lesions is not a license to accept substandard resection. Despite the benign nature of these masses, recurrence is possible, resulting in complications such as mass effects and possible embolization. Furthermore, patients with recurrence may have to undergo a reoperation that could have been avoided. In the worst case, some patients may be inoperable at representation.

The operator must choose an approach that allows for a safe and timely complete resection that also permits reconstruction when required. While not cancerous, a negative margin is required to avoid recurrence of the lesion. When contemplating reconstruction of cardiac defects, the surgical team needs to factor in the size of the defect to determine the appropriate surgical repair technique. Primary repair for small defects is appropriate, and patch repair is suitable for larger defects. We recommend patch repair for any defect that requires any significant tension to close and repair dehiscence to limit morbidity that could otherwise been avoided. When determining the repair material to be used, the operator must take into account the patient’s age and potential need for future transcatheter intervention.

Available patch materials include autologous pericardium, bovine pericardium, CorMatrix (CorMatrix Cardiovascular, Roswell, GA, USA), and Dacron patch (C. R. Bard, Inc., Murray Hill, NJ, USA). All of these materials can be used as patches and provide a durable result; however, the surgical team needs to factor in that an intra-atrial Dacron patch would likely preclude the future ability to perform a transcatheter transatrial procedure and may consider autologous pericardium for reconstruction.

In rare cases, leaving benign tissue behind or debulking a benign intracardiac tumor may be an acceptable option in ultra-high-risk elderly patients.

Commandment 5: Understanding the Ministernotomy Approach

Compared with all other minimally invasive techniques, the ministernotomy approach is the most similar to the full sternotomy approach. Tumor location is the critical aspect when deciding whether to perform an upper or lower approach. Upper sternotomy is ideally suited for lesions of the aorta and aortic valve as well as the SVC and certain left ventricular lesions, whereas lower partial sternotomy is best for intra-atrial or intraventricular lesions. Once the approach is decided, the next decision is whether the sternotomy will be J or T. Most cases can be performed with just a J sternotomy, with T being reserved as an intraoperative decision to improve visualization for optimal resection and reconstruction.

Arterial and venous cannulation should be performed centrally unless anatomical features make it too difficult to perform or unsafe to repair after decannulation. Percutaneous groin cannulation is an acceptable strategy. An approach that minimizes stroke risk and optimizes exposure is a central arterial cannulation with percutaneous venous femoral cannulation. Once the chest is opened and on cardiopulmonary bypass, the surgical procedure should proceed as any regular full sternotomy case. Tools that help with a ministernotomy approach include miniature chest retractors and shafted instruments. A reticulating flexible cross-clamp or a Chitwood clamp can also help improve the size of the operative field. Another important fact to consider is that a ministernotomy case can be performed with the current instrumentation that is already available at all institutions that perform a standard sternotomy approach.

Commandment 6: Understanding the Minithoracotomy Approach

The minithoracotomy approach for intracardiac tumors virtually always means a right thoracotomy approach. The vast majority of these cases will be performed from a right chest approach via the second, third, or fourth interspace working port, with the fourth being the most common. The second interspace is used when the mass is located either in the ascending aorta, aortic valve, or in the left ventricular outflow tract. Lesions in the SVC may be approached via second interspace access as well; however, a third interspace approach is usually preferred. The fourth interspace approach is most commonly used for intracardiac masses that are located in any of the 4 chambers of the heart.

Preoperative paravertebral block may be considered for optimal postoperative pain control. These cases are usually performed with the ability to selectively isolate the right lung. Double-lumen endotracheal intubation or single-lumen intubation with a bronchial blocker is usually performed. The procedure access is through a 3 to 5 cm incision and virtually always requires peripheral cannulation, usually femoral. The incision is in the midaxillary to anterior axillary line for right-sided masses and midaxillary to lateral axillary line for left-sided masses. Preoperative imaging will help determine the optimal interspace and incision location. A soft-tissue retractor is a helpful tool to improve visualization. In addition, it protects the skin and soft tissue from tumor cell exposure. For these case, specialized small chest retractors are utilized with the addition of an atrial lift component for most cases. Shafted instruments are a definite requirement for these approaches. Standard instrumentation alone will not suffice in most cases, and the team should have all the required tools prior to embarking on these procedures. Cross-clamping can be performed directly or with endoballoon as previously described. The surgical resection and reconstruction strategy and techniques are the same as for a sternotomy approach. The tumor must be fully resected. The main difference is the use of the shafted instruments. It is recommended to be familiar with these instruments in open cases prior to utilizing these tools during a minimally invasive case as the surgeon loses 4 degrees of freedom by utilizing a shafted instrument. An important consideration when performing a minithoracotomy procedure is the availability of a thoracoscope; while not utilized to perform the case, it may be needed for visualization in certain instance or for identification of injuries or bleeds.

Commandment 7: Understanding the VATS Approach

The VATS approach can be utilized as a tool to improve visualization in a minithoracotomy approach or as part of a total endoscopic approach. In this section we will focus on the latter. The main advantage of the total endoscopic approach is significantly reduced invasiveness compared with the minithoracotomy and the VATS minithoracotomy. Beyond improved visualization, the surgical procedure becomes even more minimally invasive.

A 1 inch working port is created followed by the placement of the soft-tissue retractor. This working port is then used temporarily to place the remaining ports under direct visualization. A camera port is made anterior to the working port, and the remaining 2 ports are placed 5 to 8 cm away from the working port, one cephalad and the other caudad. The important concept of triangulation and avoiding instrument interference applies for intracardiac resection as in all other thoracoscopic cases. The port placement is the same as in any VATS mitral valve repair case. The working port size is determined by the size of the tumor mass. Anesthesiologic, cannulation, and myocardial protection strategies are similar to the minithoracotomy cases. At any point during the case at which the surgical strategy or patient safety may be compromised, the working port should be extended and the case converted to a minithoracotomy case.

Commandment 8: Understanding the Robotic Approach

The robotic approach can be via minithoracotomy or total endoscopic (Supplemental Video). The approach used will depend on surgeon comfort and intracardiac masses size. The anesthesiologic considerations are the same as for the VATS approach.

The vast majority of these cases will be performed from a right chest approach via the second, third, or fourth interspace working port, with the fourth being the most common. Port placement should be optimized to avoid collision and facilitate a quick and easy resection with reconstruction as needed. Inappropriate port placement can lead to prolonged cross-clamp time or, worse, result in a compromised exposure or procedure. The working port should be large enough to remove the mass to avoid having to either lose the tumor in the chest or have to enlarge it mid-procedure. The vast majority of intracardiac tumors are approached via the fourth interspace.

The da Vinci Xi robot (Intuitive Surgical, Sunnyvale, CA, USA) is used with the camera port through the working incision (arm 2) or via a separate incision. Three additional ports include DeBakey forceps or Rosano (arm 1), atrial retractor (arm 3), and scissors/needle driver (arm 4) with patient positioning and port location identical to those used for robotic mitral valve surgery. Cannulation is performed peripherally and myocardial protection done by direct approach or by endoballoon. Consideration for SVC venous cannulation can optimize drainage and visualization for these cases.

Benign intracardiac tumors are the ideal pathologies to benefit from robotic approach. These patients usually have good physiology and cardiac reserve and can benefit the most from the least invasiveness of this procedure with postoperative day 1 or 2 discharge.

The surgical team should be experienced and comfortable with the robotic approach. The team should understand the instrumentation, understand the steps of the case, and understand how to reconstruct the defect after resection if required. While these cases may appear less demanding than a mitral repair, it can at times require highly advanced techniques to perform the resection and even more so for the reconstruction.

Commandment 9: Percutaneous Approach

In recent years, the percutaneous removal of intracardiac masses has become more routine, mostly used for the removal of venous thrombus, clot in transit, or valvular vegetation. For examples, both the AngioVac (AngioDynamics, Latham, NY, USA) and Inari systems (Inari Medical, Irvine, CA, USA) have been used to remove intracardiac masses. Approved for clot removal on the right side of the heart, these systems have been used off-label to remove left-sided cardiac masses. The advantage of the percutaneous approach is that it is much less invasive and more readily tolerated. This approach can be used for tumor removal when the diagnosis is uncertain between thrombus/vegetation or tumor. The retrieved tissue can then be analyzed and a decision on further treatment can be made subsequent to the pathological result.

The percutaneous approach can also be used in nonoperable patients for palliation of tumor mass effects. Tumor removal or debulking can be performed in such cases where full resection is not the goal.

Commandment 10: Education

Education is a cornerstone of our profession, and minimally invasive surgery is a technique that is of paramount importance to be passed on to our trainees. The utilization of videoscopic imaging has greatly helped in training. It allows the primary surgeon to be able to mentor the residents and fellows through a minimally invasive procedure. Many of these cases are technically less challenging than the routine minimally invasive cases, such as a minimally invasive or robotic mitral repair. A left atrial myxoma resection is a perfect case for a senior minimally invasive surgeon to help train and mentor a junior minimally invasive surgeon.

Conclusions

While benign in nature, intracardial lesions require treatment with the same dedication and skill as any other cardiac pathology. The vast majority of these patients can be treated with a minimally invasive option. Understanding the minimally invasive tools available and principles for a safe resection and reconstruction will benefit our patients and our surgical specialty.