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The Incidental Finding of a Patent Foramen Ovale During Cardiac Surgery: Should It Always Be Repaired? A Core Review

Sukernik, Mikhail R. MD, PhD*; Bennett-Guerrero, Elliott MD

doi: 10.1213/01.ane.0000278735.06194.0c
Cardiovascular Anesthesia: Review Article
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CME

With the increased use of intraoperative transesophageal echocardiography, patent foramen ovale (PFO) has become a common finding during heart surgery. This finding presents a difficult dilemma for cardiac surgeons, since the impact of intraoperatively diagnosed PFOs on postoperative outcome is unknown. Changes in the surgical plan required for closure of a PFO subject the patient to the possibility of additional risk. On the other hand, a decision to not close a PFO exposes the patient to unclear immediate and long-term consequences. Deciding whether or not to close a PFO currently depends on the clinicians’ personal preferences, the probability of intraoperative and postoperative hypoxemia, and any anticipated deviation from the initial surgical plan. Most clinicians agree that an intraoperatively diagnosed PFO must be closed when surgery leads to a high risk of hypoxemia (e.g., left ventricular assist devices placement, heart transplantation); should be closed in most cases when minimal deviation from the initial surgical plan is needed for PFO closure (e.g., mitral valve or tricuspid valve surgeries); and probably, should be closed during heart surgeries performed without atriotomy and bicaval cannulation when the risk of perioperative or remote PFO-related complications is increased. The recent development of percutaneous methods of PFO closure provides a valuable backup for those cases when PFO is not closed and postoperative hypoxemia or other complications may be attributable to the uncorrected PFO.

IMPLICATIONS: The incidental diagnosis of patent foramen ovale is often encountered on echocardiographic examination during cardiac surgery. We review the embryology, physiology, and proper methods for detection along with perioperative implications and decision-making processes that may lead to immediate, delayed, or no intervention.

From the *Department of Anesthesiology, Pennsylvania State University College of Medicine, Hershey, Pennsylvania; and †Duke Clinical Research Institute, Durham, North Carolina.

Accepted for publication May 31, 2007.

Address correspondence and reprint requests to Mikhail R. Sukernik, MD, PhD, Department of Anesthesiology, Penn State Milton S. Hershey Medical Center, P.O. Box 850, H-187, Hershey, PA 17033. Address e-mail to mrs21@columbia.edu.

Patent foramen ovale (PFO) presents a unique challenge to clinicians because of the frequent prevalence of this condition (1,2) and its unclear clinical significance in most cases. The low incidence of PFO-related complications makes it difficult to study PFO closure in a prospective randomized trial, which leaves the true incidence of PFO-related complications unknown. Nevertheless, more and more published case reports and case–control studies (3–16) implicate PFO as a causative factor for hypoxemia and systemic thromboembolism. PFO can cause hypoxemia and embolic phenomena when right atrial (RA) pressure exceeds the left atrial (LA) pressure, or when preferential flow from the inferior vena cava towards the PFO persists as in the prenatal circulation (17–19). These conditions may occur during the perioperative period as a result of the effect of mechanical ventilation, pulmonary embolism, right ventricular failure, an altered anatomic relationship between the inferior vena cava and interatrial septum, or an increase in intraabdominal pressure (Table 1).

Table 1

Table 1

With the increased use of intraoperative transesophageal echocardiography (TEE), PFO has become a common finding during heart surgery. This finding presents a difficult dilemma for cardiac surgeons, since the effect of intraoperatively diagnosed PFOs on postoperative outcome is unknown. Changes in the surgical plan required for closure of a PFO subject the patient to a possible additional risk. On the other hand, a decision to not close a PFO exposes the patient to uncertain immediate and long-term consequences.

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EMBRYOLOGY, ANATOMY, PHYSIOLOGY, AND DEFINITIONS

During prenatal life, foramen ovale (Fig. 1) is an opening bordered on the right side by the septum secundum, and on the left side by the septum primum (25), which allows blood flow from the RA to the LA. After birth, when LA pressure exceeds RA pressure, the PFO closes functionally with permanent closure due to adhesion occurring within the first year of life (26). When the flap-like valve formed by the septum primum fails to fuse with the septum secundum, the foramen ovale stays open and right-to-left shunt may occur if conditions leading to increased RA pressure develop. These conditions include right ventricular failure (5,27), tricuspid regurgitation (28), and pericardial tamponade (29). In patients with no obvious right heart lesions, right-to-left shunt may develop due to: 1) instantaneous changes in the difference between RA and LA pressure during each cardiac cycle, 2) respiration-induced transiently positive RA–LA pressure gradient, or 3) preferential flow from the inferior vena cava towards the PFO (30). If the flap-like valve formed by the septum primum does not cover the PFO completely, left-to-right shunt may develop. This often occurs in patients with left-sided cardiac lesions, since these can increase LA size and pressure (31). Although a large PFO is sometimes considered to be a functional atrial septal defect (ASD), this should not be confused with true ASD, particularly of the secundum type. Septum secundum ASD can be defined as a deficiency in the development of the septum secundum, leading to a lack of coverage and sealing of the foramen secundum. PFO, on the other hand, is failure of the flap-like valve, formed by the septum primum, to fuse with the septum secundum (Fig. 1). With TEE examination of the interatrial septum between 30 and 90 degrees at the midesophageal level, PFO can be distinguished from septum secundum ASD in the majority of cases. PFO appears as a separation of the two layers of interatrial septum on two dimensional (2D) echocardiography with left-to-right shunt, if present, almost parallel to the septum (Figs. 2 and 3). In contrast, a septum secundum ASD is represented on 2D-echo by interruption of the interatrial septum with color flow perpendicular to the interatrial septum (Figs. 4 and 5).

Figure 1

Figure 1

Figure 2

Figure 2

Figure 3

Figure 3

Figure 4

Figure 4

Figure 5

Figure 5

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PFO INCIDENCE

A PFO is found in approximately one-quarter of postmortem examinations (Table 2). Thompson and Evans (1) in a postmortem study identified a “pencil patent” PFO (0.6–1 cm) in 6% of individuals and a “probe patent” PFO (0.2–0.6 cm) in 29% of individuals. Hagen et al. (2) found a PFO in 263 of 965 autopsies. PFO ranged in size from 1 to 19 mm, with the size increasing and the prevalence decreasing with increasing age. They did not find a significant difference in the incidence and size of PFO between men and women. Penther performed 500 consecutive autopsies and found an average PFO surface area of 0.5 cm2 (range, 0.2–1.5 cm2). There was no association between PFO frequency and age, sex or underlying cardiac pathology (32).

Table 2

Table 2

PFO is highly associated with motility of the interatrial septum throughout the cardiac cycle and atrial septal aneurysm (protruding >10 mm beyond the plane of the interatrial septum). Louie et al. (33) identified some motility of the septum primum in 73% of patients with PFO. In contrast, 56% of patients without PFO had no motion of septum primum. Mugge et al. (34) found that 54% of patients with atrial septal aneurysm demonstrated interatrial shunting, in the majority of cases through a PFO. Louie et al. (33) also demonstrated that maximal diameter of the fossa ovalis is larger in patients with (1.4 ± 0.4 cm) than without PFO (1.0 ± 0.3). Schneider et al. found an association between PFO and a Chiari network. They suggested that by directing the blood from the inferior vena cava preferentially toward the interatrial septum in adult life, a Chiari network may contribute to the persistence of a PFO and formation of an atrial septal aneurysm and increase the chances of paradoxical embolism (35).

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PFO DETECTION

In the absence of ASD, detection of interatrial shunt is essential for the diagnosis of PFO. Modern methods of PFO detection include TEE, transthoracic echocardiography (TTE), transcranial Doppler, and possibly, magnetic resonance imaging (MRI). Although TTE with second harmonic imaging is a promising method, TEE is generally considered to be the “gold standard” based on comparisons with postmortem studies and with other methods (Table 3) (36–38). Schneider et al. (36) validated the use of TEE for PFO detection by comparing TEE with autopsy findings in 35 consecutive patients. All nine PFOs were correctly identified by color Doppler and eight of nine were diagnosed by means of a contrast study. These findings correspond to sensitivities of 100% and 89%, respectively. The specificity of both methods was 100%. In contrast, Konstadt et al. (41), using TEE for PFO detection in 50 patients undergoing elective cardiac surgery, were able to identify PFO in 11 patents (22%) using a combination of echocardiography contrast and color Doppler study. Color flow through the shunt was seen in only three patients. However, in two of these three patients, a contrast study failed to identify a PFO, which suggests that color Doppler interrogation of the interatrial septum has incremental value in PFO detection. Di Tullio et al. (38) compared TTE and transcranial Doppler with TEE for PFO detection and found that transcranial Doppler was more sensitive than TTE (68% and 47%, respectively), although both methods were 100% specific. The transcranial Doppler technique to detect PFO is based on the transient enhancement of an ultrasound signal reflected from air bubbles passing through cerebral arteries. It is a blind technique and, similar to contrast echocardiography, relies on the creation of a temporary pressure gradient between the RA and LA with a provocative maneuver. Augoustides et al. (39) studied the ability of multiplane TEE to diagnose PFO. They concluded that a stepwise approach using midesophageal four-chamber and bicaval views with combination of color flow Doppler and contrast echocardiography, with and without provocative maneuver, is needed to maximize the PFO detection rate. Advances in ultrasound technology, however, have significantly improved TTE accuracy in PFO detection. TTE with second harmonic imaging was compared with TEE in several studies. It was demonstrated that TTE is as at least as accurate as TEE when second harmonic echocardiography was used (40,42,43). Second harmonic imaging is based on forming an image from the second harmonic component of the backscattered signal, which has twice the frequency of the emitted ultrasound wave. Second harmonic imaging significantly improves echocardiography quality in difficult-to-image patients by increasing signal-to-noise ratio with and without use of echocardiography contrast. It improves delineation of atrial structures and enhances the visualization of microbubbles (42). Nusser et al. (44) compared cardiac MRI (CMRI) with TEE for PFO detection and found that current CMRI is inferior to TEE for PFO detection.

Table 3

Table 3

The accuracy of TEE in the assessment of PFO size was validated by Schuchlenz et al. by comparing TEE data with balloon PFO sizing during catheter PFO closure. They found that size of the contrast bubble cloud closely correlated with PFO size only if contrast was injected in the femoral, but not in the cubital vein. They also found a good correlation between PFO size measured by balloon and distance between the septum primum and septum secundum (45).

Although TEE is still a gold standard technique for PFO detection, it is a semi-invasive and an expensive tool. In addition, the procedure is uncomfortable for awake patients. TTE and transcranial Doppler are noninvasive, less expensive, well established alternatives and may be used for screening purposes. With improvements in TTE technology, it is likely that TTE will replace other PFO detection methods in most circumstances in the near future.

When TEE is used in cardiac surgery, a search for a PFO should be performed as part of a complete diagnostic examination. A large PFO can be identified with 2D echocardiography by observing a clear separation between the septum primum and septum secundum (Fig. 2); in most cases, passage of contrast material (usually agitated saline) or color flow through the defect should be demonstrated to establish the diagnosis. Under normal circumstances, LA pressure exceeds RA pressure; hence, a provocative procedure that temporarily reverses this relationship must be applied to demonstrate the passage of the contrast through the interatrial septum. Provocative procedures include an abrupt release of a Valsalva maneuver or coughing in awake patients and abrupt release of positive airway pressure during mechanical ventilation. Greim et al. (46) demonstrated that abrupt release of airway pressure of 30 cm H2O in a positively ventilated patient is superior to the Valsalva maneuver in detecting PFO. Either maneuver initially causes a reduction of blood flow into the thorax due to an increase in intrathoracic pressure. The subsequent abrupt decrease of the intrathoracic pressure causes blood to rapidly enter the thoracic cavity and fill the RA, creating a temporary transatrial pressure gradient (RA > LA), which lasts until flow equilibrates. Agitated saline, blood, or commercial echocardiography contrast injected IV at this time will traverse the PFO from right-to-left, demonstrating its presence and confirming the diagnosis (Fig. 6). There is no evidence that any one contrast material is preferable to another. When saline or the patient’s blood is used, intensive agitation using two 10- or 20-mL syringes connected through a double stopcock system is important to achieve complete opacification of the RA. In our experience, rapid injection through the central rather than peripheral line leads to better opacification of the RA with injection of a smaller volume of contrast. The contrast material must appear in the LA within three cardiac cycles, since a delayed appearance in the LA usually indicates transpulmonary passage of the contrast. Contrast-based methods may lead to false-negative results when LA pressure far exceeds RA pressure and the pressure gradient cannot be reversed with any provocative maneuver. This is because rapid filling of the RA upon release of a provocative maneuver does not create a high enough RA pressure to overcome increased LA pressure as in significant mitral regurgitation or left ventricular failure. Transient bulging of the interatrial septum towards the LA immediately after release of a provocative maneuver is a good indicator of a transient positive pressure gradient between the RA and LA. The presence of left-to-right flow between the septum primum and septum secundum (Fig. 3) proves the existence of a PFO, but its absence does not exclude it, since the left-to-right shunt occurs only if the flap-like valve formed by the septum primum, is incompetent. A detailed intraoperative TEE evaluation after PFO closure is extremely important because of the possibility of residual shunt (47) and surgical error (48). We use and recommend the following technique of intraoperative TEE:

Figure 6

Figure 6

  1. The fossa ovalis area of the interatrial septum is visualized from the midesophageal level between a 0° and 90° view (Fig. 7).
  2. Figure 7

    Figure 7

  3. The distance between the septum primum and septum secundum is assessed and, when technically possible, measured.
  4. Color flow mapping with the Nyquist limit set at 30 cm/s is performed:
    1. Without a provocative maneuver to search for a left-to-right shunt (Clip 1).
    2. With a provocative maneuver (abrupt release of sustained positive pressure of 20 cm H2O), while continuously imaging with color flow Doppler (Clip 2).
  5. If the color Doppler study is negative, a contrast study is performed with the injection of 10 mL of agitated saline and release of positive airway pressure (20 cm H2O as soon as the contrast material is visualized in the RA (Clip 3).
  6. If a decision is made to close a PFO, color Doppler and contrast studies have to be repeated after weaning from cardiopulmonary bypass and before protamine administration.
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METHODS OF PFO CLOSURE

Surgical PFO closure. The standard surgical technique of PFO closure includes cardiopulmonary bypass and cardioplegic arrest. The operation can be performed through median sternotomy, ministernotomy, or right thoracotomy (49). With the development of robotic surgical systems (e.g., Da Vinchi Surgical System, Intuitive Surgical, Inc., Sunnyvale, CA), totally endoscopic PFO closure has became possible (50). Most surgeons use bicaval cannulation to provide a bloodless field and facilitate surgical exposure of the interatrial septum. A frequent incidence of residual interatrial shunt (73%) has been described after surgical PFO closure (47).

Percutaneous PFO closure is a relatively safe and effective method, with success rates ranging between 86% and 100% (51,52). There are several different devices available for transcatheter PFO closure. Use of these devices in patients with a history of cryptogenic stroke revealed a small risk of recurrent events, most likely related to incomplete closure or thrombus formation (25). The available data suggest that risk of complications is device-dependent (53,54). Implantation of the Amplatzer device (AGA Medical, Plymouth, MN) appears to have the most favorable outcome. In the work of Schwerzmann et al., comparison of Amplatzer with PFO-STAR device (Cardia Inc., Burnsville, MN) revealed residual shunt 6 mo after implantation, with an incidence of 6% and 34%, respectively. The risk of thromboembolic events 3.5 yr after implantation was also lower in the Amplatzer group (2.7% vs 17.7%, respectively) (55).

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UNEXPECTED PFO FINDING DURING CARDIAC SURGERY

The routine use of TEE has led to an increase in PFO detection as an incidental finding during cardiac surgery. The intraoperative diagnosis of a PFO leads to the dilemma during surgery of whether the PFO should be corrected. The clinician must make this decision within a very short period, often without the opportunity to discuss the issue with the patient, patient’s family, or patient’s cardiologist (56). Currently, there are not enough clinical data available to guide the clinician’s decision in the majority of cases. There is general agreement that a PFO should be closed when development of a significant right-to-left shunt after surgery is highly likely (Table 4). An example of this is placement of a left ventricular assist device, because the unloaded left heart will create a right-to-left shunt through the PFO with subsequent hypoxemia (57). Heart transplantation presents another situation when PFO closure is necessary. Hypoxemia resulting from a previously silent PFO was described after heart transplantation (58). The transplanted heart usually faces relatively high pulmonary vascular resistance in the recipient, and that can provoke right-to-left shunting. This is why a meticulous search for a PFO needs to be performed in the donor heart, and if found, the PFO needs to be closed. Closure of a PFO diagnosed during surgery also appears to be prudent when almost no alteration of the surgical plan would be needed to perform this procedure, e.g., surgeries with planned atriotomies for the planned primary procedure (mitral or tricuspid valve replacement). In the retrospective study of Click et al. (59), PFOs were closed in 88 of 100 intraoperative findings; however, the PFOs were not closed when the primary surgical procedure did not include atriotomy.

Table 4

Table 4

Closure of an intraoperatively diagnosed PFO during heart surgeries performed without atriotomy and bicaval cannulation is a subject of debate. PFO closure in these cases, e.g., on-pump coronary artery bypass graft (CABG) surgery or aortic valve replacement surgery, requires in most cases additional interventions such as bicaval cannulation, opening of the RA, and prolongation of cardiopulmonary bypass. Sukernik et al. (60) conducted a national survey of 734 US cardiac surgeons on the management of intraoperatively found PFO during CABG. Those who responded (64%) used TEE for a PFO search in approximately one-third of all CABG surgeries. During planned on-pump CABG surgery, 27.9% of respondents always closed an intraoperatively diagnosed PFO, whereas 10.2% of respondents never closed an intraoperatively diagnosed PFO. During planned off-pump CABG surgery, 27.6% of surgeons never changed their plan, and 11% of respondents always converted the procedure to on-pump CABG to close the PFO. The majority of respondents decided whether to close a PFO based on the size of the PFO, the RA pressure, and a history of possible paradoxical embolism. Patient age had little effect on the surgeon’s decision. Diagnosis of a PFO in a patient scheduled for off-pump CABG is even more problematic, as a decision to close the PFO requires the use of cardiopulmonary bypass. If the surgeon decides to continue with the off-pump CABG, it must be recognized that the presence of a PFO might have implications during the off-pump CABG procedures. Several case reports have been published demonstrating the possibility of intraoperative oxygen desaturation secondary to the development of a right-to-left shunt, which occurred when the heart was elevated for surgical exposure of the posterior branches of the coronary arteries (61,62).

Surgical versus percutaneous PFO closure in cardiac surgical patients. Although no direct comparison between surgical and percutaneous PFO closure has been made, it makes sense to perform surgical closure during concomitant cardiac surgery. On the other hand, since PFO is a common finding, but postoperative PFO-related complications are rare, percutaneous PFO closure may be available as a backup procedure if, for example, hypoxemia develops in the postoperative period, and a PFO found during surgery is left open. Wang et al. (63) successfully used this novel approach when right-to-left shunting developed after cardiac surgery.

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SUMMARY

The clinical significance of the majority of PFOs found during cardiac surgery is unknown. A decision to close a PFO or not currently depends on the clinicians’ personal preferences, the probability of intraoperative and postoperative hypoxemia and any anticipated deviation from the initial surgical plan. The recent development of percutaneous methods of PFO closure provides a valuable backup for those cases in which PFO is not closed and postoperative hypoxemia or other complications arise that may be attributable to the uncorrected PFO.

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ACKNOWLEDGMENTS

We thank William Davidson, MD (Director, Hershey Medical Center Echo Laboratory), for assistance in obtaining the ECHO images presented.

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