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Anesth Analg 2001;92:1111-1116
© 2001 International Anesthesia Research Society


CARDIOVASCULAR ANESTHESIA

The Detection of Interatrial Flow Patency in Awake and Anesthetized Patients: A Comparative Study Using Transnasal Transesophageal Echocardiography

Clemens-A. Greim, MD, Herbert Trautner, MD, Katharina Krämer, MD, Peter Zimmermann, MD, Christian C. Apfel, MD, and Norbert Roewer, MD

Department of Anesthesiology, University Hospital Würzburg, Würzburg, Germany

Address correspondence and reprint request to C.-A. Greim, MD, Klinik für Anaesthesiologie der Universität Würzburg, Josef-Schneider-Str. 2, 97080 Würzburg, Germany. Address e-mail to cgreim{at}anaesthesie.uni-wuerzburg.de


    Abstract
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 
The Valsalva maneuver in the awake patient and the ventilation maneuver in the tracheally intubated anesthetized patient are two provocation methods to detect a patent foramen ovale (PFO) by means of contrast transesophageal echocardiography. In 60 patients undergoing posterior fossa surgery, a contrast agent was administered via a peripheral vein during a Valsalva maneuver immediately before anesthesia induction, followed by central venous administration during a ventilation maneuver in the same patients when anesthetized and endotracheally intubated. We evaluated both maneuvers with a 32-element monoplane transnasal transesophageal echocardiography probe to trace the atrial flow of the contrast agent in a 90° bicaval view. A maneuver was rated positive when more than four bubbles appeared in the left atrium during the first three cardiac cycles after intrathoracic pressure release. The right atrial cross-sectional area before pressure release, and the peak septal excursion during atrial contrast opacification, were measured. McNemar’s test was used to assess a paired dichotomous response on the two maneuvers for a significant difference. In 56 patients, the ventilation maneuver was significantly (P < 0.037) more often positive for PFO (n = 14) than the Valsalva maneuver (n = 7). Although there was no difference in the methods regarding the peak septal excursion, the mean right atrial area before pressure release was significantly smaller during the ventilation maneuver than during the Valsalva maneuver (11.2 ± 3.1 cm2 vs 14.4 ± 3.3 cm2, n = 42, P < 0.05). In the patients with a positive ventilation, but a negative Valsalva maneuver, the discrepancy was even larger (10.9 ± 4.4 cm2 vs 16.3 ± 4.2 cm2, n = 7, P < 0.001). We conclude that the ventilation maneuver is superior to the Valsalva maneuver in detecting PFO. Our data suggest that a peak pressure of 30 cm H2O during the ventilation maneuver achieves a more pronounced reduction in right atrial load and allows right atrial pressure to exceed left atrial pressure when intrathoracic pressure is released.

Implications: A controlled ventilation maneuver in anesthetized patients immediately before posterior fossa surgery may be superior to the preoperative Valsalva maneuver in detecting a patent foramen ovale by contrast transesophageal echocardiography. This approach identifies patients at high risk for paradoxic embolism, but it is not practical for preoperative identification of patients who might benefit from patent foramen ovale closure before surgery.


    Introduction
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 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 
The incidence of a patent foramen ovale (PFO) in nearly one-fourth of the normal population is associated with the risk for paradoxical air embolism, e.g., when patients must undergo neurosurgical procedures in the sitting position (14). Strategies to identify PFO include the performance of contrast transesophageal echocardiography (TEE), which has the same specificity but an increased sensitivity to the transthoracic approach (5). However, preoperative TEE imaging with conventional ultrasound probes puts additional psychological and physical stress on patients and is cost and time intensive, in particular when TEE follows initial diagnostic attempts using transthoracic echocardiographic imaging for PFO.

In the current study, we used a miniaturized ultrasound probe for the assessment of PFO immediately before anesthesia induction and during ventilation. Because of its small size and specific shape, this probe can be inserted transnasally (6). Although ultrasound is emitted and received by only 32 elements compared with 64 elements of a standard TEE probe, the device allows for identical sonographic imaging in supine positioned awake and anesthetized patients (6,7). We hypothesized that this technique would allow for a comparison of two standardized contrast echocardiographic methods to detect PFO—the Valsalva maneuver in the awake patient and the ventilation maneuver in the anesthetized patient.


    Methods
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 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 
With approval from the institutional ethics committee and written, informed patient consent, 60 neurosurgical patients (ASA II) scheduled for elective posterior fossa surgery were prospectively investigated between November 1998 and October 1999. Patients with evidence of increased intracranial pressure, cardiac, or respiratory disease were excluded from the study. Patients received midazolam 7.5 mg orally 30 min before arrival in the induction room. After cannulation of the antecubital vein and topical administration of xylometazoline and 1% lignocaine on the nasopharyngeal mucosa, a monoplane 5.0-MHz TEE probe with 32 transducer elements (Hewlett-Packard, Andover, MA) was inserted in the esophagus via the nasal route with the patients in the supine position as described previously (6,7). Hemodynamic monitoring included electrocardiogram, pulse oximetry, and noninvasive blood pressure measurement. Before the investigation was started, patients received 500 mL of IV infusion, and the infusion rate was then continued at 100 mL/h.

Echocardiography was performed by an anesthetist certified in TEE. A standard examination, including transgastric and transesophageal standard views, was performed in all patients. For the investigation, a "narrow cut" view of the interatrial septum and both atria was selected, as described previously (8), centering on the fossa ovalis and with the septum perpendicular to the ultrasound beam ( Fig. 1, top). The patients were then asked to perform a Valsalva maneuver as had been explained to them by the anesthetist during the preoperative assessment the previous day. Careful attention was directed to assure that the right atrium decreased in size during the strain phase of the maneuver. An injection of 10 mL of a contrast agent (Echovist 300®; Berlex Canada, Lachine, PQ) followed by a 10-mL isotonic saline bolus was given via the peripheral forearm venous catheter. This agent is a microbubble-based ultrasound contrast medium, composed of galactose-stabilized bubbles that do not survive passage through the lungs (9). The patients released the strain on command, when opacification of the right atrium occurred. During the maneuver, the left atrium was observed for evidence of interatrial flow patency to the microbubble solution. A maneuver was judged positive as described previously (10), when more than four bubbles appeared in the left atrium near the fossa ovalis during the first three cardiac cycles after release of increased intrathoracic pressure (Fig. 1, bottom). Results were obtained from on-line echocardiograms by one observer, and rated negative when no microbubbles occurred within three cardiac cycles. The Valsalva maneuver was repeated once in case of negative results, if no septal movement toward the left atrium had occurred on release of intrathoracic pressure. After induction of anesthesia, tracheal intubation and central venous and radial arterial catheterization, all patients were normoventilated without positive end-expiratory pressure and had a second evaluation for PFO. Ten milliliters of the contrast agent followed by a 5-mL isotonic saline bolus were injected through the central venous catheter during manual intermittent positive pressure ventilation, when airway pressure was kept at 30 cm H2O. The injection was started when the right atrium had decreased in size, and airway pressure was released, when the right atrium became opacified. The ventilation maneuver was repeated once in case of negative results, if no septal movement toward the left atrium had occurred on release of intrathoracic pressure.



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Figure 1. Transesophageal echocardiograms of a patient with a positive ventilation maneuver. Top, While airway pressure is kept at 30 cm H2O, the right atrial size decreases. Bottom, Immediately after airway pressure release and contrast opacification of the right atrium (RA), intracavitary occurrence of multiple bubbles in the left atrium (LA) within two cardiac cycles indicates an open foramen ovale and a right-to-left atrial shunt (arrow).

 
The contrast echocardiographic sequences were recorded on videotape and were later analyzed for PFO by an investigator blinded to the on-line obtained results. In addition, the cross-sectional area of the right atrium immediately before intrathoracic pressure release, and the peak right-to-left atrial septum deviation during atrial systole after pressure release, were quantified by tracing the right atrial border and measuring the maximum of septal excursion during the cardiac cycle as described previously (5).

All patients were operated on in a semiseated supine position with the head positioned above the knees. Transnasal TEE monitoring was continued intraoperatively for the detection of venous and paradoxical air embolism. In addition, patients were routinely monitored for air embolism with unidimensional precordial Doppler and continuous end-tidal PCO2 measurements. All patients had a neurological assessment on the first postoperative day, when awake and extubated, and were evaluated by an otolaryngologist to assess possible traumatization by the ultrasound probe.

Data were tested for normal distribution by the Kolmogorov-Smirnov test. Mean values and standard deviations of hemodynamic variables and echocardiographic measurements were tested for a difference in both maneuvers by using Student’s t-tests. To investigate a paired dichotomous response, we used McNemar’s test (11) with the Yates continuity correction for small sample size to compare differences in the results of both maneuvers. Differences were considered significant at P < 0.05.


    Results
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 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 
Biometric data of 60 consecutive patients included in the study are shown in Table 1. Transnasal insertion of the TEE probe was possible with topical anesthesia alone in 46 of 60 patients (77%). Ten patients (17%) felt uncomfortable or anxious and required additional systemic analgesia or sedation (fentanyl 100 µg or thiopentone 50 mg), but remained cooperative as judged by response on simple commands (squeezing hands, head lifting) and were well oxygenated during the probe placement. Four patients (6%) were excluded from further data acquisition: two patients had a high demand of systemic analgosedation followed by a lack of cooperation. In one patient, the probe could not be inserted because of an unexpected anatomic barrier inhibiting probe insertion, and another patient was excluded from the study because echocardiographic images of sufficient quality could not be obtained. The hemodynamic data of patients during the procedure are shown in Table 2.


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Table 1. Biometric Data of All Patients Undergoing Transesophageal Echocardiography for the Detection of a Patent Foramen Ovale
 

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Table 2. Hemodynamic Variables at Baseline and 1 Min After Transnasal Insertion of the Esophageal Ultrasound Probe (M 1), 1 Min After Valsalva Maneuver (M 2), Before the Ventilation Maneuver (M 3), and 1 Min After Intrathoracic Pressure Release (M 4)
 
Data for comparative analysis of PFO detection methods were collected from 56 patients. No echocardiographic signs for pulmonary hypertension, valvular disease, or pathological left-to-right atrial pressure gradient were detected. The Valsalva maneuver in the awake patients was positive in 7 of 56 patients (12%). During general anesthesia, these patients also had a positive ventilation maneuver, but the ventilation maneuver detected a right-to-left atrial shunt during anesthesia in seven additional patients. Based on these data, a PFO was diagnosed in 14 of 56 patients (24%). The discordance in both method results was significant (P = 0.037). Discrepancies in judgement of the on-line and off-line observers occurred for the Valsalva maneuver in two patients (4%) and for the ventilation maneuver in one patient (2%). These maneuvers were rated negative.

The data for the right atrial cross-sectional area and the atrial septum deviation as defined above are presented in Table 3. Measurements were obtained from 42 patients with echocardiograms outlining >75% of the right atrial border. The maximum of atrial septal excursion was 0.5 ± 0.2 cm (Valsalva maneuver) versus 0.5 ± 0.1 cm (ventilation maneuver) with no significant difference. In contrast, the mean right atrial area before pressure release was significantly smaller during the ventilation maneuver than during the Valsalva maneuver (11.2 ± 3.1 cm2 vs 14.4 ± 3.3 cm2, P < 0.05). In the patients with a positive ventilation, but a negative Valsalva maneuver, the discrepancy was highly significant (P < 0.001) (Table 3).


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Table 3. Right Atrial Cross-Sectional Area During Atrial Systole at Increased Intrathoracic Pressure, and Peak Right-to-Left Atrial Septum Deviation After Release of Intrathoracic Pressure in 42 Patients Undergoing Valsalva and Ventilation Maneuvers
 
The average time required for neurosurgery was 6.3 ± 0.8 h (mean ± SD). Venous air embolism with >20 microbubbles per echocardiographic frame occurred at least once in 23% of all patients and in 3 of 14 patients with PFO. In one patient with PFO, right atrial air detection was followed by significant clinical signs of pulmonary embolism, and aspiration from the atrial catheter rendered 120 mL of air. Neither in this, nor in the other patients, was paradoxic air embolism evidenced, as judged by intraoperative TEE imaging and postoperative neurological assessment. Differences between precordial Doppler- and TEE-based diagnoses of air entry into the right atrium were not seen. Later off-line analysis of the videotapes with regard to PFO showed no significant discrepancy compared with the on-line results and verified the study findings. Postoperative examination by the otolaryngologist did not reveal any nasal or mucopharyngeal lesions, and there were no complaints by the patients that could be related to perioperative transnasal TEE.


    Discussion
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 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 
Although the possible complications that derive from an open interatrial septum are potentiated during cranial surgery under general anesthesia when patients are in an upright position, the number of reports on air embolism and associated hazards has decreased over the years. Because recent surveys are not available, it is unclear whether general precautions in the intraoperative management have reduced the complication rate, whether preoperative echocardiography has led to specific measures taken in patients at identified risk of paradoxical embolism, or whether the incidence of complications has persisted, but has not been reported. The current role of preoperative echocardiography in combination with the Valsalva maneuver thus is not well defined in these patients. Moreover, some studies suggest that intraoperative TEE in combination with a ventilation maneuver may more effectively detect right-to-left atrial shunts (3,8). In the current study, we therefore assessed foramen ovale flow patency by a modified TEE approach using a miniaturized probe that is well tolerated by awake patients (6,7), and compared the two different diagnostic maneuvers.

The results of the present study can be summarized as follows: 1. in 77% of patients, the transnasal TEE approach combined with the Valsalva maneuver could be performed immediately before anesthesia induction without evidence of psychological stress or prolonged hemodynamic changes; 2. in combination with contrast monoplane TEE, the Valsalva maneuver in the awake patients was less sensitive for PFO than the ventilation maneuver in the same patients when anesthetized; and 3. in patients with PFO, no paradoxic air embolism was detected during intraoperative venous air entry.

The incidence of PFO in the normal population is approximately 25%, as determined by postmortem examinations (1,2). The 24% incidence of a positive ventilation maneuver in our study patients was close to this rate, suggesting that this diagnostic test in combination with TEE may not only be highly sensitive, but also specific. In this regard, both the Valsalva maneuver and transthoracic echocardiography may be inferior in their diagnostic potency. Using the Valsalva maneuver with transthoracic echocardiography, PFO incidence has been reported in a range of 10% to 24% of patients (12,13). In contrast, the Valsalva maneuver in combination with the transesophageal approach detected shunting through PFO in 22%–39% (14,15). The Valsalva/TEE combination thus has to be considered a sensitive preoperative approach to identify PFO as a risk factor in certain neurosurgical patients (15). However, in these patients, the potential of a preoperative TEE investigation for physical and psychological stress, for complications of this semiinvasive procedure, and for a small cost-benefit relation, are disadvantages of the method. With the patient under general anesthesia, TEE is less stressful and, combined with a ventilation maneuver, may reveal more PFO than preoperative echocardiography. Our study does not provide data on the true PFO incidence, as would be obtained in a postmortem examination and we can only speculate on the sensitivity and specificity of the combined TEE/ventilation approach.

The superiority of the ventilation maneuver compared with Valsalva in our study may be explained by considering several criteria for right-to-left atrial shunting. Because the interatrial pressure gradient is a major variable for detecting PFO, the discrepancy of both maneuvers in combination with TEE may be explained by a higher pressure gradient established during the ventilation maneuver. Determination of transmural pressure in both atria would have been adequate for documentation; however, this was not feasible in our patients. The observation of the atrial septum deviation after airway pressure release has been recommended as a replacement for a rather invasive hemodynamic monitoring to estimate the atrial pressure gradient (16); however, we assessed the peak atrial septum excursion in patients with PFO during both maneuvers and found no significant difference. In contrast, the right atrial cross-sectional area immediately before pressure release was remarkably smaller during the ventilation maneuver, particularly in patients with a positive ventilation, but a negative Valsalva maneuver. We doubt that premedication weakened the individual performance of the Valsalva maneuver, because the patients with PFO were fully awake when performing Valsalva, and only one patient with a test discrepancy in detecting PFO had received additional systemic analgesia. It can be assumed that during the ventilation maneuver, the intrathoracic pressure release from a plateau of 30 cm H2O led to a more pronounced atrial load and pressure increase and hence interatrial pressure gradient, than was achieved by the awake patients performing the Valsalva maneuver. It has been speculated in previous reports that such a high pressure plateau may be required in single cases for right atrial pressure to exceed left atrial pressure (8), but in our study, it may have assured a positive right-to-left atrial pressure gradient in all patients. We conclude from our results that the right atrial size before intrathoracic pressure release, as represented by the right atrial cross-sectional area, may be a good predictor for the achievement of a right-to-left atrial pressure gradient once intrathoracic pressure is released.

Our results support previous work that compared the Valsalva and ventilation maneuvers, but used both transthoracic and transesophageal imaging (3). Only one study found the ventilation maneuver inferior to the Valsalva maneuver (17), but in that study the authors combined the Valsalva maneuver with transthoracic echocardiography rather than with TEE. Because we used TEE via the nasal route, our data on both maneuvers are presumably the first to be based on an identical biatrial sonographic imaging. Although transthoracic and TEE methods both allow for biatrial viewing, different imaging angles and ultrasound frequencies may influence the resonation of the microspheres in the contrast agent solution, which may affect the results. In this regard, our study focused on the different maneuvers independent of the imaging modalities. Rather than using color flow mapping, we used the contrast echocardiographic approach as the more sensitive and specific technique for detecting PFO and a right-to-left atrial shunt (18). In contrast, color Doppler imaging will provide evidence of a persistent left-to-right atrial shunt more likely than contrast TEE (19). Other specific technical considerations address the imaging of the atria, which in our study was only possible in the transverse plane. A rapid multiple plane or even a three-dimensional approach would have been desirable to detect all bubbles within the left atrium, but use of a monoplane probe limited our investigation to standard bicaval imaging. Another limitation may be related to the presence of only 32 transducer elements in the particular TEE probe we used. However, previous investigations demonstrated the good quality of images from this probe when compared with standard transducer probes (6,7).

A crucial advantage of the ventilation versus the Valsalva maneuver for the detection of PFO is that diagnostic efficacy is independent of the patient’s cooperation. The procedure can be performed with much better coordination of contrast agent injection, right atrial opacification, and release of the airway pressure, whereas with Valsalva, the patient has to cooperate on commands to simultaneously achieve opacification and a maximum right atrium-left atrium pressure gradient. In this regard, there was a shortcoming of our study, because for the Valsalva maneuver, the contrast agent was injected into a peripheral venous catheter, whereas for the ventilation maneuver, it was injected into the superior vena cava. With this different injection protocol, the coincidence of left atrial opacification and peak right atrial pressure may have varied more with Valsalva than with the ventilation maneuver; however, our study protocol was adapted to the Valsalva procedure as it is performed in clinical routine (13).

Despite intraoperative venous air embolism in up to 50% of neurosurgical patients (20), the actual risk of morbidity is very small (4,21). The diagnosis of PFO, however, may necessitate monitoring that not only detects right atrial air but also paradoxical air embolism. The use of TEE for monitoring neurosurgical patients at risk of venous air embolism has been extensively addressed (2124). The evidence that intraoperative TEE improves clinical outcome in patients undergoing upright neurosurgical procedures (25), may be strengthened by our results concerning the diagnosis of PFO. Other clinical advantages of intraoperative TEE are obvious, because it provides two-dimensional information by operator-directed cardiac imaging, and combines diagnostic and monitoring capabilities. When used as a monitor device during operations of long duration, some risk for the patient lies in the fixed probe placement for hours, because mucosal lesions may occur. A sore throat and other reversible complaints have been reported in patients undergoing TEE monitoring with conventional ultrasound probes during either cardiac or neurosurgical procedures (26,27). Our systematic approach of postoperative patient complaints, however, did not reveal any complications that could be related to transnasal TEE.

In summary, the current study shows that the ventilation maneuver in combination with contrast TEE is superior to the Valsalva maneuver in detecting PFO, when end-inspiratory pressure during the ventilation maneuver is held at 30 cm H2O before pressure release. Intraoperative TEE may be used instead of the preoperative investigation for PFO, but this may limit the therapeutic options in case an atrial shunt is detected. The diagnosis of a PFO in the already anesthetized patient, however, may suggest changes in the patient position and the surgical approach, before the operation is started. Whether such consequences would have an impact on clinical outcome remains to be elucidated.


    References
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 

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Accepted for publication December 28, 2000.




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Lippincott, Williams & Wilkins Anesthesia & Analgesia® is published for the International Anesthesia Research Society® by Lippincott Williams & Wilkins and Stanford University Libraries' HighWire Press®. Copyright 2001 by the International Anesthesia Research Society. Online ISSN: 1526-7598   Print ISSN: 0003-2999 HighWire Press