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Pages 133-139 (February 2011)
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Vol. 64. Issue 2.
Pages 133-139 (February 2011)
DOI: 10.1016/j.rec.2010.10.014
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Diagnosis and Quantification of Patent Foramen Ovale. Which Is the Reference Technique? Simultaneous Study With Transcranial Doppler, Transthoracic and Transesophageal Echocardiography
Diagnóstico y cuantificación del foramen oval permeable. ¿Cuál es la técnica de referencia? Estudio simultáneo con Doppler transcraneal, ecocardiografia transtorácica y transesofágica
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Teresa González-Alujasa,
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mtegonzalez@vhebron.net

Corresponding author: Pg. Vall d’Hebron, 119-129, 08035 Barcelona, Spain. mtegonzalez@vhebron.net
, Artur Evangelistaa, Estevo Santamarinab, Marta Rubierab, Zamira Gómez-Boscha, José F. Rodríguez-Palomaresa, Gustavo Aveglianoa, Carlos Molinab, José Álvarez-Sabínb, David García-Doradoa
a Laboratorio de Ecocardiografía, Servicio de Cardiología, Hospital General Universitari Vall d’Hebron, Barcelona, Spain
b Servicio de Neurología, Hospital General Universitari Vall d’Hebron, Barcelona, Spain
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Introduction and objectives

Patent foramen ovale (PFO) is the most common cause of cryptogenic stroke in patients younger than 55. Transesophageal echocardiography (TEE) has been accepted as the reference diagnostic technique. The purpose of this study was to compare the accuracy of transthoracic echocardiography (TTE), TEE and transcranial Doppler (TCD) in the diagnosis and quantification of patent foramen ovale.

Methods

We studied 134 patients prospectively. Simultaneous TTE with TCD and TEE with TCD were performed, using agitated saline solution to detect right to left shunt.

Results

In 93 patients diagnosed with PFO, the shunt was visualized at baseline by TCD in 69% of cases, by TTE in 74% and by TEE in 58%. The Valsalva maneuver produced a similar improvement in shunt diagnosis with all 3 techniques (26%-28%). TTE and TCD showed higher sensitivity (100% vs 97%; non significant difference) than TEE in the diagnosis of PFO (86%; P<.001). TCD performed during TEE did not diagnose 12 (13%) shunts previously diagnosed during TTE. Similarly, TEE underestimated shunt severity.

Conclusions

TTE enables adequate diagnosis and quantification of PFO. TEE is less sensitive and tends to underestimate the severity of the shunt.

Keywords:
Echocardiography
Transcranial Doppler
Patent foramen ovale
Introducción y objetivos

El foramen oval permeable (FOP) es la causa más frecuente de ictus criptogénico en menores de 55 años. La ecocardiografía transesofágica (ETE) ha sido aceptada como la técnica diagnóstica de referencia. El propósito del estudio es comparar la exactitud de la ecocardiografía transtorácica (ETT), la ETE y el Doppler transcraneal (DTC) en el diagnóstico y la cuantificación del FOP.

Métodos

Se estudió de forma prospectiva a 134 pacientes. Se practicaron simultáneamente DTC y ETT, y DTC y ETE con moderada sedación, utilizando la inyección de suero salino agitado para detectar cortocircuito derecha-izquierda.

Resultados

Se diagnosticó FOP a 93 pacientes. El cortocircuito se visualizó basalmente por DTC en el 69% de los FOP, por ETT en el 74% y por ETE en el 58%. La maniobra de Valsalva aumentó el diagnóstico del cortocircuito de forma similar en las tres técnicas (26-28%). La ETT y el DTC mostraron mayor sensibilidad (el 100 y el 97%; diferencias no significativas) que la ETE en el diagnóstico de FOP (86%; p<0,001). El DTC practicado durante la ETE no diagnosticó 12 (13%) cortocircuitos previamente diagnosticados en el estudio durante la ETT. La severidad del cortocircuito también se subestimó mediante la ETE.

Conclusiones

La ETT permite un adecuado diagnóstico y cuantificar la severidad del FOP. La ETE tiene menor sensibilidad y tiende a subestimar la severidad del cortocircuito.

Palabras clave:
Ecocardiografía
Doppler transcraneal
Foramen oval permeable
Full Text
Introduction

Patent foramen ovale (PFO) has been associated with several disease processes such as paradoxical embolism in cryptogenic stroke,1 arterial gas embolism due to decompression,2 or platypnea-orthodeoxia syndrome.3 In recent years, the role of PFO in cryptogenic stroke and migraine and its therapeutic management has generated debate4,5,6,7,8,9,10 and the clinical method of choice for the diagnosis and quantification of right-to-left shunt remains undecided.11,12,13 Agitated saline serum has been used in transthoracic echocardiography (TTE), transesophageal echocardiography (TEE) and transcranial Doppler ultrasound (TCD) in the detection of intracardiac shunts. Although TEE has been considered the reference technique in PFO diagnosis, recent studies have suggested that it leads to false negatives due to the problems involved in performing the Valsalva maneuver.14,15,16,17 On the other hand, its association with atrial septal aneurysm (ASA) and its assessment of the severity of the shunt have been associated with an increased risk of recurrence.18,19 The use of TTE with harmonic imaging has led to the improved assessment of interatrial shunt.14,15,16,17,20 Few studies have analyzed the most suitable strategy for the diagnosis and quantification of PFO. The aim of the present study was to compare the results obtained by the simultaneous performance of TEE with TCD and of TTE with TCD in the diagnosis and quantification of shunt due to PFO and to define the most suitable diagnostic strategy for its assessment in clinical practice.

Methods

We conducted a prospective study which included 134 patients (75 men and 59 women, mean age 46.4±14.2 [17–75] years) referred to the echocardiography laboratory by the neurology department to rule out PFO after presenting transient stroke (28; 21%), stroke (91; 68%), or migraine episodes (15; 11%). The study was approved by the Vall d’Hebron Hospital Ethics Committee and all the patients had previously given signed informed consent. Previous intracranial or extracranial arterial disease, abnormalities on TCD, or lacunar infarction were ruled out using computed tomography or magnetic resonance imaging. Table 1 shows the characteristics of the study population.

Table 1. Demographic Characteristics of the Population.

Patients 134
Age (years) 46.4±14.2 (17–75)
Men 75 (56)
Women 59 (44)
Smoking 57 (43)
Hypertension 31 (23)
Diabetes mellitus 12 (9)
Dyslipidemia 35 (26)

Data are expressed as n (%) or mean±standard deviation (range).

Protocol

TCD with TTE were performed simultaneously and then, 5minutes later, TCD with TEE, using agitated saline solution to detect right-to-left shunt. The patient was in left lateral decubitus position during both studies. The Valsalva maneuver, which all patients had been taught to perform, was considered effective when there was a peak Doppler flow velocity reduction>25% in the middle cerebral artery21 (Figure 1).

Figure 1. Transcranial Doppler ultrasound recording during Valsalva maneuver. The arrow indicates the beginning of the Valsalva maneuver.

Transcranial Doppler Ultrasound

The TCD study was performed using a TCD 100 ML system (Spencer Technology, Seattle, Washington, USA) and MultiDop X4 (DWL Electronic Systems, Sipplingen, Germany). Middle cerebral artery flow was monitored through the temporal bone window using a 2MHz transducer. The TCD transducer was kept in place with an elastic headband fitted with the probe at a depth of 65mm with stable insonation. The study was performed by a neurologist specialized in this technique and blinded to the results of the echocardiographic study.

The middle cerebral artery blood flow velocity value obtained by TCD, simultaneously performed with TTE and with TEE, served as a reference to confirm the effectiveness of the Valsalva maneuver.

Transthoracic Echocardiography

All the studies were performed using the Vivid 7 system (General Electric, Milwaukee, Wisconsin, USA) fitted with a 4.3MHz multi-frequency probe with harmonic imaging. The apical 4-chamber view was used to optimize visualization of the atria, ventricles and interatrial septum (Figure 2). In total, 3 patients had a suboptimal acoustic window, but were not excluded from the study. ASA was diagnosed when there was a ≥10-mm midline shift in anatomical M-mode or when total bidirectional shift was >15mm.

Figure 2. Transthoracic echocardiography showing contrast medium passing through the patent foramen ovale.

Transesophageal Echocardiography

TEE with color Doppler was performed using the same system fitted with a 2.9-8MHz multi-frequency probe. To improve tolerance to the test, patients were sedated with intravenously administered midazolam at a starting dose of 2mg followed by 2-mg increments until tolerance was reached and the patient felt comfortable. Blood pressure, heart rate and oxygen saturation were monitored. Baseline values were recorded during TTE and once every minute during TEE. An N-550 pulse oximeter (Nellcor, Boulder, Colorado, USA) and an automatic M4-I Intellisense blood pressure gauge (Omron, Schaumburg, Illinois, USA) were used.

In line with the study aims, the area of the atrial septum in which the foramen ovale was located was visualized in the sagittal plane between 90o and 110o in the caval view (Figure 3). Maximum PFO diameter was measured during the Valsalva maneuver at the distal extreme of the tract formed by the ostium primum and ostium secundum. ASA was diagnosed using the same criteria described for the TTE study.

Figure 3. Transesophageal echocardiography showing contrast medium passing through the patent foramen ovale.

Agitated Saline Contrast Test

A mixture of 9mL physiological saline and 1mL air was agitated 10 times in 210-mL syringes connected to a 3-way stopcock to exchange the air-saline mix and achieve good dilution. The bolus of saline solution was injected via an antecubital vein. The study was not begun until adequate filling of the right atrium was achieved. At least 2 injections were administered at baseline and up to 2 injections with the Valsalva maneuver in both the TTE and TEE studies. The Valsalva maneuver was begun when the contrast filled the right atrium and was maintained for >5s; the shunt was assessed during the first 3 heartbeats following the Valsalva maneuver. During TEE, the passage of contrast medium through the PFO was assessed; if its passage was not visualized, additional injections were administered and the openings of the pulmonary veins assessed to rule out intrapulmonary shunt.

Diagnosis and Quantification

The TTE or TEE contrast studies were considered positive for PFO when bubbles were observed in the left atrium within the first 3 heartbeats after opacification of the right atrium, whether at baseline or after the Valsalva maneuver. The severity of the shunt was quantified as mild (<10 microbubbles), moderate (10-20 microbubbles), or severe (>20).16 Right-to-left shunt was diagnosed when TCD detected microsignals in the middle cerebral artery, and the degree of severity was quantified according to established criteria22 (Figure 4). A definitive diagnosis of PFO was established when there was concordance between the 2 techniques in their diagnosis.

Figure 4. Quantification of the shunt by transcranial Doppler ultrasound.

Statistical Analysis

Sensitivity, specificity and predictive values were determined by the percentage of patients with true positive and true negative results (95% confidence interval). The criteria applied for diagnosing true positives and true negatives was concordance between 2 of the 3 techniques (TTE, TEE and TCD) in the diagnosis of PFO. The diagnostic accuracy of TCD was established during simultaneous TTE study, since in clinical practice TCD is performed without sedation. Continuous values were expressed as mean±standard deviation. The kappa test was used to assess concordance in quantifying the severity of the shunts using different methods. The SPSS 13.0 software package was used for statistical analysis. A P value of <0.05 was used as a cutoff for statistical significance.

Results

In total, 93 (69%) of the 134 patients studied were diagnosed with PFO.

Diagnosis of Right-to-Left Shunt

The right-to-left shunt was visualized at baseline by TTE in 69 patients (74%), TCD in 64 (69%), and TEE in just 54 (58%). The Valsalva maneuver was effective in all TTE studies. In 10 patients, the Valsalva maneuver was considered ineffective during TEE, thus external abdominal compression was performed until a reduction >25% in peak blood flow velocity was obtained in the middle cerebral artery. The Valsalva maneuver produced a similar improvement in the diagnosis of right-to-left shunt not visualized at baseline in each of the 3 techniques: TTE 24/93 (26%), TCD 26/93 (28%), and TEE 26/93 (28%). The sensitivity, specificity, and predictive values of the 3 techniques are shown in Table 2.

Table 2. Diagnosis of Patent Foramen Ovale Using Different Imaging Techniques.

  Sensitivity, % Specificity, % PPV, % NPV, %
Transcranial Doppler ultrasound 97 98 99 93
Transthoracic echocardiography 100 100 100 100
Transesophageal echocardiography 86 100 100 76

NPV, negative predictive value; PPV, positive predictive value.

Differences in the Diagnosis of Patent Foramen Ovale

During the TTE study, TCD failed to diagnose 3 mild shunts and gave a false positive in 1 patient with a pulmonary arteriovenous fistula, showing the contrast medium reaching the left atrium from a pulmonary vein (Figure 5). TCD performed during the TEE study failed to diagnose 2 mild shunts shown by TEE and gave the same false positive in the patient with pulmonary arteriovenous fistula. In 13 patients, TEE did not diagnose a shunt shown by TTE, which was mild in 11 cases, moderate in 1 and severe in 1 (Table 3). TCD performed simultaneously with TTE diagnosed 12 (13%) shunts more than when TCD was performed simultaneously with TEE; of these, 10 were mild, 1 moderate and 1 severe.

Figure 5. Transthoracic echocardiography in apical 4-chamber view showing contrast-filled right cavities and bubbles arriving from the right inferior pulmonary vein (arrow) in the left atrium.

Table 3. Echocardiographic Characteristics and Sedation Dose in Cases of False Negatives by Transesophageal Echocardiography.

Patient Shunt on TCD Shunt on TTE ASA Midazolam (mg) during TEE
1 No Mild No 8
2 No Mild Yes 10
3 No Mild No 8
4 Mild Mild No 8
5 Mild Mild No 6
6 Mild Mild Yes 5
7 Mild Mild No 12
8 Mild Mild Yes 8
9 Mild Mild No 10
10 Mild Mild Yes 8
11 Moderate Mild No 6
12 Moderate Moderate Yes 8
13 Severe Severe No 9

Abbreviations: ASA, atrial septal aneurysm; TCD, transcranial Doppler ultrasound; TEE, transesophageal echocardiography; TTE, transthoracic echocardiography.

The dose of midazolam was similar in the group of patients in whom the results of TTE and TEE were in concordance and the group in whom results differed (8.1±3.2mg vs 8.2±1.3mg, respectively). During the TEE study, heart rate increased (74±18 bpm vs 94±18 bpm; P<.001), whereas there was a decrease in systolic blood pressure (121±11 mmHg vs 101±32 mmHg; P<.05) and oxygen saturation (98%±2% vs 93%±4%; P<.001). There were no significant differences in diastolic blood pressure (72±8 mmHg vs 72±10 mmHg).

Quantification of the Shunt

Shunt was quantified as severe by TTE in 69% of the patients (64/93), by TCD in 76% (68/90) and by TEE in 59% (47/80) (Figure 6). In the quantification of shunt, concordance between TTE and TCD was 93% (84/90) (κ=0.83; P<.0001); between TEE and TCD, 74% (59/80) (κ=0.41; P<.0001); and between TTE and TEE, 81% (65/80) (κ=0,59; P<.0001). As visualized by TEE, PFO size during the Valsalva maneuver was 3.81±2.62mm in the patients with shunt and only 0.3±0.8mm in the patients without shunt (P<.001). PFO diameter was greater in the patients with a more severe shunt as determined by TTE; thus, in patients with a mild shunt the diameter was 2.3±1.3mm; with moderate shunt, 3.6±1.6mm; and with severe shunt, 5.6±3.5mm (P<.001).

Figure 6. Quantification of the shunt using the 3 techniques. TCD, transcranial Doppler ultrasound; TEE, transesophageal echocardiography; TTE, transthoracic echocardiography.

Atrial Septal Aneurysm

In 57 patients with right-to-left shunt, TEE study diagnosed ASA (61%), whereas in the patients without PFO ASA was only found in 5/41 patients (12%). TTE study diagnosed ASA in all patients except for one. The patients with PFO and ASA more often presented moderate or severe shunt than the patients with PFO without ASA (71% vs 13%; P<.001).

Discussion

This study assessed a large series of patients to rule out the presence of right-to-left shunt, and demonstrated that TTE is superior to TEE in the diagnosis of PFO. TEE gave a false negative in more than 10% of the patients and tended to underestimate the severity of right-to-left shunt. TCD performed simultaneously with TTE and with TEE showed that these false negatives were not due to the imaging technique used itself, since TCD performed during TEE also gave a similar number of false negatives. TEE is less sensitive than TTE in the diagnosis of right-to-left shunt at baseline, with a similar number of cases diagnosed with Valsalva maneuver. The results are of clinical importance, since they suggest that TEE does not provide greater accuracy in the diagnosis and quantification of PFO than TTE or TCD. TEE would be indicated only in the presence of poor echocardiographic windows or when assessing the morphological characteristics of PFO before percutaneous closure.

Diagnosis of Patent Foramen Ovale by Different Imaging Techniques

Several studies have assessed the usefulness of TCD6,13,23, TTE14,15,16,17,20 and TEE24,25 in the diagnosis of PFO, but differences in the results obtained have led to great controversy. Neurologists have widely used TCD to diagnose PFO. Comparative studies with TEE suggest that its sensitivity is higher than 90%, but that its specificity is 65%-90%.15,26,27 Several studies have suggested that the low specificity of TCD may be due to extracardiac shunts.26 In the present study, there was good concordance between the TCD performed simultaneously with the 2 echocardiographic techniques, with only 1 false positive due to a right-to-left shunt arising from a pulmonary fistula. TCD did not detect 3 mild shunts diagnosed by TTE and 2 mild shunts diagnosed by TEE. These results show that a limitation of TCD is that it cannot be used to visualize the contrast medium entering the right atrium, and thus the Valsalva maneuver may not be performed whenthe right atrium is completely filled with contrast, and consequently mild shunts may be overlooked.

Several previous studies highlighted the low sensitivity of TTE compared to TEE, because interatrial shunt was detected in only 31%-47% of cases.27,28 The suboptimal quality of the images is considered the most limiting factor.29 Nevertheless, with the introduction of harmonic imaging, image quality and the detection of microbubbles in agitated serum have markedly improved. Recent studies have noted that TTE with harmonic imaging and TEE have similar accuracy in the detection of right-to-left atrial shunt14,20,30 and it is accepted that, when image quality is good, TTE can be effective in the detection of PFO.31

In young patients without clinical evidence of heart disease or atrial fibrillation, TTE appears to be effective in the diagnosis and quantification of PFO. Recently, preliminary studies have suggested the possible use of 3-dimensional TTE for this diagnosis.32,33

False Negatives on Transesophageal Echocardiography

in total, 13 of the 93 patients with PFO (14%) were not diagnosed on TEE; 2 had moderate-severe shunt. In some studies, TEE obtained false negatives in the diagnosis of PFO, which wereattributed to a poorly performed Valsalva maneuver.26 In the study conducted by Kúlhet al,14 interatrial shunt was not diagnosed on TEE in 6 of 57 patients with PFO diagnosed by TTE.

Both sedation and esophageal intubation are considered limiting factors when performing an adequate Valsalva maneuver. Nevertheless, in our series, the Valsalva maneuver contributed to a similar number of positive diagnoses on TTE (26%) and on TEE using moderate sedation (33%). Strikingly, without the Valsalva maneuver, TTE diagnosed shunt in 74% of patients and TEE in only 58%. Souteyrand et al15 showed that at baseline TTE diagnosed shunt in 50% of patients, whereas TEE with moderate sedation (midazolam 5mg) only diagnosed shunt in 33%. There is no definitive explanation for these results, but it is possible that the delicate balance between intra-atrial pressures34 can be modified by small hemodynamic changes due to sedation or esophageal intubation itself.

The present study is the first to use TCD simultaneously with TTE and with TEE, showing that, under moderate sedation and with esophageal intubation, TCD has reduced sensitivity to detect right-to-left shunt. On the other hand, continuous monitoring during the procedure demonstrated significant reductions in systemic systolic blood pressure and an increase in heart rate. This hemodynamic response can be explained by the fact that midazolam moderately reduces systolic blood pressure and also the mean pulmonary blood pressure.35,36 On the other hand, low-dose atropine and the difficulties involved in the test itself can explain tachycardia during TEE. It may be that these hemodynamic changes or intubation hinder the reversal of the interatrial right-to-left pressure gradient34 and thus the passage of microbubbles between the atria.

Severity of Right-to-Left Shunt and Assessment of Atrial Septal Aneurysm

This study demonstrated that TEE can underestimate the severity of shunt, probably due to the difficulty involved in performing an adequate Valsalva maneuver in sedated patients. PFO size (maximum separation) during the Valsalva maneuver was significantly greater depending on the degree of shunt, and it was observed that all the patients who had a PFO diameter >4mm presented moderate or severe shunt.

ASA is frequently associated with PFO and increases the risk of stroke recurrence.4,37 Although TCD cannot be used to diagnose ASA, both TTE and TEE are of use in its detection. Harmonic imaging facilitates diagnosis by TTE, with accuracy similar toTEE. In the present study, 57 of the patients with PFO presented ASA (61%), whereas among the patients without PFO only 5/41 patients (12%) presented ASA.

Limitations

The results of the present study are only applicable to the selected population group. The patients received moderate sedation that was slightly higher than that administered in other series. TEE is a semi-invasive test that is poorly tolerated without sedation, especially in the young population. In this regard, we followed the same sedation protocol as for other indications of the technique, since the assumption that the degree of intolerance would be greater for this indication appeared questionable. Although the patients were instructed in the correct performance of the Valsalva maneuver and its effectiveness was verified by a 25% reduction in middle cerebral artery peak flow velocity on TCD, this does not mean that the intensity of the Valsalva maneuver was identical to that performed without sedation and without esophageal intubation. The study did not analyze observer or interobserver variability, given that the greatest variability is generated by administration of the contrast medium and the effectiveness of the Valsalva maneuver, rather than by reviewing the acquired images, and that it was considered unethical to repeat the tests, given the study design.

Conclusions

TTE with harmonic imaging and the administration of agitated physiological saline solution enables adequate assessment and quantification of right-to-left shunt due to PFO. TEE with moderate sedation tends to give false negatives and underestimates the severity of the shunt. However, the TEE technique would be especially indicated in cases of poor image quality or to accurately assess the morphology of the interatrial partition when PFO closure is planned.

Conflicts of interest

None declared.

Acknowledgements

We would like to thank the registered nurses Rosa M. García and Carmen Abad for their invaluable assistance and collaboration in conducting the studies.

Received 14 April 2010
Accepted 12 October 2010

Corresponding author: Pg. Vall d’Hebron, 119-129, 08035 Barcelona, Spain. mtegonzalez@vhebron.net

Bibliography
[1]
Schuchlenz HW, Weihs W, Horner S, Quehenberger F..
The association between the diameter of a patent foramen ovale and the risk of embolic cerebrovascular events..
Am J Med, 109 (2000), pp. 456-462
[2]
Knauth M, Ries S, Pohimann S, Kerby T, Forsting M, Daffertshofer M, et al..
Cohort study of multiple brain lesions in sport divers: role of a patent foramen ovale..
BMJ, 314 (1997), pp. 701-705
[3]
Godart F, Rey C, Prat A, Vincentelli A, Chmait A, Francart C, et al..
Atrial right-to-left shunting causing severe hipoxaemia despite normal right-sided pressures: report of 11 consecutive cases corrected by percutaneous closure..
Eur Heart J, 21 (2000), pp. 483-489
[4]
Agmon Y, Khandheria BK, Meissner I, Gentile F, Whisnant JP, Sicks JD, et al..
Frequency of atrial septal aneurysms in patients with cerebral ischemic events..
Circulation, 99 (1999), pp. 1942-1944
[5]
Kerut EK, Norfleet WT, Plotnick GD, Giles T.D..
Patent foramen ovale: a review of associated conditions and the impact of physiological size..
J Am Coll Cardiol, 38 (2001), pp. 613-623
[6]
Serena J, Martí-Fàbregas J, Santamarina E, Rodríguez JJ, Pérez-Ayuso MJ, Masjuán J, et al..
Recurrent stroke and massive right-to-left shunt. Results from the prospective spanish multicenter (CODICIA) Study..
Stroke, 39 (2008), pp. 3131-3136
[7]
Mesa D, Franco M, Suárez de Lezo J, Muñoz J, Rus C, Delgado M, et al..
Prevalencia de foramen oval permeable en pacientes jóvenes con accidente isquémico cerebral de causa desconocida..
Rev Esp Cardiol, 56 (2003), pp. 662-668
[8]
Meier B..
Catheter-based closure of the patent foramen ovale..
Circulation, 120 (2009), pp. 1837-1841
[9]
Natanzon A, Goldman M.E..
Patent foramen ovale: anatomy versus pathophysiology. Which determines stroke risk?..
J Am Soc Echocardiogr, 16 (2003), pp. 71-76
[10]
Hara H, Virmani R, Ladich E, Mackey-Bojack S, Titus J, Reisman M, et al..
Patent foramen ovale: current pathology, pathophysiology, and clinical status..
J Am Coll Cardiol, 46 (2005), pp. 1768-1776
[11]
Woods T, Patel A..
A critical review of patent foramen ovale. Detection using saline contraste echocardiography: when bubbles lie..
J Am Soc Echocardiogr, 19 (2006), pp. 215-222
[12]
Attaran RR, Ata I, Kudithipudi V, Foster L, Sorrell V.L..
Procol for optimal detection and exclusion of a patent foramen ovale using transthoracic echocardiography with agitated saline microbubbles..
Echocardiography, 23 (2006), pp. 616-622
[13]
Droste DW, Lakemeier S, Wichter T, Stypmann J, Dittrich R, Ritter M, et al..
Optimizing the technique of contrast transcranial Doppler ultrasound in the detection of right-to-left shunts..
Stroke, 33 (2002), pp. 2211-2216
[14]
Kühl HP, Hoffmann R, Merx MW, Franke A, Klötzsch C, Lepper W, et al..
Transthoracic echocardiography using second harmonic imaging diagnostic alternative to transesophageal echocardiography for atrial right to left shunt in patients with cerebral embolic events..
J Am Coll Cardiol, 34 (1999), pp. 1823-1830
[15]
Souteyrand G, Motreff P, Lusson JR, Rodríguez R, Geoffroy E, Dauphin C, et al..
Comparison of transthoracic echocardiography using second harmonic imaging, transcranial Doppler and transesophageal echocardiography fort he detection of patent foramen ovale in stroke patients..
Eur J Echocardiogr, 7 (2006), pp. 147-154
[16]
Van Camp G, Franken P, Melis P, Cosyns B, Schoors D, Vanoverschelde J.L..
Comparison of transthoracic echocardiography with second harmonic imaging with transesophageal echocardiography in the detection of right to left shunts..
Am J Cardiol, 86 (2000), pp. 1284-1287
[17]
Daniels C, Weytjens C, Cosyns B, Schoors D, De Sutter J, Paelinck B, et al..
Second harmonic transthoracic echocardiography: the new reference screening method fort he detection of patent foramen ovale..
Eur J Echocardiogr, 5 (2004), pp. 449-452
[18]
Mattioli AV, Bonetti L, Aquilina M, Olidani A, Longhini C, Mattioli G..
Association between atrial septal aneurysm and patent foramen ovale in young patients with recent stroke and normal carotid arteries..
Cerebrovasc Dis, 15 (2003), pp. 4-10
[19]
Homma S, Di Tullio MR, Sacco RL, Mihalatos D, Li Mandri G, Mohr J.P..
Characteristics of patent foramen ovale associated with cryptogenic stroke: a biplane transesophageal echocardiographic study..
Stroke, 25 (1994), pp. 582-586
[20]
Trevelyan J, Steeds R.P..
Comparison of transthoracic echocardiography with harmonic imaging with transoesophageal echocardiography fort he diagnosis of patent foramen ovale..
Postgrad Med J, 82 (2006), pp. 613-614
[21]
Zanette EM, Mancini G, De Castro S, Solaro M, Cartoni D, Chiarotti F..
Patent foramen ovale and transcranial Doppler. Comparison of different procedures..
Stroke, 27 (1996), pp. 2251-2255
[22]
Nemec JJ, Marwich TH, Lorig RJ, Davison MB, Chimowitz MI, Litowitz H, et al..
Comparison of transcranial doppler ultrasound and transesophageal contrast echocardiography in the detection of interatrial right-to-left shunts..
Am J Cardiol, 68 (1991), pp. 1498-1502
[23]
Job FP, Ringelstein EB, Grafen Y, Frachskampf FA, Doherty C, Stockmanns A, et al..
Comparison of transcranial contrast doppler sonography and transesophageal contrast echocardiography for the detection of patent foramen ovale in young stroke patients..
Am J Cardiol, 74 (1994), pp. 381-384
[24]
Hausmann D, Mügge A, Becht I, Daniel W.G..
Diagnosis of patent foramen ovale by transesophageal echocardiography and association with cerebral and peripheral embolic events..
Am J Cardiol, 70 (1992), pp. 668-672
[25]
Pearson AC, Labovitz AJ, Tatineni S, Gomez C.R..
Superiority of transesophageal echocardiography in detecting cardiac source of embolism in patients with cerebral ischemia of uncertain etiology..
J Am Coll Cardiol, 17 (1991), pp. 66-72
[26]
Droste DW, Kriete JU, Stypman J, Castrucci M, Wichter T, Tietje R, et al..
Contrast transcranial doppler ultrasound in the detection of right-to-left shunts..
Stroke, 30 (1999), pp. 1827-1832
[27]
Zito C, Dattilo G, Oreto G, Di Bella G, Lamari A, Iudicello R, et al..
Patent foramen ovale: comparison among diagnostic strategies in cryptogenic stroke and migraine..
Echocardiography, 26 (2009), pp. 495-502
[28]
Di Tullio M, Sacco RL, Venketasubramanian N, Sherman D, Mohr JP, Homma S..
Comparison of diagnostic techniques for the detection of a patent foramen ovale in stroke patients..
Stroke, 24 (1993), pp. 1020-1024
[29]
Belkin RN, Pollack BD, Ruggiero ML, Alas LL, Tatini U..
Comparison of transesophageal and transthoracic echocardiography with contrast and color flow Doppler in the detection of patent foramen ovale..
Am Heart J, 128 (1994), pp. 520-525
[30]
Clarke NR, Timperley J, Kelion AD, Banning A.P..
Transthoracic echocardiography using second harmonic imaging with Valsalva manoeuvre for the detection of right to left shunts..
Eur J Echocardiogr, 5 (2004), pp. 176-181
[31]
Pepi M, Evangelista A, Nihoyannopoulos P, Flachskampf FA, Athanassopoulos G, Colonna P, et al..
Recommendations for echocardiography use in the diagnosis and management of cardiac sources of embolism..
Eur J Echocardiogr, 11 (2010), pp. 461-476
[32]
Monte I, Grasso S, Licciardi S, Badano L.P..
Head-to-head of real-time three-dimensional transthoracic echocardiography with transthoracic and transesophageal two-dimensional contrast echocardiography for the detection of patent foramen ovale..
Eur J Echocardiogr, 11 (2010), pp. 245-249
[33]
Maffè S, Dellavesa P, Zenone F, Paino AM, Paffoni P, Perucca A, et al..
Transthoracic second harmonic two-and three-dimensional echocardiography for detection of patent foramen ovale..
Eur J Echocardiogr, 11 (2010), pp. 57-63
[34]
Pfleger S, Haase K, Stark S, Latsch A, Simonis B, Scherhag A, et al..
Haemodynamic quantification of different provocation manoeuvres by simultaneous measurement of right and left atrial pressure: implications for the echocardiographic detection of persistent foramen ovale..
Eur J Echocardiogr, 2 (2001), pp. 88-93
[35]
Carrasco G, Cabré L, Sobrepera G, Costa J, Molina R, Cruspinera A, et al..
Synergistic sedation with propofol and midazolam in intensive care patients after coronary artery bypass grafting..
Crit Care Med, 26 (1998), pp. 844-851
[36]
Pomane C, Paullin M, Fernández C, Vignon E, Francois G..
Hemodynamic effects of 2 different doses of midazolam in combination with fentanyl for induction of anesthesia in surgery of the abdominal aorta..
Ann Fr Anesth Reanim, 3 (1984), pp. 168-170
[37]
Mügge A, Daniel WG, Angermann C, Spes C, Khandheria BK, Kronzon I, et al..
Atrial septal aneurysm in adult patients. A multicenter study using transthoracic and transesophageal echocardiography..
Circulation, 91 (1995), pp. 2785-2792
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Revista Española de Cardiología (English Edition)

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