Three-Dimensional Agitated Saline Contrast Transesophageal Echocardiography for the Diagnosis of Patent Foramen Ovale

doi:10.21203/rs.3.rs-4895463/v1

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Research Article

Three-Dimensional Agitated Saline Contrast Transesophageal Echocardiography for the Diagnosis of Patent Foramen Ovale

https://doi.org/10.21203/rs.3.rs-4895463/v1

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Background

Patent foramen ovale (PFO) is a three-dimensional (3D) and dynamic structure, making it challenging to diagnose with 2D imaging. We aimed to develop a practical protocol for 3D agitated saline contrast (ASC) transesophageal echocardiography (TEE), evaluate its feasibility, and identify implications for the diagnosis of patent foramen ovale (PFO) in patients with ischemic stroke.

Methods

In 158 patients (52 women; age: 63.6 ± 14.0 years) with ischemic stroke who were referred for TEE to evaluate the cardiac source of embolism, TEE was performed using the EPIQ CVx ultrasound system (Philips Medical Systems, Andover, MA) with a 2–8 MHz transesophageal matrix array transducer (X8-2t). ASC tests were performed with 2D and 3D images. According to the results of each method, patients were classified into four groups: no shunt, possible PFO, definite PFO, and intrapulmonary shunt.

Results

The practical 3D ASC protocol consisted of two images: one in the 90°–120° bicaval view and another in the 40°–70° short-axis view. These images were acquired to include both the left upper pulmonic vein and interatrial septum at the mid-esophageal position. Image acquisition and analysis of 3D TEE images were feasible in 150 patients (94.9%). By applying the 3D ASC protocol, 32 patients (21.3%) were reclassified into another group, and 16 (10.7%) had their diagnosis changed. Definite PFO cases increased from 20 (13.3%) to 35 (23.3%) patients.

Conclusion

The practical 3D TEE protocol for diagnosing PFO was feasible in patients with ischemic stroke. Adding a practical 3D ASC protocol to 2D TEE aids in the accurate diagnosis of PFO.

Three-dimensional

Agitated saline contrast

Transesophageal echocardiography

Patent foramen ovale

Patent foramen ovale (PFO) has been known to cause cryptogenic stroke and recurrent ischemic stroke in various clinical situations [1–3]. Therefore, it is clinically important to accurately diagnose PFO and evaluate its functional grade and structure to appropriately select patients who require PFO closure and prevent recurrent stroke [4–6]. An agitated saline contrast (ASC) study based on 2D transesophageal echocardiography (TEE) has been used as the gold standard for PFO diagnosis [7–9]. In the real world, TEE is particularly useful in evaluating PFO anatomy in patients with cryptogenic stroke and suspected PFO [10]. However, because the 2D image only shows one plane in the 3D space, it has limited accuracy in identifying the PFO opening and often makes it challenging to capture air bubbles entering the left atrium (LA). In addition, the differential diagnosis of PFO from extracardiac shunt remains challenging in clinical practice even if the three-to-five-beat rule is applied [8, 11, 12]. This is because capturing the atrial septum and pulmonary vein on one screen in 2D images is difficult; therefore, checking the path and 3D direction of the air bubble movement is challenging. Consequently, ambiguous cases can be misdiagnosed as false-positive or false-negative PFO in the ASC test [13].

Three-dimensional image acquisition during TEE has become common in various clinical situations due to recent advances in 3D TEE techniques [14–16]. Some efforts have been made to utilize 3D TEE for the detection and structural evaluation of PFO [17, 18]. Theoretically, 3D TEE can visualize the entire PFO anatomy and surrounding structures and is likely to show high certainty in differentiating intracardiac shunt from extracardiac shunt [18]. However, in real clinical practice, poor image quality during the Valsalva maneuver, the requirement of recording 3D images for at least ten beats after relieving the Valsalva maneuver, and patient discomfort during the additional acquisition time for 3D images are major barriers to the application of 3D techniques in evaluating the cause of paradoxical right-to-left shunt. Considering that the spatial and temporal resolutions of 3D TEE have improved remarkably, we speculated that 3D TEE could be of practical use for PFO diagnosis and intrapulmonary shunt (IPS) discrimination if a protocol that minimizes the necessity of additional images is applied. Therefore, we attempted to develop a practical protocol to detect PFO using 3D TEE, evaluate its feasibility, and explore the advantages and incremental value of 3D TEE compared to 2D TEE in detecting PFO in patients with ischemic stroke.

Study population

We enrolled 158 patients with ischemic stroke who underwent TEE between April 2021 and January 2023 at Severance Cardiovascular Hospital, Seoul, Korea, for the evaluation of the cardiac source of embolism. Ischemic stroke was confirmed by a focal neurological deficit with sudden onset and by magnetic resonance imaging findings. Patients’ clinical information was obtained at the time of TEE. National Institutes of Health Stroke Scale (NIHSS) scores and stroke etiology were investigated. The etiologies were classified into three categories: embolic stroke of undetermined source (ESUS), atherosclerosis, and lacunar infarction [19]. A total of 150 patients were included in the final analysis after excluding eight patients with unsuitable images because of inappropriate Valsalva maneuvers or poor image quality. The study was approved by the Institutional Review Board of Yonsei University Health System (IRB number: 4-2023-0318) and was conducted following the Declaration of Helsinki.

Diagnosis of PFO using 2D and 3D TEE

TEE was performed using the EPIQ CVx ultrasound system (Philips Medical Systems, Andover, MA, USA) equipped with a 2–8 MHz transesophageal matrix array transducer (X8-2t), which has the benefit of faster data processing, improved image quality, and tailored examination tools. Standard 2D assessments were performed as recommended by the American Society of Echocardiography [20]. The same examiner acquired the 3D dataset of the PFO at the end of the standard 2D examination.

Based on the 2D and 3D TEE results, patients were classified as no shunt, possible PFO, definite PFO, or IPS. If no air bubbles appeared in the LA, the patient was classified into the no-shunt group. The presence of PFO is determined by agitated saline bubbles shunting to the LA within three cardiac cycles (grade 1, fewer than 10 bubbles; grade 2, 10–30 bubbles; and grade 3, > 30 bubbles) and is often augmented by the Valsalva maneuver, which provokes bubbles to pass with elevated right atrial pressure [8]. Definite PFO was diagnosed when the separation of the septum primum and the secundum was visualized with the air bubbles of agitated saline solution passing through it [21]. Possible PFO was defined as meeting the diagnostic criteria for PFO (appearance of air bubbles in the LA within five cardiac beats after opacification of the RA) but does not satisfy the criteria for definite PFO. If air bubbles appeared in LA after three or more cardiac cycles and were observed inside the pulmonary veins moving into the LA, the patient was classified into the IPS group. In patients with PFO confirmed by 3D imaging, the number of bubbles was compared with that in 2D images [22]. Atrial septal aneurysm (ASA) was defined as ≥ 10 mm of excursion from the midline [23]. A complex aortic plaque was defined as a plaque that protrudes at least 4 mm into the aortic lumen or a plaque that is associated with ulceration or mobile features [24]. Both 2D cine loops and real-time 3D echocardiographic datasets were stored digitally in raw format and analyzed using the software embedded in TEE (namely, EPIQ CVx).

Novel 3D protocol for PFO

The most important principle of the novel 3D TEE protocol for PFO detection was that the 3D image should facilitate the demonstration of a PFO en face and demonstrate its relationship with surrounding structures, including the right atrium, LA, and aorta. Furthermore, to differentiate PFO from IPS, which also shows the appearance of air bubbles in the LA, a view demonstrating both the atrial septum and pulmonic vein might be helpful. The new protocol should not only satisfy the above principles and maximize the advantages of 3D images but should also be practical by minimizing the additional effort of the examiner, the time required for image acquisition, and the patient’s inconvenience. This was considered feasible if the 3D TEE images included the interatrial septum, LA, and pulmonary vein.

Statistical analysis

Continuous variables are presented as means ± standard deviations, and categorical variables are expressed as percentages of the total group. Each 2D and 3D TEE image was evaluated by three blinded observers and a single observer at two different time points. The interobserver and intra-observer variabilities in the diagnosis of PFO and IPS were assessed by calculating the k statistics using the Fleiss method [25].

Baseline characteristics

Table 1 shows the baseline characteristics of the study population. The mean age was 63.6 ± 14.1 years, and 52 patients (34.7%) were female. Among the patients, 112 (74.7%) had hypertension, 57 (38.0%) had diabetes mellitus, 22 (14.7%) had atrial fibrillation, and 93 (59.2%) had dyslipidemia. The etiologies of stroke were ESUS in 127 patients (84.7%), atherosclerosis in 15 patients (10.0%), and lacunar infarction in seven patients (4.7%). The mean NIHSS score was 1.0 (interquartile range: 0.0–3.0), and 23 patients (14.6%) had a history of ischemic stroke. Two-dimensional echocardiography showed LAA thrombus in one patient (0.7%), spontaneous echo contrast in the LAA in five patients (3.3%), ASA in seven patients (4.7%), and complex atheroma in the aortic arch or descending thoracic aorta in 11 patients (7.3%). PFO was diagnosed in 43 patients (28.7%) using 2D TEE, and PFO grades 1, 2, and 3 were observed in 28 (65.1%), 10 (23.3%), and five (11.6%) patients, respectively (Table 2).

Table 1

Baseline characteristics of the study population
	N = 150
Age, years	63.6 ± 14.1
Female, n (%)	52 (34.7)
Body mass index, kg/m²	25.4 ± 3.3
Hypertension, n (%)	112 (74.7)
Diabetes mellitus, n (%)	57 (38.0)
Dyslipidemia, n (%)	93 (59.2)
Atrial fibrillation, n (%)	22 (14.7)
Smoking, n (%)	41 (27.3)
Etiology of Stroke, n (%)
ESUS	128 (85.3)
Atherosclerosis	15 (10.0)
Lacunar	7 (4.7)
NIHSS	1.0 (0.0–3.0)
Recurrent ischemic stroke, n (%)	23 (14.6)

ESUS, Embolic stroke of Undetermined Source; NIHSS, National. Institute of Health Stroke Scale; 2D, two-dimensional; LAA, left atrial appendage

Table 2

2D and 3D characteristics of transesophageal echocardiography
	N = 150
2D
LAA thrombus, n (%)	1 (0.7)
Spontaneous echo contrast in LAA, n (%)	5 (3.3)
LAA emptying velocity, cm/s	70.4 ± 24.5
Complex atheroma, n (%)	11 (7.3)
Atrial septal aneurysm, n (%)	7 (4.7)
2D agitated saline contrast study
No shunt, n (%)	96 (64.0)
Definite PFO, n (%)	20 (13.3)
Possible PFO, n (%)	23 (15.3)
Intrapulmonary shunt, n (%)	11 (7.4)
Grading of PFO, n (%)	43 (28.7)
Grade 1 (< 10 air bubbles)	28 (65.1)
Grade 2 (10–30 air bubbles)	10 (23.3)
Grade 3 (> 30 air bubbles)	5 (11.6)
3D agitated saline contrast study
No shunt, n (%)	97 (64.7)
Definite PFO, n (%)	35 (23.3)
Possible PFO, n (%)	5 (3.3)
Intrapulmonary shunt, n (%)	13 (8.7)

LAA, left atrial appendage; 2D, two-dimensional; PFO, patent foramen ovale; 3D, three-dimensional

Development of a practical 3D TEE protocol for PFO

Figure 1 shows the practical 3D TEE protocol, which consists of two images: one in the 90°–120° degree bicaval view (Fig. 1A and Supplementary Video 1) and another in the 40°–70° degree short-axis view. These images were acquired to include both the left upper pulmonic vein and interatrial septum at the mid-esophageal position (Fig. 1B and Supplementary Video 2). Recordings were started at the time of the right atrium filling with agitated saline and relief of the Valsalva maneuver and lasted for at least 10 cardiac cycles. The 2D image was converted into a live 3D image using the 3D zoom mode in each view after adjusting the pyramidal datasets to include the IAS, particularly the PFO outlet within the LA side. The 3D images were prospectively stored for a loop length of 20 beats. The recording began when air bubbles filled the right atrium, which was immediately followed by the Valsalva maneuver. Multiple 3D display layouts were used during the recording and simultaneously displayed a 3D volume image and two multiplanar reformation images.

Feasibility of the newly developed 3D protocol

Image acquisition and analysis of the 3D TEE images were feasible in 150 patients (94.9%), and only eight patients had unsuitable 3D images among those who underwent 3D TEE. In the early stages of protocol development, the time required to obtain 3D images according to the protocol was 8.0 ± 3.2 minutes. However, after passing the learning curve with approximately 20 cases, the time required to obtain 3D images was reduced to 5.5 ± 2.3 minutes; the patients complained of minor discomfort only.

Incremental diagnostic value of the newly developed 3D protocol

Among the 150 patients, 2D TEE showed possible PFO in 23 patients (15.3%), definite PFO in 20 patients (13.3%), IPS in 11 patients (7.4%), and no air bubbles in the LA in 96 patients (64.0%).

When 3D TEE images were analyzed for 96 patients in the no-shunt group as categorized using 2D TEE, three patients were identified as having definite PFO, and one patient was identified as having IPS. Among the 23 patients judged as having possible PFO by 2D TEE, only five remained as having possible PFO after applying 3D TEE. A total of 18 patients (78.2%) were reclassified into the other groups: six with no shunt, 13 with definite PFO (Fig. 2A, Supplementary Video 3–4), and four with IPS (Fig. 2B, Supplementary Video 5–6). Most patients with definite PFO in 2D TEE also had definite PFO in 3D TEE. Eleven cases were judged as IPS in 2D TEE, and seven cases were reclassified as no shunt in 3D TEE. By applying the practical 3D ASC protocol to TEE, 32 patients (21.3%) were reclassified into another group, and 16 patients (10.7%) had their diagnosis changed. The number of patients classified as having definite PFO increased from 20 (13.3%) to 35 (23.3%) (Fig. 3).

Interobserver and intra-observer variability

Each observer diagnosed the shunt from 2D and 3D ASC-TEE (Table 3). The overall interobserver k value was 0.83 (0.77–0.89) in the 2D analysis and 0.89 (0.83–0.96) in the 3D analysis. The overall intra-observer k value was 0.83 (0.73–0.92) in the 2D analysis and 0.90 (0.83–0.97) in the 3D analysis (Table 4).

Table 3

Diagnosis of the shunt from 2D and 3D agitated saline contrast TEE by each observer
	Observer
	1	2	3
2D agitated saline contrast TEE
No shunt, n (%)	96 (64.0)	86 (57.3)	87 (58.0)
Definite PFO, n (%)	15 (10.0)	20 (13.3)	15 (10.0)
Possible PFO, n (%)	28 (18.7)	24 (16.0)	27 (18.0)
IPS, n (%)	11 (7.3)	20 (13.4)	21 (14.0)
3D agitated saline contrast TEE
No shunt, n (%)	98 (65.3)	93 (62.0)	95 (63.3)
Definite PFO, n (%)	36 (24.0)	35 (23.3)	33 (22.0)
Possible PFO, n (%)	5 (3.3)	7 (4.7)	7 (4.7)
IPS, n (%)	11 (7.3)	15 (10.0)	15 (10.0)

2D, two-dimensional; TEE, transesophageal echocardiography; PFO, patent foramen ovale; IPS, intrapulmonary shunt.

Table 4

Interobserver and intraobserver variability in the analysis of 2D and 3D TEE images
	Examiner 1	Examiner 2	Examiner 3
2D
Examiner 1	0.83 (0.73–0.92)	0.77 (0.69–0.86)	0.84 (0.75–0.93)
Examiner 2			0.74 (0.62–0.85)
Examiner 3
3D
Examiner 1	0.90 (0.83–0.97)	0.91 (0.84–0.98)	0.92 (0.86–0.99)
Examiner 2			0.83 (0.73–0.93)
Examiner 3

Overall k statistics for 2D (Fleiss method): 0.83 (0.77–0.89).

Overall k statistics for 3D (Fleiss method): 0.89 (0.83–0.96).

This study revealed the feasibility of a practical protocol of 3D ASC-TEE for PFO diagnosis. The 3D TEE protocol can directly and simultaneously observe the interatrial septum and pulmonic vein in 3D space and can determine the route of air bubbles entering the LA during the ASC test, thus leading to an accurate diagnosis of PFO compared with 2D TEE. In addition, because only two image acquisitions were performed, patient discomfort and time consumption could be minimized. This study provides a basis for the clinical application of a practical 3D protocol because it is important to accurately diagnose PFO in patients when evaluating the cardioembolic source of ischemic stroke.

When performing 2D TEE to evaluate a cardiac embolic source, many ambiguous cases are encountered in which a few air bubbles are observed in the LA without the definite separation of the septum primum and secundum or air bubbles coming into the LA from the pulmonary vein. In this study, 23 patients (15.3%) were likely to have PFO; however, this was unclear. Among these patients, 19 had a clear diagnosis of PFO. One patient had no shunt, and five were diagnosed with IPS. Thirteen of the 23 patients were diagnosed with definite PFO, thus adding to the certainty of the diagnosis by 3D TEE. By contrast, almost all patients with definite PFO in 2D TEE were also confirmed as having definite PFO in 3D TEE. Thus, it is more helpful in clinical practice to apply the 3D ASC protocol in cases where a definite PFO cannot be diagnosed using 2D TEE.

Figure 4 displays the number of air bubbles in the LA in 2D and 3D ASC-TEE in 35 patients diagnosed with definite PFO in 3D TEE. The number of air bubbles in 3D space was significantly higher than in 2D space because air bubbles are more visible in 3D space (9.1 ± 8.7 vs. 15.7 ± 14.1, P = 0.013). This result highlights the need to increase the standard number of air bubbles in the LA in the grading of PFO on 3D TEE.

Strengths and drawbacks of 3D ASC-TEE in diagnosing PFO

Real-time 3D TEE provides more detailed information on the interatrial septum than 2D TEE [17, 18, 21]. Three-dimensional TEE helps directly locate the site of separation of the PFO slit opening into the LA and observe microbubbles crossing through the PFO because it provides a live spatial image. In addition, 3D TEE acquires images of the entire LA space, including the interatrial septum, even when taken only once. Therefore, diagnosis through post-analysis after acquisition is possible, which can reduce examination time and patient discomfort. By contrast, 2D TEE requires multiple images to be acquired until a diagnosis is made. Therefore, patients with an ambiguous diagnosis from 2D TEE could be more accurately diagnosed by adding the 3D TEE technique via a comprehensive observation of the entire atrial septum and adjacent structures.

However, there are a few drawbacks to 3D TEE images. First, the image quality depends on the examiner's skill and ability to perform proper Valsalva maneuvers. Second, a 3D image has a lower temporal resolution than a 2D image. The narrowing of the sector of acquisition or multibeat acquisitions, typically used to improve temporal resolution, is difficult to apply to dynamically fluttering structures.

Future Perspectives

No standard for grading the severity of PFO based on the results of 3D TEE is present. In this study, the number of air bubbles in the 3D space of the LA was higher than that in the 2D space. In addition, even in the 3D images, there is no evidence that all the air bubbles in the LA were counted. Future perspectives for diagnosing PFO using 3D TEE would be to use color-coded air bubbles for easy tracking or to accurately count the number and time difference of air bubbles using artificial intelligence. If there are more advantages to 3D than 2D when applying new technology, the time for PFO diagnosis can be shortened by using only 3D instead of 2D in the future [26].

Study Limitations

This study had several limitations. First, this was a single-center study that was conducted using TEE equipment from a specific vendor. TEE was conducted by physicians familiar with 3D echoes by using advanced TEE probes and machines; therefore, it will be difficult to apply our results to different situations. Second, there is no gold standard for determining which 2D and 3D results are the most accurate. However, the results of some cases of PFO occlusion or CT pulmonary angiogram revealed that a 3D image could provide a more accurate diagnosis than a 2D image. Third, there are still cases in which the diagnosis is unclear even after applying the 3D protocol.

The 3D ASC-TEE protocol developed for the diagnosis of PFO is practical and feasible (94.9%) in patients with ischemic stroke. Three-dimensional TEE would be helpful for the accurate diagnosis of PFO not only in structural evaluation but also in functional evaluation in the era of transcatheter PFO closure. Therefore, this practical 3D TEE protocol for PFO could be applied as a routine clinical procedure for evaluating the cardiac source of embolism.

ASA

atrial septal aneurysm

ASC

agitated saline contrast

IPS

intrapulmonary shunt

left atrium

PFO

patent foramen ovale

TEE

transesophageal echocardiography

TTE

transthoracic echocardiography

Ethics approval and consent to participate

The study was approved by the Institutional Review Board of Yonsei University Health System (IRB number: 4-2023-0318) and was conducted in accordance with the Declaration of Helsinki.

Consent for publication

Not applicable

Availability of data and materials

The datasets generated and/or analysed during the current study are not publicly available due to limitations from the ethics committees in order to protect sensitive personal data.

Competing interests

The authors declare that they have no competing interests.

Funding

Nothing to declare.

Authors' contributions

SG and CS conceptualized this study. The data curation was carried out by SG, KK, HL, IC, and GH. Investigation efforts were made by SG and KK. The methodology was developed by SG, IC, JH, and CS. The project supervision was provided by CS. The original draft was written by SG. The review and editing were done by SG and CS. All authors read and approved the final manuscript.

Acknowledgments

We would like to express sincere gratitude to Hee Jeong Lee, Kyung Eun Ha, and Kyu-Yong Ko for their invaluable assistance in acquiring the echocardiographic images.

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No competing interests reported.

Video1.mp4
Supplementary Video 1. Practical 3D TEE protocol. Mid-esophageal 90°–120° degree bicaval view.
Video2.mp4
Supplementary Video 2. Practical 3D TEE protocol. Mid-esophageal 40°–70° degree short-axis view.
Video3.mp4
Supplementary Video 3. Air bubbles detected in LA without PFO slit separation; possible PFO in 2D TEE
Video4.mp4
Supplementary Video 4. Air bubbles detected in LA with PFO slit separation observed; definite PFO in 3D TEE
Video5.mp4
Supplementary Video 5. Air bubbles appeared in LA within 5 cardiac cycles after opacification of RA without PFO slit separation observed in 2D TEE; possible PFO
Video6.mp4
Supplementary Video 6. Air bubbles coming from the left pulmonic vein; IPS in 3D TEE

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Three-Dimensional Agitated Saline Contrast Transesophageal Echocardiography for the Diagnosis of Patent Foramen Ovale

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Abstract

Background

Methods

Results

Conclusion

Figures

Background

Methods

Study population

Diagnosis of PFO using 2D and 3D TEE

Novel 3D protocol for PFO

Statistical analysis

RESULTS

Baseline characteristics

Development of a practical 3D TEE protocol for PFO

Feasibility of the newly developed 3D protocol

Incremental diagnostic value of the newly developed 3D protocol

Interobserver and intra-observer variability

DISCUSSION

Strengths and drawbacks of 3D ASC-TEE in diagnosing PFO

Future Perspectives

Study Limitations

Conclusions

Abbreviations

Declarations

References

Additional Declarations

Supplementary Files

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