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Abstract

Background and Purpose— Carotid intima-media thickness (CIMT) is associated with systemic atherosclerosis and cardioembolic conditions and predicts the risk of recurrent strokes. We sought to establish the relationship between CIMT and cardiovascular sources of embolus (CSE) on transesophageal echocardiography (TEE) and hypothesized that a noninvasive strategy of CIMT assessment and transthoracic echocardiography bubble study would identify patients with ischemic stroke or transient ischemic attack in whom TEE would provide little incremental diagnostic yield.

Methods— In 180 patients with ischemic stroke or transient ischemic attack of undetermined origin referred for TEE, we prospectively performed CIMT measurement/plaque screen (Phase 1, n=96) or CIMT measurement/plaque screen and transthoracic echocardiography bubble study (Phase 2, n=84) before TEE. Phase 1 results were used to construct receiver operating characteristic curves to demonstrate the ability of CIMT to detect CSE on TEE and to identify the optimal CIMT cutoff value for prospective strategy testing (Phase 2).

Results— In Phase 1, CIMT was found to correlate with TEE markers of aortic atherosclerosis, including complex aortic plaques, and combined CSE. The optimal CIMT cutoff for detection of CSE on TEE was 0.78 mm. In Phase 2, a positive noninvasive strategy test (CIMT ≥0.78 mm, +carotid plaque, and/or a positive transthoracic echocardiography bubble study) was present in 61%. The prevalence of CSE on TEE was significantly higher among those with a positive compared with a negative noninvasive strategy test (65% versus 9%, P<0.001), and this strategy had a sensitivity of 92% and a negative predictive value of 91% for the detection of any CSE on TEE.

Conclusion— In patients with stroke or transient ischemic attack of undetermined origin, a noninvasive strategy of CIMT assessment/plaque screen and transthoracic echocardiography bubble study can identify patients in whom further invasive evaluation with TEE will be of low diagnostic yield.

The tumor was removed intact via the IVC using TEE guidance without requiring CPB. After removal of the mass, the TEE showed no residual tumor and normal cardiac function (Figure 2, Panel D). The removed tumor divided to a cystic and solid head (Figure 3, Panel D). The TEE findings matched well with the tumor in the IVC and in the RA (Figure 3, Additional File 1). The patient tolerated the surgery well. The pathological review described the mass as a low-grade endometrial stromal sarcoma (ESS) with a cyst located at the cephalad portion of the tumor.

Discussion

Transesophageal echocardiography can be critical in discovering, evaluating and localizing a right atrial mass. The differential diagnosis of right atrial masses ranges from congenital malformations, primary or secondary, benign or malignant tumors, thrombi and cysts. Congenital malformations include Eustachian valve, prominent crista terminalis or lipomatous hypertrophy [5,6]. A primary right atrial tumor can be a myxoma, rhabdomyoma, or angiosarcoma [1,7,8]. Secondary tumors can reach the heart through the inferior vena cava and invade the right atrium as solid masses, such as renal and hepatocellular carcinoma, uterine leiomyoma or Wilms tumors [1]. Among right atrial masses, right atrial cysts are rare and may represent hydatid, blood, bronchogenic cysts, cardiac varices or right coronary artery aneurysms [1,9,10]. Based on the appearance and location of the right atrial cysts, echocardiography helps in the differential diagnosis as follows:

A hydatid cyst in the right atrium is very rare and can appear as a multi-cystic mass with septations, calcifications and daughter cysts attached to the inter-atrial septum [11]. Multiple hydatid cysts can be close to the inferior and superior vena cava [12]. Blood cysts are congenital echolucent blood-filled nodules located on the endocardium, particularly along the lines of closure of heart valves [13]. Mobile oval blood cyst can be attached to the right atrial wall causing right coronary occlusion or as a round cyst attached to the inter-atrial septum with a thin, demarcated wall and echolucent core [14,15].

Intra-cardiac bronchogenic cysts are very rare. They appear as single thin walled homogenous cysts, similar to blood cysts [16]. They can be seen as intra-septal cystic masses on the right aspect of the inter-atrial septum causing complete AV block or as right atrial cysts attached to the inter-atrial septum [17,18].

Cardiac varix can be connected to the right atrial free wall as a large cystic lesion [10]. A right coronary aneurysm can appear as a cyst in the right atrium attached to the anterior wall with demonstrated flow within the mass by color Doppler [16]. A septal aneurysm [19], atrial thrombi [20], rhabdomyoma [1], myxoma [21] or angiosarcoma [2,8] might show cystic appearance also. Right atrial cysts associated to a secondary tumor can be diagnosed by the identification of the location and nature of the primary tumor.

In this case report, ESS as a secondary tumor invaded the IVC and RA. In our patient a thin-walled RA cyst was an unexpected finding as a continuation of an invading tumor not initially appreciated on CT. A retrospective review of the images did not indicate the presence of a RA mass at first. Even after knowing the presence of a cyst, a more detailed examination of the images of the RA raised the suspicion for an intra-atrial mass, but was not conclusive for an intra-atrial cyst (Figure 1, Panel B). The negative readings on CT are partially due to the differential composition of the solid tumor head versus the fluid filled cyst, as well as the mixing artifact secondary to the contrast load in the right atrium. This raises awareness to the need for additional analysis of radiological images in patients with IVC tumors, as well as the importance of the echo studies in confirming the intracardiac presence of these tumors.

Using color Doppler and air bubbles as contrast material a circumscribed cyst was detected and localized close to the IVC. Further TEE examination revealed that the tumor was divided into a solid and tubular part in the IVC and the cyst was connected to the tubular part. Two case reports with leiomyoma described similar structure where the cyst was connected with a tubular structure [3,22]. A literature review showed that low-grade ESS invaded the IVC in 19 patients. It extended into the right heart cavities in 9/19 patients (4 into the RA, 3 into the right ventricle and 2 into the pulmonary artery) [1]. No cystic appearance of ESS was described in these cases. There is only one case report in which an intraabdominal ESS had cystic manifestation [23]. This is the first case report of cystic appearance of low-grade ESS in the RA.

The clinical presentation of secondary tumors invading the IVC and RA includes signs and symptoms secondary to obstruction to forward flow in the right side of the heart. The most common clinical picture may present as right heart failure syndrome, syncopal episodes or both [3]. The presentation of ESS was unique in our case considering that the patient was essentially asymptomatic with an extended invasion into the IVC and RA. In addition, the recurrence of the tumor was detected more than 20 years after hysterectomy. This latency period was also seen in a case report of a low-grade ESS invading the IVC, the RA, the RV and obstructing the right ventricular outflow track 33 years after hysterectomy [24].

Given the high recurrence rates of ESS and the potential for aggressive invasion and progressive obstruction of the IVC, right heart surgical resection is the best treatment option [4]. Surgical resection of most of these tumors with cardiac invasion required CPB. In the present case, the tumor was resected through the IVC without CPB, using TEE to guide and evaluate the excision process.

We believe that ESS with intracardiac invasion should be considered in the differential diagnosis of intraatrial cystic masses.

Consent

Written informed consent was obtained from the patient for publication of this case report and any accompanying images. A copy of the written consent is available for review by the Editor-in-Chief of this journal.

Competing interests

The authors declare that they have no competing interests.

Authors' contributions

CW collected the references and wrote the manuscript. JS contributed in writing the manuscript, making figures and revision of the paper. PR reviewed the CT and MRI images and helped to incorporate the data into the manuscript. TS initiated the paper and mentored the writing of the manuscript. All authors report no conflicts of interest and approved the final manuscript.

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