European Journal of Radiology 84 (2015) 933–939
Contents lists available at ScienceDirect
European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad
The imaging features of neurologic complications of left atrial myxomas Wei-Hua Liao a , Divya Ramkalawan a , Jian-Ling Liu a , Wei Shi a , Chi-Shing Zee b , Xiao-Su Yang c , Guo-Liang Li c , Jing Li c , Xiao-Yi Wang a,∗ a
Department of Radiology, Xiangya Hospital, Central South University, Changsha 410008, Hunan, China Department of Radiology, Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, USA c Department of Neurology, Xiangya Hospital, Central South University, Changsha 410008, Hunan, China b
a r t i c l e
i n f o
Article history: Received 19 September 2014 Received in revised form 27 December 2014 Accepted 2 February 2015 Keywords: Left atrial myxoma Cerebral complications Neuroimaging
a b s t r a c t Background: Neurologic complications may be the first symptoms of atrial myxomas. Understanding the imaging features of neurologic complications of atrial myxomas can be helpful for the prompt diagnosis. Objective: To identify neuroimaging features for patients with neurologic complications attributed to atrial myxoma. Methods: We retrospectively reviewed the medical records of 103 patients with pathologically confirmed atrial myxoma at Xiangya Hospital from January 2009 to January 2014. The neuroimaging data for patients with neurologic complications were analyzed. Results: Eight patients with atrial myxomas (7.77%) presented with neurologic manifestations, which constituted the initial symptoms for seven patients (87.5%). Neuroimaging showed five cases of cerebral infarctions and three cases of aneurysms. The main patterns of the infarctions were multiplicity (100.0%) and involvement of the middle cerebral artery territory (80.0%). The aneurysms were fusiform in shape, multiple in number (100.0%) and located in the distal middle cerebral artery (100.0%). More specifically, high-density in the vicinity of the aneurysms was observed on CT for two patients (66.7%), and homogenous enhancement surrounding the aneurysms was detected in the enhanced imaging for two patients (66.7%). Conclusion: Neurologic complications secondary to atrial myxoma consist of cerebral infarctions and aneurysms, which show certain characteristic features in neuroimaging. Echocardiography should be performed in patients with multiple cerebral infarctions, and multiple aneurysms, especially when aneurysms are distal in location. More importantly, greater attention should be paid to the imaging changes surrounding the aneurysms when myxomatous aneurysms are suspected and these are going to be the relevant features in our article. © 2015 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Cardiac myxomas are the most common primary tumor of the heart, and approximately 75% are found in the left atrium [1,2]. These tumors arise from subendocardial multipotential mesenchymal cells, and two anatomic types have been observed: solid and papillary types [2]. The clinical presentation correlates well with the anatomic types. Solid tumors are more likely to present with symptoms of congestive heart failure, while papillary tumors are more likely to embolize to the cerebral and other peripheral vessels [3,4]. Clinically, neurologic symptoms occurred in 29% of patients
∗ Corresponding author. Tel.: +86 731 84327285. E-mail address: [email protected] (X.-Y. Wang). http://dx.doi.org/10.1016/j.ejrad.2015.02.005 0720-048X/© 2015 Elsevier Ireland Ltd. All rights reserved.
with myxoma, and also were the initial presentation in 12% of patients without any past history of cardiac manifestations [5,6]. Therefore, it is important to understand the imaging features of neurologic complications, which can be helpful to suspect cardiac myxoma and to decide whether echocardiography should be performed. The pathology of neurological manifestation secondary to left atrial myxoma is threefold: cerebral arterial embolism causing cerebral infarctions, aneurysms and intraparenchymal metastases [7–9]. Since the first reported description of a stroke caused by a cardiac myxoma in 1952 [10], there have been a handful of published case reports and series describing atrial myxoma and secondary cerebral infarctions. The number of reported cases of myxomatous aneurysms was also increasing gradually, but most were single case reports [6,11–13]. We report the clinical case
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series of neurologic complications related to atrial myxoma seen during a period of 5 consecutive years at Xiangya Hospital. We aim to summarize the imaging characteristics of two neurological complications, and expect to find some unique imaging features that have not been reported previously. 2. Methods Using the medical records database of patients at Xiangya Hospital, we searched for the diagnosis myxoma from January 1, 2009 to January 1, 2014, and selected 103 patients with pathologically-confirmed atrial myxoma. With institutional review board approval, we reviewed medical records to identify patients who underwent neurologic imaging: computed tomography (CT) or magnetic resonance imaging (MRI), computed tomography angiography (CTA) or magnetic resonance angiography (MRA), or digital subtraction angiography (DSA) or neurologic consultation. According to the neuroimaging, we identified the lesions for patients: infarction (stage, number, location), and aneurysm (shape, number, location). Based on the time from infarction, T1WI, T2WI, diffusion weighted imaging (DWI), and apparent diffusion coefficient (ADC), we described different phases of infarction as acute, subacute or chronic [14]. Using commonly accepted arterial territories [15], the location of the lesions was classified as follows: internal carotid artery (ICA), anterior cerebral artery (ACA), middle cerebral artery (MCA), posterior cerebral artery (PCA), basilar artery (BA) and posterior inferior cerebellar artery (PICA). Multiple infarcts and aneurysms were defined as more than two in number [16]. We also analyzed the changes surrounding the aneurysms on both non contrast-enhanced and contrast-enhanced imaging and found that these changes are of utmost importance in making the final diagnosis in cases of peripheral aneurysms. 3. Results The diagnosis of atrial myxoma had been reached after imaging modalities like cardiac ultrasound including chest CT, and histopathological examination after surgical examination (Fig. 1). Eight of the 103 patients with atrial myxoma (7.77%) developed neurologic complications as shown in Table 1. Up to 75% of these eight patients had papillary type of tumor. However, the most common type of tumor among the total number of 103 patients was the solid type (62.5%). The neurologic symptoms of the eight patients were the initial presentations for 7 of them (87.5%), and there was only one patient who initially presented with cardiac manifestations, and experienced neurologic symptoms one year after atrial myxoma resection. These eight patients were subjected to neuroimaging, which showed 5 cases of cerebral infarctions and three cases of aneurysms. For the five cases of cerebral infarctions, three patients presented acute lesions coexisting with subacute lesions, and two patients showed acute lesions. The main patterns of the infarctions were multiplicity (five out of five patients, 100.0%) and location in the MCA (four out of five patients, 80.0%), PICA (two out of five patients, 40.0%), PCA (one out of five patients, 20.0%) and combined MCA/ACA (one out of five patients, 20.0%). In addition, four patients had involvement of multiple vascular territories (Fig. 1). The aneurysms were mostly fusiform in shape, multiple in number (three out of three patients, 100.0%), and located in the distal MCA (three out of three patients, 100.0%) and the distal PCA (two out of three patients, 66.7%). Although most of the aneurysms were fusiform, few saccular aneurysms were also noted as shown in patient 1 (Fig. 3). Aneurysms coexisted with chronic infarctions for two patients. In addition, we found the high-density lesions in the
vicinity of the aneurysms on CT for 2 patients (patient 1 and 2, Figs. 2 and 3), which presented as gyral pattern of marked signal loss on T2WI. It was also notable that homogenous enhancement surrounding the aneurysms was detected on contrast enhanced CT for 2 patients (patient 2 and 3, Fig. 2). It is worthy to note that aneurysms involving peripheral arteries elsewhere, that is, arteries other than cerebral arteries were not documented in any of our patients. 4. Discussion Cardiac myxoma is believed to arise from subendocardial multipotential mesenchymal cells in the fossa ovalis, and is located in the left atrium in 75% of cases either in the solid or papillary form [17]. The tumor is therefore typically attached to the interatrial septum. Females are more commonly affected with a male: female ratio of 1:2, and the average age at onset being between 30 and 60 years [18]. A triad of symptoms is recognized [19]: (1) valvular obstruction: left-sided obstruction presenting with dyspnea, orthopnea, pulmonary edema; and right-sided obstruction presenting with symptoms of right heart failure; (2) embolic events: any arterial bed may be affected, mostly systemic circulation, for example brain or extremities, because most tumors are left sided; and (3) constitutional symptoms such as fever, weight loss, fatigue, muscle weakness, myalgia, and arthralgia. The manifestation of constitutional symptoms is related to an overproduction of interleukin-6. Multiple studies have shown that cardiac myxoma cells have multiple potentials of differentiation and produce growth factors and cytokines [20]. Presentation varies depending on the size, location, and mobility of the tumor. Approximately 20% of patients are asymptomatic, which makes the diagnosis difficult. Neurological symptoms related to left atrial myxomas may occur before or at the time of primary tumor diagnosis. As illustrated in this study, neurologic manifestations consisting of hemiparesis, hypoesthesia of limbs, headache, attacks of seizures, dysarthria and so on, may precede cardiac myxoma manifestations or may present alone, underlining the need for appropriate investigations of the imaging feature of neurologic complications. In this study, we found that 75% of the eight patients with neurologic presentation had papillary type of tumor. However, among the total 103 patients, the more common type of tumor was of the solid type (62.5%). The mobility, not the size, of the myxoma appears to be related to embolic potential. The risk of embolization of cardiac myxomas is thought to be related to tumor morphology, with friable and gelatinous papillary myxomas more likely to embolize than firm and fibrous solid lesions [21]. Emboli preferentially lodge in the MCA branches, and rarely in ACA. Thus, most infarctions associated with left atrial myxomas are commonly located in the midsection (posterior frontal, anterior parietal, and superior temporal) of the MCA distribution. We report eight cases (7.77%) of neurologic complications of atrial myxomas out of 103. Similar results were obtained in the Mayo clinic series where out of the 74 patients, in 9 (12%) neurological symptoms were the initial presenting feature [6]. The common neurologic complications are cerebral infarction due to thromboembolism. Cerebral arteries are common sites of embolism associated with left atrial myxomas owing to the hemodynamics of the blood flow out of the heart. Neuroimaging usually shows multiple phases of infarcts: acute, subacute and chronic, suggesting repetitive thromboembolic events. Involvement of multiple vascular territories is distinctive for a proximal embolic source, as in our patients. Another complication of atrial aneurysms is the occurrence of myxomatous aneurysms. The prevalence of myxoma-related cerebral aneurysms in our study was higher than that previously reported, probably due to the lack of systematic imaging
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Fig. 1. Patient 7 had multiple infarctions (acute and subacute). (A) T2WI and (B) FLAIR showing multiple infarctions (hyperintense lesions in both parietal lobes and the left splenium of corpus callosum). (C) DWI and (D) ADC map showing acute infarction (hyperintense on DWI and hypointense on ADC maps) in the right parietal lobe and subacute infarction (hyperintense on DWI and isointense on ADC map) in the left parietal lobe and left splenium of corpus callosum. (E) Cardiac ultrasound showing left atrial myxoma of size 26 × 18 mm attached to the interatrial septal wall with a 4 mm wide pedicle. (F) Saggital CT with contrast showing atial myxoma (arrow). (G) Photomicrograph of histopathologic specimen from parietal lesion showed abundant hemosiderin and moderate myxoid matrix.
evaluation in previous studies. The typical imaging features of these aneurysms include fusiform shape, multiplicity and distal location. The pathogenesis of myxomatous aneurysms is not fully understood as of now. The original hypothesis put forward by Stoane et al. was that perivascular damage may be due to vascular occlusion by tumor material followed by scarring and pseudoaneurysm formation [22]. Later histopathological evidence showed active invasion of the vasa vasorum by viable tumor emboli, thereby leading to destruction of the architecture of arterial walls similar to the
mechanism of mycotic aneurysms. Current hypothesis, therefore, assumes that tumor materials from cardiac myxomas embolize into the vasa vasorum of peripheral arteries and proliferate into the vessel wall. This leads to a weakening of subintimal tissue, such as the internal elastic lamina, and thereafter aneurysm formation [24]. Aneurysm formation associated with atrial myxoma is therefore not caused by blood-flow dynamics but by myxomatous tumor embolization and invasion into the vessel wall. Aneurysms coexisting with chronic infarctions can show myxomatous embolization
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Table 1 Clinical and imaging features of patients with neurologic complications of left atrial myxomas. Patient no./sex/age (yrs)
Neurological symptoms (before or after resection of atrial myxoma)
Neuroimaging methods
Type of lesions (aneurysms or infractions)
Location of lesions
Changes surrounding aneurysms
1/M/33
Headache, attacks of seizures (after)
CT, MRI, DSA
Multiple aneurysms (including local encephalomalacia)
High-density lesion on CT, marked signal loss on T2WI
2/F/28
Worsening headache, fever (before)
CT, CTA, MRI, DWI
Multiple aneurysms (including local encephalomalacia)
3/F/36
Right hypoaesthesia (before)
CT, CTA, DSA
Multiple aneurysms
Left ACA, both MCAs, both PCAs, (encephalomalacia in left MCA) Both MCAs, both PCAs, both PICAs, (encephalomalacia in left MCA) Left MCA, right PCA
4/M/16
Right hemiparesis (before)
CT, MRI, MRA, DWI
5/F/22
Left hemiparesis and hypoaesthesia (before) Dysarthria, right facial palsy, right hemiparesis (before) Dysarthria, left hemiparesis (before) Dysarthria, right hemiparesis (before)
CT, MRI
Multiple infarctions (acute) Multiple infarctions (acute and subacute) Multiple infarctions (acute) Multiple infarctions (acute and subacute) Multiple infarctions (acute and subacute)
6/F/38 7/F/59 8/F/47
CT, MRI, DWI CT, MRI, MRA, DWI MRI, MRA, DWI
occurred before the formation of aneurysm, and suggests the correlation between embolization and aneurysm. The cerebral aneurysm associated with atrial myxoma has been described as having angiographic features similar to those of septic emboli, including multiplicity, peripheral location, and fusiform appearance [23,24]. Due to the possibility that other types of aneurysms could present with the similar morphologic pattern, some authors believe that applicability of these findings to the specific case of myxomatous aneurysms
High-density lesion and homogenous enhancement on CT
Left PCA, both PICAs
Homogenous enhancement on CT –
Right MCA, both PICAs
–
Left MCA
–
Left ACA, both MCAs
–
Left ICA, right MCA
–
is unclear [25]. This is indeed a difficult situation encountered in daily routine practice. We found some interesting features, as outlined below, which may help to overcome this clinical dilemma. In our study, we found persistently high-density on plain CT adjacent to the aneurysms. This was an interesting feature of myxomatous aneurysms, which has only been mentioned and not emphasized in a few previous reports [26,27]. This kind of high-density lesion surrounding aneurysms on CT was
Fig. 2. Patient 2 had multiple aneurysms. (A) CT with multiple rounded high-density lesions in both frontal and parietal lobes. (B) MIP reconstruction images from the CTA showing high-density lesion in the vicinity of cerebral granular aneurysms. (C) Contrast-enhanced CT showing homogenous enhancement surrounding the aneurysms. (D) 3D reconstruction images and (E) and (F) MIP reconstruction image from the CTA clearly confirming multiple cerebral fusiform aneurysms involving distal segments of cerebral arteries on both sides.
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Fig. 3. Patient 1 had multiple aneurysms. (A–C) CT scan of the brain showing multiple foci of high density lesions in both frontal and parietal lobes (numbered 2 in A and black arrow in B and C) surrounded by low density edema (numbered 1 in A). (D) T2WI demonstrating multiple lesions located adjacent to cerebral sulci presenting with gyral pattern of marked signal loss on T2WI (black arrows). (E) Reconstructed MIP image from MRA revealing multiple distal aneurysms involving segments of MCA and ACA, long black arrow shows a saccular aneurysm and short black arrow shows a fusiform aneurysm. (F) DSA image showing multiple fusiform (angled arrow) and saccular (horizontal arrow) aneurysm involving the PCA territory shown during angiography of the left vertebral artery. (G) T2WI with local encephalomalacia in the head of the left caudate nucleus (black arrow).
histopathologically verified to be the accumulation of myxoid matrix and hemosiderin, but not calcification [26]. Atrial myxomas which are the embolic source are also histologically characterized by the accumulation of myxoid material and stellate cells. We believe that this CT finding is one of the imaging features, among others described below, which may help in narrowing down the diagnosis of peripheral cerebral arterial aneurysms. It was interesting to note that the high-density was persistent on follow-up imaging. This can be suggestive of repeated and slight hemorrhage
(just like errhysis) in the vicinity of the aneurysms. The hyperdense appearance of these aneurysms on plain CT scan is supposed to be due to deposition of myxoid matrix and hemosiderin [28]. In addition, we noted the presence of obvious and homogenous enhancement surrounding most aneurysms in two patients on contrast-enhanced imaging. This was not reported previously and was another point of interest to us. A rational explanation for this imaging feature was the accumulation and proliferation of myxomatous tumor cells, granulation tissue, neovascularization, and
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hematoma organizing in the vicinity of the aneurysms. Angiogenesis or neovascularization is a complex biological process which is regulated by a number of cytokines or growth factors, like IL-6. As we have seen earlier, these are secreted by the myxomatous tumor cells [20]. This finding on contrast-enhanced CT is therefore another helpful feature in the diagnostic work-up of distal aneurysms. We also observed changes surrounding these aneurysms on MR imaging, notably, signal loss on T2WI. This finding may be explained as being a result of the combined effects of the dense deposits of hemosiderin (hypointense) and iron breakdown products surrounding the hemorrhagic aneurysms following chronic and recurrent hemorrhage [29]. Therefore, we see that there are specific imaging features in both CT, unenhanced and enhanced alike, and MRI which are helpful in making the definitive diagnosis of myxomatous aneurysms. The abnormal changes adjacent to aneurysms on both nonenhanced and contrast-enhanced imaging, caused by repeated hemorrhage or myxomatous tumor cells which can transgress outside the aneurysmal wall progressively[25], is a notable imaging feature and may contribute to differential diagnosis of intracranial peripheral aneurysms, such as infectious aneurysms and traumatic aneurysms. Infectious aneurysms, which present with a similar morphologic pattern, that is fusiform shape, multiplicity and located on distal vessels, are more prone to rupture, resulting in subarachnoid hemorrhage or acute hematoma in the vicinity of the aneurysms [30,31]. Traumatic aneurysms, resulting from direct penetrating head injuries or blunt head trauma, may be associated with other traumatic lesions [32]. Another cardiac condition also leading to a similar pattern of brain infarcts is patent foramen ovale (PFO), by means of paradoxical emboli through abnormal intracardiac or intrapulmonary communication between the right and left circulations [33]. The difference is that there is no apparent cardiac source on the left side of the heart or in the proximal arterial tree (ascending aorta) in PFO. Another difference is that no perilesional changes are observed in case of PFO. Peripherally located arterial aneurysms may be either neoplastic (secondary to myxoma), mycotic (infectious secondary to endocarditis) or traumatic in origin [34]. With such a broad differential diagnosis, we have to rely on other tell-tale signs. We found the presence of abnormal changes adjacent to these aneurysms on both non-enhanced and contrast-enhanced imaging and these were unique features, which could contribute to the differential diagnosis of peripheral aneurysms. These perilesional changes are the highlights of our article and are essentially seen on both CT and MR images. Our article therefore brings to light new information for diagnosing myxomatous aneurysms. First, we found high-density on non-enhanced CT adjacent to the aneurysms and this change is persistent on follow-up. Second, we also observed the presence of obvious and homogeneous enhancement surrounding the aneurysms on contrast-enhanced CT. These changes showed up as loss of signal intensity on T2WI on MR scanning. In conclusion, the common neurologic complications are cerebral infarction due to thromboembolism. Neuroimaging usually shows multiple infarcts of varying stages of chronicity: acute, subacute to chronic. Accordingly, echocardiography should be performed in patients with suspected embolic events, especially when cerebral infarcts with multiple territorial lesions and multiple phases are detected. The occurrence of myxoma-associated aneurysms is another manifestation of delayed neurological complications caused by left atrial myxoma. These aneurysms are characteristically distal in location, fusiform in shape and multiple in number. More attention should be paid to the changes surrounding the aneurysms on both non-enhanced and contrastenhanced imaging when myxomatous aneurysms are suspected. These important features are what help not only in differentiating
myxomatous aneurysms from other causes of distal cerebral arterial aneurysms but also in making a definitive diagnosis. Funding This work was supported by the National Natural Science Foundation of China (No. 81000596) and Postdoctoral Science Foundation of China (No. 2013M531815). Conflict of interest statement The authors report no conflict of interest. The authors alone are responsible for the content and writing of the paper. References [1] Reynen K. Cardiac myxomas. N Engl J Med 1995;333:1610–7. [2] Blondeau P. Primary cardiac tumors: French studies of 533 cases. Thorac Cardivasc Surg 1990;38:192–5. [3] Shimono T, Makino S, Kanamori Y, et al. Left atrial myxomas: using gross anatomic tumor types to determine clinical features and coronary angiographic findings. Chest 1995;107:674–9. [4] Swartz MF, lutz CJ, Chandan VS, et al. Atrial myxomas: pathologic types, tumor location, and presenting symptoms. J Card Surg 2006;21:435–40. [5] Pinede L, Duhaut P, Loire R. Clinical presentation of left atrial cardiac myxoma: a series of 112 consecutive cases. Medicine (Baltimore) 2001;80:159–72. [6] Lee VH, Connolly HM, Brown Jr RD. Central nervous system manifestations of cardiac myxoma. Arch Neurol 2007;64:1115–20. [7] Rodriguez FJ, Brown RD, Mohr JP, et al. Embolic atrial myxoma with neoplastic aneurysm formation and haemorrhage: a diagnostic challenge. Neuropathol Appl Neurobiol 2006;32:213–6. [8] Roeltgen DP, Weimer GR, Patterson LF. Delayed neurologic complications of left atrial myxoma. Neurology 1981;31:8–13. [9] Budzilovich G, Aleksic S, Greco A, et al. Malignant cardiac myxoma with cerebral metastases. Surg Neurol 1979;11:461–9. [10] Goldberg HP, Glenn F, Dotter CT, et al. Myxoma of the left atrium: diagnosis made during life with operative and post-mortem findings. Circulation 1952;6:762–7. [11] Chen HJ, Liou CW, Chen L. Metastatic atrial myxoma presenting as intracranial aneurysms with hemorrhage: case report. Surg Neurol 1993;40:61–4. [12] Day AL, Gaposchkin CG, Yu CJ, et al. Spontaneous fusiform middle cerebral artery aneurysms: characteristics and a proposed mechanism of formation. J Neurosurg 2003;99:228–40. [13] New PFJ, Price DL, Carter B. Cerebral angiography in cardiac myxoma. Radiology 1970;96:335–45. [14] Yousem DM, Grossman RI, editors. Neuroradiology: the requisites. 3rd ed Philadelphia, PA: Mosby Elsevier Inc.; 2010. [15] Tatu L, Moulin T, Bogousslavsky J, et al. Arterial territories of the human brain: brainstem and cerebellum. Neurology 1996;47:1125–35. [16] Wong KS, Gao S, Chan YL, et al. Mechanisms of acute cerebral infarctions in patients with middle cerebral artery stenosis: a diffusion-weighted imaging and microemboli monitoring study. Ann Neurol 2002;52:74–81. [17] Grebenc ML, Rosado de christenson ML, Burke AP, et al. Primary cardiac and pericardial neoplasms: radiologic–pathologic correlation. Radiographics 2000;20:1073–103. [18] McCarthy PM, Piehler JM, Schaff HV, et al. The significance of multiple, recurrent and “complex” cardiac myxomas. J Thorac Cardiovasc Surg 1986;91:389–96. [19] Schoepf UJ. CT of the heart, principles and applications. Totowa, NJ: Humana Press; 2005. [20] Mendoza CE, Rosado MF, Bernal L. The role of interleukin-6 in cases of cardiac myxoma. Clinical features, immunologic abnormalities, and a possible role in recurrence. Tex Heart Inst J 2001;28:3–7. [21] Burke A, Virmani R. Tumors of the heart and great vessels. Atlas of tumor pathology. Washington, DC: Armed Forces Institute of Pathology; 1996. [22] Stoane L, Allen JH, Collins HA. Radiologic observations in cerebral embolization from left heart myxomas. Radiology 1966;87:262–6. [23] Jean WC, Walski-Easton SM, Nussbaum ES. Multiple intracranial aneurysms as delayed complications of an atrial myxoma: case report. Neurosurgery 2001;49:200–3. [24] Burton C, Johnston J. Multiple cerebral aneurysms and cardiac myxoma. N Engl J Med 1970;282:35–6. [25] Eddleman CS, Gottardi-Littell NR, Bendok BR, et al. Rupture of cerebral myxomatous aneurysm months after resection of the primary cardiac tumor. Neurocrit Care 2010;13:252–5. [26] Hwang BJ, Connelly MM, Lev MH. Distinctive MR imaging appearance of hemorrhagic cerebral aneurysms associated with atrial myxoma. Am J Roentgenol 2001;177:925–7. [27] Nucifora PG, Dillon WP. MR diagnosis of myxomatous aneurysms: report of two Cases. Am J Neuroradiol 2001;22:1349–52. [28] Moggio RA, Pucillo AL, Schechter AG, et al. Primary cardiac tumors: diagnosis and management in 14 cases. NY State J Med 1992;92:49–52.
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Contents lists available at ScienceDirect
European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad
The imaging features of neurologic complications of left atrial myxomas Wei-Hua Liao a , Divya Ramkalawan a , Jian-Ling Liu a , Wei Shi a , Chi-Shing Zee b , Xiao-Su Yang c , Guo-Liang Li c , Jing Li c , Xiao-Yi Wang a,∗ a
Department of Radiology, Xiangya Hospital, Central South University, Changsha 410008, Hunan, China Department of Radiology, Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, USA c Department of Neurology, Xiangya Hospital, Central South University, Changsha 410008, Hunan, China b
a r t i c l e
i n f o
Article history: Received 19 September 2014 Received in revised form 27 December 2014 Accepted 2 February 2015 Keywords: Left atrial myxoma Cerebral complications Neuroimaging
a b s t r a c t Background: Neurologic complications may be the first symptoms of atrial myxomas. Understanding the imaging features of neurologic complications of atrial myxomas can be helpful for the prompt diagnosis. Objective: To identify neuroimaging features for patients with neurologic complications attributed to atrial myxoma. Methods: We retrospectively reviewed the medical records of 103 patients with pathologically confirmed atrial myxoma at Xiangya Hospital from January 2009 to January 2014. The neuroimaging data for patients with neurologic complications were analyzed. Results: Eight patients with atrial myxomas (7.77%) presented with neurologic manifestations, which constituted the initial symptoms for seven patients (87.5%). Neuroimaging showed five cases of cerebral infarctions and three cases of aneurysms. The main patterns of the infarctions were multiplicity (100.0%) and involvement of the middle cerebral artery territory (80.0%). The aneurysms were fusiform in shape, multiple in number (100.0%) and located in the distal middle cerebral artery (100.0%). More specifically, high-density in the vicinity of the aneurysms was observed on CT for two patients (66.7%), and homogenous enhancement surrounding the aneurysms was detected in the enhanced imaging for two patients (66.7%). Conclusion: Neurologic complications secondary to atrial myxoma consist of cerebral infarctions and aneurysms, which show certain characteristic features in neuroimaging. Echocardiography should be performed in patients with multiple cerebral infarctions, and multiple aneurysms, especially when aneurysms are distal in location. More importantly, greater attention should be paid to the imaging changes surrounding the aneurysms when myxomatous aneurysms are suspected and these are going to be the relevant features in our article. © 2015 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Cardiac myxomas are the most common primary tumor of the heart, and approximately 75% are found in the left atrium [1,2]. These tumors arise from subendocardial multipotential mesenchymal cells, and two anatomic types have been observed: solid and papillary types [2]. The clinical presentation correlates well with the anatomic types. Solid tumors are more likely to present with symptoms of congestive heart failure, while papillary tumors are more likely to embolize to the cerebral and other peripheral vessels [3,4]. Clinically, neurologic symptoms occurred in 29% of patients
∗ Corresponding author. Tel.: +86 731 84327285. E-mail address: [email protected] (X.-Y. Wang). http://dx.doi.org/10.1016/j.ejrad.2015.02.005 0720-048X/© 2015 Elsevier Ireland Ltd. All rights reserved.
with myxoma, and also were the initial presentation in 12% of patients without any past history of cardiac manifestations [5,6]. Therefore, it is important to understand the imaging features of neurologic complications, which can be helpful to suspect cardiac myxoma and to decide whether echocardiography should be performed. The pathology of neurological manifestation secondary to left atrial myxoma is threefold: cerebral arterial embolism causing cerebral infarctions, aneurysms and intraparenchymal metastases [7–9]. Since the first reported description of a stroke caused by a cardiac myxoma in 1952 [10], there have been a handful of published case reports and series describing atrial myxoma and secondary cerebral infarctions. The number of reported cases of myxomatous aneurysms was also increasing gradually, but most were single case reports [6,11–13]. We report the clinical case
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series of neurologic complications related to atrial myxoma seen during a period of 5 consecutive years at Xiangya Hospital. We aim to summarize the imaging characteristics of two neurological complications, and expect to find some unique imaging features that have not been reported previously. 2. Methods Using the medical records database of patients at Xiangya Hospital, we searched for the diagnosis myxoma from January 1, 2009 to January 1, 2014, and selected 103 patients with pathologically-confirmed atrial myxoma. With institutional review board approval, we reviewed medical records to identify patients who underwent neurologic imaging: computed tomography (CT) or magnetic resonance imaging (MRI), computed tomography angiography (CTA) or magnetic resonance angiography (MRA), or digital subtraction angiography (DSA) or neurologic consultation. According to the neuroimaging, we identified the lesions for patients: infarction (stage, number, location), and aneurysm (shape, number, location). Based on the time from infarction, T1WI, T2WI, diffusion weighted imaging (DWI), and apparent diffusion coefficient (ADC), we described different phases of infarction as acute, subacute or chronic [14]. Using commonly accepted arterial territories [15], the location of the lesions was classified as follows: internal carotid artery (ICA), anterior cerebral artery (ACA), middle cerebral artery (MCA), posterior cerebral artery (PCA), basilar artery (BA) and posterior inferior cerebellar artery (PICA). Multiple infarcts and aneurysms were defined as more than two in number [16]. We also analyzed the changes surrounding the aneurysms on both non contrast-enhanced and contrast-enhanced imaging and found that these changes are of utmost importance in making the final diagnosis in cases of peripheral aneurysms. 3. Results The diagnosis of atrial myxoma had been reached after imaging modalities like cardiac ultrasound including chest CT, and histopathological examination after surgical examination (Fig. 1). Eight of the 103 patients with atrial myxoma (7.77%) developed neurologic complications as shown in Table 1. Up to 75% of these eight patients had papillary type of tumor. However, the most common type of tumor among the total number of 103 patients was the solid type (62.5%). The neurologic symptoms of the eight patients were the initial presentations for 7 of them (87.5%), and there was only one patient who initially presented with cardiac manifestations, and experienced neurologic symptoms one year after atrial myxoma resection. These eight patients were subjected to neuroimaging, which showed 5 cases of cerebral infarctions and three cases of aneurysms. For the five cases of cerebral infarctions, three patients presented acute lesions coexisting with subacute lesions, and two patients showed acute lesions. The main patterns of the infarctions were multiplicity (five out of five patients, 100.0%) and location in the MCA (four out of five patients, 80.0%), PICA (two out of five patients, 40.0%), PCA (one out of five patients, 20.0%) and combined MCA/ACA (one out of five patients, 20.0%). In addition, four patients had involvement of multiple vascular territories (Fig. 1). The aneurysms were mostly fusiform in shape, multiple in number (three out of three patients, 100.0%), and located in the distal MCA (three out of three patients, 100.0%) and the distal PCA (two out of three patients, 66.7%). Although most of the aneurysms were fusiform, few saccular aneurysms were also noted as shown in patient 1 (Fig. 3). Aneurysms coexisted with chronic infarctions for two patients. In addition, we found the high-density lesions in the
vicinity of the aneurysms on CT for 2 patients (patient 1 and 2, Figs. 2 and 3), which presented as gyral pattern of marked signal loss on T2WI. It was also notable that homogenous enhancement surrounding the aneurysms was detected on contrast enhanced CT for 2 patients (patient 2 and 3, Fig. 2). It is worthy to note that aneurysms involving peripheral arteries elsewhere, that is, arteries other than cerebral arteries were not documented in any of our patients. 4. Discussion Cardiac myxoma is believed to arise from subendocardial multipotential mesenchymal cells in the fossa ovalis, and is located in the left atrium in 75% of cases either in the solid or papillary form [17]. The tumor is therefore typically attached to the interatrial septum. Females are more commonly affected with a male: female ratio of 1:2, and the average age at onset being between 30 and 60 years [18]. A triad of symptoms is recognized [19]: (1) valvular obstruction: left-sided obstruction presenting with dyspnea, orthopnea, pulmonary edema; and right-sided obstruction presenting with symptoms of right heart failure; (2) embolic events: any arterial bed may be affected, mostly systemic circulation, for example brain or extremities, because most tumors are left sided; and (3) constitutional symptoms such as fever, weight loss, fatigue, muscle weakness, myalgia, and arthralgia. The manifestation of constitutional symptoms is related to an overproduction of interleukin-6. Multiple studies have shown that cardiac myxoma cells have multiple potentials of differentiation and produce growth factors and cytokines [20]. Presentation varies depending on the size, location, and mobility of the tumor. Approximately 20% of patients are asymptomatic, which makes the diagnosis difficult. Neurological symptoms related to left atrial myxomas may occur before or at the time of primary tumor diagnosis. As illustrated in this study, neurologic manifestations consisting of hemiparesis, hypoesthesia of limbs, headache, attacks of seizures, dysarthria and so on, may precede cardiac myxoma manifestations or may present alone, underlining the need for appropriate investigations of the imaging feature of neurologic complications. In this study, we found that 75% of the eight patients with neurologic presentation had papillary type of tumor. However, among the total 103 patients, the more common type of tumor was of the solid type (62.5%). The mobility, not the size, of the myxoma appears to be related to embolic potential. The risk of embolization of cardiac myxomas is thought to be related to tumor morphology, with friable and gelatinous papillary myxomas more likely to embolize than firm and fibrous solid lesions [21]. Emboli preferentially lodge in the MCA branches, and rarely in ACA. Thus, most infarctions associated with left atrial myxomas are commonly located in the midsection (posterior frontal, anterior parietal, and superior temporal) of the MCA distribution. We report eight cases (7.77%) of neurologic complications of atrial myxomas out of 103. Similar results were obtained in the Mayo clinic series where out of the 74 patients, in 9 (12%) neurological symptoms were the initial presenting feature [6]. The common neurologic complications are cerebral infarction due to thromboembolism. Cerebral arteries are common sites of embolism associated with left atrial myxomas owing to the hemodynamics of the blood flow out of the heart. Neuroimaging usually shows multiple phases of infarcts: acute, subacute and chronic, suggesting repetitive thromboembolic events. Involvement of multiple vascular territories is distinctive for a proximal embolic source, as in our patients. Another complication of atrial aneurysms is the occurrence of myxomatous aneurysms. The prevalence of myxoma-related cerebral aneurysms in our study was higher than that previously reported, probably due to the lack of systematic imaging
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Fig. 1. Patient 7 had multiple infarctions (acute and subacute). (A) T2WI and (B) FLAIR showing multiple infarctions (hyperintense lesions in both parietal lobes and the left splenium of corpus callosum). (C) DWI and (D) ADC map showing acute infarction (hyperintense on DWI and hypointense on ADC maps) in the right parietal lobe and subacute infarction (hyperintense on DWI and isointense on ADC map) in the left parietal lobe and left splenium of corpus callosum. (E) Cardiac ultrasound showing left atrial myxoma of size 26 × 18 mm attached to the interatrial septal wall with a 4 mm wide pedicle. (F) Saggital CT with contrast showing atial myxoma (arrow). (G) Photomicrograph of histopathologic specimen from parietal lesion showed abundant hemosiderin and moderate myxoid matrix.
evaluation in previous studies. The typical imaging features of these aneurysms include fusiform shape, multiplicity and distal location. The pathogenesis of myxomatous aneurysms is not fully understood as of now. The original hypothesis put forward by Stoane et al. was that perivascular damage may be due to vascular occlusion by tumor material followed by scarring and pseudoaneurysm formation [22]. Later histopathological evidence showed active invasion of the vasa vasorum by viable tumor emboli, thereby leading to destruction of the architecture of arterial walls similar to the
mechanism of mycotic aneurysms. Current hypothesis, therefore, assumes that tumor materials from cardiac myxomas embolize into the vasa vasorum of peripheral arteries and proliferate into the vessel wall. This leads to a weakening of subintimal tissue, such as the internal elastic lamina, and thereafter aneurysm formation [24]. Aneurysm formation associated with atrial myxoma is therefore not caused by blood-flow dynamics but by myxomatous tumor embolization and invasion into the vessel wall. Aneurysms coexisting with chronic infarctions can show myxomatous embolization
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Table 1 Clinical and imaging features of patients with neurologic complications of left atrial myxomas. Patient no./sex/age (yrs)
Neurological symptoms (before or after resection of atrial myxoma)
Neuroimaging methods
Type of lesions (aneurysms or infractions)
Location of lesions
Changes surrounding aneurysms
1/M/33
Headache, attacks of seizures (after)
CT, MRI, DSA
Multiple aneurysms (including local encephalomalacia)
High-density lesion on CT, marked signal loss on T2WI
2/F/28
Worsening headache, fever (before)
CT, CTA, MRI, DWI
Multiple aneurysms (including local encephalomalacia)
3/F/36
Right hypoaesthesia (before)
CT, CTA, DSA
Multiple aneurysms
Left ACA, both MCAs, both PCAs, (encephalomalacia in left MCA) Both MCAs, both PCAs, both PICAs, (encephalomalacia in left MCA) Left MCA, right PCA
4/M/16
Right hemiparesis (before)
CT, MRI, MRA, DWI
5/F/22
Left hemiparesis and hypoaesthesia (before) Dysarthria, right facial palsy, right hemiparesis (before) Dysarthria, left hemiparesis (before) Dysarthria, right hemiparesis (before)
CT, MRI
Multiple infarctions (acute) Multiple infarctions (acute and subacute) Multiple infarctions (acute) Multiple infarctions (acute and subacute) Multiple infarctions (acute and subacute)
6/F/38 7/F/59 8/F/47
CT, MRI, DWI CT, MRI, MRA, DWI MRI, MRA, DWI
occurred before the formation of aneurysm, and suggests the correlation between embolization and aneurysm. The cerebral aneurysm associated with atrial myxoma has been described as having angiographic features similar to those of septic emboli, including multiplicity, peripheral location, and fusiform appearance [23,24]. Due to the possibility that other types of aneurysms could present with the similar morphologic pattern, some authors believe that applicability of these findings to the specific case of myxomatous aneurysms
High-density lesion and homogenous enhancement on CT
Left PCA, both PICAs
Homogenous enhancement on CT –
Right MCA, both PICAs
–
Left MCA
–
Left ACA, both MCAs
–
Left ICA, right MCA
–
is unclear [25]. This is indeed a difficult situation encountered in daily routine practice. We found some interesting features, as outlined below, which may help to overcome this clinical dilemma. In our study, we found persistently high-density on plain CT adjacent to the aneurysms. This was an interesting feature of myxomatous aneurysms, which has only been mentioned and not emphasized in a few previous reports [26,27]. This kind of high-density lesion surrounding aneurysms on CT was
Fig. 2. Patient 2 had multiple aneurysms. (A) CT with multiple rounded high-density lesions in both frontal and parietal lobes. (B) MIP reconstruction images from the CTA showing high-density lesion in the vicinity of cerebral granular aneurysms. (C) Contrast-enhanced CT showing homogenous enhancement surrounding the aneurysms. (D) 3D reconstruction images and (E) and (F) MIP reconstruction image from the CTA clearly confirming multiple cerebral fusiform aneurysms involving distal segments of cerebral arteries on both sides.
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Fig. 3. Patient 1 had multiple aneurysms. (A–C) CT scan of the brain showing multiple foci of high density lesions in both frontal and parietal lobes (numbered 2 in A and black arrow in B and C) surrounded by low density edema (numbered 1 in A). (D) T2WI demonstrating multiple lesions located adjacent to cerebral sulci presenting with gyral pattern of marked signal loss on T2WI (black arrows). (E) Reconstructed MIP image from MRA revealing multiple distal aneurysms involving segments of MCA and ACA, long black arrow shows a saccular aneurysm and short black arrow shows a fusiform aneurysm. (F) DSA image showing multiple fusiform (angled arrow) and saccular (horizontal arrow) aneurysm involving the PCA territory shown during angiography of the left vertebral artery. (G) T2WI with local encephalomalacia in the head of the left caudate nucleus (black arrow).
histopathologically verified to be the accumulation of myxoid matrix and hemosiderin, but not calcification [26]. Atrial myxomas which are the embolic source are also histologically characterized by the accumulation of myxoid material and stellate cells. We believe that this CT finding is one of the imaging features, among others described below, which may help in narrowing down the diagnosis of peripheral cerebral arterial aneurysms. It was interesting to note that the high-density was persistent on follow-up imaging. This can be suggestive of repeated and slight hemorrhage
(just like errhysis) in the vicinity of the aneurysms. The hyperdense appearance of these aneurysms on plain CT scan is supposed to be due to deposition of myxoid matrix and hemosiderin [28]. In addition, we noted the presence of obvious and homogenous enhancement surrounding most aneurysms in two patients on contrast-enhanced imaging. This was not reported previously and was another point of interest to us. A rational explanation for this imaging feature was the accumulation and proliferation of myxomatous tumor cells, granulation tissue, neovascularization, and
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hematoma organizing in the vicinity of the aneurysms. Angiogenesis or neovascularization is a complex biological process which is regulated by a number of cytokines or growth factors, like IL-6. As we have seen earlier, these are secreted by the myxomatous tumor cells [20]. This finding on contrast-enhanced CT is therefore another helpful feature in the diagnostic work-up of distal aneurysms. We also observed changes surrounding these aneurysms on MR imaging, notably, signal loss on T2WI. This finding may be explained as being a result of the combined effects of the dense deposits of hemosiderin (hypointense) and iron breakdown products surrounding the hemorrhagic aneurysms following chronic and recurrent hemorrhage [29]. Therefore, we see that there are specific imaging features in both CT, unenhanced and enhanced alike, and MRI which are helpful in making the definitive diagnosis of myxomatous aneurysms. The abnormal changes adjacent to aneurysms on both nonenhanced and contrast-enhanced imaging, caused by repeated hemorrhage or myxomatous tumor cells which can transgress outside the aneurysmal wall progressively[25], is a notable imaging feature and may contribute to differential diagnosis of intracranial peripheral aneurysms, such as infectious aneurysms and traumatic aneurysms. Infectious aneurysms, which present with a similar morphologic pattern, that is fusiform shape, multiplicity and located on distal vessels, are more prone to rupture, resulting in subarachnoid hemorrhage or acute hematoma in the vicinity of the aneurysms [30,31]. Traumatic aneurysms, resulting from direct penetrating head injuries or blunt head trauma, may be associated with other traumatic lesions [32]. Another cardiac condition also leading to a similar pattern of brain infarcts is patent foramen ovale (PFO), by means of paradoxical emboli through abnormal intracardiac or intrapulmonary communication between the right and left circulations [33]. The difference is that there is no apparent cardiac source on the left side of the heart or in the proximal arterial tree (ascending aorta) in PFO. Another difference is that no perilesional changes are observed in case of PFO. Peripherally located arterial aneurysms may be either neoplastic (secondary to myxoma), mycotic (infectious secondary to endocarditis) or traumatic in origin [34]. With such a broad differential diagnosis, we have to rely on other tell-tale signs. We found the presence of abnormal changes adjacent to these aneurysms on both non-enhanced and contrast-enhanced imaging and these were unique features, which could contribute to the differential diagnosis of peripheral aneurysms. These perilesional changes are the highlights of our article and are essentially seen on both CT and MR images. Our article therefore brings to light new information for diagnosing myxomatous aneurysms. First, we found high-density on non-enhanced CT adjacent to the aneurysms and this change is persistent on follow-up. Second, we also observed the presence of obvious and homogeneous enhancement surrounding the aneurysms on contrast-enhanced CT. These changes showed up as loss of signal intensity on T2WI on MR scanning. In conclusion, the common neurologic complications are cerebral infarction due to thromboembolism. Neuroimaging usually shows multiple infarcts of varying stages of chronicity: acute, subacute to chronic. Accordingly, echocardiography should be performed in patients with suspected embolic events, especially when cerebral infarcts with multiple territorial lesions and multiple phases are detected. The occurrence of myxoma-associated aneurysms is another manifestation of delayed neurological complications caused by left atrial myxoma. These aneurysms are characteristically distal in location, fusiform in shape and multiple in number. More attention should be paid to the changes surrounding the aneurysms on both non-enhanced and contrastenhanced imaging when myxomatous aneurysms are suspected. These important features are what help not only in differentiating
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