Magnetic resonance imaging characteristics of cardiac hydatid cyst

Clinical Imaging 51 (2018) 202–208

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Magnetic resonance imaging characteristics of cardiac hydatid cyst ⁎

T

Ravza Yılmaz , Yunus Emre Akpınar, Zuhal Bayramoglu, Halil Ibrahim Ozyavuz, Omer Faruk Unal, Memduh Dursun Istanbul University, Istanbul Medical Faculty, Radiology Department, Capa, Fatih, Istanbul TR 34098, Turkey

A R T I C LE I N FO

A B S T R A C T

Keywords: Magnetic resonance imaging Cardiac hydatid cyst Cardiac cysts Cardiac magnetic resonance imaging Peripheral rim enhancement of cardiac cysts

Purpose: The purpose of this article is to describe the magnetic resonance imaging (MRI) features of cardiac hydatid disease and show the specific findings in the diagnosis of hydatic cysts. Materials and methods: A retrospective review of cardiac MRI records between 2015 and 2017, 7 patients (3 males, 4 females; age range: 14–74) were identified with the histologic diagnosis of cardiac hydatid disease. Cardiac MRI examinations were performed in order to investigate the cardiac cystic-solid lesion obtained via previous echocardiography (ECG) and thorax computed tomography. 1.5 Tesla magnetic field power generation capacity was used and the images were acquired with ECG trigger. Results: There is variation in signal characteristics of cysts on T1-weighted and T2-weighted images. Early contrast enhancement was not observed in the any of lesions on contrast-enhanced series. In all lesions examined, peripheral contrast enhancement was observed in the late contrast enhanced series, independent from the internal structure and signal intensity. Conclusions: MRI reveals the exact anatomic location and nature of the cyst structures. Peripheral enhancement of non-enhancing lesion is very valuable for diagnosis of cardiac hydatids on MRI.

1. Introduction Hydatid disease is a parasitic infection caused by larvae of Echinococcus granulosus, which is still endemic in some parts of the world. Domestic dogs and cats are the primary carriers of echinococcal organisms. Humans are infected as intermediary carriers when they eat raw or unwashed and uncooked vegetables and swallow parasitic ova. After the person digests the contaminated food, the embryo of the parasite is released into the intestinal tract and carried to the liver by the portal circulation [1]. Hydatid cysts are surrounded by periparasitic host tissue (pericyst) embracing the larval endocyst. The cyst inside the laminated layer, or hyaline membrane is covered by a multipotential germinal layer that leads to the production of brood capsules and protoscolices [1]. Cardiac involvement is an uncommon presentation of hydatid cyst disease, accounting for approximately 0.5–2% of all hydatidosis cases, and mainly occurring as part of a systemic infection [2]. In cases with cardiac involvement, the left ventricle is the most frequently (50%–60%) affected part, but the interventricular septum (10%–20%), right ventricle (5%–15%), pericardium (7%), pulmonary artery (6%), and right or left atrium (5%–8%) may also be involved [3,4]. Cardiac involvement occurs by invasion of the myocardium, first through the coronary artery circulation. The second route of infestation is the ⁎

Corresponding author. E-mail address: [email protected] (R. Yılmaz).

https://doi.org/10.1016/j.clinimag.2018.05.016 Received 14 January 2018; Received in revised form 22 May 2018; Accepted 24 May 2018 0899-7071/ © 2018 Published by Elsevier Inc.

pulmonary vein from rupture of pulmonary echinococcal cysts into the vein or the portal system from invasion of hepatic hydatid cysts [3,5]. Signs and symptoms of cardiac hydatid disease are extremely variable and associated with the location and the size of the cysts. Most of the patients with cardiac echinococcosis have no symptoms because hydatid cysts, which are located in the heart, grow very slowly. The most common symptom is precordial pain. Only approximately 10% of patients, especially those with large hydatid cysts, have clinical manifestations [3]. If the cyst compresses the coronary arteries, it may cause angina pectoris. A compression of the bundle of His may result in conduction abnormalities. Mitral stenosis can be simulated when the cyst lies in the left atrium obstructing the cardiac outflow. Pericarditis, anaphylactic shock, systemic and pulmonary embolisms are major complications of the cardiac involvement. The most commonly used hydatid cyst classification is the Gharbi classification. It is classified hydatid cyst images into 5 types. Type 1, walled, unilocular, pure fluid collection; type 2, fluid collection with a detached a membrane; type 3, fluid collection with multiple septa and/or daughter cysts; type 4, heterogenic, hypo-hyperechogenic fluid collection; type 5, calcification of a section of the wall or completely calcified cyst [6]. Magnetic resonance imaging (MRI) is an excellent modality demonstrating with its higher soft tissue contrast that allow distinguishing circulating blood and soft tissue as well as demonstrating cardiac

203

Peripheral − Mildly hyperintense heterogeneous

24

14

27

15

35

53

2

3

4

5

6

7

EF, ejection fraction of left ventricle.

74 1

⁎

46%

39

Type 4

28 × 41 × 30

Single

Multilocule

Thick (3)

+

−

Mildly hypointense heterogeneous

Peripheral − Hyperintense − − 42 39%

Type 4

56 × 70 × 100

Single

Multilocule

Thick (2,5) Thick (4,1) Unilocule Single 51 × 43 × 47 Type1 31 40%

Unilocule Single 66 × 54 × 39 43 35%

Type2

Unilocule Single 56 × 44 × 49 29 41%

Type 3

Unilocule Single 41 × 29 × 29 Type 3 41 45%

Hyperintense − −

Hyperintense

−

Peripheral − + −

Hyperintense

Hypointense − +

Mildly hyperintense heterogeneous Hyperintense

Peripheral −

Peripheral − Isointense +

_

Mildly hyperintense Hyperintense

Peripheral + Hyperintense − − Unilocule Single 61 × 47 × 57 Type 1 39 55%

Middiastolic left ventricle diameter (mm) Ventricular function (EF⁎) Location Age Case

Table 1 Magnetic resonance imaging features of cardiac hydatic cysts.

The patients were aged 14–74 years (mean: 34.5 ± years). Only one lesion was depicted in all patients. Two of these lesion is multilocular (2/7) and the remaining (5/7) were unilocular. Presence of daughter cysts in hydatid cyst was seen in two patients and detached membranes were seen in one patient. Two of the lesions were type 1, one was type 2, two were type 3 and two were type 4 hydatic cyst according to Gharbi classification. One of the lesions was located in the supero-posterior portion of the left atrium and did not create any indentation towards the heart chambers. Two of the remaining lesions were localized in the interventricular septum and three of seven lesions were localized in the left ventricular freewall. One of the lesion was depicted in the intramyocardial localization of the left ventricular anterior-superior wall and formed bulging from the septum anterior to the right ventricle. Another lesion was localized to the left ventricular postero-lateral wall and had an exophytic extension towards the paracardiac area. In the images examined, the longest axis of the lesions ranged from 41 mm to 66 mm. Left ventricle size and ejection fraction were reported in the Table 1. Lesions were hyperintense in five patients and hypointense in one patient and isointense in one patient on T1-weighted images. One of these lesions was heterogeneously hypointense. On T2-weighted images, all of the lesions were hyperintense. The lesions located ventricular myocardium caused low ejection fraction and one of them shows heterogeneous signal intensity. The wall thickness of these lesions is based on a 2 mm cut-off value. One of the lesions had a wall

Gharby classification

Size (mm)

3. Results

Thin (1,8) Thick (5,3) Thick (2,6) Thin (2,1)

Membrane detachment Single/ multiple

Unilocule/ multilocule

Thin/ thick wall (mm)

Daughter cyst

T1-weighted signal

T2-weighted signal

A total of 7 patients (3 males, 4 females; age range: 14–74) with a pathologic diagnosis of cardiac hydatid disease were retrospectively screened and evaluated from the hospital PACS system which includes cardiac MRI images archived. The study was approved by the hospital local ethics committee. Patients included in the study, were referred to our hospital for various reasons such as chest pain, dyspnea or palpitation. All patients underwent transthoracic echocardiography (ECG), three patients additionally underwent thorax computed tomography (CT). Cardiac MRI examinations were performed in order to investigate the cardiac cysticsolid lesion obtained via previous echocardiography and thorax CT. In our study, MRI device (Symphony, Siemens Medical Solutions) with 1.5 Tesla magnetic field power generation capacity was used and the images were acquired with ECG trigger. The obtained MRI sequences were T1-weighted spin echo (TR/TE: 700/26; matrix size: 133 × 256; slice thickness of 5 mm), T2-weighted spin echo (TR/TE: 800/81; matrix size: 133 × 256; slice thickness of 5 mm) echo-planar cine true fast imaging with steady-state precession (50/170; matrix size: 256 × 256; slice thickness: 6 mm) and dark blood (TR/TE 800/26; matrix size: 256 × 256; slice thickness: 6 mm). First pass myocardial perfusion imaging and late gadolinium enhancement known as myocardial delayed enhancement is performed. Late contrast enhanced obtained as 10–20 min following intravenous injection of 0.1–0.2 mmol/kg gadolinium-based contrast agent. For delayed phase images 3D inversion recovery-prepared single shot gradient-echo sequence (turbo FLASH) with the following parameters (TR/TE: 700/3.3 ms; TI: 300 ms; flip angle: 25; acquisition matrix: 133 × 256) on short axis plane of heart and if necessary long axis images were obtained. Also mid-diastolic left ventricle diameter and ejection fraction of left ventricle for functional evaluation were measured in all patients.

Left atrium/ exophytic Left vent, intramyocardial Interventricular septum Left vent, intramyocardial/ exophytic Interventricular septum Left atrioventricular septum/exophytic Left ventricle ant. intramyocardial

2. Materials and methods

Hyperintense

Hypointense ring on T2weighted

Late enhancement

anatomy with a global view. Experience with MRI findings of patients with cardiac hydatid disease is still limited [3,4,7,8]. In this article, we describe the MRI features of cardiac hydatid disease and provide detailed description of peripheral enhancement that can be an important sign in the diagnosis of hydatid cysts.

Peripheral

Clinical Imaging 51 (2018) 202–208

R. Yılmaz et al.

Clinical Imaging 51 (2018) 202–208

R. Yılmaz et al.

Fig. 1. (case 1*): 74 year-old male patient. The cyst (star) is hyperintense on pre-contrast fat-sat T1-weighted (a) and T2-weighted (b) axial images. At the cyst wall, peripheral rim-shaped hypointensity (arrow) is seen on T2-weighted axial image (b). On vertical long axis two chambers cine image (c), the cyst (star) is seen next to the left atrium. Delayed phase axial image and peripheral rim enhancement (arrow) around the cyst wall is seen (d).

Transthoracic echocardiography is the elementary imaging technique but it carries several well described limitations, including operator dependence, restricted field of view in patients with a large body habitus, and limited views of the left ventricular apex and the right heart chambers. CT provides useful information in detecting specific findings and performs better than transthoracic echocardiography by distinguishing cysts from solid tumors such as myxomas or fibromas both by CT density measurements and also analysis of enhancement after intravenous contrast injection [4]. Current limitations of this technique include a significant radiation dose, and lower temporal resolution compared with echocardiography and cardiac MRI. The development of increasing magnet strengths and surface coil channels and postprocessing techniques, and sophisticated myocardial soft-tissue characterization sequences have made cardiac MRI a powerful tool in the workup of many complex cardiac conditions [11]. MRI can give precious knowledge on both the lesion morphology and its relation to other cardiac and extracardiac structures and thereby can guide the surgery. A cardiac hydatid cyst usually appears as an oval or spherical lesion that is hypointense on T1-weighted images and with a signal intensity more than or equal to cerebrospinal fluid on T2-weighted images. The hypointense peripheral ring on T2-weighted images, which represents

thickness below this value (1.8 mm) and the others had a wall thickness above the 2 mm limit (mean value: 2.9 mm). On T2-weighted images, only one of the lesions had hypointense rim (Fig. 1). On the first pass myocardial perfusion sequence, signal enhancement was not observed in any of the lesions. In all lesions examined, peripheral contrast enhancement was observed in the late contrast enhanced series, independent from the internal structure and signal intensity (Table 1). 4. Discussion Cardiac hydatid cyst is rare and involves other organs in approximately 50% of cases [9,10]. Patients often present with nonspecific features, early and accurate diagnosis of this condition is crucial to avoid complications, such as rupture. As in other parts of the body, the cardiac hydatid cyst can be single or multiple, uniloculated or multiloculated, or thin or thick-walled. The wall of the parasitic cyst consists of a germinal layer (endocyst) and a laminated proteinaceous membrane (ectocyst). The host reacts against the cyst by forming a dense fibrous capsule (pericyst), which contains blood vessels that provide nutrients to the parasite. Calcification of the cyst wall, presence of daughter cysts, and detached membranes are relatively more specific for cardiac hydatid disease (Fig. 2). 204

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Fig. 2. (case 3*): 14 year-old female patient. The cyst (star) is hypointense on precontrast T1-weighted image (a). Signal characteristic of the cyst is mildly hyperintense on T2-weighted axial image (b) Daughter cysts (stars) is seen within the cyst (arrows) located in the interventricular septum on short axis (c) and longitudinal axis cine images (d). On sagittal (e) and short axis (f) T1-weighted delayed phase cardiac images after contrast injection, peripheral rim enhancement (arrows) is seen around the cyst.

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Fig. 3. (case 4*): 27 year-old male patient who suffers from palpitation and dyspnoea. The cyst (white arrows) that includes detached membranes (small arrows), is hyperintense on T2-weighted images (a) and mildly hyperintense on T1-weighted axial (b) images because of high intensity content The cyst (star) located in left ventricle posterior wall myocardium is seen on short axis (c) and four chambers (d) cine images. On delayed phase short axis series (e), peripheral rim enhancement (arrows) is seen in the cyst wall.

the pericyst, is indicated in the literature as a typical finding for hydatid cysts [7,12]. Walther et al. reported that, this may be related to developmental stages of hydatid cysts and simple viable hydatid cysts appear with low-intensity rim surrounding high-signal cyst contents [13]. This hypointense ring was not observed in one patient in our case

series and is not commonly seen in part of the cases of cardiac hydatic cysts [4,14,15]. Imaging findings range from purely cystic lesions to a completely solid appearance which can be difficult to differentiate from heart tumors. Postcontrast early-late phase images show a cystic lesion with 206

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Fig. 4. (case 7*): 53 year-old male patient who was diagnosed with a complex multilocular cyst at echocardiography examination in the left ventricle anterior wall myocardium. On T1 weighted image (a) the cyst (arrows) is mildly hyperintense and on T2 weighted image (b) the cyst (arrows) is mildly hypointense. On the short axis T1-weighted and T2 weighted images, the cyst is seen with heterogeneous signal intensity. Short axis cine image (c), heterogeneous internal structure because of solid component is seen within the cyst (stars). Short axis delayed phase image (d) minimal peripheral rim enhancement (arrow) is seen.

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peripheral enhancement in all of our patients. Even in the appearance of a simple cyst or solid appearance, presence of daughter cysts or detached membranes; peripheral enhancement of a non-enhancing lesion is extremely valuable for diagnosis of cardiac hydatids (Figs. 3 and 4). Differential diagnosis depends on the localization of hydatid cysts. It must be differentiated from benign cysts or neoplasms such as thymic cysts, pericardial cysts, dermoid cysts and cystic teratomas [15]. Pericardial cysts fail to enhance on contrast enhanced images with both cardiac CT and MRI [16,17]. Although there is significant variation in signal characteristics on T1-weighted and T2-weighted images, almost all cardiac and pericardial neoplasms enhance with gadolinium administration [18–20]. In case of a suspected hydatid cyst, presence of the wall structure and peripheral contrast enhancement are crucial to distinguish it from other cardiac masses.

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5. Conclusion Cardiac hydatid disease should be our preferential differential diagnosis in the presence of thick walled structures and peripheral contrast enhancement in an oval or spherical shaped mass on MRI when patients' clinical appearance is appropriate for hydatid disease. Conflict of interest None of the authors have any conflicts of interest to declare. 207

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