Pericardial Recesses Mimicking Mediastinal Adenopathy on CT

Thin-section computed tomography (CT) has improved the detection of pericardial recesses and sinuses. Physiologic fluid in the pericardial recesses and sinuses can mimic mediastinal adenopathy. The misinterpretation of pericardial recesses and other benign pericardial entities in the oncologic setting can lead to inappropriate staging and management. Knowledge of the anatomy of the pericardium with emphasis on the imaging of different pericardial recesses on CT is important to avoid misdiagnosis, unnecessary further investigations, and/or biopsy.


Introduction
The pericardium is a thin, relatively avascular, fibrous sac that envelops the heart. The pericardium consists of the visceral and parietal pericardium. Composed of a thin layer of mesothelial cells, the visceral pericardium lines the epicardial surface of the heart [1]. The parietal pericardium is composed of the outer fibrous component and inner a doublelayered inner serosa. The outer fibrous component of the parietal pericardium attaches to the diaphragm, sternum, and great vessels [1]. The inner serosal layer is composed of a thin layer of mesothelial cells [2]. The potential space between the visceral and parietal serous layers is termed the pericardial cavity. The pericardial cavity normally contains up to 50 mL of fluid [3]. The pericardial cavity contains the transverse and oblique sinuses, which further subdivide into the pericardial recesses ( Figure 1) [4]. Thin-section computed tomography (CT) has improved the detection of pericardial recesses and sinuses [5,6]. The various appearances of these spaces are known to mimic mediastinal adenopathy. Misinterpretation of these normal findings and variants can lead to incorrect staging, unnecessary follow-up, and inappropriate treatment. Furthermore, pericardial anatomy is essential in the epicardial approach for cardiac electrophysiological interventions to treat cardiac arrhythmias refractory to conventional endocardial ablation. We review normal pericardial anatomy and mimics/pitfalls on CT, magnetic resonance imaging (MRI), and positron emission tomography-CT (PET-CT).

Imaging Features
Imaging features that allow confident diagnosis of pericardial recesses include typical locations, fluid attenuation/signal characteristics, lack of mass effect on neighboring structures, and contiguity with pericardial spaces. Mediastinal adenopathy typically demonstrates reniform shape and lobular margins. In contrast to pericardial recess fluid, adenopathy typically has soft tissue attenuation and may demonstrate contrast enhancement. Areas of low-attenuation can be seen in areas of necrosis. Additionally, adenopathy may exert mass effect on neighboring structures. In cases where CT is indeterminate, MRI and PET-CT may be helpful in distinguishing adenopathy from pericardial fluid. Simple

Imaging Features
Imaging features that allow confident diagnosis of pericardial recesses include typical locations, fluid attenuation/signal characteristics, lack of mass effect on neighboring structures, and contiguity with pericardial spaces. Mediastinal adenopathy typically demonstrates reniform shape and lobular margins. In contrast to pericardial recess fluid, adenopathy typically has soft tissue attenuation and may demonstrate contrast enhancement. Areas of low-attenuation can be seen in areas of necrosis. Additionally, adenopathy may exert mass effect on neighboring structures. In cases where CT is indeterminate, MRI and PET-CT may be helpful in distinguishing adenopathy from pericardial fluid. Simple pericardial recess fluid shows low signal intensity on T1-weighted images, high signal intensity on T2-weighted images, and steady-state free precession sequences [7]. Lymphadenopathy and pericardial tumors can have variable signal intensity on MRI depending on its composition and typically demonstrates postcontrast enhancement. On 18-fluorodeoxyglucose (FDG)-PET-CT, pericardial recesses do not show FDG uptake, while lymphadenopathy and pericardial tumors can have variable uptake depending on composition.

Transverse Sinus
The transverse sinus is positioned caudal and posterior to the aorta and the pulmonary trunk and cephalad to the left atrium (LA) (Figure 2) [4]. The transverse sinus gives rise to four recesses that extend between the great vessels and the LA: the superior aortic recess, inferior aortic recess, left pulmonic recess, and right pulmonic recess. J. Respir. 2022, 2, FOR PEER REVIEW 3 pericardial recess fluid shows low signal intensity on T1-weighted images, high signal intensity on T2-weighted images, and steady-state free precession sequences [7]. Lymphadenopathy and pericardial tumors can have variable signal intensity on MRI depending on its composition and typically demonstrates postcontrast enhancement. On 18fluorodeoxyglucose (FDG)-PET-CT, pericardial recesses do not show FDG uptake, while lymphadenopathy and pericardial tumors can have variable uptake depending on composition.

Transverse Sinus
The transverse sinus is positioned caudal and posterior to the aorta and the pulmonary trunk and cephalad to the left atrium (LA) (Figure 2) [4]. The transverse sinus gives rise to four recesses that extend between the great vessels and the LA: the superior aortic recess, inferior aortic recess, left pulmonic recess, and right pulmonic recess.

Superior Aortic Recess
The cranial extent of the transverse sinus is the superior aortic recess, which can be subdivided into the right lateral, posterior, and anterior portions. The right lateral portion extends along the right side of the ascending aorta to the level of the sternal angle. The posterior portion has a characteristic half-moon shape and extends behind the posterior part of the ascending aorta, and is also referred to as the superior pericardial recess (Figure 3) [4]. The anterior portion of the superior aortic recess passes anterior to the aorta and pulmonary artery, forming a characteristic cleft between the great vessels [8,9]. The anterior portion of the superior aortic recess in the aorto-pulmonic window (APW) is termed the APW recess and can mimic adenopathy ( Figure 4) [4]. the transverse sinus. Soft tissue attenuation and enhancement help distinguish adenopathy or metastatic disease from recess fluid. Ao = ascending aorta, LAA = left atrial appendage, PA = pulmonary artery. Reprinted from Shroff, G.S et al. Pitfalls in oncologic imaging of the pericardium on CT and PET/CT [4].

Superior Aortic Recess
The cranial extent of the transverse sinus is the superior aortic recess, which can be subdivided into the right lateral, posterior, and anterior portions. The right lateral portion extends along the right side of the ascending aorta to the level of the sternal angle. The posterior portion has a characteristic half-moon shape and extends behind the posterior part of the ascending aorta, and is also referred to as the superior pericardial recess ( Figure  3) [4]. The anterior portion of the superior aortic recess passes anterior to the aorta and pulmonary artery, forming a characteristic cleft between the great vessels [8,9]. The anterior portion of the superior aortic recess in the aorto-pulmonic window (APW) is termed the APW recess and can mimic adenopathy ( Figure 4) [4]. A lesser-known variant is the "high riding" superior pericardial recess (HRSPR), which extends cephalad into the right paratracheal region between the brachiocephalic vessel and trachea [10]. Contiguity between the caudal aspect of the high-riding and the superior pericardial recess on CT and MRI enables distinguishing this entity from lymphadenopathy or other cystic mediastinal lesions [2]. The reported incidence of the HRSPR ranges from 2-7% [6,10].

Inferior Aortic Recess
The crescent shaped inferior aortic recess extends caudally to the level of the aortic valve, posterior to the ascending aorta and anterior to the left atrium [11].

Right and Left Pulmonic Recesses
The right and left pulmonic recesses are caudal to the right and left pulmonary arteries [11]. Fluid within the pulmonic recesses can mimic adenopathy ( Figure 5) [4].  A lesser-known variant is the "high riding" superior pericardial recess (HRSPR), which extends cephalad into the right paratracheal region between the brachiocephalic vessel and trachea [10]. Contiguity between the caudal aspect of the high-riding and the superior pericardial recess on CT and MRI enables distinguishing this entity from lymphadenopathy or other cystic mediastinal lesions [2]. The reported incidence of the HRSPR ranges from 2-7% [6,10].

Inferior Aortic Recess
The crescent shaped inferior aortic recess extends caudally to the level of the aortic valve, posterior to the ascending aorta and anterior to the left atrium [11].

Right and Left Pulmonic Recesses
The right and left pulmonic recesses are caudal to the right and left pulmonary arteries [11]. Fluid within the pulmonic recesses can mimic adenopathy ( Figure 5) [4].
A B

Oblique Sinus
The oblique sinus is located posterior to the left atrium and anterior to the esophagus. Typically, a fat plane can be observed between the oblique sinus and the esophagus [12] ( Figure 6) [4]. The oblique sinus is separated from the transverse sinus by a double reflection of serous pericardium [8]. Fluid in the oblique sinus can be misinterpreted as abnormalities related to the esophagus, descending thoracic aorta, and subcarinal lymph nodes [4,13] (Figure 7).
representing pericardial metastatic disease (*) in the left pulmonic recess. Arrow de pericardial metastasis along the right heart. Soft tissue attenuation and enhancem guish adenopathy or metastatic disease from recess fluid. PA = pulmonary artery Shroff, G.S et al. Pitfalls in oncologic imaging of the pericardium on CT and PET/C

Oblique Sinus
The oblique sinus is located posterior to the left atrium and anterior to Typically, a fat plane can be observed between the oblique sinus and the ( Figure 6) [4]. The oblique sinus is separated from the transverse sinus by a tion of serous pericardium [8]. Fluid in the oblique sinus can be misinterp malities related to the esophagus, descending thoracic aorta, and subcarina [4,13] (Figure 7).

Pericardial Cavity Proper
The pericardial cavity proper gives rise to three recesses: right and left pulmonary venous recesses and the postcaval recess.

Postcaval Recess
The postcaval (or retrocaval) recess is located posterior to the superior vena cava, extending from the right pulmonary vein cranially to the level of the right pulmonary artery ( Figure 1C) [4].

Pericardial Cavity Proper
The pericardial cavity proper gives rise to three recesses: right and left pulmonary venous recesses and the postcaval recess.

Postcaval Recess
The postcaval (or retrocaval) recess is located posterior to the superior vena cava, extending from the right pulmonary vein cranially to the level of the right pulmonary artery ( Figure 1C) [4].

Right and Left Pulmonary Venous Recesses
The right and left pulmonary venous recesses are positioned between the superior and inferior pulmonary veins, where the pericardium is attached to the venous adventitia [11,14]. Fluid accumulation in the right pulmonary venous recess is a commonly reported finding and can be mistaken for bronchopulmonary adenopathy. Truong et al. evaluated the imaging characteristics of six patients with fluid in the pericardial sleeve recess mistaken for adenopathy, finding that the fluid in the anterior and posterior components to be spindle shaped, and fluid within the superior and inferior components to be ovoid [14]. Adenopathy usually occurs on one side of the vein. Pericardial pulmonary venous recess fluid has no attributable mass effect on the right inferior pulmonary vein, whereas adenopathy can cause mass effect and narrowing of the vein [4,14] (Figures 8 and 9).

Right and Left Pulmonary Venous Recesses
The right and left pulmonary venous recesses are positioned between the superior and inferior pulmonary veins, where the pericardium is attached to the venous adventitia [11,14]. Fluid accumulation in the right pulmonary venous recess is a commonly reported finding and can be mistaken for bronchopulmonary adenopathy. Truong et al. evaluated the imaging characteristics of six patients with fluid in the pericardial sleeve recess mistaken for adenopathy, finding that the fluid in the anterior and posterior components to be spindle shaped, and fluid within the superior and inferior components to be ovoid [14]. Adenopathy usually occurs on one side of the vein. Pericardial pulmonary venous recess fluid has no attributable mass effect on the right inferior pulmonary vein, whereas adenopathy can cause mass effect and narrowing of the vein [4,14] (Figures 8 and 9).

Additional Pitfalls in Pericardial Imaging
Infectious and inflammatory conditions can result in FDG uptake on PET-CT. A few potential pitfalls include hypermetabolic brown fat, acute pericarditis, and epipericardial fat necrosis.

Additional Pitfalls in Pericardial Imaging
Infectious and inflammatory conditions can result in FDG uptake on PET-CT. A few potential pitfalls include hypermetabolic brown fat, acute pericarditis, and epipericardial fat necrosis.

Hypermetabolic Brown Fat
Brown fat (or brown adipose tissue) has a smaller cell size, higher mitochondrial density, and increased vascularity compared with white fat tissue. It is found in the cervical, supraclavicular, paravertebral, axillary, mediastinal, and abdominal regions [15]. High physiologic uptake of FDG can be seen in activated brown fat, which can be mistaken for malignancy or potentially obscure small metastases. Brown fat activation is associated with younger age, lower body mass index, and lower temperature environments [15]. Although it can be easily recognized when bilateral and symmetric in distribution and corresponding low attenuation on CT, focal FDG uptake can be seen in the setting of lipomatous hypertrophy of the interatrial septum (LHIS) (Figure 10) [4]. LHIS is a benign finding, in which adipose tissue (including brown adipose) increases between the myocardial fibers of the interatrial septum [16].

Hypermetabolic Brown Fat
Brown fat (or brown adipose tissue) has a smaller cell size, higher mitochondrial density, and increased vascularity compared with white fat tissue. It is found in the cervical, supraclavicular, paravertebral, axillary, mediastinal, and abdominal regions [15]. High physiologic uptake of FDG can be seen in activated brown fat, which can be mistaken for malignancy or potentially obscure small metastases. Brown fat activation is associated with younger age, lower body mass index, and lower temperature environments [15]. Although it can be easily recognized when bilateral and symmetric in distribution and corresponding low attenuation on CT, focal FDG uptake can be seen in the setting of lipomatous hypertrophy of the interatrial septum (LHIS) (Figure 10) [4]. LHIS is a benign finding, in which adipose tissue (including brown adipose) increases between the myocardial fibers of the interatrial septum [16].

Acute Pericarditis
Acute inflammation of the pericardium can be due to infection, drug reaction, radiation therapy, cardiac injury, systemic inflammatory processes, and metabolic conditions [17]. CT and MRI findings include smooth or nodular pericardial thickening (>4 mm), enhancement, and effusion ( Figure 11) [4]. Focal or diffuse FDG uptake can be seen in both neoplastic and nonneoplastic causes [18]. The overlap in imaging findings can make differentiating neoplastic and nonneoplastic causes difficult, and careful correlation with extracardiac findings, laboratory analysis, and history is needed.

Acute Pericarditis
Acute inflammation of the pericardium can be due to infection, drug reaction, radiation therapy, cardiac injury, systemic inflammatory processes, and metabolic conditions [17]. CT and MRI findings include smooth or nodular pericardial thickening (>4 mm), enhancement, and effusion ( Figure 11) [4]. Focal or diffuse FDG uptake can be seen in both neoplastic and nonneoplastic causes [18]. The overlap in imaging findings can make differentiating neoplastic and nonneoplastic causes difficult, and careful correlation with extracardiac findings, laboratory analysis, and history is needed.

Epipericardial Fat Necrosis
Epipericardial fat necrosis (or pericardial fat necrosis) is a self-limited process that can be a source of chest pain. The CT findings include fat attenuation surrounded by a rim of soft tissue with fat stranding, similar in appearance to epiploic appendagitis [19] ( Figure 12) [4]. Associated pericardial and pleural effusions can be seen [17,19]. Focal FDG uptake can be seen on PET-CT [20]. These findings could mimic cardiophrenic adenopathy or pericardial metastasis. Resolution should be seen on follow-up imaging. Avoiding misdiagnosis of this self-limited process can prevent inappropriate staging or testing. J. Respir. 2022, 2, FOR PEER REVIEW 12

Epipericardial Fat Necrosis
Epipericardial fat necrosis (or pericardial fat necrosis) is a self-limited process that can be a source of chest pain. The CT findings include fat attenuation surrounded by a rim of soft tissue with fat stranding, similar in appearance to epiploic appendagitis [19] (Figure 12) [4]. Associated pericardial and pleural effusions can be seen [17,19]. Focal FDG uptake can be seen on PET-CT [20]. These findings could mimic cardiophrenic adenopathy or pericardial metastasis. Resolution should be seen on follow-up imaging. Avoiding misdiagnosis of this self-limited process can prevent inappropriate staging or testing.

Conclusions
The pericardial recesses are commonly observed on cross-sectional imaging, particularly with the advent of thin-section computed tomography. Physiologic fluid in the pericardial recesses and sinuses can mimic mediastinal adenopathy. The misinterpretation of pericardial recesses and other benign pericardial entities in the oncologic setting can lead to inappropriate staging and management. Knowledge of the anatomy of the pericardium and awareness of the spectrum of imaging appearances of different pericardial recesses on CT are essential to avoid misdiagnosis, unnecessary investigations, and/or biopsy.
Author Contributions: J.M.A. prepared the original draft of the manuscript. All authors contributed to obtaining images, manuscript revision, and final approval the submitted version. All authors have read and agreed to the published version of the manuscript.
Funding: This research received no external funding.

Data Availability Statement:
No new data were created or analyzed in this study. Data sharing is not applicable to this article.