MR Imaging of the Perihepatic Space

The perihepatic space is composed of different spaces, mainly the right subphrenic and subhepatic spaces. The liver is surrounded by the visceral peritoneum, which usually contains a small amount of serous fluid. The spread of inflammatory and tumoral processes to the perihepatic space is dependent on the distribution and dynamics of the peritoneal fluid. The latter is determined by hydrostatic pressure and the effect of gravity as well as peritoneal recesses and mesenteric reflections. Liver disease conditions may also extend to the liver capsule and subsequently to the perihepatic space. Extension from other peritoneal or extraperitoneal sites may follow the communication pathways through the hepatic ligaments to the perihepatic space ( 1 ). Computed tomography (CT) is the usual cross-sectional imaging technique with which the perihepatic space abnormalities are discovered and evaluated. However, as magnetic resonance imaging (MRI) is being used more widely, it is crucial to be familiar with the appearance of these lesions on MRI. Moreover, the optimal contrast resolution of MRI allows better detection and characterization of some lesions in the perihepatic space compared to CT. The purpose of this article was to describe the MRI characteristics of abnormalities of the perihepatic space and highlight and illustrate the value of MRI over CT in this setting.

Tumoral involvement of the perihepatic space may occur as an extrahepatic extension of a malignant liver lesion, but also as dissemination from a tumor located elsewhere via the lymphatic route or from being spread to the peritoneal space (e.g., from the undersurface of the diaphragm or Morison's pouch). CT and MRI features of perihepatic carcinomatosis include thickening, nodules, or masses in the peritoneum around the liver. Moreover, peritoneal enhancement after contrast medium intravenous administration may be abnormal in perihepatic peritoneal carcinomatosis. This enhancement is optimally detected five minutes after contrast medium injection. The subphrenic space is commonly involved, particularly on the right side, because of the preferential flow of peritoneal fluid into this space from the right paracolic gutter. Disease in this space is best depicted on contrast-enhanced reformatted coronal and sagittal MRI. MRI is very sensitive to small volumes of peritoneal carcinomatosis, showing thin peripheral lines of enhancement adjacent to the liver. MRI may improve the detection of carcinomatosis, thus facilitating the diagnosis of this disease condition and help in the evaluation of the peritoneal carcinomatosis index ( 20 21 ). The advantages of MRI are related to its superior contrast resolution and diffusion-weighted MRI, which allows detection and characterization of carcinomatosis nodules, particularly in the round ligament fossa and the hepatic hilum ( Figs. 5 , 6 ) ( 22 23 24 ). Pseudomyxoma peritonei (PMP) is characterized by the presence of a large amount of mucin in the abdomen due to neoplastic mucin-secreting cells, typically from an appendiceal primary tumor. MRI features include signs like those seen in peritoneal carcinomatosis. However, the high signal on T2-weighted MRI, the extent to which scalloping is present, the loculation of the peritoneal effusions, the predominance of lesions in the perihepatic space, and involvement of the greater omentum. At the same time, the gastrointestinal tract is rarely involved, signs highly suggestive of PMP ( 20 25 ). The assessment of perihepatic involvement, especially that of the hepatic pedicle, lesser omentum, and hepatoduodenal ligament infiltration, is crucial, as these sites are associated with incomplete cytoreductive surgery ( 25 ). MRI, due to its superior contrast resolution, both with T2, diffusion, and gadolinium-enhanced T1-weighted sequences, allows improved detection and characterization of the perihepatic space, particularly when involvement is subtle or doubtful ( Figs. 7 , 8 ). Diffuse peritoneal leiomyomatosis findings include peritoneal nodules with histologic features similar to those of uterine leiomyomas ( 26 ). Malignant transformation is rare. MRI may have added value compared to CT for the characterization of homogeneous well-delineated soft-tissue perihepatic nodules, showing small well-delineated regular peritoneal nodules displaying low signal intensity on T2-weighted images and intermediate signal intensity on T1-weighted images. The nodules are homogeneously enhanced after intravenous administration of gadolinium chelates. Peritoneal fibromas are even rarer ( Fig. 9 ).

The intestines, mainly the colon, may interpose temporarily or permanently between the liver and the diaphragm, which is known as Chilaiditi syndrome ( 5 ). Usually, it is an asymptomatic and incidental imaging finding. The gallbladder may very rarely be found wandering in a perihepatic position, even in the absence of acute volvulus in elderly persons. Varices may also be found around the liver as a consequence of portal hypertension. Fat may be found, although rarely, medially and adjacent to the lumen of the inferior vena cava, near the hepatic confluence. Lastly, the omentum may be used as packing material in hepatobiliary surgery, which then appears as a fatty mass in the perihepatic space ( 6 ). Perihepatic fluid collection may result from accumulation of ascites, blood, bile, chyle, pancreatic necrosis, or urine. MRI, due to its high-contrast resolution, may allow a better depiction of hemorrhagic content than CT and may thus provide a more precise definition of the location of a lesion. Perihepatic fluids are hypointense on T1-weighted images, even during the hepatobiliary phase. Conversely, bile leaking into the perihepatic fluid will appear as a high signal intensity on late enhanced T1-weighted sequences after intravenous administration of specific hepatobiliary contrast agents ( Fig. 2 ) ( 7 ). However, it has been shown that peritoneal fluids may display a signal intensity that increases progressively over time, even in the absence of any biliary leakage on T1-weighted gradient-echo sequences after injection of gadobenate dimeglumine (Gd-BOPTA) ( 8 ). CT is the most frequently used imaging technique for assessment and follow-up of acute pancreatitis and collections. MRI is an appropriate alternative for the characterization of fluid collections, particularly solid debris and fat necrosis ( 9 ). Pseudocysts and acute necrotic collections are usually peripancreatic, but they may occasionally be located in the perihepatic space ( 10 11 ). The clinical presentation and treatment of the different disease conditions that may involve the perihepatic space are listed in Table 1 .

The liver is surrounded by the Glisson capsule, an extrusion of the visceral peritoneum, except for the bare area, which is attached to the diaphragm. The suspensory ligaments of the liver include the coronary ligaments, the triangular ligaments, and the falciform ligament. The falciform ligament, composed of a double fold of peritoneum ( 1 ) and containing the obliterated umbilical vein, connects the anterior abdominal wall and the diaphragm to the liver. This ligament separates segments 2 and 3 from segment 4 ( Fig. 1A ). The falciform ligament forms a partial barrier between the right and left subphrenic space yet allows the transfer of fluid from one side to the other. The inferior part of the falciform ligament is elongated by the Teres ligament. The coronary ligament, contiguous with the falciform ligament and composed of left and right ligaments, is the largest attachment of the liver to the diaphragm. The triangular ligaments are formed by fusion of inferior and superior reflections of the coronary ligaments. The left triangular ligament is short and does not compartmentalize the left subphrenic space, unlike the right triangular ligament, which is long and separates the right subphrenic space from the right subhepatic space ( 2 ). The lesser omentum is divided into two parts: the gastrohepatic and the hepatoduodenal ligaments. The gastrohepatic ligament connects the lesser curve of the stomach to the liver and contains the coronary vein and left gastric artery. The hepatoduodenal ligament connects the duodenum to the liver and hosts the portal vein, hepatic artery, common hepatic duct, and part of the cystic duct. The subhepatic space is divided into an anterior and a posterior space. The anterior subhepatic space is located posteriorly to the portal vein and freely communicates with the lesser sac via the Winslow foramen ( 3 ). The posterior subhepatic space is known as the Morison's pouch and is contiguous with the anterior right Gerota fascia ( 4 ). The perihepatic space includes the right subphrenic space, the subhepatic space, the lesser sac, and the left perihepatic space. Peritoneal disease extends to the perihepatic space in a clockwise direction through the right paracolic gutter to the Morrison's pouch and the right subphrenic space. Right subphrenic pathology can spread to the left subphrenic space and anterior wall. Hepatobiliary disease can spread to the perihepatic space and peritoneum through the falciform ligament. The hepatoduodenal ligament constitutes a route for the spread of pancreatic disease to the porta hepatis and liver ( Fig. 1B ). The anatomy, as described above, is presented in an animated picture ( Supplementary Video 1 ).

Assessing the perihepatic origin of a lesion versus its intrahepatic origin presents a major challenge, particularly when the lesion is large. It may be straightforward when the tumor is completely surrounded by liver parenchyma, indicating that it is intrahepatic, when the liver parenchyma is compressed and displaced, and when there is a fat layer between the tumor and the liver parenchyma indicating its extrahepatic origin. In other situations, other signs may be helpful such as identifying an arterial supply to a pedunculated tumor originating from the hepatic arteries, which suggests an intrahepatic location of the tumor. Identifying the tumor center may also suggest that the tumor is probably extrahepatic when the center is outside the liver. Some signs may help differentiate between right hepatic and right retroperitoneal lesions. Large tumors, such as those found in the inferior vena cava or the right portal bifurcation, may displace the vessels. A large tumor arising from the right liver can increase the distance between the right anterior and the right posterior portal branches, while large extrahepatic tumors displace vessels differently. For example, a large adrenocortical carcinoma will displace the inferior vena cava and the portal branches anteriorly and clockwise. A summary is displayed in an animated picture ( Supplementary Video 2 ).

Depending on peritoneal anatomy and pressure gradients, abdominal infections are more likely to extend to the right side than to the left, and the perihepatic space, mainly the retrohepatic space, is regularly involved. Small foreign bodies, such as stercoliths left behind after an appendectomy, or dropped gallstones after a cholecystectomy, may get trapped in the perihepatic space, with subsequent formation of an abscess ( 12 ). The latter are generally small and discovered up to several years after the operation. They are increasingly being found owing to the development of laparoscopic procedures and may result in iterative febrile flareups whose origins are often underdiagnosed ( 13 14 ). Although CT is often sufficient for the detection of stercoliths, it may not always show a dropped gallstone with pure cholesterol content ( Fig. 3 ). Unlike CT, MRI can detect all types of stones, even those that are small or non-calcified. Stones appear as hyperintense foci on T1-weighted images or as small hypointense abnormalities on both T1- and T2-weighted sequences. Echinococcosis is a parasitic infection caused by the larva of the tapeworm Echinococcus. The two main forms include cystic hydatid disease ( Echinococcus granulosus ) and the less frequent alveolar hydatid disease ( Echinococcus multilocularis ). In both these forms, a cyst may rupture in the perihepatic space ( 15 16 17 ). MRI is the best imaging technique for characterizing these lesions and defining their extension, both intra and extrahepatically, particularly to the subdiaphragmatic area and hepatic hilum. It best shows the multivesicular cystic structure of a lesion, depicted as areas of high T2 signal intensity ( Fig. 4 ) ( 18 ). In both forms of echinococcosis, diagnosis is confirmed by specific serum antibodies detected in blood and confirmed by immunoassay. Abdominal tuberculosis, although very rare, is increasingly encountered, even in developed countries. Hepatic and peritoneal involvement is usually seen with active thoracic tuberculous infection. However, the occurrence of isolated perihepatic tuberculosis with small abscesses in the perihepatic space has been described, although the exact mechanism remains unclear ( 19 ).

The perihepatic space is frequently involved by a whole spectrum of diseases. The first objective of the radiological analysis is to confirm the perihepatic origin of the lesion. The identification of the nature of the lesion then relies on both CT and MRI features and clinical presentation. Detection of the extent of the disease and identification of its nature is optimally performed with MRI, particularly for infectious entities such as stone-related perihepatic abscesses, echinococcosis, perihepatic carcinomatosis, PMP, and perihepatic endometriosis. Radiologists should thus be familiar with abnormal MRI features of the perihepatic space and be aware of the potential role and added value of this imaging technique in the evaluation of the perihepatic space.

Most splenic implantations into the peritoneal cavity are found after a trauma to the spleen that has required a splenectomy, potentially leaving behind some fragments of the spleen. Splenosis can be spread by a capsular or intrahepatic extension ( Fig. 10 ). MRI patterns of a single well-defined mass, which is similar to that of healthy spleen parenchyma on all sequences, along with a relevant history, should allow the diagnosis ( 27 ). Fitz-Hugh-Curtis syndrome is frequently caused by Neisseria gonorrhoeae or Chlamydia trachomatis infections and have been reported as occurring in up to 59% of patients with pelvic inflammatory disease. It presents as a hepatic capsular and subcapsular enhancement after contrast medium intravenous administration, predominantly seen along the right antero-inferior hepatic surface on post-contrast arterial-phase CT or MRI ( Fig. 11 ) ( 28 29 ) due to inflammation of the hepatic capsule and edema. The diagnosis can be confirmed by laparoscopy, which allows visualization of the classic adhesions resembling violin strings and isolating the infectious agent responsible for the pelvic disease. Endometriosis may involve the diaphragm in approximately 1.5% of cases, and is symptomatic in nearly half of the cases ( 30 ). Pelvic endometriosis is almost always present. The hypothesized mechanism is that of retrograde menstruation of endometrial cells through the fallopian tubes with a clockwise peritoneal circulation through the right paracolic gutter towards the ipsilateral subdiaphragmatic area due to negative subdiaphragmatic pressure. Abdominal and liver MRI, including coronal fatsuppressed T1-weighted sequences, is the best imaging technique for diagnosing diaphragmatic endometriosis ( 31 ). Rousset et al. ( 30 ), in a series of 23 women with confirmed diaphragmatic endometriosis, showed a sensitivity of MRI of up to 83% for the detection of abnormalities in the perihepatic space. Lesions were mostly posterior nodules, although plaques and micronodular clustered lesions could also be found. The strength of the perihepatic endometriosis signal depends on the age of the lesions. Implants are typically hyperintense on T1-weighted and hypointense on T2-weighted MRI sequences ( Figs. 12 , 13 ) ( 32 ). Intraperitoneal focal fat infarctions include processes ranging from torsion of an epiploic appendage to infarction of the greater omentum. They may thus be found in the perihepatic space, mainly as a result of torsion of an epiploic appendage or omental infarction ( 33 ). Acute abdominal pain is the most common symptom. Differentiation between omental infarction and intraperitoneal focal fat infarction relies on the value of maximal diameter, the presence of a peripheral rim-like region, and the central dot sign. Of note, the post-infarction appendage can detach and wander around in the peritoneal cavity, covered by a fibrous capsule. It may even become lodged between the diaphragm and the superior surface of the liver ( 34 ), often on Glisson's capsule. MRI optimally depicts the fat content of these well-circumscribed small lesions and may show signal loss on opposed phased gradient-echo MRI ( Fig. 14 ).