Imaging Features of Main Hepatic Resections: The Radiologist Challenging

Liver resection is still the most effective treatment of primary liver malignancies, including hepatocellular carcinoma (HCC) and cholangiocarcinoma (CCA), and of metastatic disease, such as colorectal liver metastases. The type of liver resection (anatomic versus non anatomic resection) depends on different features, mainly on the type of malignancy (primary liver neoplasm versus metastatic lesion), size of tumor, its relation with blood and biliary vessels, and the volume of future liver remnant (FLT). Imaging plays a critical role in postoperative assessment, offering the possibility to recognize normal postoperative findings and potential complications. Ultrasonography (US) is the first-line diagnostic tool to use in post-surgical phase. However, computed tomography (CT), due to its comprehensive assessment, allows for a more accurate evaluation and more normal findings than the possible postoperative complications. Magnetic resonance imaging (MRI) with cholangiopancreatography (MRCP) and/or hepatospecific contrast agents remains the best tool for bile duct injuries diagnosis and for ischemic cholangitis evaluation. Consequently, radiologists should be familiar with the surgical approaches for a better comprehension of normal postoperative findings and of postoperative complications.

In the field of liver resection, according to the Brisbane 2000 terminology, liver resections could be classified as anatomic and not anatomic resection [10]. The type of liver resection (anatomic versus non anatomic resection) depends on different features, mainly on the type of malignancy (primary liver neoplasm versus metastatic lesion), size of tumor, its relation with blood and biliary vessels, and the volume of future liver remnants (FLT) [10]. Knowledge of the liver resection main type is necessary for the radiologist to recognize the radiological common features of post-operative findings, and to identify the possible postoperative complications.
Ultrasonography (US) is the first-line diagnostic tool to use in post-surgical phase. However, computed tomography (CT), due to its comprehensive assessment, allows a more accurate evaluation and more normal findings than the possible postoperative complications. Magnetic resonance imaging (MRI) with cholangiopancreatography (MRCP) and/or hepatospecific contrast agents remains the best tool for bile duct injuries diagnosis and for ischemic cholangitis evaluation [6].
The purpose of this narrative review is to report the main liver resection, focusing on the definition of anatomic versus non anatomic resection, and on the main regular postoperative radiological features.

Type of Resection
Hepatectomies can be classified as anatomic and non anatomic resections.

Anatomic Liver Resection
Anatomic liver resection is defined as the complete removal of the liver parenchyma confined within the responsible portal territory. The portal ramifications define anatomical portions of the liver. In particular, the first order division of portal ramification defines the "hemi-liver", the second order division defines the "section", while the third order division defines the segment.
The term anatomic segmentectomy is utilized to describe the surgical approach that determine the elimination of a portion of liver parenchymal which correspond to a Couinaud segment. Otherwise, with "subsegmentectomy", we identify a surgical approach to determine the partial removal of liver tissue within the portal territories of less than a Couinaud's segment [11].
Anatomic sectionectomy corresponds to the comprehensive elimination of tissues of the second order portal venous branches. these approaches are classified considering the eliminated section. For example, the right anterior is the elimination of the right anterior, including segments 5 and 8, while the right posterior is the elimination of the right posterior, including segments 6 and 7.
The surgical procedure that causes the elimination of the liver to the right of the middle hepatic vein is defined as right hepatectomy. This resection includes segments 5, 6, 7, and 8. When in addition to right hepatectomy, segment 4 is resected, we obtained an extended right hepatectomy, also named right trisectionectomy.
With regard to the elimination of the liver parenchyma to the left of the middle hepatic vein, this approach is the left hepatectomy and includes the segments 2, 3, and 4. For extended left hepatectomy, also named as left trisectionectomy, the additional removal of segments 5 and 8 is intended.

Non Anatomic Liver Resection
The surgical procedure known as parenchyma-sparing hepatectomy (PSH) is a limited non anatomical liver resection (Figures 3 and 4). In contradiction of anatomic resections, which involve systematic anatomical hepatic resection, this strategy allows to spare a certain future remnant liver volume and minimize surgical stress and operative risks [12][13][14][15].

Non Anatomic Liver Resection
The surgical procedure known as parenchyma-sparing hepatectomy (PSH) is a limited non anatomical liver resection (Figures 3 and 4). In contradiction of anatomic resections, which involve systematic anatomical hepatic resection, this strategy allows to spare a certain future remnant liver volume and minimize surgical stress and operative risks [12][13][14][15].   The PSH procedure should allow an R0 resection (corresponds to resection for cure or complete remission) with negative surgical margins. Compared to the anatomical resection (AR) approach, it is more technically challenging, since anatomic landmarks, as lobar or sectorial vessels, are not used as a guide to identify the resection margins. There- The PSH procedure should allow an R0 resection (corresponds to resection for cure or complete remission) with negative surgical margins. Compared to the anatomical resection (AR) approach, it is more technically challenging, since anatomic landmarks, as lobar or sectorial vessels, are not used as a guide to identify the resection margins. Therefore, intraoperative ultrasound plays a key role during PSH, allowing the identification of lesions, the relationship of the lesion with the vital structures (e.g., hepatic veins, portal structures), and the parenchymal transection plan [16].
Although the cut off to obtain negative margins has usually been 1 cm, the introduction of new chemotherapeutic agents has allowed the reduction of this margin at 1 mm, in colorectal metastases (CLM), with good oncological results [17]. Moreover, it has been demonstrated that these new treatments are responsible for similar overall survival (OS) among R0 patients and patients with microscopic positive margins (R1) [18,19]. Hence, surgical resection should also be performed in R1 subgroup patients [18,19].
In addition, according to the new surgical oncology group suggestions, in the absence of extrahepatic disease, the only limits to surgical treatment of CLM patients is correlated to the post procedural liver parenchymal that should be sufficient to prevent liver failure (PLF) [20].
Thanks to the use of the intraoperative US, it is possible to detach lesions from major vessels and to perform accurate flow analysis, preserving communicating vessels among main hepatic veins that should assure an adequate outflow to the liver even after main hepatic vein resection [21][22][23][24]. The use of this new procedural technique opened the opportunity to achieve new liver resection sub-types, which could substitute conventional hepatectomies ( Figure 5), considering the patient characteristics, to obtain a more personalized treatment [24-30].

Two Stage Hepatectomy and ALLPS
Two stage hepatectomy and associating liver partition with portal vein ligation for staged hepatectomy (ALPPS) are two strategies of treatment for liver disease in patients with insufficient liver function [32].
With regard to two stage hepatectomy, this approach includes two phases: In the first, to obtain hypertrophy of future liver remnant (FLR), the surgeons and/or radiologists perform a surgical ligation or radiological embolization of the portal vein, so that, the redistribution of portal flow induces parenchymal hypertrophy. In the second phase, the surgical approach is performed to remove target lesions.
The ALPPS includes parenchymal splitting and portal vein ligation in the first stage [33]. Complete redistribution of portal blood flow causes FLR hypertrophy. Although this approach increases the patient number that can be subjected to liver resection, it is correlated with significant operative morbidity and mortality [34].

Treatment and Imaging Assessment
Imaging, with regard to hepatic resection, should be employed in different phases: staging, treatment planning, intra-treatment evaluation, and treatment response assessment, which includes technical success, treatment efficacy, and complications .
With regard to "technical success", this is due to the ability of treating the lesion according to the procedure [61], while "technique efficacy", that should be distinguished from "technical success", is the "complete resection", also named R0, of a macroscopic lesion [61]. Complications, defined as any unpredicted deviation from a procedural course, and/or adverse events, recognized as any possible damage correlated to the procedure, should be evaluated according to standardized classification, as the Common Terminology Criteria for Adverse Events and the Clavien-Dindo classification [62]. In addition, any adverse events should be classified considering the severity and the time of occurrence (e.g., during, in post-procedural phase, or late) [61][62][63][64].
Ultrasound assessment, also with the employment of contrast medium (CEUS), is a relatively new tool, utilized for problem solving during treatment phases and surveillance [122][123][124][125][126][127][128][129][130][131][132], although the critical point of interest is due to the possibility of real time procedure efficacy assessment. In fact, CEUS allows to detect perfusion change during the procedure, and bearing in mind the higher temporal resolution and the possibility of repeating this diagnostic exam several times in a short period, it is a secure and cost-effective tool for treatment outcome assessment [130][131][132].
Usually, US is the first tool employed during the post-surgical phase to assess abdominal complications and to evaluate treatment efficacy. CT with contrast agents, normally, is utilized as a follow-up tool to evaluate efficacy and recurrence, while it is the first tool employed in emergency setting (e.g., major complications as posthepatectomy hemorrhage (PHH)) [35-37]. MRI with cholangiopancreatography sequences (MRCP) or with hepatospecific contrast agent (EOB-MRI) is the best modality for diagnosis of early postoperative bile duct injuries and ischemic cholangitis, while during follow-up this tool is a problem solver for indeterminate liver lesions, e.g., new lesions versus abscesses [35-37].

Post-Surgical Imaging Findings
The post-surgical radiological assessment should be distinguished early, during the first hours after surgery, with a follow-up at the time of discharge and an oncological followup taking into account the main guidelines in relation to the type of cancer treated [133][134][135].
Normally, a diagnostic assessment, during the first hours after surgical procedure is only required in case suspected complications, such as a bleeding or biliary lesion [136][137][138][139], while at the time of discharge US assessment is required. CT or MRI should be performed to confirm complications.
At US assessment, free fluid may present a hypoechoic collection in the posterior recesses or, in the presence of blood, inhomogeneously iso-hypoechoic or hyperechoic [140][141][142][143][144][145][146][147]. In this case, a clinical laboratory evaluation is mandatory, considering the proposal of the International Study Group of Liver Surgery (ISGLS) [148], in which we found a novel definition and staging of PHH. According to these guidelines, PHH is defined as a drop in haemoglobin level >3 g/dL compared to the post-operative baseline level (i.e., haemoglobin level immediately after surgery), with three grades of severity (A-B-C), depending on the therapeutic strategy required [148].
Biloma is an encapsulated collection of bile outside the biliary tree [35]. At US assessment, it may appear as simple fluid collections [35]. If a biloma is supplied, we have a bile leaks. A definition for bile leak was standardized by the ISGLS [165]. The leakage may be due to an incompetent bile-digestive anastomosis or a bile ducts damage during the surgical procedure [166][167][168][169][170][171]. At US or CT examination, bile leaks may appear as a non-spe- At US assessment, surgical margins may appear hyperechoic compared to surrounding liver parenchymal. In addition, the radiologist should evaluate the presence of post-surgical fluid collections. These entities may be due to the presence of haematomas (50%), bilomas (25%) and abscesses (25%) [35].
At US assessment, surgical margins may appear hyperechoic compared to surrounding liver parenchymal. In addition, the radiologist should evaluate the presence of postsurgical fluid collections. These entities may be due to the presence of haematomas (50%), bilomas (25%) and abscesses (25%) [35].
Biloma is an encapsulated collection of bile outside the biliary tree [35]. At US assessment, it may appear as simple fluid collections [35]. If a biloma is supplied, we have a bile leaks. A definition for bile leak was standardized by the ISGLS [165]. The leakage may be due to an incompetent bile-digestive anastomosis or a bile ducts damage during the surgical procedure [166][167][168][169][170][171]. At US or CT examination, bile leaks may appear as a non-specific collection near the resection margins [165]. MRI with gadolinium-based hepatobiliary contrast agent (EOB-MRI) allows for proper site detection so as to classify the leakage sub-type (Figure 7) [161][162][163][164][165][166][167][168][169][170][171][172][173][174][175][176][177]. On EOB-phase, bile leak is detected as an active overflow of contrast agent outside the biliary tree and inside the fluid collection [35].  Air artefacts within a supra-fluid collection that do not show central perfusion at color Doppler assessment in patients with high grade fever is suggestive of an abscess [35]. CT confirms the diagnosis showing the typical features of a double target appearance, characterized by a central hypodense core of fluid surrounded by a hyperdense rim and a hypodense outer ring [35]. The use of haemostatic glues on the resective margins could mimic an abscess due to the presence of hypodense microbubbles [78]. An accurate clinical evaluation (absence of fever and inflammation indices) allows a correct diagnosis [78].
The radiological appearance of remnant liver parenchymal is complex and is correlated to the type of surgical procedure, the segment resected (ore more segment), the quality of residual parenchymal (cirrhotic or chemotherapy-induced steatohepatitis) [178]. A nontypical finding is the hepatitis due to treatment, that can be hepatocellular, cholestatic, or mixed [140,178]. During imaging assessment, it is possible to find hepatomegaly, perihepatic fluid, lymphadenopathy, and periportal edema [140]. The main feature is the gallbladder wall thickening or gallbladder fossa edema. On US assessment, typical findings are a parenchymal echogenicity decreasing with an increase of the portal vein conspicuity (known as "starry sky") [178]. On CT or MRI evaluation, it appears as liver attenuation decreasing or diffuse hyperintensity in T2-weigthed (T2-W) sequences [140,178]. During contrast medium evaluation, a heterogeneous parenchymal enhancement, due to perfusion re-assessment, could be detected. Severe cholestatic hepatitis on MRCP appears as a decreasing of the tertiary bile ducts number [178].
Clinically, vein thrombosis may be asymptomatic or may cause abdominal pain if the superior mesenteric vessels are involved due to bowel congestion or ischemia [158,190,191]. When not detected, collateral vessels will grow, and the patient will develop portal vein cavernous transformation [192]. Otherwise, arterial thrombosis may cause liver failure, sepsis, or abscess [160].
On US assessment, a limited thrombus is seen as an echogenic area within vessel, in the absence or with a slow portal flow on Doppler images. In addition, on color Doppler US, vein thrombosis is characterized by the loss of a triphasic waveforms pattern with a decrease in hepatic vein velocity and in portal flow [35,193]. On CT contrast study evaluation, arterial or portal thrombosis appears as an intraluminal filling defect of the hepatic artery or portal vein, during arterial and porta phase, respectively. Venous thrombosis could be intercepted on unenhanced CT as intraluminal hyperattenuating spots within the vessel [35]. In addition, during arterial phase and correlated to the compensatory augmentation of local arterial flow, it is possible to find a segmental enhancement (transient arterial hyperenhancement-THAD) of the tributary liver parenchyma [35].

Follow-Up Assessment
During the follow-ups scheduled in relation to the patient's cancer history, the findings described at discharge change [140].
With regard to remnant liver parenchyma, hepatitis is replaced by hepatic regeneration, so radiologist should know the type of surgical procedure to correctly localize new lesions [140]. Otherwise, the correct localization is possible with the identification of the main arterial and venous branches, and so as a biliary tree [140].  This tissue should be correctly distinguished from new lesions, expressions of disease recurrence [140,[194][195][196][197][198][199][200][201][202][203]. On US assessment, scar tissue is iso-hyperecoic without contrast

Two Stage Hepatectomy and ALLPS Assessment
With regard to two stage hepatectomy and ALLPS radiological evaluation, these procedures cause a selective portal vein occlusion to obtain a hypertrophy of future liver remnant [32][33][34]. So, in this context, the radiologist should evaluate vein thrombosis and the liver parenchymal compared to pre-treatment diagnostic study. However, the assessment of hepatic regeneration is a volumetric evaluation, and this is not correlated to the real parenchymal functionality [220][221][222].

Conclusions
The knowledge of the main type of liver resection is necessary for the radiologist to recognize the radiological common features of post-operative findings and identify the possible postoperative complications.
US is the first-line imaging examination during the postoperative monitoring. However, CT is of greater value for identifying normal findings after surgery, and the possible postoperative complications. MRI is the best modality for the diagnosis of early postoperative bile duct injuries and to assess recurrence.