DOI: 10.1148/rg.264055120
RadioGraphics 2006;26:1067-1084
© RSNA, 2006
Intraoperative US of the Liver: Techniques and Clinical Applications1
Jonathan B. Kruskal, MD, PhD and
Robert A. Kane, MD, FACR
1 From the Abdominal Imaging Section, Department of Radiology, Clinical Center 302B, Beth Israel Deaconess Medical Center, 1 Deaconess Rd, Boston MA 02215. Presented as an education exhibit at the 2004 RSNA Annual Meeting. Received May 13, 2005; revision requested June 20; revision received and accepted August 9. Authors have no financial relationships to disclose.
Address correspondence to J.B.K. (e-mail: jkruskal{at}bidmc.harvard.edu).
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Abstract
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Intraoperative ultrasonography (US) of the liver provides the operating surgeon with useful real-time diagnostic and staging information that may result in an alteration in the planned surgical approach. Current applications for intraoperative US of the liver include tumor staging, metastatic survey, guidance for metastasectomy and various tumor ablation procedures, documentation of vessel patency, evaluation of intrahepatic biliary disease, and guidance for whole-organ or split-liver transplantation. To obtain the most useful information with intraoperative US, the sonographer should use a dedicated transducer and a scanning method appropriate for the purpose of the examination. In addition, the radiologist must be familiar with the relevant intraoperative and vascular anatomy and the spectrum of normal and abnormal findings and should be alert to the pitfalls that frequently occur in the interpretation of intraoperative US images of the liver.
© RSNA, 2006
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Introduction
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Intraoperative ultrasonography (US) of the liver is used with increasing frequency as an aid for surgical planning during hepatic segmental or lobar resection, metastasectomy, and adult living-related right-lobe liver transplantation. Intraoperative US provides vital information to the surgeon during the procedure, information that may affect surgical decision making (1,2). To an inexperienced operator, performing US during an open surgical procedure might seem daunting at first. However, a basic knowledge of the technical and transducer requirements, as well as of methods for scanning the liver and interpreting real-time US images, allows the radiologist to provide useful information to the operating surgeon during the procedure. The purpose of this review is to describe the basic technical requirements for performing intraoperative US of the liver and to illustrate the available equipment and transducer options and the various scanning techniques that may be used. The relevant intraoperative anatomy and the spectrum of normal and abnormal findings are described, along with the US features and artifacts that are frequently observed in the intraoperative setting. Finally, various applications for intraoperative US of the liver are described, including tumor staging, metastatic survey, guidance for metastasectomy and tumor ablation, documentation of vessel patency, evaluation of intrahepatic biliary disease, and guidance for whole-organ or split-liver transplantation. Examples of US findings are provided for each application.
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Equipment
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Transducer Requirements
Dedicated intraoperative transducers should be used for intraoperative US of the liver. Typically, 5-MHz side-fire T-shaped linear- or curvilinear-array transducers are used. For liver imaging, the transducer should fit comfortably against the palm of the hand and between the fingers (Fig 1) to allow imaging of both the high dome and the right lateral segments of the liver. End-fire transducers may be used, but their role is limited, since they cannot be inserted easily into the right sub-phrenic space. Transducers should have color Doppler flow and pulsed Doppler imaging capabilities and should provide good near-field resolution.
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Figure 1. Photograph shows the position in which the specially designed intraoperative transducer should be held, cradled between the fingers and resting against the palm of the hand. In this way, not only can easily exposed segments of the liver be imaged but the transducer also can access more challenging locations such as the high dome and the right lateral margin.
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Transducer Sterilization
Four options are available for rendering the transducer sterile. Sterile condom sheaths are most commonly used and are essential for laparoscopic US. Specially designed sheaths are available for dedicated intraoperative transducers. The sheath must be long (typically about 1.5 m) so that the entire length of the electrical supply cord is covered, and it should fit snugly around the transducer to avoid artifacts. Care should be taken when placing the sheathed transducer near surgical retractors, which may cause a loose-fitting sheath to tear.
Ethylene oxide gas sterilization with high-temperature aeration also may be used to sterilize both the probe and the supply cord. The turnaround is 16–24 hours, which is slow, and several vendors claim that this method of sterilization may damage the skin of the transducer tip.
Low-temperature hydrogen peroxide gas plasma sterilization techniques (Sterrad; Advanced Sterilization Products, Irvine, Calif) were introduced more recently. These systems allow the completion of an entire sterilization cycle in 2–3 hours, are safe to use with heat-sensitive equipment, and enable the use of a sterile transducer without a condom sheath.
The use of a glutaraldehyde or dialdehyde solution requires that the transducer be immersed for 4 hours. However, because of the inflammatory reaction that such agents induce at visceral contact, most surgeons and institutions prefer that they no longer be used.
Transducer Use in the Operating Room
In our experience, it is most helpful when the scrub nurse passes the sterile gel and sheath to the radiologist, who then allows the sonographer to carefully place the transducer into the gel-filled sheath and pull the sheath over the length of the cord. It is important to ensure that the covered cord is kept off the ground and away from all equipment, a task facilitated by clamping the cord to the edge of the operating field. Care should always be taken to avoid sharp objects that may tear the sheath, such as surgical retractors or forceps.
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Administration of Intraoperative US
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To minimize the time that a radiologist spends outside the radiology department, whenever possible, we insist that all intraoperative studies be booked ahead of time so that personnel (physicians and sonographers) and equipment are readied and all necessary probe covers and transducers are available for use. For all scheduled intraoperative studies, we have committed to being present in the operating room, scrubbed and ready to perform US, within 15 minutes of receiving the call from the operating room. From experience, this has optimized time utilization and minimized waiting time in the operating room.
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Technique for US of the Liver
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Typically, no coupling gel is required in the intraoperative setting, since the natural surface moisture of the liver is more than adequate for acoustic coupling.
The radiologist must observe sterile technique; wear standard surgical apparel, including a gown, mask, and cap; and scrub according to local institutional policies (typically, for a minimum of 2 minutes). The US examination is an integral component of the surgical procedure, and the radiologist performing the examination is a full member of the operating team. The radiologist should ensure that there is adequate space for scanning, typically to the patient’s right side; should ask that the lights be dimmed; and should ensure that the monitor on which images are displayed is positioned nearby and easily visible. It is always helpful to review all cross-sectional imaging studies before performing intraoperative US and to understand the reasons for the intraoperative study and the specific requirements of the surgeon. Since the time to perform US varies with operator experience, it is important to establish at the outset whether the study is a general search for metastases or simply an attempt to localize an impalpable lesion situated deep within the liver.
The radiologist must be familiar with the hepatic segmental anatomy (Fig 2a). To image the liver, sequential overlapping sagittal strokes should be performed with the transducer held in a transverse position, starting at the most lateral margin of the left lateral segment II and extending toward the right side (Fig 2b). In this way, the entire liver can be scanned. However, the extent of liver scanning depends on the indication for the imaging study and on the extent of hepatic mobilization and incision of ligaments. Lesions in the very near field may be difficult to image; bathing the field with sterile saline may help (Fig 3), or imaging may be performed from the opposite surface of the liver. The focal zone must be appropriately positioned; both near and far zones must be visible when segments IV, V, and VIII are imaged. In our experience, the most challenging portions to image are the posterior portion of the high dome and the blind areas of the liver. At times, it might be necessary to scan from the inferior surface of the liver; the sonographer then should be reminded to reverse or invert the images as the probe is inverted.
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Figure 2a. Intraoperative anatomy and scanning technique. (a) Diagram shows the Couinaud classification system for liver segmentation. This is the system most commonly used by hepatic surgeons and other physicians to describe the hepatic anatomy. (b) Photograph and superimposed white line show a useful method for scanning of the entire liver during an intraoperative US survey for metastases, with multiple overlapping sagittal sweeps performed while the transducer is held in a transverse position.
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Figure 2b. Intraoperative anatomy and scanning technique. (a) Diagram shows the Couinaud classification system for liver segmentation. This is the system most commonly used by hepatic surgeons and other physicians to describe the hepatic anatomy. (b) Photograph and superimposed white line show a useful method for scanning of the entire liver during an intraoperative US survey for metastases, with multiple overlapping sagittal sweeps performed while the transducer is held in a transverse position.
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Figure 3a. Water standoff used for better characterization of superficial lesions in the near field of the liver. (a) US image shows a small hypoechoic lesion (arrow) just below the liver capsule. (b) US image obtained after bathing the liver in saline solution for improved acoustic coupling demonstrates a small, superficial, simple cyst (arrow).
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Figure 3b. Water standoff used for better characterization of superficial lesions in the near field of the liver. (a) US image shows a small hypoechoic lesion (arrow) just below the liver capsule. (b) US image obtained after bathing the liver in saline solution for improved acoustic coupling demonstrates a small, superficial, simple cyst (arrow).
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Relevant Intraoperative Anatomy
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The radiologist should be familiar with the hepatic segmental anatomy as it is observed in the operating room. It is easiest to identify the hepatic veins cranially while the transducer is held in a transverse midline position and angled toward the beating heart. Only light pressure should be applied to the liver surface, since venous return via the retrohepatic vena cava is easily restricted in the intraoperative setting. Situated more inferiorly, the portal veins are used to determine the segmental anatomy. This is best achieved by placing the transducer on the undersurface of the liver, over segment IV, and angling the transducer toward the porta hepatis.
Specific arteries that are frequently relevant to the operating surgeon include a replaced right hepatic artery that arises from the superior mesentric artery and courses posterior to the portal vein (Fig 4), as well as a replaced or accessory left hepatic artery that arises from the left gastric artery and courses through the ligamentum venosum (Fig 5).
Absence or partial obliteration of the hyperechoic stripe that represents the ligamentum venosum may be indicative of an isoechoic lesion adjacent to the caudate lobe of the liver (Fig 6). Depending on the nature of the surgical procedure, the size and location of accessory hepatic veins also should be documented for the surgeon (Fig 7).
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Figure 4. Replaced right hepatic artery. Intraoperative color Doppler US image shows a replaced artery (arrow) that arises from the superior mesenteric artery (arrowhead) and courses between the portal vein (PV), which is anterior to it, and the more posteriorly located vena cava (IVC).
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Figure 5a. Replaced left hepatic artery. (a) Intraoperative gray-scale US image shows a replaced artery that courses through the ligamentum venosum (arrow), which is located anterior to the caudate lobe and vena cava (IVC). (b) Intraoperative color Doppler US image demonstrates the presence of flow through the replaced vessel, which arises from the left hepatic artery. (c) Intraoperative color Doppler US image shows not only the replaced artery (small arrow) that courses through the echogenic ligamentum venosum but also a potentially significant collateral vessel (large arrow) that connects the portal vein with the vena cava in the caudate lobe. The depiction of such vessels is important for the planning of any surgical resection in this anatomic region.
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Figure 5b. Replaced left hepatic artery. (a) Intraoperative gray-scale US image shows a replaced artery that courses through the ligamentum venosum (arrow), which is located anterior to the caudate lobe and vena cava (IVC). (b) Intraoperative color Doppler US image demonstrates the presence of flow through the replaced vessel, which arises from the left hepatic artery. (c) Intraoperative color Doppler US image shows not only the replaced artery (small arrow) that courses through the echogenic ligamentum venosum but also a potentially significant collateral vessel (large arrow) that connects the portal vein with the vena cava in the caudate lobe. The depiction of such vessels is important for the planning of any surgical resection in this anatomic region.
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Figure 5c. Replaced left hepatic artery. (a) Intraoperative gray-scale US image shows a replaced artery that courses through the ligamentum venosum (arrow), which is located anterior to the caudate lobe and vena cava (IVC). (b) Intraoperative color Doppler US image demonstrates the presence of flow through the replaced vessel, which arises from the left hepatic artery. (c) Intraoperative color Doppler US image shows not only the replaced artery (small arrow) that courses through the echogenic ligamentum venosum but also a potentially significant collateral vessel (large arrow) that connects the portal vein with the vena cava in the caudate lobe. The depiction of such vessels is important for the planning of any surgical resection in this anatomic region.
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Figure 6. Colorectal cancer metastases in the liver. Intraoperative US image of segments I and II of the liver shows an ill-defined infiltrative metastasis located primarily in the caudate lobe. The tumor has obliterated the normally echogenic ligamentum venosum (arrow).
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Figure 7. Colorectal cancer metastases in the liver. Intraoperative gray-scale US image shows an ill-defined colorectal cancer metastasis (large arrow) that has grown into and occludes the right hepatic vein (RHV), as well as a small superior accessory right hepatic vein (small arrows) that drains into the vena cava. The identification of the accessory vein was important for surgical planning of metastasectomy in this patient.
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Blind Areas of the Liver
Imaging of certain areas of the liver is particularly challenging in the intraoperative setting. These areas include the high dome of the lateral right lobe, access to which frequently requires dissection of the falciform and triangular ligaments. The posterior subdiaphragmatic bare area of the liver may be difficult to image, and surface lesions, typically hamartomas, are also difficult to identify, especially when the transducer provides poor near-field resolution or the depth of field or focal zone is not adequately altered. In these situations, the operator should consider using a water standoff (Fig 3) or scanning from the opposite surface of the liver.
Hepatic Pseudolesions
Foci of fatty infiltration that occur in cirrhosis or in patients undergoing chemotherapy may appear quite discrete in the intraoperative setting, when US image resolution is far better than at transcutaneous examination. The fat foci are typically soft and deformable by the US transducer, and vessels are frequently identified that course through their centers (Fig 8). Sparing typically occurs in the bare areas of the liver and in the region adjacent to the porta hepatis and may produce acoustic shadowing (Fig 9). Focal accumulations of fat also may be secondary to perfusion restrictions caused by lesions (Fig 10). Fat foci should not cause any bulging or protrusion of the liver capsule (Fig 11). When focal fat is identified, it is important to image the liver parenchyma adjacent to the region of fat, since other benign entities, such as angiomyolipomas, may have a similar appearance but may require surgical removal (Fig 12).
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Figure 8. Focal fatty replacement. Intraoperative US image demonstrates a well-circumscribed area of increased echogenicity at the bifurcation of the main portal vein (large arrows). Note the small vessel that courses through the center of the fatty region (small arrow). In the intraoperative setting, areas of focal fatty replacement are often compressible.
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Figure 9a. Focal fatty sparing. (a) Intraoperative US image depicts an ill-defined hypoechoic region (arrows) that abuts the right portal vein in a patient with diffuse fatty replacement of the liver. (b) Intraoperative US image demonstrates peripheral subcapsular hypoechoic regions (arrows) consistent with focal fatty sparing. Peripheral regions of fatty sparing or replacement should not produce any bulging in the liver contours.
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Figure 9b. Focal fatty sparing. (a) Intraoperative US image depicts an ill-defined hypoechoic region (arrows) that abuts the right portal vein in a patient with diffuse fatty replacement of the liver. (b) Intraoperative US image demonstrates peripheral subcapsular hypoechoic regions (arrows) consistent with focal fatty sparing. Peripheral regions of fatty sparing or replacement should not produce any bulging in the liver contours.
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Figure 10. Hepatocellular carcinoma and focal fatty sparing. Intraoperative image obtained during a US-guided metastasectomy demonstrates a hypoechoic hepatocellular carcinoma (arrow) adjacent to a peripheral region of focal fatty sparing (arrowhead). Note the adjacent echogenic region consistent with steatosis.
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Figure 11. Colorectal cancer metastasis in the liver. Intraoperative US image demonstrates a lobular, hypoechoic, solitary metastasis (small arrows) that produces bulging of the liver contours (large arrows).
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Figure 12. Angiomyolipoma. Intraoperative US image shows an isolated lesion in segment VI of the liver (arrows). The fat component is echogenic and easily visible, but other components of the lesion are less easily seen in the intraoperative setting.
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Surgery-specific US Features
At intraoperative US of the liver, certain features may appear that the radiologist should be aware of. The cut margin of a liver segment is often echogenic because of small amounts of gas that enter the parenchyma and sinusoids after cautery or sonication, techniques commonly used for segmental resection (Fig 13a, 13b). The cut margin of partially resected tumors also may appear echogenic because of gas bubbles in the tumor remnant (Fig 14). Imaging during cautery produces bandlike artifacts (Fig 15). Accumulations of air adjacent to the vena cava (Fig 16), in the gallbladder fossa (Fig 17), or in surgical packing material (Fig 18) may simulate intravenous air or produce acoustic shadowing. Palpation of the posterior surface of the liver, which is frequently used to maneuver the liver for better imaging, also may result in acoustic shadowing that simulates mucinous metastases (Fig 19). Cautery on the liver surface, which is often performed to mark subjacent lesions, produces acoustic shadowing that must be distinguished from that produced by superficial tumors (Fig 20).
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Figure 13a. Artifacts from sonication of the liver surface. (a) Intraoperative image demonstrates small echogenic bubbles (arrow) that entered the liver parenchyma at the cut surface during segmentectomy with high-frequency sonication. (b, c) Intraoperative images show intrahepatic gas bubbles in hepatic segments remote from the site of sonication (b) and gas bubbles localized to the perisinusoidal space around a tumor (arrow in c).
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Figure 13b. Artifacts from sonication of the liver surface. (a) Intraoperative image demonstrates small echogenic bubbles (arrow) that entered the liver parenchyma at the cut surface during segmentectomy with high-frequency sonication. (b, c) Intraoperative images show intrahepatic gas bubbles in hepatic segments remote from the site of sonication (b) and gas bubbles localized to the perisinusoidal space around a tumor (arrow in c).
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Figure 13c. Artifacts from sonication of the liver surface. (a) Intraoperative image demonstrates small echogenic bubbles (arrow) that entered the liver parenchyma at the cut surface during segmentectomy with high-frequency sonication. (b, c) Intraoperative images show intrahepatic gas bubbles in hepatic segments remote from the site of sonication (b) and gas bubbles localized to the perisinusoidal space around a tumor (arrow in c).
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Figure 14a. Focal nodular hyperplasia. (a) Intraoperative image demonstrates a large nodular lesion between the right (RHV) and middle hepatic veins (MHV). Note the homogeneous nature of this benign tumor, which effaces the vessels but has not occluded them. (b) Intraoperative image from repeat US of the liver after attempted resection of the mass shows the echogenic cut surface of the liver (arrows) and an adjacent isoechoic area of residual tumor between the right (RHV) and middle (MHV) hepatic veins.
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Figure 14b. Focal nodular hyperplasia. (a) Intraoperative image demonstrates a large nodular lesion between the right (RHV) and middle hepatic veins (MHV). Note the homogeneous nature of this benign tumor, which effaces the vessels but has not occluded them. (b) Intraoperative image from repeat US of the liver after attempted resection of the mass shows the echogenic cut surface of the liver (arrows) and an adjacent isoechoic area of residual tumor between the right (RHV) and middle (MHV) hepatic veins.
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Figure 15a. Cautery artifact. (a) Intraoperative image in a patient with hepatocellular carcinoma and a thrombus in the left portal vein (arrow) shows curvilinear echogenic bands in the far field, artifacts of cautery performed during image acquisition. (b) Intraoperative image in another patient with infiltrative hepatocellular carcinoma shows more linear bandlike echogenic artifacts that radiate from the transducer location.
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Figure 15b. Cautery artifact. (a) Intraoperative image in a patient with hepatocellular carcinoma and a thrombus in the left portal vein (arrow) shows curvilinear echogenic bands in the far field, artifacts of cautery performed during image acquisition. (b) Intraoperative image in another patient with infiltrative hepatocellular carcinoma shows more linear bandlike echogenic artifacts that radiate from the transducer location.
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Figure 17. Intraoperative image obtained immediately after cholecystectomy and prior to a hepatic lobar resection shows a linear echogenic band with posterior acoustic shadowing, an artifact caused by air in the gallbladder fossa.
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Figure 18. Intraoperative image shows acoustic shadowing that obscures structures adjacent to the liver. The artifact was caused by surgical packing material placed around the liver surface or in the surgical bed.
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Figure 19. Acoustic shadowing produced by palpation of the posterior liver surface. Intraoperative image of the right lobe of the liver demonstrates acoustic shadowing caused by two echogenic foci in the far field, artifacts that resemble colorectal cancer metastases.
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Figure 20a. Mucinous colorectal cancer metastases. (a) Intraoperative image demonstrates acoustic shadowing produced by a small, superficial colorectal cancer metastasis. Note the thin rim of normal liver tissue superficial to this metastasis. (b) Intraoperative image obtained during US-guided hepatic metastasectomy shows acoustic shadowing produced by cautery of the liver capsule (large arrow). Cautery was performed lateral to a large, solitary metastasis (small arrows) to mark the planned surgical margin of approximately 1 cm.
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Figure 20b. Mucinous colorectal cancer metastases. (a) Intraoperative image demonstrates acoustic shadowing produced by a small, superficial colorectal cancer metastasis. Note the thin rim of normal liver tissue superficial to this metastasis. (b) Intraoperative image obtained during US-guided hepatic metastasectomy shows acoustic shadowing produced by cautery of the liver capsule (large arrow). Cautery was performed lateral to a large, solitary metastasis (small arrows) to mark the planned surgical margin of approximately 1 cm.
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Applications of Intraoperative US of the Liver
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Survey for Primary or Metastatic Lesions
When surveying the liver, the radiologist should use a systematic approach to image all hepatic segments in the near, intermediate, and far fields, to satisfactorily identify any primary lesions and metastases (Fig 21).
Current transducer resolution permits the identification of lesions larger than 2 mm. Sensitivity of more than 90% has been documented for detection of lesions in the liver, with positive and negative predictive values of 90% and 78%, respectively (3).
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Figure 21a. Colorectal cancer metastases. (a) Intraoperative image demonstrates a small, hypoechoic colorectal cancer metastasis (arrow) in segment VI of the liver. Note the adjacent kidney, which, in the intraoperative setting, may have an echotexture similar to that of the liver. (b) Intraoperative image shows a well-circumscribed echogenic colorectal cancer metastasis (arrow) in a superficial location in the far field.
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Figure 21b. Colorectal cancer metastases. (a) Intraoperative image demonstrates a small, hypoechoic colorectal cancer metastasis (arrow) in segment VI of the liver. Note the adjacent kidney, which, in the intraoperative setting, may have an echotexture similar to that of the liver. (b) Intraoperative image shows a well-circumscribed echogenic colorectal cancer metastasis (arrow) in a superficial location in the far field.
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Data from our institution show that intraoperative US routinely results in the identification of 25%–35% more lesions in the liver than does preoperative imaging (4), but the difference may be decreasing with improvements in the resolution achievable with cross-sectional modalities. Intraoperative US may depict only the hyperechoic rim surrounding isoechoic metastases. It is also important to image lesions in two planes, since some colorectal cancer metastases may resemble adjacent vessels (Fig 22).
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Figure 22. Mucinous colorectal cancer metastasis adjacent to the portal vein. Intraoperative image demonstrates acoustic shadowing produced by a small colorectal cancer metastasis (large arrow). Note that the adjacent portal vein (small arrows), although it has a somewhat similar echogenic appearance due to collagen within its wall, is not accompanied by acoustic shadowing.
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Lesion Characterization
Although the appearance of many liver tumors at intraoperative US is similar to that at transabdominal US, some tumors have a different intraoperative appearance. Hemangiomas vary widely in appearance but are typically soft and do not contain visible flow or increased flow relevant to the adjacent liver parenchyma (Fig 23a). Small hemangiomas that were not detected at preoperative imaging are frequently identified during intraoperative US. Fibrosed hemangiomas are identified by their peripheral echogenic rim (Fig 23b, 23c).
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Figure 23a. Hepatic hemangiomas. (a) Intraoperative image shows a large, solitary hemangioma (large arrows) that was found incidentally at US during gastric surgery. In the intraoperative setting, such lesions are palpably soft, and on Doppler US images they do not demonstrate more flow than that in the adjacent liver parenchyma. The morphologic features of hepatic hemangiomas may vary at intraoperative US: The lesion in this case effaces the right hepatic vein (small arrows) but has not caused occlusion or thrombus formation. (b, c) Intraoperative images show small (arrow in b) and larger (arrows in c) fibrosed hemangiomas that differ in appearance from their more common, homogeneously echogenic counterparts.
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Figure 23b. Hepatic hemangiomas. (a) Intraoperative image shows a large, solitary hemangioma (large arrows) that was found incidentally at US during gastric surgery. In the intraoperative setting, such lesions are palpably soft, and on Doppler US images they do not demonstrate more flow than that in the adjacent liver parenchyma. The morphologic features of hepatic hemangiomas may vary at intraoperative US: The lesion in this case effaces the right hepatic vein (small arrows) but has not caused occlusion or thrombus formation. (b, c) Intraoperative images show small (arrow in b) and larger (arrows in c) fibrosed hemangiomas that differ in appearance from their more common, homogeneously echogenic counterparts.
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Figure 23c. Hepatic hemangiomas. (a) Intraoperative image shows a large, solitary hemangioma (large arrows) that was found incidentally at US during gastric surgery. In the intraoperative setting, such lesions are palpably soft, and on Doppler US images they do not demonstrate more flow than that in the adjacent liver parenchyma. The morphologic features of hepatic hemangiomas may vary at intraoperative US: The lesion in this case effaces the right hepatic vein (small arrows) but has not caused occlusion or thrombus formation. (b, c) Intraoperative images show small (arrow in b) and larger (arrows in c) fibrosed hemangiomas that differ in appearance from their more common, homogeneously echogenic counterparts.
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Bull’s-eye or target-shaped lesions may represent metastases from colon cancer, carcinoid tumors, focal nodular hyperplasia, or sarcomas (Fig 24). These lesions may or may not contain calcifications, which characteristically are seen in mucinous colorectal cancer metastases (Fig 25). Colon cancer metastases frequently are isoechoic to the adjacent liver parenchyma and may be identified by occlusion or displacement of vessels; they also are frequently surrounded by an ill-defined hypoechoic rim. Fine calcifications in mucinous tumors, if unaccompanied by acoustic shadowing, may simulate hemangiomas; however, unlike hemangiomas, metastatic tumors frequently produce shadowing (Fig 26).
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Figure 24. Targetlike carcinoid metastasis. Intraoperative image shows a targetlike lesion (arrows) with a central hyperechoic region. Several types of hepatic tumors may have this appearance—most commonly, colorectal cancer metastases, in which the central region of echogenicity represents calcification, and carcinoid metastases.
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Figure 25. Mucinous colorectal cancer metastasis. Intraoperative image shows an isolated metastasis with central mucinous calcifications that produce acoustic shadowing. Note the proximity of the tumor to the vena cava (IVC), middle hepatic vein (MHV), and right hepatic vein (RHV).
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Figure 26. Mucinous colorectal cancer metastasis. Intraoperative image shows a metastasis with internal calcifications (arrows) that produce acoustic shadowing, which obscures the caudate lobe posteriorly. In this situation, the obscured segments of the liver should be imaged from other angles.
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Benign and malignant tumors frequently coexist (Fig 27). The radiologist should be aware that metastases that are similar in size and that arise from a single primary neoplasm typically have similar US appearances, whereas metastases of different sizes may have varying US appearances. Therefore, if two or more lesions of similar size have differing US appearances, it is likely that one set represents the neoplasm and the other set represents something else, such as hemangiomas.
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Figure 27. Hepatocellular carcinoma and hemangioma in a 51-year-old man. Intraoperative color Doppler image demonstrates a predominantly hypoechoic mass in the high dome in segment VII of the liver and an adjacent small echogenic hemangioma (arrow). Note the absence of flow in the mass.
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Guidance for Tumor Resection and Metastasectomy
To best evaluate tumor resectability, the radiologist first must document the full extent of intrahepatic disease, including the presence or absence of vascular occlusion or invasion (Fig 28). US-guided biopsy may be necessary if lesions with atypical features are identified. When searching for metastases, the radiologist should give careful attention to all lobes and segments of the liver, especially to small segments such as the caudate lobe (Fig 29). Since hepatocellular carcinoma frequently invades major vessels and colorectal cancer metastases occasionally do so, the hepatic and portal venous systems also must be evaluated, and the porta hepatis should be assessed for lymphadenopathy. Documentation of the proximity of lesions to adjacent vessels depends in part on the planned surgical technique; typically, margins of 1–2 cm are required for adequate lesion resection (Fig 30). If a lesion is identified in the liver, many surgeons cauterize the liver capsule overlying the lesion to mark the planned surgical approach, especially when performing a nonsegmental wedge resection. Such cautery produces acoustic shadowing (Fig 30).
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Figure 28. Vascular invasion by a colorectal cancer metastasis. Intraoperative image demonstrates invasion of the right hepatic vein (large arrow) and the vena cava (small arrow) by a colorectal cancer metastasis (CRC). Accurate intraoperative US localization of this lesion in segment VII of the liver facilitated its surgical resection.
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Figure 29. Isolated colorectal metastasis in the caudate lobe. Intraoperative image demonstrates an almost isoechoic lesion in the caudate lobe (arrows), as well as an echogenic accumulation of air in the medial portion of the ligamentum teres, a normal finding in the intraoperative setting.
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Figure 30. Superficial colorectal cancer metastasis. Intraoperative image depicts a hypoechoic lesion (arrows) superficial to the right portal vein (RPV) and separated from it by a margin of normal tissue, an important finding for surgical planning. The round area of echogenicity lateral to the tumor was caused by cautery of the liver capsule to mark the surgical resection margin.
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It is not uncommon for the radiologist to be called back to the operating room to document the extent of a resection and to determine whether any residual tumor is present. For some tumors (typically, those in inaccessible or challenging locations, such as sites at the confluence of hepatic veins), it is possible that small amounts of residual tumor may be identified (Fig 14b), and intraoperative US then can provide information to guide the additional resection.
Evaluation of Vessel Patency
Color Doppler flow and pulsed Doppler US are frequently used to distinguish dilated bile ducts and blood vessels (Fig 31). The radiologist must be familiar with normal and variant hepatic vascular anatomy and should not place undue pressure on the liver surface, since such pressure may result in the compression of vessels, especially the vena cava.
When a thrombus is identified in a vessel, it may be important to distinguish between a tumor-associated thrombus that is avascular and a tumor thrombus that has an arterial waveform at pulsed Doppler evaluation (Fig 32).
Since a tumor thrombus is likely to render a tumor unresectable, an intraoperative US–guided biopsy of the thrombus may be necessary for diagnostic purposes. It is always important to exclude the presence of a thrombus in critical areas such as the hepatic vein confluence (Fig 33), the right atrium, and the intrahepatic and extrahepatic portal vein. Extrahepatic tumors, especially renal cell carcinoma, may extend into the vena cava, and such extension may be observed at intraoperative US (Fig 34). Since both benign and malignant tumors can efface vessels, it is important to distinguish the displacement and effacement of vessels (Fig 35), which are not contraindications to tumor resection, from the invasion and occlusion of vessels, which are contraindications to resection.
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Figure 31. Periductal cholangiocarcinoma. Intraoperative color Doppler US image depicts the precise relationship between the periductal cholangiocarcinoma (large arrow) and the right hepatic duct (small arrows), information that helped spare the right ductal system during resection of the left lobe of the liver.
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Figure 32. Thrombus. Intraoperative color Doppler flow image obtained during US-guided metastasectomy in a patient with hepatocellular carcinoma shows a thrombus in the left portal vein (arrows).
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Figure 33. Vascular invasion by metastasis. Intraoperative US image demonstrates a colorectal cancer metastasis (arrow) that has invaded the distal portion of the right hepatic vein (RHV) at its confluence with the adjacent vena cava (IVC). In this setting, if resection is performed, segment VII (posterior to the right hepatic vein) and segment VIII (anterior to the right hepatic vein) of the liver are likely to be resected.
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In the intraoperative setting, Doppler US may be performed for depiction of patency and flow direction in surgically created portosystemic shunts and for disease characterization and surgical planning in patients with Budd-Chiari syndrome. Depending on the nature of the surgical procedure, it might be necessary to perform Doppler US for evaluation of the extrahepatic portal venous system and for guidance of venotomy and clot removal.
Liver Transplantation
Intraoperative US is useful in cadaveric liver transplantations, in which the documentation of vessel patency and evaluation of anastomoses may be required. Intraoperative US is also helpful when there is inadvertent injury to the hepatic arteries, including dissection, or when interposition grafts are used to bridge recipient and donor vessels. Intraoperative US guidance is usually required during the harvesting phase of adult right-lobe split-liver transplantation, to help identify the relatively avascular resection plane 1–2 cm to the right of the middle hepatic vein. For these procedures, intraoperative US is also used to depict and localize the intrahepatic location of hepatic veins that drain segments V and VIII and to localize and characterize any accessory hepatic veins that may require the creation of separate anastomoses during implantation (Fig 36).
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Figure 36. Image obtained for planning of a living-related split-liver transplantation shows the relatively avascular plane between the right and left lobes of the liver (between segments VII and VIII); the insertion sites of the middle (MHV) and right hepatic veins (RHV) into the vena cava (IVC); and the location and size of the veins that drain into the middle hepatic vein from segments V, VII, and VIII (arrows).
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In an implanted cadaveric liver, a thrombus may be identified in excluded vascular remnants such as the remnant vena cava, and the thrombus may even extend into adjacent hepatic veins. In this setting, intraoperative US is used for guidance of thrombectomy (Fig 37).
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Abstract
Introduction
