(Radiology. 1999;210:451-458.)
© RSNA, 1999
Regenerative Nodules in Liver Cirrhosis: Findings at CT during Arterial Portography and CT Hepatic Arteriography with Histopathologic Correlation
Jae Hoon Lim, MD1,
Eung Yeop Kim, MD1,
Won Jae Lee, MD1,
Hyo Keun Lim, MD1,
Young Soo Do, MD1,
In-Wook Choo, MD1 and
Cheol Keun Park, MD2
1 Departments of Radiology (J.H.L., E.Y.K., W.J.L., H.K.L., Y.S.D., I.W.C.)
2 Diagnostic Pathology (C.K.P.), Samsung Medical Center, College of Medicine, Sungkyunkwan University, 50 Irwon-dong, Kangnam-ku, Seoul 135-710, South Korea.
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Abstract
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PURPOSE: To determine the appearance of regenerative nodules in patients with liver cirrhosis at computed tomography (CT) during arterial portography (CTAP) and CT hepatic arteriography (CTHA).
MATERIALS AND METHODS: CTAP and CTHA of the liver were performed in 28 consecutive patients with hepatocellular carcinoma (HCC) who were scheduled to undergo partial resection of the liver. Helical CTAP was performed after contrast material injection into the superior mesenteric artery followed by helical CTHA after contrast material injection into the hepatic artery. CT scans were analyzed for the presence of identifiable nodules and their size; results were correlated with gross and microscopic findings.
RESULTS: Resected livers showed cirrhosis in 20 patients, chronic hepatitis in four, and normal liver in four. Among the 20 patients with cirrhosis, regenerative nodules were demonstrated as enhancing 3–10-mm nodules surrounded by lower attenuation fibrous septa 0.8–1.5 mm thick at CTAP in seven patients and nonenhancing nodules of the same size surrounded by enhancing fibrous septa at CTHA in 15 patients. The degree of fibrosis determined the conspicuity of nodules.
CONCLUSION: Regenerative nodules in cirrhotic liver are visualized as enhancing nodules surrounded by lower attenuation thin septa at CTAP and nonenhancing nodules surrounded by enhancing fibrous septa at CTHA. CTHA is more sensitive than CTAP in depicting regenerative nodules (P < .005).
Index terms: Liver, blood supply, 95.79 • Liver, cirrhosis, 761.794 • Liver, CT, 761.12114, 761.12115, 761.12116 • Liver, nodules, 761.3198 • Liver neoplasms, diagnosis, 761.3198, 761.323
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Introduction
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CT during arterial portography (CTAP) is the most sensitive modality in the depiction of small liver lesions; therefore, it is the preferred method of preoperative work-up of candidates for hepatic surgery, particularly for detection of small hepatic tumors such as hepatocellular carcinoma (HCC) (1,2) and metastatic tumors (3–6). CT hepatic arteriography (CTHA) can depict hypervascular hepatic masses or even hypovascular metastases, as it can be performed in conjunction with CTAP and appears to be more informative when combined with CTAP (7–11). The appearance of cirrhotic liver parenchyma at CTAP and CTHA are frequently the background from which abnormal nodules such as HCC or dysplastic nodules stand out. Patients with advanced cirrhosis often have decreased or reversed portal flow due to portal hypertension and portosystemic shunt, and it is difficult to attain adequate parenchymal contrast enhancement during CTAP (12). CTAP is often nonspecific, frequently depicting benign lesions such as cysts and hemangiomas or false-positive perfusion defects (13). Peterson et al (14) reported that the most common benign nodular lesions depicted at CTAP were regenerative nodules. Lower attenuation nodules or the mottled appearance of hepatic parenchyma due to regenerative nodules and fibrosis simulate neoplasms, and this makes it difficult to interpret CTAP studies (12,14). The spectrum of focal liver lesions in patients with liver cirrhosis ranges from benign to malignant, including regenerative nodules, low-grade dysplastic nodules, high-grade dysplastic nodules, dysplastic nodules with subfoci of HCC, and HCC (15). Therefore, it is necessary to differentiate regenerative nodules from other nodules, including HCC, at CTAP and CTHA.
To our knowledge, there have been few articles that have described the appearance of regenerative nodules at CTAP (7,12,14) and only one that has done so with their appearance at CTHA (7). The purpose of this study was to describe the appearance of regenerative nodules at CTAP and CTHA on the basis of histopathologic correlation.
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MATERIALS AND METHODS
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From July 1996 to March 1997, 89 patients were referred for CTAP and CTHA to help evaluate them for surgical resection of HCC. Of these, 36 consecutive patients underwent hepatic resection as a treatment of HCC. Eight patients with arterioportal shunt at CTHA because of HCC and previous liver biopsy, or early portal vein opacification through the gastric antrum, duodenum, or pancreas caused by inadvertent injection of contrast material into the gastroduodenal artery were excluded because true CTHA was not possible. The other 53 patients excluded from our study did not undergo surgery because they had two or more HCCs in both lobes, poor liver function, or refused surgery.
The study population consisted of 28 patients (25 men, three women; age range, 34–69 years; mean age, 51 years) who underwent hepatic surgery: transplantation (n = 1), lobectomy (n = 16), segmentectomy (n = 8), or subsegmentectomy or wedge resection (n = 3). Before CTAP and CTHA, ultrasonography, magnetic resonance imaging, or helical dynamic CT disclosed 29 masses in 28 patients: One patient had two masses, one in the right lobe and the other in the medial segment of the left lobe. CTAP and CTHA were performed to help confirm the absence of tumor in the other hepatic lobe. The interval from the CTAP and CTHA procedure to surgery was 4–151 days (mean, 16.4 days).
With bilateral femoral artery punctures, two catheters were selectively placed, one in the superior mesenteric artery and the other in the common hepatic artery or replaced right hepatic artery from the superior mesenteric artery, depending on arterial variation. Before CTAP and CTHA, celiac and superior mesenteric angiography was performed for the evaluation of HCC vascularity and vascular anatomy by using 50–60 mL of nonionic contrast material ([iopamidol] Iopamiro 300; Bracco, Milan, Italy). Among the four patients with hepatic arterial variations, there were three in whom the right hepatic artery arose from the superior mesenteric artery and one in whom both the right and left hepatic arteries arose from the superior mesenteric artery.
The patients underwent CTAP and CTHA 20–30 minutes after angiography. For CTAP, a 5-F catheter was placed in the superior mesenteric artery and 90 mL of nonionic contrast material (iopamidol; Bracco) was injected, and CT scanning was performed 25 seconds after the start of injection at a speed of 2.5 mL/sec with a power injector. For CTHA, the other 5-F catheter was placed in the common hepatic artery or in the replaced right hepatic artery if the right hepatic artery arose from the superior mesenteric artery, and 45 mL of contrast material was injected. Scanning was performed 5 seconds after the start of injection at a speed of 1.5 mL/sec. When the liver was supplied by two arteries, each artery was selected one by one, and CT was performed twice. By using a helical CT scanner (HiSpeed Advantage; GE Medical Systems, Milwaukee, Wis), scans were obtained in a craniocaudal direction with 7-mm collimation, 7 mm/sec table speed, 120 kVp, and 180 mAs during a single breath-hold helical acquisition of 25–30 seconds, depending on liver size.
CT scans were reviewed jointly in one session by three radiologists (J.H.L., E.Y.K., W.J.L.) who were blinded to the histopathologic results. A consensus opinion was recorded; when there was a disagreement, the majority opinion was recorded. The well-enhanced liver parenchyma at CTAP and CTHA was evaluated, and the areas of perfusion defects caused by HCC or arterioportal shunts were not evaluated.
Innumerable enhancing nodules surrounded by lower attenuation septa at CTAP and nonenhancing nodules surrounded by enhancing septa at CTHA were regarded as cirrhotic regenerative nodules. The size of more than 20 regenerative nodules and the thickness of fibrous septa were measured by means of enlarged images (x5~x10) on the 2K x 2K monitor of a picture archiving and communication system. The extremes of the largest and smallest nodules were not recorded. The depiction of regenerative nodules at CTAP and CTHA was statistically analyzed by means of the McNemar test. Findings at CTAP and CTHA were correlated with regenerative nodules in the resected specimens in terms of nodule size and degree of fibrosis. One pathologist blind to the radiologic findings reviewed the gross and microscopic findings of resected specimens. The size of more than 20 regenerative nodules was measured by using a divider, and the range representing the majority of nodules was recorded with the largest and smallest nodules excluded. The degree of fibrosis was classified as mild when the mean thickness of septa was about 0.5 mm, moderate when the mean thickness of septa was about 1.0 mm, and severe when the mean thickness of septa was about 1.5 mm on gross specimens and was correlated with conspicuity at CTAP and CTHA.
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RESULTS
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The resected livers containing HCC showed cirrhosis in 20 patients, chronic hepatitis in four patients, and normal liver in four patients. All 20 patients with liver cirrhosis showed mixed micronodular (nodules 
3 mm) and macronodular (nodules > 3 mm) cirrhosis. Liver cirrhosis was due to postnecrotic liver injury caused by hepatitis B viral infection in all patients, and the size of the regenerative nodules was 2–10 mm in diameter. There was no case of micronodular cirrhosis. The thickness of the fibrous septa was 0.2–1.5 mm. The thickness of fibrous septa surrounding regenerative nodules varied from nodule to nodule and from area to area.
At CTAP, regenerative nodules were seen in seven of 20 patients with cirrhosis as innumerable, homogeneously enhancing, round nodules 3–10 mm in diameter (80% of regenerative nodules were 3–8 mm in diameter) surrounded by barely visible low-attenuation septa 0.8–1.5 mm thick (Fig 1a). Visibility of nodules varied from area to area, but the nodules were more discrete and prominent at peripheral parts of the liver (Figs 1a, 2a), probably because nodules bulged out of the liver contour. In two patients, the nodules were visualized diffusely in the entire liver parenchyma (more than 75%) (Fig 1); in the other five patients, the nodules were visualized in part of the liver (30%–75%), mainly at the dome area and peripheral part of the liver parenchyma, and the rest of the parenchyma was heterogeneous (Fig 2). Very tiny higher attenuation dots in the center of the regenerative nodules were seen in two patients (Fig 3) and probably represented portal veins. Among the remaining 13 patients with cirrhosis with no discernible nodules, two patients showed heterogeneity of the liver parenchyma and 11 patients showed normal homogeneous hepatic parenchyma (Fig 4a); in these patients, gross inspection of specimens showed smaller regenerative nodules (<5 mm) surrounded by a lesser degree of fibrosis. No nodules were visible at CTAP in the eight patients with hepatitis or normal liver (Fig 5); in these patients, the liver parenchyma was homogeneous at CTAP.
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Figure 1a. (a) CTAP and (b) CTHA scans obtained in a 52-year-old man with macronodular cirrhosis. The right hepatic artery arises from the superior mesenteric artery as a replaced right hepatic artery; therefore, two series of CTHA scans were obtained with injection of contrast material into the right and left hepatic arteries one after the other. (a) CTAP scan shows innumerable small enhancing regenerative nodules (arrowheads) of cirrhosis surrounded by lower attenuation thin fibrous septa. One or two small ovoid perfusion defects (arrow) were not confirmed surgically. More than 90% of the regenerative nodules are enhanced and visible. (b) CTHA scan of the left hepatic lobe shows many nonenhancing regenerative nodules surrounded by well-enhanced fibrous septa in the left hepatic lobe. More than 90% of the regenerative nodules are visible. Many nodules contain central enhancing dots (arrowheads) that represent the hepatic arterioles in the regenerative nodules. Only the left hepatic artery was catheterized. (c) Photograph of the cut surface of the resected specimen shows regenerative nodules; the majority are 3–10 mm and are surrounded by thick fibrous septa 0.3–1.5 mm thick. Fibrosis is uneven and irregularly distributed. Note the nodularity of the liver surface due to the regenerative nodules (arrowhead).
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Figure 1b. (a) CTAP and (b) CTHA scans obtained in a 52-year-old man with macronodular cirrhosis. The right hepatic artery arises from the superior mesenteric artery as a replaced right hepatic artery; therefore, two series of CTHA scans were obtained with injection of contrast material into the right and left hepatic arteries one after the other. (a) CTAP scan shows innumerable small enhancing regenerative nodules (arrowheads) of cirrhosis surrounded by lower attenuation thin fibrous septa. One or two small ovoid perfusion defects (arrow) were not confirmed surgically. More than 90% of the regenerative nodules are enhanced and visible. (b) CTHA scan of the left hepatic lobe shows many nonenhancing regenerative nodules surrounded by well-enhanced fibrous septa in the left hepatic lobe. More than 90% of the regenerative nodules are visible. Many nodules contain central enhancing dots (arrowheads) that represent the hepatic arterioles in the regenerative nodules. Only the left hepatic artery was catheterized. (c) Photograph of the cut surface of the resected specimen shows regenerative nodules; the majority are 3–10 mm and are surrounded by thick fibrous septa 0.3–1.5 mm thick. Fibrosis is uneven and irregularly distributed. Note the nodularity of the liver surface due to the regenerative nodules (arrowhead).
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Figure 1c. (a) CTAP and (b) CTHA scans obtained in a 52-year-old man with macronodular cirrhosis. The right hepatic artery arises from the superior mesenteric artery as a replaced right hepatic artery; therefore, two series of CTHA scans were obtained with injection of contrast material into the right and left hepatic arteries one after the other. (a) CTAP scan shows innumerable small enhancing regenerative nodules (arrowheads) of cirrhosis surrounded by lower attenuation thin fibrous septa. One or two small ovoid perfusion defects (arrow) were not confirmed surgically. More than 90% of the regenerative nodules are enhanced and visible. (b) CTHA scan of the left hepatic lobe shows many nonenhancing regenerative nodules surrounded by well-enhanced fibrous septa in the left hepatic lobe. More than 90% of the regenerative nodules are visible. Many nodules contain central enhancing dots (arrowheads) that represent the hepatic arterioles in the regenerative nodules. Only the left hepatic artery was catheterized. (c) Photograph of the cut surface of the resected specimen shows regenerative nodules; the majority are 3–10 mm and are surrounded by thick fibrous septa 0.3–1.5 mm thick. Fibrosis is uneven and irregularly distributed. Note the nodularity of the liver surface due to the regenerative nodules (arrowhead).
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Figure 2a. (a) CTAP and (b) CTHA scans obtained in a 58-year-old man with micro- and macronodular cirrhosis. (a) CTAP scan shows slightly heterogeneous liver parenchyma. Several suspicious enhancing nodules (arrowheads) are visualized at the anterior and left lateral part of the left hepatic lobe along the peripheral part of the liver. Less than 10% of the regenerative nodules are visible. (b) CTHA scan shows numerous nonenhancing regenerative nodules surrounded by very highly enhancing fibrous septa and demonstrates nodules (arrowheads) in about 50% of the liver parenchyma. The peripheral part of the liver parenchyma is not satisfactorily enhanced, and regenerative nodules are not distinctly visible. (c) Photograph of the cut surface of the resected specimen shows regenerative nodules (arrows); the majority are 2–7 mm and are surrounded by fibrous septa 0.5–1.0 mm thick.
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Figure 2b. (a) CTAP and (b) CTHA scans obtained in a 58-year-old man with micro- and macronodular cirrhosis. (a) CTAP scan shows slightly heterogeneous liver parenchyma. Several suspicious enhancing nodules (arrowheads) are visualized at the anterior and left lateral part of the left hepatic lobe along the peripheral part of the liver. Less than 10% of the regenerative nodules are visible. (b) CTHA scan shows numerous nonenhancing regenerative nodules surrounded by very highly enhancing fibrous septa and demonstrates nodules (arrowheads) in about 50% of the liver parenchyma. The peripheral part of the liver parenchyma is not satisfactorily enhanced, and regenerative nodules are not distinctly visible. (c) Photograph of the cut surface of the resected specimen shows regenerative nodules (arrows); the majority are 2–7 mm and are surrounded by fibrous septa 0.5–1.0 mm thick.
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Figure 2c. (a) CTAP and (b) CTHA scans obtained in a 58-year-old man with micro- and macronodular cirrhosis. (a) CTAP scan shows slightly heterogeneous liver parenchyma. Several suspicious enhancing nodules (arrowheads) are visualized at the anterior and left lateral part of the left hepatic lobe along the peripheral part of the liver. Less than 10% of the regenerative nodules are visible. (b) CTHA scan shows numerous nonenhancing regenerative nodules surrounded by very highly enhancing fibrous septa and demonstrates nodules (arrowheads) in about 50% of the liver parenchyma. The peripheral part of the liver parenchyma is not satisfactorily enhanced, and regenerative nodules are not distinctly visible. (c) Photograph of the cut surface of the resected specimen shows regenerative nodules (arrows); the majority are 2–7 mm and are surrounded by fibrous septa 0.5–1.0 mm thick.
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Figure 3a. (a) CTAP and (b) CTHA scans obtained in a 56-year-old man with micro- and macronodular liver cirrhosis. (a) CTAP scan shows many enhancing regenerative nodules in the right lobe and slightly heterogeneous enhancement of the left lobe. The majority of the nodules in the right hepatic lobe contain central enhancing dots (arrowheads) suggestive of portal venules. (b) CTHA scan shows heterogeneity of the liver parenchyma and several ill-defined poorly enhancing nodules (arrowheads) that represent the regenerative nodules. Note a hepatic arteriole in the center of one of the regenerative nodules. (c) Photomicrograph shows a regenerative nodule surrounded by thick fibrous septa (black arrows). Note the portal triad (curved white arrows) and portal venule (straight white arrow) within the nodule. (Hematoxylin-eosin stain; original magnification, x100.)
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Figure 3b. (a) CTAP and (b) CTHA scans obtained in a 56-year-old man with micro- and macronodular liver cirrhosis. (a) CTAP scan shows many enhancing regenerative nodules in the right lobe and slightly heterogeneous enhancement of the left lobe. The majority of the nodules in the right hepatic lobe contain central enhancing dots (arrowheads) suggestive of portal venules. (b) CTHA scan shows heterogeneity of the liver parenchyma and several ill-defined poorly enhancing nodules (arrowheads) that represent the regenerative nodules. Note a hepatic arteriole in the center of one of the regenerative nodules. (c) Photomicrograph shows a regenerative nodule surrounded by thick fibrous septa (black arrows). Note the portal triad (curved white arrows) and portal venule (straight white arrow) within the nodule. (Hematoxylin-eosin stain; original magnification, x100.)
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Figure 3c. (a) CTAP and (b) CTHA scans obtained in a 56-year-old man with micro- and macronodular liver cirrhosis. (a) CTAP scan shows many enhancing regenerative nodules in the right lobe and slightly heterogeneous enhancement of the left lobe. The majority of the nodules in the right hepatic lobe contain central enhancing dots (arrowheads) suggestive of portal venules. (b) CTHA scan shows heterogeneity of the liver parenchyma and several ill-defined poorly enhancing nodules (arrowheads) that represent the regenerative nodules. Note a hepatic arteriole in the center of one of the regenerative nodules. (c) Photomicrograph shows a regenerative nodule surrounded by thick fibrous septa (black arrows). Note the portal triad (curved white arrows) and portal venule (straight white arrow) within the nodule. (Hematoxylin-eosin stain; original magnification, x100.)
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Figure 4a. (a) CTAP and (b) CTHA scans obtained in a 66-year-old woman with micro- and macronodular cirrhosis. (a) CTAP scan shows homogeneous attenuation of the liver parenchyma with no discernible nodular enhancement. Note that the contour of the liver is quite nodular, reflecting the regenerative nodules. (b) CTHA scan shows many small nodules surrounded by highly enhancing fibrous septa in about 50% of the liver parenchyma. Note the tiny enhancing central dots in the nodules (arrowheads). The posterior segment of the right hepatic lobe is not well opacified and shows inhomogeneous texture with barely visible nodules. (c) Photograph of the cut surface of the resected specimen shows 2–6-mm regenerative nodules (arrows) surrounded by fibrous septa 0.2–0.5 mm thick. The thickness of fibrous septa is different from one area to another.
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Figure 4b. (a) CTAP and (b) CTHA scans obtained in a 66-year-old woman with micro- and macronodular cirrhosis. (a) CTAP scan shows homogeneous attenuation of the liver parenchyma with no discernible nodular enhancement. Note that the contour of the liver is quite nodular, reflecting the regenerative nodules. (b) CTHA scan shows many small nodules surrounded by highly enhancing fibrous septa in about 50% of the liver parenchyma. Note the tiny enhancing central dots in the nodules (arrowheads). The posterior segment of the right hepatic lobe is not well opacified and shows inhomogeneous texture with barely visible nodules. (c) Photograph of the cut surface of the resected specimen shows 2–6-mm regenerative nodules (arrows) surrounded by fibrous septa 0.2–0.5 mm thick. The thickness of fibrous septa is different from one area to another.
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Figure 4c. (a) CTAP and (b) CTHA scans obtained in a 66-year-old woman with micro- and macronodular cirrhosis. (a) CTAP scan shows homogeneous attenuation of the liver parenchyma with no discernible nodular enhancement. Note that the contour of the liver is quite nodular, reflecting the regenerative nodules. (b) CTHA scan shows many small nodules surrounded by highly enhancing fibrous septa in about 50% of the liver parenchyma. Note the tiny enhancing central dots in the nodules (arrowheads). The posterior segment of the right hepatic lobe is not well opacified and shows inhomogeneous texture with barely visible nodules. (c) Photograph of the cut surface of the resected specimen shows 2–6-mm regenerative nodules (arrows) surrounded by fibrous septa 0.2–0.5 mm thick. The thickness of fibrous septa is different from one area to another.
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Figure 5a. (a) CTAP and (b) CTHA scans obtained in a 39-year-old woman with HCC surrounded by normal parenchyma. (a) CTAP scan shows a large, round perfusion defect due to HCC (M) in the right lobe. The normal liver parenchyma shows homogeneous enhancement without nodules. (b) CTHA scan shows a very well enhanced, oval HCC (M). The rest of the normal liver parenchyma is heterogeneous. (c) Photograph of the cut surface of the resected specimen shows normal homogeneous hepatic parenchyma without any nodules or fibrosis. The arrows point to the portal veins.
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Figure 5b. (a) CTAP and (b) CTHA scans obtained in a 39-year-old woman with HCC surrounded by normal parenchyma. (a) CTAP scan shows a large, round perfusion defect due to HCC (M) in the right lobe. The normal liver parenchyma shows homogeneous enhancement without nodules. (b) CTHA scan shows a very well enhanced, oval HCC (M). The rest of the normal liver parenchyma is heterogeneous. (c) Photograph of the cut surface of the resected specimen shows normal homogeneous hepatic parenchyma without any nodules or fibrosis. The arrows point to the portal veins.
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Figure 5c. (a) CTAP and (b) CTHA scans obtained in a 39-year-old woman with HCC surrounded by normal parenchyma. (a) CTAP scan shows a large, round perfusion defect due to HCC (M) in the right lobe. The normal liver parenchyma shows homogeneous enhancement without nodules. (b) CTHA scan shows a very well enhanced, oval HCC (M). The rest of the normal liver parenchyma is heterogeneous. (c) Photograph of the cut surface of the resected specimen shows normal homogeneous hepatic parenchyma without any nodules or fibrosis. The arrows point to the portal veins.
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At CTHA, regenerative nodules were seen in 15 of 20 patients with cirrhosis as innumerable, round, nonenhancing nodules 3–10 mm in diameter, diffusely scattered and surrounded by highly enhancing septa (Figs 1b, 2b, 4b). The liver at CTHA looked like a honeycomb. The thickness of enhancing septa was 0.8–1.5 mm. The nodules were visualized diffusely in the entire liver (area, more than 75%) (Fig 1b) in six patients and in a part of the liver (area, 50%–75%) (Figs 2b, 4b) in nine patients. In one patient, numerous enhancing nodules were visualized, and these were considered regenerative nodules (Fig 6b). Microscopic examination of this specimen disclosed hepatic arterial structure within many regenerative nodules (Fig 6c), and the arterial supply made some of the nodules opacified and enhanced at CTHA. We suspected that, in these nodules, there was a compensatory or reciprocal increase in hepatic arterial flow because portal venous flow was diminished for some reason. Some of the regenerative nodules in this patient had lower attenuation at CTAP (Fig 6a). One or two tiny enhancing dots were seen within the lower attenuation nodules (Figs 1b, 3b, 4b) in four patients and were probably the hepatic arterial branches within the regenerative nodules found at histopathologic examination. In four patients with mild cirrhosis and smaller nodules, the hepatic parenchyma was heterogeneous, but there were no visible regenerative nodules. In one patient with mild cirrhosis, the liver parenchyma was homogeneous. None of the eight patients with chronic hepatitis or normal liver had nodules at CTHA. Four patients with chronic hepatitis had heterogeneous hepatic parenchyma, and two patients with chronic hepatitis had homogeneous parenchyma. Three patients with normal liver had homogeneous liver parenchyma, and one patient with normal liver had heterogeneous liver parenchyma (Fig 5).
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Figure 6a. (a) CTAP and (b) CTHA scans obtained in a 53-year-old man with micro- and macronodular liver cirrhosis. The liver was removed for transplantation, and there was one high-grade dysplastic nodule in the lower part of the right lobe and five low-grade dysplastic nodules in the superior part of the right lobe. (a) CTAP scan shows heterogeneous enhancement of the liver parenchyma with several small, round, lower attenuation nodules (arrowheads). These nodules were also considered regenerative nodules, as there were no dysplastic nodules or HCC at this level of the resected liver. The arrow points to the coronary vein with contrast material refluxing into it from the main portal vein. (b) CTHA scan shows many enhancing nodules (arrowheads) that most likely represent regenerative nodules. About 20% of the liver parenchyma is occupied by these enhancing nodules. There were no pathologic dysplastic nodules or HCC at this level. Enhancing nodules at CTHA may reflect diminished portal flow to some of the regenerative nodules and a reciprocal increase in hepatic arterial flow. Some of these nodules at CTHA coincide in location with lower attenuation nodules at CTAP in a. (c) Photomicrograph of the resected liver tissue shows a hepatic arteriole (white solid arrow) within one of the regenerative nodules. The portal triads (open arrows) were incorporated in the process of formation of a large regenerative nodule, and the portal veins (black solid arrows) and hepatic arterioles were captured within the regenerative nodule. (Hematoxylin-eosin stain; original magnification, x100.)
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Figure 6b. (a) CTAP and (b) CTHA scans obtained in a 53-year-old man with micro- and macronodular liver cirrhosis. The liver was removed for transplantation, and there was one high-grade dysplastic nodule in the lower part of the right lobe and five low-grade dysplastic nodules in the superior part of the right lobe. (a) CTAP scan shows heterogeneous enhancement of the liver parenchyma with several small, round, lower attenuation nodules (arrowheads). These nodules were also considered regenerative nodules, as there were no dysplastic nodules or HCC at this level of the resected liver. The arrow points to the coronary vein with contrast material refluxing into it from the main portal vein. (b) CTHA scan shows many enhancing nodules (arrowheads) that most likely represent regenerative nodules. About 20% of the liver parenchyma is occupied by these enhancing nodules. There were no pathologic dysplastic nodules or HCC at this level. Enhancing nodules at CTHA may reflect diminished portal flow to some of the regenerative nodules and a reciprocal increase in hepatic arterial flow. Some of these nodules at CTHA coincide in location with lower attenuation nodules at CTAP in a. (c) Photomicrograph of the resected liver tissue shows a hepatic arteriole (white solid arrow) within one of the regenerative nodules. The portal triads (open arrows) were incorporated in the process of formation of a large regenerative nodule, and the portal veins (black solid arrows) and hepatic arterioles were captured within the regenerative nodule. (Hematoxylin-eosin stain; original magnification, x100.)
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Figure 6c. (a) CTAP and (b) CTHA scans obtained in a 53-year-old man with micro- and macronodular liver cirrhosis. The liver was removed for transplantation, and there was one high-grade dysplastic nodule in the lower part of the right lobe and five low-grade dysplastic nodules in the superior part of the right lobe. (a) CTAP scan shows heterogeneous enhancement of the liver parenchyma with several small, round, lower attenuation nodules (arrowheads). These nodules were also considered regenerative nodules, as there were no dysplastic nodules or HCC at this level of the resected liver. The arrow points to the coronary vein with contrast material refluxing into it from the main portal vein. (b) CTHA scan shows many enhancing nodules (arrowheads) that most likely represent regenerative nodules. About 20% of the liver parenchyma is occupied by these enhancing nodules. There were no pathologic dysplastic nodules or HCC at this level. Enhancing nodules at CTHA may reflect diminished portal flow to some of the regenerative nodules and a reciprocal increase in hepatic arterial flow. Some of these nodules at CTHA coincide in location with lower attenuation nodules at CTAP in a. (c) Photomicrograph of the resected liver tissue shows a hepatic arteriole (white solid arrow) within one of the regenerative nodules. The portal triads (open arrows) were incorporated in the process of formation of a large regenerative nodule, and the portal veins (black solid arrows) and hepatic arterioles were captured within the regenerative nodule. (Hematoxylin-eosin stain; original magnification, x100.)
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As the cirrhotic process is diffuse and the size of regenerative nodules was variable, it was impossible to make one-to-one comparisons between the scans and the histopathologic findings in terms of the size and shape of individual nodules. Nodules were demonstrated at CTAP and CTHA when they were larger than 5 mm in diameter. Regenerative nodules were depicted better at CTHA (15 of 20 patients) than at CTAP (seven of 20 patients), and this was statistically significant (P < .005; McNemar test). When the nodules were smaller than 5 mm, most of the nodules were not clearly seen at CTHA, and especially not at CTAP. The degree of fibrosis is relatively well correlated with degree of conspicuity of nodules at CTAP and CTHA; when fibrosis was severe, the nodules were better defined. Again, it was not possible to make a one-to-one comparison between the conspicuity of nodules at CT and the histopathologic degree of fibrosis.
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DISCUSSION
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Liver cirrhosis is a progressive, diffuse process of architectural disorganization characterized by fibrosis and the formation of structurally abnormal parenchymal nodules involving the entire liver. These two features, regenerative nodules and fibrosis, are combined in varying proportions, and the resultant morphologic appearances encompass a wide spectrum. Micronodular cirrhosis is characterized by a preponderance of uniform nodules less than 3 mm in diameter and is usually accompanied by narrow, regular fibrous septa (16). Macronodular cirrhosis has a more varied and heterogeneous appearance. The nodules generally exceed 3 mm, their size varying greatly and reaching a centimeter in diameter, and the fibrosis is typically unevenly and irregularly arrayed (Fig 1c). Alcoholic and biliary cirrhosis are usually micronodular cirrhosis, while cirrhosis associated with chronic active hepatitis, including hepatitis B and C, is macronodular cirrhosis (16). It is not unusual for elements of micro- and macronodular cirrhosis to coexist in the same liver.
The fibrous septa manifest as bridging connective tissue separating parenchymal regenerative nodules, the connective tissue containing three or more portal triads in a single strand of scar (17). The septa vary considerably in breadth and extent, and they contain inflammatory cells and arterial, venous, and biliary structures in varying numbers. As viewed in two-dimensional sections, the fibrosis surrounds the nodule completely or incompletely.
Cirrhotic liver parenchyma can develop HCC. More than 80% of all HCCs occur in patients with cirrhosis, and any nodular lesions in cirrhotic liver are of particular importance because of their proposed link with HCC (16). The appearance of cirrhotic parenchyma at CTAP and CTHA is the background from which HCC will stand out; therefore, the enhancement pattern of regenerative nodules is important in differentiating them from dysplastic nodules or HCC. Regenerative nodules may appear as high-attenuation nodules on unenhanced CT scans when the nodules contain iron (16), but there were no such cases with the conventional unenhanced CT scans obtained before CTAP and CTHA in our series. The low prevalence of iron-containing nodules on the unenhanced CT scans may be because of the difference in the cause of cirrhosis; this phenomenon has been described in the United States, where in most patients who have cirrhosis it is due to alcohol consumption and is not due to hepatitis B.
It has been well documented that characterization of nodules in hepatic cirrhosis at CT is possible by analyzing the portal and hepatic arterial supply of the nodules (18). Cirrhotic regenerative nodules are mainly supplied by portal veins (18). As the grade of malignancy increases, the hepatic arterial flow to nodular lesions tends to increase, and the portal venous supply tends to decrease (18). In this way, dysplastic nodules and HCC can be differentiated easily from regenerative nodules, as the blood supply to dysplastic nodules and HCC differs in portal venous and hepatic arterial contributions (11,18).
Although CTAP is sensitive in the depiction of small hepatic lesions (1–6), either portal venous perfusion defects or benign nodular lesions can appear as false-positive nodular lesions. Pseudolesions due to perfusion abnormalities at CTAP are flat or wedge shaped and are related to variants of vascular supply (13,19–21).
The most problematic nontumorous pseudolesions in patients with cirrhosis are regenerative nodules (14). There have been several articles regarding the appearance of regenerative nodules at CTAP. Chezmar et al (7) described regenerative nodules as distinct areas of higher attenuation. To the contrary, cirrhotic regenerative nodules were described by Oliver et al (12) as mottled lower attenuation nodules and by Peterson et al (14) as innumerable, round intraparenchymal nodules of "soft tissue attenuation" (attenuation of skeletal muscle) or "intermediate attenuation" (attenuation between skeletal muscle and normal enhanced liver parenchyma) at CTAP. These regenerative nodules posed a particular problem in patients who have cirrhosis and are at risk of HCC (12,14). Many regenerative nodules were higher in attenuation (intermediate attenuation) than HCC (soft-tissue attenuation) was, although some regenerative nodules had soft-tissue attenuation (14).
In our series, the appearance of regenerative nodules at CTAP was variable. In mild cirrhosis, regenerative nodules were not visible at all, or only the heterogeneity of the liver parenchyma was seen at CTAP. In patients with advanced cirrhosis, regenerative nodules were clearly visualized as homogeneously enhancing, round nodules surrounded by thin, lower attenuation, fibrous septa. The visibility of individual regenerative nodules depended on the size of the regenerative nodules and the degree of fibrosis histopathologically; the bigger the nodules and thicker the fibrosis, the better the nodules were visualized. Sometimes regenerative nodules were visualized as enhancing nodules with tiny central higher attenuation dots that were central portal venules.
These findings of regenerative nodules at CTAP in our series are similar to the appearance described by Chezmar et al (7) but quite different from the description by Peterson et al (14). Only two patients had nodules of lower attenuation than that of the liver parenchyma (Fig 6a), as described by Peterson et al (14). The discrepancy may be because of the difference in injection speed and amount of contrast material administered or in the delay time before CT scanning. In the delay phase of CTAP, regenerative nodules are usually of low attenuation as the fibrous septa are enhanced. Peterson et al (14) used a slow scanner, so CTAP in the later phase might show regenerative nodules of low attenuation, resulting in pseudolesions. The difference may be explained, at least in some cases, by the difference in the cause of cirrhosis. This changeability of findings depending on the phase after contrast material injection or on the cause of cirrhosis also accounts for the variability and nonspecificity of dynamic incremental CT findings in cirrhosis (16).
To our knowledge, there has been only one report describing the findings of regenerative nodules at CTHA as distinct areas of lower attenuation (7). In our series, regenerative nodules were visualized at CTHA as nonenhancing, round nodules surrounded by higher attenuation fibrous septa mimicking honeycomb. Visibility of regenerative nodules at CTHA was variable from area to area. There was also variation in the size of regenerative nodules and the thickness of fibrous septa from area to area in the same gross specimens. In a few patients with mild cirrhosis, there were no visible regenerative nodules.
The appearance of regenerative nodules at CTAP and CTHA is related to the blood supply to regenerative nodules and fibrous septa. Regenerative nodules were seen at CTAP as innumerable, homogeneously enhancing, round nodules 3–10 mm in diameter surrounded by barely visible low-attenuation septa 0.8–1.5 mm thick and at CTHA as innumerable, round, nonenhancing nodules surrounded by highly enhancing septa. Individual regenerative nodules contain normal portal venous supply (18), and these nodules will be enhanced at CTAP, while fibrous septa have lower attenuation. The reason some regenerative nodules were of lower attenuation at CTAP and higher attenuation at CTHA (Fig 6) is not clear. Dysplastic nodules or dysplastic nodules with subfoci of HCC may have hepatic arterial supply (18), but this was not the case in our study (Fig 6).
Regenerative nodules may have portal venous as well as hepatic arterial supply during the process of regenerative nodule formation; as one large regenerative nodule may be formed by the fusion of several hepatic lobules (16), hepatic arterioles within the captured portal triads may persist in the regenerative nodule (Figs 1, 3, 4). For some reason, portal venous flow is diminished in regenerative nodules, and because of a reciprocal or compensatory relationship between the portal vein and the hepatic artery, hepatic arterial flow will increase and result in regenerative nodules of higher attenuation at CTHA (Fig 6).
The fibrous septa were supplied by hepatic arterioles and the peribiliary plexus, and thus were highly enhanced at CTHA. The thickness of the fibrous septa on gross specimens determined the conspicuity of the regenerative nodules. When the fibrous septa were thick, the regenerative nodules were depicted distinctly because of the enhancement of abundant hepatic arterioles within the thick fibrous septa, but when the fibrous septa were weak and thin, the individual regenerative nodules were not distinguished well. In patients with mild cirrhosis in which the regenerative nodules were small (<5 mm) and the degree of fibrosis was mild, the regenerative nodules were not seen; only the heterogeneity or homogeneity of the liver parenchyma was visible. Regenerative nodules of micronodular cirrhosis in alcoholic or biliary cirrhosis may not be visible because the nodules are smaller than 3 mm; there was no case of micronodular cirrhosis in our series. Regenerative nodules were generally more clearly seen at CTHA than at CTAP (P < .005), especially in advanced macronodular liver cirrhosis. This may be because of the abundant hepatic arterial vascularity, including the peribiliary arterial plexus, within the fibrous septa, which are highly enhanced at CTHA.
Sometimes CTAP has limited usefulness, as portal blood flow often diminishes or reverses in severe cirrhosis (12). Good parenchymal opacification of the cirrhotic liver is a prerequisite for the depiction of small pathologic nodules such as regenerative nodules, dysplastic nodules, or small HCCs (12). The variability of appearance of liver parenchyma at CTAP and CTHA in our series may be due to incomplete parenchymal opacification caused by the various hemodynamic changes of liver cirrhosis. Even in cases with good quality of parenchymal enhancement, the presence of diffuse or irregularly scattered regenerative nodules may cause focal abnormalities that are indistinguishable from dysplastic nodules or even from small HCCs.
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Footnotes
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Address reprint requests to J.H.L.
Abbreviations: CTAP = CT during arterial portography
CTHA = CT hepatic arteriography
HCC = hepatocellular carcinoma
Author contributions: Guarantor of integrity of entire study, J.H.L.; study concepts and design, J.H.L.; definition of intellectual content, J.H.L.; literature research, J.H.L.; clinical studies, W.J.L., H.K.L., Y.S.D., I.W.C., C.K.P.; data acquisition, E.Y.K.; data analysis, E.Y.K., J.H.L.; statistical analysis, E.Y.K.; manuscript preparation, J.H.L.; manuscript review, H.K.L., Y.S.D., W.J.L., I.W.C.
Received October 10, 1997;
revision requested December 18, 1997; revision received July 2, 1998;
accepted September 8, 1998.
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TOP
Abstract
Introduction
