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British Journal of Radiology 74 (2001),142-146 © 2001 The British Institute of Radiology

Full paper

The findings of ruptured hepatocellular carcinoma on helical CT

B G Choi, MD1, S H Park, MD1, J Y Byun, MD1, S E Jung, MD1, K H Choi, MD1 and J-Y Han, MD2

1 Departments of Radiology
2 Internal Medicine, College of Medicine, The Catholic University of Korea, Korea

Correspondence: Seog Hee Park, MD, Department of Radiology, Kangnam St Mary's Hospital, 505 Banpo-Dong, Seocho-Ku, Seoul 137-701, Korea


    Abstract
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 
To evaluate the helical CT findings of ruptured hepatocellular carcinoma (HCC), 12 patients with ruptured HCC were reviewed with regard to the tumour's location, size and contour protrusion, the appearance of the mass, the enhancement pattern, multiplicity and secondary changes. All ruptured tumours were located at the periphery of the liver and had a protruding contour. The maximum diameter of tumours ranged from 2 cm to 16 cm. Discontinuity of the hepatic surface was seen in 11 cases. In eight cases, CT images during the arterial phase showed a non-enhancing low attenuating lesion with focal discontinuity and peripheral rim enhancement. Seven cases showed separation of tumour content from the peripheral enhancing rim and intraperitoneal rupture of tumour content into the perihepatic space. Because of the similar appearance to an enucleated orbital globe with remaining sclera, this was termed the "enucleation sign". As well as ruptured masses, 10 cases with non-ruptured masses also showed a non-enhancing low attenuating pattern. Seven cases showed a haematoma with high attenuation around the ruptured mass. The peripheral location, protruding contour, discontinuity of the hepatic surface and surrounding haematoma are helpful signs in the diagnosis of ruptured HCC. The "enucleation sign" may be a characteristic finding in ruptured HCC.


    Introduction
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 
Approximately 10% of hepatocellular carcinomas (HCCs) undergo spontaneous rupture [1]. Ruptured HCC is usually fatal, especially in patients with underlying liver cirrhosis who may have severe coagulation deficiencies, because surgical treatment or management of bleeding is difficult in most cases.

Acutely ruptured HCC usually requires emergency treatment owing to the high mortality, and early diagnosis is therefore essential. Diagnosis of ruptured HCC is easy if the patient is known to have HCC. Early detection of ruptured HCC is sometimes difficult when CT is the initial study and there is no known history of HCC.

Although there have been reports of CT findings in ruptured HCC [26], there is a lack of reports regarding the morphological changes of the tumour mass on helical CT. We present experience in 12 cases of HCC that underwent helical CT.


    Materials and methods
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 
HCC was diagnosed in 698 consecutive patients within our institution from 1993 to 1998 on the basis of CT, ultrasound, angiography, MRI, {alpha}-feto protein serum level or the results of biopsy or surgery. Rupture of the HCC developed in 54 of these patients. This study included 12 cases undergoing helical CT among these 54 cases. All patients were male, with a mean age of 53 years (range 30–69 years). All cases were histopathologically confirmed by ultrosound-guided fine needle aspiration biopsy (n=10) or surgery (n=2). Helical CT was obtained within a day of the onset of symptoms. Symptoms were sudden onset of abdominal distention, with abdominal pain in seven cases, diffuse abdominal discomfort in two cases and pallor with sweating in three cases. All patients underwent helical CT (Somatom Plus 4 or Somatom 3; Siemens, Erlangen, Germany) with 8 mm slice thickness, 8 mm s-1 table movement and 8 mm reconstruction interval. A bolus injection (3 ml s-1) of 150 ml non-ionic contrast medium (Optiray 320; Mallinckrodt Medical, Quebec, Canada) was given. Images of arterial (25–30 s after injection), portal (65–70 s after injection) and delayed phases (110–120 s after injection) were obtained. CT images were available before and after rupture of the tumour in four cases. The interval between CT before and after rupture was 6 days, 17 days, 28 days and 6 months in these four patients. In the remainder (n=8), rupture of the HCC was found on the initial CT without a history of liver cirrhosis or HCC. Emergency angiography and embolisation were performed in seven cases. Two cases underwent emergency surgery for simple wedge resection and bleeding control. Three cases received conservative treatment.

Three radiologists analysed the CT findings by consensus in regard to the tumour's location, size and contour protrusion, the appearance of the mass, the enhancement pattern, multiplicity and surrounding secondary changes.


    Results
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 
All ruptured tumours were located at the periphery of the liver and had a protruding contour. The maximum diameter of tumours ranged from 2 cm to 16 cm (mean±1 SD=7.8±3.93 cm). Discontinuity of the hepatic surface was noted in 11 cases (91.7%). In 8 cases (66.7%), CT images during the arterial phase showed a non-enhancing low attenuating lesion with focal discontinuity. Definite peripheral rim enhancements were obvious in six cases and subtle in two cases. Seven of eight cases showed separation of the tumour content from the peripheral enhancing rim and intraperitoneal rupture of tumour content into the perihepatic space. Because of its similar appearance to an enucleated orbital globe with remaining sclera, this was termed the "enucleation sign" (Figures 1Go and 2Go). During the delayed phase, peripheral rim enhancement became isodense or slightly hyperdense relative to liver parenchyma in seven cases (Figure 3Go).



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Figure 1. 64-year-old man with ruptured hepatocellular carcinoma (HCC) during follow-up study. (a) Arterial phase CT shows a well enhancing mass with protruding contour in the right hepatic dome (arrows). Marked ascites present. (b) After 28 days, the tumour contents have ruptured beyond the hepatic surface, with subtle rim enhancement (enucleation sign). Marginal discontinuity is noted (arrows). Newly developed low attenuating lesions are noted on the posterior aspect of the ruptured HCC.

 


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Figure 2. 69-year-old man with ruptured hepatocellular carcinoma (HCC) during follow-up study. (a) Delayed phase CT shows a large mass with protruding contour in the right hepatic dome. Marginal disruption is suspected (arrows). Definite signs of HCC rupture were not found on physical examination. (b) 6 days later, CT was repeated because of abdominal distention with abdominal pain. Tumour rupture into the intraperitoneal space is seen on portal phase CT. Markedly decreased attenuation is noted within the lesion.

 


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Figure 3. 56-year-old man with ruptured hepatocellular carcinoma on initial study. (a) Arterial phase CT shows densely enhancing peripheral rim (arrowheads) and mildly enhancing tumour in the hepatic angle. The tumour is separated with rim enhancement by the fluid density. Marginal break is noted (arrows). (b) On delayed phase at the same level, tumour enhancement has subtly reduced. The enhancing rim has become slightly hyperdense relative to liver parenchyma (arrowheads).

 
10 cases (83.3%) had multiple masses in different hepatic segments. Not only ruptured masses but also non-ruptured masses showed a non-enhancing low attenuating pattern. In particular, four cases had solid components on CT before rupture but the masses were converted to a non-enhancing low attenuating pattern after rupture (Figure 4Go). These non-enhancing low attenuating lesions were mildly enhanced on CT during the delayed phase and showed a solid component on ultrasound. In four cases, some of the hepatic parenchymal masses that were not definite on CT before rupture were newly detected as non-enhancing low attenuating lesions after rupture (Figure 4Go).



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Figure 4. 55-year-old man with ruptured hepatocellular carcinoma during follow-up study. (a) Portal phase CT shows multiple ill defined, low attenuating lesions with solid components in the right and caudate lobe. A nodular high density in the caudate lobe (arrow) represents lipiodol uptake by the lesion during previous transarterial injection. (b) After 17 days, almost all the lesions have become non-enhancing low attenuating, and further low attenuating nodular lesions are now detected (arrows). The non-enhancing low attenuating lesions are larger in area and have more distinct margins than the initial detected lesions (arrowheads). A ruptured mass is not suspected.

 
Seven cases had a haematoma with high attenuation around the ruptured mass, representing acute haemorrhage. None of the patients were haemodynamically unstable or shocked at the time of the CT examination.


    Discussion
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 
HCC sometimes grows expansively when the tumour has an encompassing fibrous capsule. It is believed that disruption of the tumour surface or tearing of a feeding artery causes rupture of a HCC, leading to haemoperitoneum and hypovolaemic shock [7]. In such cases, pressure within the tumour may be relatively high and predispose to rupture. When HCC protrudes beyond the original liver contour, the tumour may rupture more readily than one with surrounding normal parenchyma. A feeding artery may rupture in conjunction with development of ascites. Ascites in the space between the liver and the parietal peritoneum may cause separation of these structures, leading to tearing of adherent surfaces or rupture of an adjacent artery.

HCC typically has a hypervascular pattern, and its necrosis or vascular invasion with obstruction of venous flow can lead to intraperitoneal haemorrhage from rupture of the tumour. This can be life threatening, particularly in the patient with underlying liver cirrhosis and severe coagulation deficiencies.

Chearanai et al [8] suggested that during the usual course of tumour growth, some precipitating factors, inducing rupture and/or haemorrhage, could occur within the tumour tissue. Intraperitoneal haemorrhage would then result if the tumour was located under the capsule. Coagulopathy played an important role in causing haemorrhage within the tumour nodule, resulting in increased pressure followed by rupture of the nodule. Spontaneous rupture may occur after minimal trauma in an apparently healthy liver. This event could occur more frequently in patients with primary HCC in which there were areas of necrosis and when the tissue is more friable. It was also stated that the site of bleeding was tumour extension to the right diaphragm, and that respiratory movement might cause haemorrhage from the vascular and friable mass.

CT is useful in detecting HCC rupture by showing the tumour, by defining the extent of the haematoma, and by showing serial density changes with the age of the haematoma [5]. Kanematsu et al [6] believe that the peripheral location with a protruding contour is helpful in the prediction of HCC rupture, findings that were confirmed in this study. However, they also considered that the size of the tumour was a contributing factor, although a third of our patients had tumours less than 5 cm in size.

We describe the new finding of the "enucleation sign", which is owing to a non-enhancing low attenuating lesion with peripheral rim enhancement and focal discontinuity of the hepatic surface during the arterial phase. We consider that the peripheral rim enhancement does not represent a true lesion since it became isodense or slightly hyperdense relative to liver parenchyma during the delayed phase. It is presumed to be compressed normal parenchyma, although we have no histopathological correlation. We believe that the "enucleation sign" is a valuable additional sign in ruptured HCC.

Not only ruptured tumours but also non-ruptured ones were converted to a non-enhancing low attenuating pattern after rupture in our study. In addition, some of the non-enhancing low attenuating lesions that were not definite on CT before rupture were more conspicuous after rupture in four cases (Figure 4Go). This phenomenon may be because of loss of homeostatic function within the HCC itself during hypovolaemic shock, resulting in compensatory arterial vasoconstriction and preservation of venous blood flow. This may lead to ischaemic changes within the HCC. Further study would be needed to elucidate this phenomenon.

In conclusion, the peripheral location, protrusion of the contour, discontinuity of the hepatic surface, and the surrounding haematoma with high attenuation on CT are very helpful signs in the diagnosis of ruptured HCC. The enucleation sign could be specific for ruptured HCC.


    Footnotes
 
This study was supported in part by the Clinical Research Fund of the College of Medicine, The Catholic University of Korea Back

Received for publication July 13, 2000. Revision received October 12, 2000. Accepted for publication October 20, 2000.


    References
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 

  1. Primary liver cancer in Japan. Sixth report. The Liver Cancer Study Group of Japan. Cancer 1987;60:1400–11[Medline]
  2. Cates JD, Thorsen MK, Foley WD, Lawson TL. CT diagnosis of massive hemorrhage from hepatocellular carcinoma. J Comput Assist Tomogr 1987;11:81–2.[Medline]
  3. Nagata Y, Kohno S, Saga T, Ohajima K, Hosono M, Tamaki M, et al. CT manifestations of a ruptured hepatic tumor after transcatheter arterial embolization. Comput Med Imaging Graph 1989;13:419–22.[Medline]
  4. Pombo F, Arrojo L, Perez-Fontan J. Haemoperitoneum secondary to spontaneous rupture of hepatocellular carcinoma: CT diagnosis. Clin Radiol 1991;43:321–2.[Medline]
  5. Kim PN, Kim IY, Bae WK, Lee BH. Computed tomographic findings of ruptured hepatic malignancy. Gastrointest Radiol 1991;16:334–6.[Medline]
  6. Kanematsu M, Imaeda T, Yamawaki Y, Seki M, Goto H, Sone Y, et al. Rupture of hepatocellular carcinoma: predictive value of CT findings. AJR 1992;158:1247–50.[Abstract/Free Full Text]
  7. Okuda K, Nakashima T. Primary carcinoma of the liver. In: Berk JE, editor. Bockus gastroenterology (4th edn), Vol. 5. Philadelphia, PA: WB Saunders, 1985:3315–76.
  8. Chearanai O, Plengvanit U, Asavanich C, Damrongsak D, Sindhvananda K, Boonyapisit S. Spontaneous rupture of primary hepatoma: report of 63 cases with particular reference to the pathogenesis and rationale treatment by hepatic artery ligation. Cancer 1983;51:1532–6.[Medline]



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