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Congenital extrahepatic portocaval shunt (Abernethy type 2), huge liver mass, and patent ductus arteriosus—a case report of its rare clinical presentation in a young girl
Congenital Extrahepatic Portocaval Shunt (Abernethy Type 2), Huge Liver Mass, and Patent Ductus A r t e r i o s u s m A Case Report of Its Rare Clinical Presentation in a Young Girl By Yutaka Kanamori, Kohei Hashizume, Yoshihiro Kitano, Masahiko Sugiyama, Toru Motoi, and Tsuyoshi Tange
Tokyo, Japan
The authors report a case of congenital extrahepatic portocaval shunt with a hypoplastic portal vein. This type of shunt is called an A b e r n e t h y type2 shunt, w h e r e the portal vein and inferior vena cava are connected side to side, and a hypoplastic portal f l o w exists in the liver parenchyma. This case of a y o u n g girl is complicated with a cardiac a n o m a l y and a large hyperplastic nodule in the liver. This p h e n o t y p e usually is seen in the A b e r n e t h y type1 shunt, which is a side-to-end shunt with the complete absence of a portal vein. In this context, the current case is v e r y unique in its clinical mani-
ONGENITAL extrahepatic portocaval shunts are classified into 2 types1-3: one is congenital absence of the portal vein (side-to-end anastomosis, Abernethy type 1 shunt) and the other is a shunt composed of a side-to-side anastomosis with hypoplastic portal blood flow into the hepatic parenchyma (Abernethy type 2 shunt). Each type of shunt is associated with a unique clinical presentation: 32 cases of type 1 shunts have been reported, 4,5 which usually are seen in girls and often complicated with cardiac anomalies and a hepatic mass including hepatoblastoma, hepatocellular carcinoma, focal nodular hyperplasia (FNH), and hepatocellular adenoma. Type 2 shunts usually are acquired in cirrhotic livers, and the congenital extrahepatic type is far less common. 2,3 Type 2 congenital extrahepatic shunts are often seen in men and seldom complicated with other anomalies. 2 This type of shunt tends to be diagnosed as the cause of hepatic encephalopathy and severe liver dysfunction. In this report, we present a girl who had an Abernethy type 2 congenital portocaval shunt with a huge hepatic mass and patent ductus arteriosus (PDA). She also showed brain atrophy, which may have been caused by the long standing portosystemic shunt after birth. The shunt type itself should be classified as Abernethy type 2, but her clinical phenotype should be inclined to be an Abernethy type 1 shunt. This phenotype of the portocaval shunt was not reported before to our knowledge, and the case is suggestive for the etiology and treatment of the portocaval shunt itself and the hyperplastic nodule in the liver.
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Journal of Pediatric Surgery, Vol 38, No 4 (April), 2003:E15
festation, and this p h e n o t y p e has never been reported. Therefore, it is important to speculate the etiology and treatment of this kind of a b n o r m a l i t y and its associated hepatic mass. J Pediatr Surg 38:E15. Copyright 2003, Elsevier Science (USA). All rights reserved.
INDEX WORDS: Congenital extrahepatic portocaval shunt, hyperplastic nodule of the liver.
CASE REPORT The patient was a 4-yeax-old girl and referred to another hospital first for examination and treatment of a large liver mass. She had no history of the disease and was well in her general condition without anemia and jaundice. Telangiectasia was seen on her cheek. Blood tests at admission showed moderate liver-dysfunction and slight elevation of ammonia level: AST, 190 IU/L; ALT, 160 IU/L; 7-GTP, 80 IU/L; ALP, 776 IU/L; ammonia level, 59/xg/dL. Computed tomography (CT) showed a huge hepatic mass (about 9 cm in diameter) that originated from the anterior upper lobe of the liver (segment 8; Fig la). It was slightly enhanced heterogenously, and reticular low-density areas were seen after the venous infusion of contrast medium. The central scar and the so-called "wheellike appearance" of the abnormal artery were not seen (Fig lb). The first diagnosis was hemangioendothelioma of the liver. A small amount of radiation on the mass was attempted, and steroids were administered, but the size of the mass did not decrease. The patient was transferred to our hospital for surgical resection of the liver mass. In our hospital, a computed tomography (CT) scan was taken again, and the liver mass was suspected to be an adenoma or focal nodular hyperplasia (FNH). At the same time, an abnormal connection between the portal vein and inferior vena cava was detected, which was ascertained by angiography performed later. The catheter was inserted into superior mesenteric vein via the inferior vena cava, and retrograde superior mesenteric venogram showed a shunt between the portal vein and inferior vena cava (Fig lc). The venogram also showed a narrowed and tortuous portal vein (Fig lc). A huge hepatic mass was not supplied by portal blood flow and therefore detected by defect of contrast medium
From the Department of Pediatric Surgery and Department of Pathology, Tokyo University Hospital, Tokyo, Japan. Address reprint requests to Yutaka Kanamori, Department of Pediatric Surgery, Tokyo University Hospital, 7-3-1 Hongo Bunkyo-ku Tokyo 113-8655, Japan. Copyright 2003, Elsevier Science (USA). All rights reserved. 1531-5037/03/3804-0039530. 00/0 doi: 10.1053/jpsu.2003.50153
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Fig 1. A large hepatic mass and portocaval shunt with hypoplastic portal vein. (a) Computed tomogram (plain); a large hepatic mass sited in segment 8 of the liver. Its diameter was about 9 cm, and the mass was seen to be slightly low-density and heterogenous. (b) Computed tomogram (enhanced by contrast medium); the mass was heterogenously enhanced and there was an irregular and reticular low-density pattern seen in the mass. (c) Superior mesenteric venogram (early phase); a catheter was inserted into the superior mesenteric vein from the inferior vena cava via a large shunt vessel. Early phase of the selective retrograde angiogram showed both the inferior vena cava and portal vein. Portal vein was oppressed by the large hepatic mass and narrowed and tortuous. (d) Superior mesenteric venogram (late phase); a large hepatic mass was detected as filling defect of contrast medium and the volume of the liver that was enhanced by contrast medium was very small.
(Fig ld). We concluded that the patient had an extrahepatic side-to-side portocaval shunt (Abernethy type 2 shunt), and the huge liver mass was suspected to be hyperplastic changes by histologic examination of the specimen taken by needle biopsy. Echocardiography results showed that she had a patent ductus arteriosus. The patient underwent a lapaxotomy. The color of the liver was light pink (Fig 2a), and close examination of the hepatic porta showed that the splenic vein and superior mesenteric vein joined to form a common trunk, and it ran into the inferior vena cava of the retrohepatic portion from the left side of the hepatoduodenal ligament. The large liver mass was biopsied. Under monitoring, the pressure of mesenteric vein we first exposed the shunt vessel thoroughly, and the blood flow through the shunt vessel was transiently interrupted by small clump. In the meantime, the mesenteric venous pressure rose from 17 to 21 mm Hg, but the liver became swollen, and macroscopically the intestinal congestion was not observed at all. From these findings we concluded that portal hypertension caused by the shunt closure is not fatal in this case, and this large shunt vessel could be ligated safely. We closed the shunt vessel by triple ligation (Fig 2b). We did not consider partial occlusion of the shunt (eg, staged operation for shunt closure) because the shunt vessel was very large, had a very thin wall, and the site was behind the
liver. We judged it very difficult and risky to deal with this shunt vessel later. Postoperative refractory ascites caused by transient portal hypertension (Fig 3a) was seen and treated with reinfusion of the concentrated ascites into the systemic circulation five times. The fluid retention in the peritoneal cavity subsided in 2 months. Four months after the operation, 3 significant findings were apparent in late-phased celiac arteriography: (1) significant collateral flow was detected in the hepatoduodenal ligament, (2) the left gastric vein was dilated, and (3) back blood flow from splenic vein into the inferior mesenteric vein was seen (Fig 3b). The size of the mass has decreased gradually after the operation, and at 2 years after the operation it is about 4 cm in diameter. Also, the boundary between the mass and liver parenchyma has become ambiguous (Fig 3c). Liver functional scintigraphy taken after one year from the lapaxotomy showed much improvement of the liver functions (data not shown). The patient also had mild brain atrophy before the operation. This atrophy reflected the brain damage from the long-standing portosystemic shunt after birth. We had expected that further brain damage should be avoided after the shunt closure, and this expectation was one
CONGENITAL ABERNETHY SHUNT
17
i Fig 2. Intraoperative findings of the liver. (a) Liver was light pink in color and well-developed lymphatic vessels were seen on the surface. (b) A large shunt vessel was ligated. Hepatoduodenal ligament sited just at the right of this shunt vessel, containing the hypoplastic portal vein.
of the main reasons why we had closed the shunt vessel. But postoperative portal hypertension resulted in the formation of a neo portosystemic shunt, and the atrophy of the brain has continued when examined 4 months after the operation by magnetic resonance imaging (Fig 3d).
Hepatocytes in the nodule were histologically hyperplastic and had no atypia (Fig 4a). Distorted portal areas with septal fibrosis were seen within the nodule, which was containing intact interlobular arteries and bile ducts. But the portal veins were rarely detected and hypoplastic,
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Fig 3. Postoperative examinations. (a) One month after the operation; CT showed massive ascites in the peritoneal cavity and the hepatic mass slightly decreased in its size. (b) Four months after the operation; late phase celiac arteriogram showed that the blood flow from the splenic vein drained into the inferior mesenteric vein and left gastric vein is dilated. A t the same time the hepatic mass became small. Splenomegaly was apparent. (c) Two years after the operation: CT showed a low-density and ambiguous edged nodule, and its diameter was about 4 cm. The normal liver volume expanded dramatically. (d) Six months after the operation; magnetic resonance imaging showed mild brain atrophy. Dilated lateral ventricles and sulci were shown compared with those of age-corresponding children.
18
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Fig 4. Histologic findings of the hepatic nodule (H&E stain). (a) The hepatic nodule (original magnification x 100); fine septal fibrosis were seen, which ran parallel, not radiated, and did not contain numerous blood vessels as seen in FNH (arrows). Portal area was atrophic. Hepatocytes were hyperplastic but had no atypia. (b) The portal area of the hepatic nodule (original magnification x400); hepatic arteries and bile ducts were apparently normal. Portal vessels were also detected, but their number was very few. Instead, dilated abnormal capillaries were often seen (arrows) in this area. (c) The portal area outside the hepatic nodule (original magnification x200); hepatic arteries and bile ducts were normal in its size and distribution, but the portal vein was very hypoplastic and seldom detected as one vessel containing blood. Fatty degeneration and fibrous changes were not detected.
and dilated a b n o r m a l capillary vessels w e r e seen in portal areas (Fig 4b, a r r o w s ) . T h e s e features m i m i c k e d t h o s e of F N H b u t w e r e not c o m p a t ible in the f o l l o w i n g points: a n o m a l o u s arteries w e r e not d e t e c t e d in portal areas; the n o d u l e h a d no central scar; fibrous s e p t a seen in the m a s s did not radiate f r o m the central scar b u t s h o w e d l a m i n a r a r r a n g e ment, a n d t h e y w e r e finer t h a n t h o s e seen in F N H (Fig 4a, a r r o w s ) . C o n s i d e r i n g t h e s e findings, final histologic diagnosis of the n o d u l e w a s a kind o f h y p e r p l a s t i c nodule of the liver. L i v e r outside the n o d u l e s h o w e d a l m o s t n o r m a l h i s t o l o g y w i t h the e x c e p t i o n o f the portal h y p o p l a s i a (Fig 4c).
DISCUSSION
We reported the rare case of an extrahepatic portocaval shunt, Abernethy type 2 abnormality. According to our knowledge, 32 cases of Abernethy type 1 extrahepatic portocaval shunt have been reported in the world. 4,5 This type of anomaly was usually called congenital absence of the portal vein because there was no portal blood flow into the hepatic parenchyma. This anomaly occurs mostly in girls and is well known to be complicated with several other anomalies such as cardiac anomalies and hepatic tumors or hyperplastic nodules in the liver. 2-4 However, Abernethy type 2 congenital extrahepatic portocaval shunts are more uncommon, and just 5 cases have been reported. 2 They often are seen in boys and are rarely complicated with other anomalies. The clinical manifestation of our case is quite unusual in that the patient was a girl and complicated with PDA and a large hepatic nodule in spite of the Abernethy type 2 portocaval shunt. This case suggests that the classification of Abernethy type 1 and 2 shunts is not so meaningful, and they just belong to one category of developmental anomalies in the portal vein. This idea seems to be acceptable because the complicated development of
the portal vein from the vitelline duct could cause various patterns of anomalies, and there could be a wide range of the phenotype in portocaval shunts¢ In the future, more cases of portocaval shunts will be diagnosed with the progress of diagnostic devices and techniques, and the clinical entity of a portocaval shunt should be defined more clearly. We closed the shunt vessel by a surgical approach, and the pressure of the mesenteric vein rose from 17 mm Hg to 21 mm Hg. After closing the shunt, refractory ascites continued for about 2 months, and a new portosystemic shunt via collateral veins around the hepatoduodenal ligament and inferior mesenteric vein were finally formed. Congenital hypoplasia of the portal vessel bed in the liver caused the result. Barsky et al reported that surgical reconstruction of the port systemic shunt was needed after the closing of patent ductus venosus in one adult patient because of the resultant severe portal hypertension. 7 There may be no clear criteria in which portosystemic shunts could be closed without resulting fatal portal hypertension in the patients with a portosystemic shunt. Of course, in Abernethy typel shunts, it is necessary that the hypoplastic liver be replaced by a new liver for the patients to survive by connecting artery, portal vein, and choledocus. 5,8 In the current case, a huge liver nodule was diagnosed as a hyperplastic nodule, and was not compatible with FNH, but the etiology of the hyperplasia might be the same. Furthermore, these findings mimic the lesion named partial nodular transformation, which is not defined clearly as one pathologic entity yet. 9-11 Also, FNH was detected in patients with patent ductus venosus,
CONGENITAL ABERNETHY SHUNT
19
which is another type of portosystemic shunt with decreased portal blood flow. 12 Some investigators explain that the hyperplastic lesions in the liver could be brought by the predominance of the arterial blood supply in portal agenesis or portal hypoplasia.l° However, Starzl et all3 raised the possibility that the hyperplasia may be caused by the increase of the hepatic growth factors such as insulin and glucagon in the serum brought by the massive portosystemic shunt. Of course, some other hepatotrophic factors, such as hepatocyte growth factor, might also relate closely to these hypertrophic nodular formations. In our case, there should be some portal flow to the liver parenchyma judging from the result of the angiogram taken before the shunt was closed (Fig lc and d). Even in such conditions, the hyperplastic nodule resembling FNH did grow, so portal hypo- or nonperfusion in the liver parenchyma seen in Abernethy type 1 and type 2 shunts may have the important causality of the massive nodule in the liver. Nonetheless, the etiology of these hyperplastic nodular lesions in the liver remains to be clearly defined. Hepatoblastoma, hepatocellular carcinoma, and hepatocellular adenoma also were complicated with some cases of congenital absence of the portal vein. 2-5,8 Considering these facts from the pathologic point of view, hyperplastic change and tumor development of the liver cell could be understood on the same pathologic line. Hyperplastic cells may undergo some type of genetic transformation in the long course and form neoplastic nodules. Barton et al/reported the case of a type 1 shunt that was complicated with FNH at first, and 2 years later it was replaced by hepatoblastoma. In this case, it is not clear that the hepatoblastoma originated just from the FNH lesion, but the FNH lesion was completely replaced by the tumor. So it is more likely that the tumor cell originated from the hyperplastic cells in the liver. Genetic mutation of 13-catenin has recently been considered one of the most important mutations in the tumorigenesis of hepatoblastoma 14 and liver cell adenoma. 15 These mutations of the 13-catenin-encoding gene might occur
in the hyperplastic hepatic cells in patients with congenital absence of the portal vein caused by some change of microenvironment in the liver. In the clinical aspect, it also is an important fact that this hyperplastic nodule has become smaller after the shunt closure. The nodule decreased by one half in its diameter in the 2-year course after surgery, and its edge gradually became unclear (Fig 3c). Recently, it is reported that half of all FNH decreased in size or disappeared in the natural course, 1~ so it seems unnecessary to resect the hyperplastic nodule seen in patients with a portocaval shunt. Of course, it is necessary to diagnose by the several imaging techniques and biopsy whether the hepatic mass is truly a tumor or hyperplastic nodule before the shunt closure. True tumors should be resected. If the mass becomes larger after the shunt closure, re-estimation of the mass characteristics with biopsy is necessary. However, there are no reports of a hyperplastic nodule that acquired tumor characters after shunt closure. Furthermore, Raskin et a117 pointed out the risk of progressive brain damage caused in the Abernethy typel shunt. So liver transplantation should be considered if the brain damage is judged to be severe by CT or MRI examination. In this context, the prognosis of the patient is not yet defined, because she has mild brain atrophy perhaps caused by the long-standing portosystemic shunt, and now there is a new portosystemic shunt that occurred because of the inadequate portal vessel bed in the liver. She may need a liver transplant in the future. In this case we selected shunt closure as first treatment because hypoplastic portal vein was seen, and test clumping of the shunt vessel resulted in the swelling of liver parenchyme, and no congestion of the intestine was observed. But the pressure of mesenteric vein rose from 17 to 21 mm Hg, and refractory portal hypertension continued after the surgery. In the future we should be more discreet in choosing the treatment for this kind of shunt, shunt ligation, or liver transplant even if the portal vein is patent and shunt closure is not fatal.
REFERENCES 1. Abernethy J: Account of two instances of uncommon formation in the viscera of the human body. Philos Trans R Soc Lond (Biol) 83:59-66, 1793 2. Howard ER, Davenport M: Congenital extraJaepatic portocaval shunts--The Abernethy malformation. J Pediatr Surg 32:494-497, 1997 3. Morgan G, Superina R: Congenital absence of the portal vein: Two cases and a proposed classification system for portasystemic vascular anomalies. J Pediatr Surg 29:1239-1241, 1994 4. Kinjo T, Aoki H, Sunagawa H, et al: Congenital absence of the portal vein associated with focal nodular hyperplasia of the liver and congenital choledochal cyst: A case report. J Pediatr Surg 36:622-625, 2001
5. ShinkaJ M, Ohhama Y, Nishi T, et al: Congenital absence of the portal vein and role of liver transplantation in children. J Pediatr Surg 36:1026-1031, 2001 6. Bellah RD, Teele RL: Anomalous portal venous connection to the suprahepatic vena cava: Sonographic demonstration. Pediatr Radiol 20:115-117, 1989 7. Barsky MF, Rankin RN, Wall WJ, et al: Patent ductus venosus: Problems in assessment and management. Can J Surg 32:271-273, 1989 8. Barton JW, Keller MS: Liver transplantation for hepatoblastoma in a child with congenital absence of the portal vein. Ped Radiol 20:113-114, 1989 9. Sherlock S, Feldman CA, Moran B, et al: Partial nodular trans-
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formation of the liver with portal hypertension. Am J Med 40:195-203, 1966 10. Nakanuma Y: Non-neoplastic nodular lesions in the liver. Pathol Int 45:703-714, 1995 11. Kondo F: Benign nodular hepatocellular lesions caused by abnormal hepatic circulation: Etiological analysis and introduction of a new concept. J Gastroenterol Hepatol 16:1319-1328, 2001 12. Jacob S, Farr G, Vun DD, et al: Hepatic manifestations of familial patent ductus venosus in adults. Gut 45:442-445, 1999 13. Starzl TE, Francavilla A, Halgrimson CG, et al: The origin, hormonal nature, and action of hepatatrophic substances in portal venous flow. Surg Gynecol Obstet 137:179-199, 1973
KANAMORI ET AL
14. Koch A, Denlhaus D, Pietsch T, et al: Childhood hepatoblastomas frequently carry a mutated degradation targeting box of the /3-catenin gene. Cancer Res 59:269-273, 1999 15. Takayasu H, Motoi T, Kanamori Y, et al: Two case report of childhood liver cell adenomas harboring/3-catenin abnormalities. Human Pathol 33:852-855, 2002 16. Di-Stasi M, Caturelli E, De-Sio I, et al: Natural history of focal nodular hyperplasia of the liver: An ultrasound study. J Clin Ultrasound 24:345-350, 1996 17. Raskin NH, Bredesen J, Ehrenfeld WK, et al: Periodic confusion caused by congenital extraJaepatic portacaval shunt. Neurology 34:666669, 1984
Tokyo, Japan
The authors report a case of congenital extrahepatic portocaval shunt with a hypoplastic portal vein. This type of shunt is called an A b e r n e t h y type2 shunt, w h e r e the portal vein and inferior vena cava are connected side to side, and a hypoplastic portal f l o w exists in the liver parenchyma. This case of a y o u n g girl is complicated with a cardiac a n o m a l y and a large hyperplastic nodule in the liver. This p h e n o t y p e usually is seen in the A b e r n e t h y type1 shunt, which is a side-to-end shunt with the complete absence of a portal vein. In this context, the current case is v e r y unique in its clinical mani-
ONGENITAL extrahepatic portocaval shunts are classified into 2 types1-3: one is congenital absence of the portal vein (side-to-end anastomosis, Abernethy type 1 shunt) and the other is a shunt composed of a side-to-side anastomosis with hypoplastic portal blood flow into the hepatic parenchyma (Abernethy type 2 shunt). Each type of shunt is associated with a unique clinical presentation: 32 cases of type 1 shunts have been reported, 4,5 which usually are seen in girls and often complicated with cardiac anomalies and a hepatic mass including hepatoblastoma, hepatocellular carcinoma, focal nodular hyperplasia (FNH), and hepatocellular adenoma. Type 2 shunts usually are acquired in cirrhotic livers, and the congenital extrahepatic type is far less common. 2,3 Type 2 congenital extrahepatic shunts are often seen in men and seldom complicated with other anomalies. 2 This type of shunt tends to be diagnosed as the cause of hepatic encephalopathy and severe liver dysfunction. In this report, we present a girl who had an Abernethy type 2 congenital portocaval shunt with a huge hepatic mass and patent ductus arteriosus (PDA). She also showed brain atrophy, which may have been caused by the long standing portosystemic shunt after birth. The shunt type itself should be classified as Abernethy type 2, but her clinical phenotype should be inclined to be an Abernethy type 1 shunt. This phenotype of the portocaval shunt was not reported before to our knowledge, and the case is suggestive for the etiology and treatment of the portocaval shunt itself and the hyperplastic nodule in the liver.
C
Journal of Pediatric Surgery, Vol 38, No 4 (April), 2003:E15
festation, and this p h e n o t y p e has never been reported. Therefore, it is important to speculate the etiology and treatment of this kind of a b n o r m a l i t y and its associated hepatic mass. J Pediatr Surg 38:E15. Copyright 2003, Elsevier Science (USA). All rights reserved.
INDEX WORDS: Congenital extrahepatic portocaval shunt, hyperplastic nodule of the liver.
CASE REPORT The patient was a 4-yeax-old girl and referred to another hospital first for examination and treatment of a large liver mass. She had no history of the disease and was well in her general condition without anemia and jaundice. Telangiectasia was seen on her cheek. Blood tests at admission showed moderate liver-dysfunction and slight elevation of ammonia level: AST, 190 IU/L; ALT, 160 IU/L; 7-GTP, 80 IU/L; ALP, 776 IU/L; ammonia level, 59/xg/dL. Computed tomography (CT) showed a huge hepatic mass (about 9 cm in diameter) that originated from the anterior upper lobe of the liver (segment 8; Fig la). It was slightly enhanced heterogenously, and reticular low-density areas were seen after the venous infusion of contrast medium. The central scar and the so-called "wheellike appearance" of the abnormal artery were not seen (Fig lb). The first diagnosis was hemangioendothelioma of the liver. A small amount of radiation on the mass was attempted, and steroids were administered, but the size of the mass did not decrease. The patient was transferred to our hospital for surgical resection of the liver mass. In our hospital, a computed tomography (CT) scan was taken again, and the liver mass was suspected to be an adenoma or focal nodular hyperplasia (FNH). At the same time, an abnormal connection between the portal vein and inferior vena cava was detected, which was ascertained by angiography performed later. The catheter was inserted into superior mesenteric vein via the inferior vena cava, and retrograde superior mesenteric venogram showed a shunt between the portal vein and inferior vena cava (Fig lc). The venogram also showed a narrowed and tortuous portal vein (Fig lc). A huge hepatic mass was not supplied by portal blood flow and therefore detected by defect of contrast medium
From the Department of Pediatric Surgery and Department of Pathology, Tokyo University Hospital, Tokyo, Japan. Address reprint requests to Yutaka Kanamori, Department of Pediatric Surgery, Tokyo University Hospital, 7-3-1 Hongo Bunkyo-ku Tokyo 113-8655, Japan. Copyright 2003, Elsevier Science (USA). All rights reserved. 1531-5037/03/3804-0039530. 00/0 doi: 10.1053/jpsu.2003.50153
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KANAMORI ET AL
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m
Fig 1. A large hepatic mass and portocaval shunt with hypoplastic portal vein. (a) Computed tomogram (plain); a large hepatic mass sited in segment 8 of the liver. Its diameter was about 9 cm, and the mass was seen to be slightly low-density and heterogenous. (b) Computed tomogram (enhanced by contrast medium); the mass was heterogenously enhanced and there was an irregular and reticular low-density pattern seen in the mass. (c) Superior mesenteric venogram (early phase); a catheter was inserted into the superior mesenteric vein from the inferior vena cava via a large shunt vessel. Early phase of the selective retrograde angiogram showed both the inferior vena cava and portal vein. Portal vein was oppressed by the large hepatic mass and narrowed and tortuous. (d) Superior mesenteric venogram (late phase); a large hepatic mass was detected as filling defect of contrast medium and the volume of the liver that was enhanced by contrast medium was very small.
(Fig ld). We concluded that the patient had an extrahepatic side-to-side portocaval shunt (Abernethy type 2 shunt), and the huge liver mass was suspected to be hyperplastic changes by histologic examination of the specimen taken by needle biopsy. Echocardiography results showed that she had a patent ductus arteriosus. The patient underwent a lapaxotomy. The color of the liver was light pink (Fig 2a), and close examination of the hepatic porta showed that the splenic vein and superior mesenteric vein joined to form a common trunk, and it ran into the inferior vena cava of the retrohepatic portion from the left side of the hepatoduodenal ligament. The large liver mass was biopsied. Under monitoring, the pressure of mesenteric vein we first exposed the shunt vessel thoroughly, and the blood flow through the shunt vessel was transiently interrupted by small clump. In the meantime, the mesenteric venous pressure rose from 17 to 21 mm Hg, but the liver became swollen, and macroscopically the intestinal congestion was not observed at all. From these findings we concluded that portal hypertension caused by the shunt closure is not fatal in this case, and this large shunt vessel could be ligated safely. We closed the shunt vessel by triple ligation (Fig 2b). We did not consider partial occlusion of the shunt (eg, staged operation for shunt closure) because the shunt vessel was very large, had a very thin wall, and the site was behind the
liver. We judged it very difficult and risky to deal with this shunt vessel later. Postoperative refractory ascites caused by transient portal hypertension (Fig 3a) was seen and treated with reinfusion of the concentrated ascites into the systemic circulation five times. The fluid retention in the peritoneal cavity subsided in 2 months. Four months after the operation, 3 significant findings were apparent in late-phased celiac arteriography: (1) significant collateral flow was detected in the hepatoduodenal ligament, (2) the left gastric vein was dilated, and (3) back blood flow from splenic vein into the inferior mesenteric vein was seen (Fig 3b). The size of the mass has decreased gradually after the operation, and at 2 years after the operation it is about 4 cm in diameter. Also, the boundary between the mass and liver parenchyma has become ambiguous (Fig 3c). Liver functional scintigraphy taken after one year from the lapaxotomy showed much improvement of the liver functions (data not shown). The patient also had mild brain atrophy before the operation. This atrophy reflected the brain damage from the long-standing portosystemic shunt after birth. We had expected that further brain damage should be avoided after the shunt closure, and this expectation was one
CONGENITAL ABERNETHY SHUNT
17
i Fig 2. Intraoperative findings of the liver. (a) Liver was light pink in color and well-developed lymphatic vessels were seen on the surface. (b) A large shunt vessel was ligated. Hepatoduodenal ligament sited just at the right of this shunt vessel, containing the hypoplastic portal vein.
of the main reasons why we had closed the shunt vessel. But postoperative portal hypertension resulted in the formation of a neo portosystemic shunt, and the atrophy of the brain has continued when examined 4 months after the operation by magnetic resonance imaging (Fig 3d).
Hepatocytes in the nodule were histologically hyperplastic and had no atypia (Fig 4a). Distorted portal areas with septal fibrosis were seen within the nodule, which was containing intact interlobular arteries and bile ducts. But the portal veins were rarely detected and hypoplastic,
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Fig 3. Postoperative examinations. (a) One month after the operation; CT showed massive ascites in the peritoneal cavity and the hepatic mass slightly decreased in its size. (b) Four months after the operation; late phase celiac arteriogram showed that the blood flow from the splenic vein drained into the inferior mesenteric vein and left gastric vein is dilated. A t the same time the hepatic mass became small. Splenomegaly was apparent. (c) Two years after the operation: CT showed a low-density and ambiguous edged nodule, and its diameter was about 4 cm. The normal liver volume expanded dramatically. (d) Six months after the operation; magnetic resonance imaging showed mild brain atrophy. Dilated lateral ventricles and sulci were shown compared with those of age-corresponding children.
18
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Fig 4. Histologic findings of the hepatic nodule (H&E stain). (a) The hepatic nodule (original magnification x 100); fine septal fibrosis were seen, which ran parallel, not radiated, and did not contain numerous blood vessels as seen in FNH (arrows). Portal area was atrophic. Hepatocytes were hyperplastic but had no atypia. (b) The portal area of the hepatic nodule (original magnification x400); hepatic arteries and bile ducts were apparently normal. Portal vessels were also detected, but their number was very few. Instead, dilated abnormal capillaries were often seen (arrows) in this area. (c) The portal area outside the hepatic nodule (original magnification x200); hepatic arteries and bile ducts were normal in its size and distribution, but the portal vein was very hypoplastic and seldom detected as one vessel containing blood. Fatty degeneration and fibrous changes were not detected.
and dilated a b n o r m a l capillary vessels w e r e seen in portal areas (Fig 4b, a r r o w s ) . T h e s e features m i m i c k e d t h o s e of F N H b u t w e r e not c o m p a t ible in the f o l l o w i n g points: a n o m a l o u s arteries w e r e not d e t e c t e d in portal areas; the n o d u l e h a d no central scar; fibrous s e p t a seen in the m a s s did not radiate f r o m the central scar b u t s h o w e d l a m i n a r a r r a n g e ment, a n d t h e y w e r e finer t h a n t h o s e seen in F N H (Fig 4a, a r r o w s ) . C o n s i d e r i n g t h e s e findings, final histologic diagnosis of the n o d u l e w a s a kind o f h y p e r p l a s t i c nodule of the liver. L i v e r outside the n o d u l e s h o w e d a l m o s t n o r m a l h i s t o l o g y w i t h the e x c e p t i o n o f the portal h y p o p l a s i a (Fig 4c).
DISCUSSION
We reported the rare case of an extrahepatic portocaval shunt, Abernethy type 2 abnormality. According to our knowledge, 32 cases of Abernethy type 1 extrahepatic portocaval shunt have been reported in the world. 4,5 This type of anomaly was usually called congenital absence of the portal vein because there was no portal blood flow into the hepatic parenchyma. This anomaly occurs mostly in girls and is well known to be complicated with several other anomalies such as cardiac anomalies and hepatic tumors or hyperplastic nodules in the liver. 2-4 However, Abernethy type 2 congenital extrahepatic portocaval shunts are more uncommon, and just 5 cases have been reported. 2 They often are seen in boys and are rarely complicated with other anomalies. The clinical manifestation of our case is quite unusual in that the patient was a girl and complicated with PDA and a large hepatic nodule in spite of the Abernethy type 2 portocaval shunt. This case suggests that the classification of Abernethy type 1 and 2 shunts is not so meaningful, and they just belong to one category of developmental anomalies in the portal vein. This idea seems to be acceptable because the complicated development of
the portal vein from the vitelline duct could cause various patterns of anomalies, and there could be a wide range of the phenotype in portocaval shunts¢ In the future, more cases of portocaval shunts will be diagnosed with the progress of diagnostic devices and techniques, and the clinical entity of a portocaval shunt should be defined more clearly. We closed the shunt vessel by a surgical approach, and the pressure of the mesenteric vein rose from 17 mm Hg to 21 mm Hg. After closing the shunt, refractory ascites continued for about 2 months, and a new portosystemic shunt via collateral veins around the hepatoduodenal ligament and inferior mesenteric vein were finally formed. Congenital hypoplasia of the portal vessel bed in the liver caused the result. Barsky et al reported that surgical reconstruction of the port systemic shunt was needed after the closing of patent ductus venosus in one adult patient because of the resultant severe portal hypertension. 7 There may be no clear criteria in which portosystemic shunts could be closed without resulting fatal portal hypertension in the patients with a portosystemic shunt. Of course, in Abernethy typel shunts, it is necessary that the hypoplastic liver be replaced by a new liver for the patients to survive by connecting artery, portal vein, and choledocus. 5,8 In the current case, a huge liver nodule was diagnosed as a hyperplastic nodule, and was not compatible with FNH, but the etiology of the hyperplasia might be the same. Furthermore, these findings mimic the lesion named partial nodular transformation, which is not defined clearly as one pathologic entity yet. 9-11 Also, FNH was detected in patients with patent ductus venosus,
CONGENITAL ABERNETHY SHUNT
19
which is another type of portosystemic shunt with decreased portal blood flow. 12 Some investigators explain that the hyperplastic lesions in the liver could be brought by the predominance of the arterial blood supply in portal agenesis or portal hypoplasia.l° However, Starzl et all3 raised the possibility that the hyperplasia may be caused by the increase of the hepatic growth factors such as insulin and glucagon in the serum brought by the massive portosystemic shunt. Of course, some other hepatotrophic factors, such as hepatocyte growth factor, might also relate closely to these hypertrophic nodular formations. In our case, there should be some portal flow to the liver parenchyma judging from the result of the angiogram taken before the shunt was closed (Fig lc and d). Even in such conditions, the hyperplastic nodule resembling FNH did grow, so portal hypo- or nonperfusion in the liver parenchyma seen in Abernethy type 1 and type 2 shunts may have the important causality of the massive nodule in the liver. Nonetheless, the etiology of these hyperplastic nodular lesions in the liver remains to be clearly defined. Hepatoblastoma, hepatocellular carcinoma, and hepatocellular adenoma also were complicated with some cases of congenital absence of the portal vein. 2-5,8 Considering these facts from the pathologic point of view, hyperplastic change and tumor development of the liver cell could be understood on the same pathologic line. Hyperplastic cells may undergo some type of genetic transformation in the long course and form neoplastic nodules. Barton et al/reported the case of a type 1 shunt that was complicated with FNH at first, and 2 years later it was replaced by hepatoblastoma. In this case, it is not clear that the hepatoblastoma originated just from the FNH lesion, but the FNH lesion was completely replaced by the tumor. So it is more likely that the tumor cell originated from the hyperplastic cells in the liver. Genetic mutation of 13-catenin has recently been considered one of the most important mutations in the tumorigenesis of hepatoblastoma 14 and liver cell adenoma. 15 These mutations of the 13-catenin-encoding gene might occur
in the hyperplastic hepatic cells in patients with congenital absence of the portal vein caused by some change of microenvironment in the liver. In the clinical aspect, it also is an important fact that this hyperplastic nodule has become smaller after the shunt closure. The nodule decreased by one half in its diameter in the 2-year course after surgery, and its edge gradually became unclear (Fig 3c). Recently, it is reported that half of all FNH decreased in size or disappeared in the natural course, 1~ so it seems unnecessary to resect the hyperplastic nodule seen in patients with a portocaval shunt. Of course, it is necessary to diagnose by the several imaging techniques and biopsy whether the hepatic mass is truly a tumor or hyperplastic nodule before the shunt closure. True tumors should be resected. If the mass becomes larger after the shunt closure, re-estimation of the mass characteristics with biopsy is necessary. However, there are no reports of a hyperplastic nodule that acquired tumor characters after shunt closure. Furthermore, Raskin et a117 pointed out the risk of progressive brain damage caused in the Abernethy typel shunt. So liver transplantation should be considered if the brain damage is judged to be severe by CT or MRI examination. In this context, the prognosis of the patient is not yet defined, because she has mild brain atrophy perhaps caused by the long-standing portosystemic shunt, and now there is a new portosystemic shunt that occurred because of the inadequate portal vessel bed in the liver. She may need a liver transplant in the future. In this case we selected shunt closure as first treatment because hypoplastic portal vein was seen, and test clumping of the shunt vessel resulted in the swelling of liver parenchyme, and no congestion of the intestine was observed. But the pressure of mesenteric vein rose from 17 to 21 mm Hg, and refractory portal hypertension continued after the surgery. In the future we should be more discreet in choosing the treatment for this kind of shunt, shunt ligation, or liver transplant even if the portal vein is patent and shunt closure is not fatal.
REFERENCES 1. Abernethy J: Account of two instances of uncommon formation in the viscera of the human body. Philos Trans R Soc Lond (Biol) 83:59-66, 1793 2. Howard ER, Davenport M: Congenital extraJaepatic portocaval shunts--The Abernethy malformation. J Pediatr Surg 32:494-497, 1997 3. Morgan G, Superina R: Congenital absence of the portal vein: Two cases and a proposed classification system for portasystemic vascular anomalies. J Pediatr Surg 29:1239-1241, 1994 4. Kinjo T, Aoki H, Sunagawa H, et al: Congenital absence of the portal vein associated with focal nodular hyperplasia of the liver and congenital choledochal cyst: A case report. J Pediatr Surg 36:622-625, 2001
5. ShinkaJ M, Ohhama Y, Nishi T, et al: Congenital absence of the portal vein and role of liver transplantation in children. J Pediatr Surg 36:1026-1031, 2001 6. Bellah RD, Teele RL: Anomalous portal venous connection to the suprahepatic vena cava: Sonographic demonstration. Pediatr Radiol 20:115-117, 1989 7. Barsky MF, Rankin RN, Wall WJ, et al: Patent ductus venosus: Problems in assessment and management. Can J Surg 32:271-273, 1989 8. Barton JW, Keller MS: Liver transplantation for hepatoblastoma in a child with congenital absence of the portal vein. Ped Radiol 20:113-114, 1989 9. Sherlock S, Feldman CA, Moran B, et al: Partial nodular trans-
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formation of the liver with portal hypertension. Am J Med 40:195-203, 1966 10. Nakanuma Y: Non-neoplastic nodular lesions in the liver. Pathol Int 45:703-714, 1995 11. Kondo F: Benign nodular hepatocellular lesions caused by abnormal hepatic circulation: Etiological analysis and introduction of a new concept. J Gastroenterol Hepatol 16:1319-1328, 2001 12. Jacob S, Farr G, Vun DD, et al: Hepatic manifestations of familial patent ductus venosus in adults. Gut 45:442-445, 1999 13. Starzl TE, Francavilla A, Halgrimson CG, et al: The origin, hormonal nature, and action of hepatatrophic substances in portal venous flow. Surg Gynecol Obstet 137:179-199, 1973
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14. Koch A, Denlhaus D, Pietsch T, et al: Childhood hepatoblastomas frequently carry a mutated degradation targeting box of the /3-catenin gene. Cancer Res 59:269-273, 1999 15. Takayasu H, Motoi T, Kanamori Y, et al: Two case report of childhood liver cell adenomas harboring/3-catenin abnormalities. Human Pathol 33:852-855, 2002 16. Di-Stasi M, Caturelli E, De-Sio I, et al: Natural history of focal nodular hyperplasia of the liver: An ultrasound study. J Clin Ultrasound 24:345-350, 1996 17. Raskin NH, Bredesen J, Ehrenfeld WK, et al: Periodic confusion caused by congenital extraJaepatic portacaval shunt. Neurology 34:666669, 1984