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DOI:10.2214/AJR.05.0795
AJR 2006; 187:W15-W19
© American Roentgen Ray Society


Clinical Observations

Inferior Phrenic Arterial Bleeding After Adult Liver Transplantation: Incidence, Clinical Manifestations, and Predictive CT Features

Seong Sook Hong1, Ah Young Kim1, Hye Jin Kim1, Kyung Won Kim1, Seung Gyu Lee2, Pyo Nyun Kim1, Moon-Gyu Lee1 and Hyun Kwon Ha1

1 Department of Radiology, Asan Medical Center, University of Ulsan College of Medicine, 388-1 Pungnap-dong, Songpa-gu, Seoul, South Korea 138-736.
2 Department of Surgery, Asan Medical Center, University of Ulsan College of Medicine, Seoul, South Korea.

Received May 9, 2005; accepted after revision August 9, 2005.

 
Address correspondence to A. Y. Kim (aykim{at}amc.seoul.kr).

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Abstract
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
OBJECTIVE. The purpose of this study was to determine the incidence of inferior phrenic arterial bleeding after liver transplantation in adult patients and to describe its clinical manifestations and predictive CT features.

CONCLUSION. Inferior phrenic arterial bleeding occurs frequently and is one of the major postoperative bleeding sites in patients undergoing liver transplantation. Awareness of its common clinical manifestations and predictive CT features is essential for prompt diagnosis and treatment of this early vascular complication, and this knowledge can help to avoid unnecessary reoperation and catastrophic hypotension.

Keywords: abdominal imaging • arteriography • CT • liver transplantation


Introduction
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Liver transplantation is currently the treatment of choice for patients with severe acute or chronic liver failure for which no other therapy is available [1, 2]. The combination of recent advances in operative technique, immunosuppression, and organ use has contributed to better posttransplantation outcome. However, there are still significant complications, particularly those of vascular origin, which can lead to graft failure and require reoperation unless prompt treatment is instituted.

Radiologic manifestations and clinical significance of main vascular complications such as hepatic arterial or venous thrombosis are well known in patients undergoing liver transplantation, but there are little data regarding postoperative bleeding in these patients. Unfortunately, we experienced some cases with a sudden decrease of hematocrit and hypotensive crisis in posttransplantation patients, in whom the bleeding originated in an inferior phrenic artery (IPA). If detection of postoperative arterial bleeding is delayed and it is not treated by open surgical vascular revision, it can be fatal [3]. With the increasing number of liver transplantations, the frequency of these complications is likely to increase. For good outcome in these patients, therefore, accurate knowledge and early recognition of these complications are essential. To our knowledge, however, no attention has previously been paid to postoperative IPA bleeding. This study was performed to determine the incidence of IPA bleeding after liver transplantation in adult patients and to describe clinical manifestations and predictive CT features.


Materials and Methods
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Patients
Between March 2000 and December 2003, 568 adult patients underwent liver transplantation in our institution. Written informed consent was obtained from each recipient, and liver transplantation was approved by the ethics committee at our institution. Among these 568 patients, IPA bleeding was confirmed by angiography in 28 patients (6 men and 22 women, ranging in age from 17 to 65 years; mean, 46 years). All patients underwent two-phase MDCT before angiography. The most common underlying disease necessitating liver transplantation was cirrhosis of the liver associated with hepatitis B or C virus (n = 14), followed by hepatocellular carcinoma (n = 11) and acute fulminant hepatitis (n = 3). These 28 recipients underwent one of the following: right-lobe (n = 16), left-lobe (n = 6), dual-graft (i.e., dual lobes from two adult living donors; n = 5), and whole-liver (n = 1) donation. Medical records, including vital signs, blood chemistry, the amount and nature of postoperative drainage in the abdomen, and the number of postoperative days, were reviewed by one coordinator retrospectively to determine clinical manifestations. Our institutional review board approved this retrospective review of images and patients' medical records.

Two-Phase MDCT
CT examinations were performed with an MDCT scanner (LightSpeed QX/i, GE Healthcare; Somatom Sensation 16, Siemens Medical Solutions). Each patient received 150 mL of iopromide (Ultravist 370, Schering), which was injected using a power injector at a flow rate of 3 mL/s through an 18-gauge angiographic catheter inserted into a forearm vein. A baseline unenhanced scan was obtained by using 5-mm collimation and a pitch of 0.75 (LightSpeed QX/i) or a pitch of 1 (Somatom Sensation 16) from the dome of the diaphragm to the lower pole of the right kidney. Arterial phase imaging was initiated within 5 seconds after enhancement of the descending aorta to 100 H, as measured by a bolus-tracking technique (Smart Prep, GE Healthcare). CT parameters for arterial phase scanning included (for LightSpeed QX/i) a pitch of 1.5, collimation of 1.25 mm, and table speed of 15 mm; and (for Somatom Sensation 16) a pitch of 1, collimation of 0.75 mm, and table speed of 12 mm; both using 120 kVp and 250 mA. Portal venous phase imaging was initiated 72 seconds after contrast injection and covered from the dome of the diaphragm to the symphysis pubis.

Image Analysis
CT scans were retrospectively reviewed by two experienced abdominal radiologists. All CT images were evaluated on a PACS monitor to determine the presence of abnormal fluid collection. CT attenuation of the abnormal fluid collection was recorded on noncontrast CT images with the same elliptic region of interest (ROI). Their distributions were recorded, focusing on the hepatic graft.

The size of the IPA and the presence and location of direct extravasation of contrast material were also evaluated. To measure the size of the right and left IPAs, the images were magnified on the PACS monitor and the anteroposterior diameter of the artery was measured just above the level of the right or left adrenal gland. To analyze size differences between both IPAs, Wilcoxon's signed rank test was used with SPSS software (version 10.0.7, SPSS), and p < 0.05 was considered to show a significant difference.


Results
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Active bleeding from the IPA was confirmed on angiography in 28 of 568 patients undergoing liver transplantation (5%); all were bleeding from the right IPA.

Clinical Manifestations
Common clinical manifestations included sudden drainage of fresh blood from the drainage tube (n = 28), an acute decrease of hemoglobin level of more than 2 mg/dL (n = 17; mean = 2.57 ± 1.84 mg/dL), and systemic hypotension (n = 14; mean = 83.57 ± 9.05 mm Hg). Of these, hypotensive crisis requiring blood transfusion of more than four pints per day was noted in nine patients. No patients showed altered liver function tests before or after the onset of bleeding. The onset of these clinical manifestations ranged from 1 to 14 days after liver transplantation (mean = 5 days).

All patients underwent two-phase CT and diagnostic angiography 1 or 2 days after the onset of clinical symptoms. At that time, tentative diagnostic interpretations of the CT scans included acute perihepatic hematoma of unknown origin (n = 14), postoperative perihepatic fluid collection of unknown origin (n = 6), and bleeding from the IPA (n = 8). Bleeding was treated with transcatheter arterial embolization in 23 patients; however, five patients finally underwent surgical revision.

CT Findings
All 28 patients showed abnormal fluid collection in the abdomen (right upper quadrant, n = 26; multiquadrant, n = 2). Two patients with a multiquadrant fluid collection received left-lobe or dual-lobe grafts. In these patients, fluid collection was unevenly distributed in both upper quadrants of the abdomen, although more was found in the right upper quadrant. The most common location of abnormal fluid collection in the right upper quadrant was the posterolateral site of the hepatic graft (n = 11), followed by posteromedial (n = 7), posteroinferior (n = 5), broad posterior (n = 3), and anterolateral (n = 2) sites. Mean CT attenuation of the abnormal fluid collections was 39.5 H, with a range from 3.7 to 78 H. Most patients showed high attenuation (> 25 H) of fluid collection surrounding the hepatic graft, suggesting an acute hematoma (26/28, 93%) [4] (Figs. 1A, 1B, and 1C).


Figure 1
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Fig. 1A 47-year-old woman with a sudden bloody discharge from the drainage tube 4 days after orthotopic liver transplantation. Unenhanced (A) and contrast-enhanced (B) axial CT images show a localized fluid collection with high attenuation (55 H) posteromedial to transplanted liver, suggesting acute hematoma (arrows). All high-attenuation lines on A and B suggest surgical drainage tubes.

 

Figure 2
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Fig. 1B 47-year-old woman with a sudden bloody discharge from the drainage tube 4 days after orthotopic liver transplantation. Unenhanced (A) and contrast-enhanced (B) axial CT images show a localized fluid collection with high attenuation (55 H) posteromedial to transplanted liver, suggesting acute hematoma (arrows). All high-attenuation lines on A and B suggest surgical drainage tubes.

 

Figure 3
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Fig. 1C 47-year-old woman with a sudden bloody discharge from the drainage tube 4 days after orthotopic liver transplantation. Anteroposterior arteriogram of right inferior phrenic artery shows extravasation (arrow) of contrast medium from this artery. This bleeding was controlled by embolization with microcoils.

 
The arterial phase of CT for all 28 patients showed both IPAs (Figs. 1A, 1B, and 1C). The mean diameter of the right IPA was 2.37 ± 0.62 mm, and the mean diameter of the left IPA was 1.74 ± 0.36 mm (p < 0.0001). Direct extravasation of contrast material from the right IPA was noted in 16 patients (57.1%) (Figs. 2A and 2B). This extravasation was well seen in the portal phase (n = 16) rather than in the arterial phase (n = 12) (Figs. 3A and 3B).


Figure 4
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Fig. 2A 25-year-old man with sudden decrease in hemoglobin level 11 days after left-lobe transplantation from a living donor. Contrast-enhanced axial CT scan obtained from hepatic venous phase shows active extravasation of contrast material (arrows) from dilated right inferior phrenic artery (arrowhead). Splenic infarction is also noted.

 

Figure 5
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Fig. 2B 25-year-old man with sudden decrease in hemoglobin level 11 days after left-lobe transplantation from a living donor. Subsequent conventional angiography reveals similar imaging features.

 

Figure 6
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Fig. 3A 45-year-old man with sudden hypotensive crisis 10 days after right-lobe transplantation from a living donor. High-attenuated fluid collection (arrows, A) is noted posterior to transplanted liver on both axial CT images obtained from arterial (A) and portal venous (B) phases. However, active leakage of contrast medium (open arrow, B) from right IPA is seen on portal venous phase alone (B).

 

Figure 7
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Fig. 3B 45-year-old man with sudden hypotensive crisis 10 days after right-lobe transplantation from a living donor. High-attenuated fluid collection (arrows, A) is noted posterior to transplanted liver on both axial CT images obtained from arterial (A) and portal venous (B) phases. However, active leakage of contrast medium (open arrow, B) from right IPA is seen on portal venous phase alone (B).

 

Discussion
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Postoperative vascular complications in liver transplant recipients are estimated to occur in 9-10% with orthotopic grafts [5, 6] and 11.8-26.4% with living donor grafts. Among various vascular complications [7], the incidence of postoperative arterial complications varies between 2% and 25% in the literature [8]. According to recent reports [3, 6], orthotopic liver transplantation results in arterial complications in 6-12.5% of cases. Arterial complications, especially those occurring in the early postoperative period, more frequently require retransplantation or surgical reconstruction [9]. Moreover, a hypotensive crisis caused by uncontrolled active bleeding leads to a catastrophic clinical status.

Our study showed that bleeding from the right IPA occurred with an incidence of 5% within the first 2 weeks after liver transplantation. Lee et al. reported postoperative bleeding in 10 of 198 patients (5.1%) with living donor liver transplantation (presented at the 2002 annual meeting of the Radiological Society of North America). In their study, nonhepatic arterial bleeding was detected more frequently than hepatic arterial bleeding (3.8% and 1.4%, respectively), the majority occurring in the right IPA. Therefore, the right IPA is one of the chief postoperative bleeding sources in liver transplant recipients.

IPAs are paired small vessels near and below the diaphragmatic aortic hiatus that supply a large part of the diaphragm. Among them, the right IPA is clinically important because it acts as an extrahepatic collateral vessel [10, 11] and runs in front of the right crus of the diaphragm and then behind the inferior vena cava [8, 9]. During liver transplantation, ligation of the right IPA is necessary for hepatectomy in the recipient and for right hepatic lobectomy in a living donor. If the ligation of this artery is not maintained adequately, bleeding from the IPA can occur after liver transplantation.

In our study, most patients with IPA bleeding suffered from viral liver cirrhosis or hepatocellular carcinoma before liver transplantation (25/28, 89%) and underwent living donor liver transplantation (27/28, 96%). We think that the bleeding tendency of the right IPA after liver transplantation is relevant to its enlarged size, which suggests a high potential of extrahepatic collateral. This artery can supply hepatic tumors or surrounding hepatic tissue [10, 11], and it is frequently enlarged in patients with liver cirrhosis, which is revealed by axial thin-section CT [12]. Although it is unclear why the mean diameter of this artery is larger in cirrhotic patients than in a healthy control group, reduced portal blood flow into the liver is thought to be a possible cause. Therefore, under these clinical situations, the right IPA is likely to be hypertrophied and to have a tendency to bleed postoperatively.

Undoubtedly, liver transplantation is a causative factor for IPA bleeding. In a liver transplant recipient, hepatectomy can cause injury to the diaphragm or perihepatic tissues during retraction of the diaphragm or dissection of the right hepatic lobe from the surrounding tissue. The risk of injury to the diaphragm or perihepatic tissue seems to increase with living donor transplantation. Because a smaller hepatic graft can be unstable in the large right upper quadrant of the abdomen, it requires stronger fixation with the adjacent diaphragm or perihepatic tissue to prevent twisting of the graft on the vascular pedicle. Our study and that by Lee at al. [13] supported this presumption.

It is also important to notice that all IPA bleeding occurred within the first 2 weeks after liver transplantation and that its main clinical manifestations included sudden decreased hemoglobin level by more than 2 mg/dL and drainage of fresh blood from the drainage tube. Most patients (82%) were well controlled by transcatheter arterial embolization. These observations suggest that most arterial bleeding might be easily controlled by radiologic intervention if diagnosed rapidly.

In this study, the most common CT finding of right IPA bleeding was localized high attenuation of fluid collection of > 25 H in the posterior portion of the right hepatic graft. Pathognomonic findings were direct extravasation of contrast material from the right IPA, although its depiction on CT was not high (37%). However, active extravasation of contrast material in the posterior portion of the hepatic graft, suggesting the possibility of right IPA bleeding, was more frequently seen on CT (57%). Consequently, sudden development of acute hematoma in the posterior aspect of the hepatic graft, and extravasation of contrast material in the same region on CT, are thought to be predictive CT findings of IPA bleeding in posttransplantation patients.

In conclusion, IPA bleeding frequently occurred within the first 2 weeks after liver transplantation, especially in recipients who underwent living donor transplantation because of liver cirrhosis or hepatocellular carcinoma. Loculated acute hematoma and the extravasation of contrast media in the posterior portion of the hepatic graft are common predictive CT findings of IPA bleeding, which is well depicted by MDCT. Manifestation of sudden hypotension, a decrease in hemoglobin, or fresh blood drainage from in-dwelling drainage tubes in the early postoperative period requires prompt and thorough attention. CT is helpful in diagnosing IPA bleeding, which can prevent the progression into an undesirable clinical status that requires surgical management.


References
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 

  1. Anand AC, Ferraz-Neto BH, Nightingale P, et al. Liver transplantation for alcoholic liver disease: evaluation of a selection protocol. Hepatology 1997;25 : 1478-1484[Medline]
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  3. Turrion VS, Alvira LG, Jimenez M, Lucena JL, Ardaiz J. Incidence and results of arterial complications in liver transplantation: experience in a series of 400 transplants. Transplant Proc2002; 34:292 -293[Medline]
  4. Federle MP, Jeffrey RB Jr. Hemoperitoneum studied by computed tomography. Radiology 1983;148 : 187-192[Abstract/Free Full Text]
  5. Legmann P, Costes V, Tudoret L, et al. Hepatic artery thrombosis after liver transplantation: diagnosis with spiral CT. AJR 1995; 164:97 -101[Abstract/Free Full Text]
  6. Cavallari A, Vivarelli M, Bellusci R, Jovine E, Mazziotti A, Rossi C. Treatment of vascular complications following liver transplantation: multidisciplinary approach. Hepatogastroenterology2001; 48:179 -183[Medline]
  7. Miller CM, Gondolesi GE, Florman S, et al. One hundred nine living donor liver transplants in adults and children: a single-center experience. Ann Surg 2001;234 : 301-311[CrossRef][Medline]
  8. Settmacher U, Stange B, Haase R, et al. Arterial complications after liver transplantation: early and late forms. Gastroenterol Hepatol 1999; 22:381 -385[Medline]
  9. Glockner JF, Forauer AR, Solomon H, Varma CR, Perman WH. Three-dimensional gadolinium-enhanced MR angiography of vascular complications after liver transplantation. AJR 2000;174 : 1447-1453[Abstract/Free Full Text]
  10. Takeuchi Y, Arai Y, Inaba Y, Ohno K, Maeda T, Itai Y. Extrahepatic arterial supply to the liver: observation with a unified CT and angiography system during temporary balloon occlusion of the proper hepatic artery. Radiology 1998;209 : 121-128[Abstract/Free Full Text]
  11. Chung JW, Park JH, Han JK, Choi BI, Kim TK, Han MC. Transcatheter oily chemoembolization of the inferior phrenic artery in hepatocellular carcinoma: the safety and potential therapeutic role. J Vasc Interv Radiol 1998; 9:495 -500[Medline]
  12. Gokan T, Hashimoto T, Matsui S, Kushihashi T, Nobusawa H, Munechika H. Helical CT demonstration of dilated right inferior phrenic arteries as extrahepatic collateral arteries of hepatocellular carcinomas. J Comput Assist Tomogr 2001;25 : 68-73[Medline]
  13. Lee SY, Ko GY, Gwon DI, et al. Living donor liver transplantation: complications in donors and interventional management. Radiology 2004;230 : 443-449[Abstract/Free Full Text]

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