Richard J. Wechsler, Anna S. Lev-Toaff,

MD MD

Suprahepatic after Orthotopic

terms:

Liver, CT,

transplantation, 982.458 #{149} Venae

761.458 cavae,

Radiology

183:545-548

761.1211

#{149} Venae CT, 982.1211

Liver, cavae, #{149}

transplantation has become an important therapeutic option for end-stage liver disease. Recognition of complications is critical in the treatment of these patients because these complications may be reversible with appropriate therapy. In particular, vascular complications are a major cause of morbidity and mortality after liver transplantation (1,2). It is impontant to detect and differentiate between various causes of liven graft dysfunction with computed tomography (CT) because this modality may be used before more invasive procedunes. Awareness of potential CT pitfalls is essential. This retrospective IVER

study

was

I From the Departments of Radiology (R.J.W., R.F., M.D., A.S.L.T., T.G.1-L), Medicine (S.J.M.), Pathology (R.R.), and Surgery (M.J.M.), Thomas Jefferson University Hospital, 111 5 11th St, Philadelphia, PA 19107. Received October 10, 1991; revision requested November 6; revision received December 26; accepted January 6, 1992.

Address .

RSNA,

reprint

1992

requests

to R.J.W.

undertaken

to analyze

the

frequency and importance of a highattenuation suprahepatic circumcaval ring on arc in patients who have undengone liver transplantation.

rounding

J.

MD

Moritz,

PATIENTS

AND

At our institution, 65 went 77 orthotopic liver between May 1984 and One hundred fourteen scans

were

(16 male 14-62

obtained The

patients undertransplantations November

1989.

abdominal

CT

in 37 of those

and 21 female

years).

METHODS

patients

37 patients

Imaging

was

sections

performed

with

at 1-cm intervals

under-

10-mm-

from the

dome of the diaphragm to the iliac crest with a fourth-generation (2020 HR or 1440 HPS; Technicare, Cleveland) or third-generation (9800 Quick; GE Medical Systems,

CT scanner.

In those

patients

without contraindications, 120 mL of 60% iothalamate meglumine (Conray 60; Mallinckrodt, St Louis) was injected at I mL/sec, with scanning beginning after a 30-second delay. Twenty-six patients were studied within 15 days of transplantation, 22 between

than 59 days suprahepatic

cava

in the

patient’s the ring assessed

clinical status. CT scans in which was absent or could not be well were considered to be negative

for this sign. The liver transplant recipients were then divided into two groups, depending on the presence or absence of the suprahepatic circumcaval ring. The arithmetic mean of daily serum ionized calcium, phosphate, and calcium phosphate product was surgery.

calculated Because

for the relatively

first 7 days after large amounts

of citrate (which binds circulating calcium) are present in blood-derived products, the amount

of packed

red blood

cells,

fresh-

frozen plasma, platelets, and cryoprecipitates administered during surgery (intraoperative blood products) was also compared for the two groups. Graft function for each group was assessed with serial determination of serum bilirubin, albuand

aminotransferase

levels.

two-tailed

Student

t test

nonpaired

samples

and

performed between

to assess the

for

The

independent

2 analysis

statistical

were

differences

groups.

two

RESULTS

gone 42 orthotopic liver transplantations. Indications for CT included evaluation of possible abscess, hemorrhage, fluid collection, pancreatitis, and hepatic dysfunction.

thick

vena

patients

aged had

the inferior

region of the suprahepatic anastomosis. Two experienced radiologists made this determination without knowledge of the

mm,

Milwaukee) 1992;

MD

#{149}

Clrcumcaval Ring: CT Finding Liver Transplantation’

A suprahepatic circumcaval ring or arc was noted on computed tomographic (CT) scans in 20 of 37 patients who had undergone 42 orthotopic liver transplantations. The patients were divided into two groups, depending on the presence or absence of this finding. The amounts of blood products transfused intraoperatively and the levels of serum calcium, phosphate, and calcium phosphate product after transplantation were determined for each group. Liver graft function was evaluated on the basis of postoperative levels of serum bilirubin, albumin, and aminotransferase. The levels of serum calcium and calcium phosphate product were higher in patients with the circumcaval ring. This group had received substantially more fresh frozen plasma and platelets at surgery. There was no difference in liver graft function between the two groups. In one case, pathologic examination demonstrated calcification within circumcaval fibrotic tissue. A suprahepatic circumcaval ring is a common finding at CT performed after liver transplantation and is probably related to elevated perioperative serum calcium levels and tissue injury. Surgeons should be made aware of this finding before performing repeat transplantation, since calcification at a potential anastomotic site may make surgery more difficult. Index

Santiago J. Munoz, MD #{149}Mark DeLaurentis, MD, PhD #{149}Raphael Rubin, MD #{149}Michael

Rick Feld, MD Thomas G. Helinik,

#{149} #{149}

and 59 days, and 16 more after transplantation. The circumcaval ring was consid-

16

ered present if there was a high-attenuation circle or arc (simulating calcium)

sur-

A suprahepatic circumcaval ring was identified in 20 of the 37 liver transplant recipients (54%). The ring was seen in eight of 26 patients (31%) scanned within 15 days of transplantation, 12 of 22 patients (54%) scanned between 16 and 59 days, and 10 of 16 patients

(62%)

scanned

after

59 days

(Fig 1). The suprahepatic circumcaval ring remained on subsequent CT scans in all patients. In fact, the cincumcaval ring tended to become more apparent on subsequent scans (Fig 2). The circumcaval ring was detected on the initial CT scan (obtained 6-49 days after surgery) in 13 of the 20 patients (65%) and on subsequent scans (obtained 21 days to 2 V2 years after surgery)

in seven

(35%).

five patients who underwent transplantation developed after the first transplantation.

Four

of the

repeat the ring In the 545

fifth patient, the circumcaval ring was not detected after the first transpbantation but was detected 6 days after the second transplantation. Two patients with the suprahepatic circumcaval ring had infrahepatic circumcaval rings (Fig 3). The actual time of appearance of the suprahepatic circumcaval ring could not be ascertained because CT scans

were

obtained

at inconstant

in-

tervals after liven transplantation for various clinical indications. The suprahepatic circumcaval ring was first detected in eight patients within 15 days

of transplantation

(Fig

4), in

eight patients between 15 and 59 days, and in four patients after 59 days. The earliest detection of the circumcaval ring occurred 6 days after surgery. There was a statistically significant (P

=

.05,

Student

t test)

difference

in

the serum ionized calcium levels of the patients who developed a circurncaval ring (n = 20) and those who did not (n = 17) (5.34 mg/dL ± 0.39 [1.33 rnmol/L ± .097] vs 4.48 mg/dL ± 0.07 [1.11 rnmol/L ± .017], respectively). Likewise, there was a statistically significant (P < .032) difference in the levels of calcium phosphate product in the patients with and without the circurncaval

ring

(23.25

±

2.59

a. (a) CT scan

obtained

1

Radiology

#{149}

this vena

segmentally

and

time, cava

clamped

the

liver

the portal vein are occluded,

veno

bypass

press

these

At

and inferior unless vcno-

is performed venous

and

is removed.

to decom-

systems.

Anasto-

To assess complications after liven transplantation, familiarity with the surgical procedure is imperative. Recipient hepatectomy necessitates dissection of the hilar structures just inferior to the liver and isolation of the subhepatic inferior vena cava postenor to the hilum. The suprahepatic vena cava is then isolated. The diaphragmatic

and

retroperitoneal

at-

tachments are excised as needed for exposure and dissection of the yessels. At completion of the hepatectorny, the hilar structures, lower inferion vena cava, and suprahepatic vena

Figure 1. CT scan obtained transplantation demonstrates cumcaval ring.

a.

I year after a complete

liver cir-

b.

Figure

2.

circumcaval plantation circumcaval

(a) CT scan

obtained

7 weeks

after

years

after

liver

ring is demonstrated. (b) CT scan and with intravenous administration arc is seen (arrowhead).

transplantation.

obtained of contrast

No

in same

patient

material.

definite

suprahepatic

41 weeks A definite

after

trans-

suprahepatic

c. liver

transplantation

obtained in same patient at a more caudal level demonstrates level in between the suprahepatic and infrahepatic anastomoses

546

arc

divided,

DISCUSSION

b. 3.

cava

vs

16.35 ± 1.37). There was no significant difference in serum phosphate levels (Fig 5). Analysis of intraoperative blood products revealed that development of the suprahepatic circumcaval ring was associated with significantly more transfusions of frozen plasma and platelets (P = .003 and .033, nespectively). There was no difference in transfusions of packed red blood cells or cryoprecipitate (Fig 6, Table 1).

Figure

Furthermore, there was no significant difference in liver graft function as shown by the arithmetic mean of daily serum bilirubin, albumin, and aminotransfcrase levels obtained in the first week after surgery (Fig 7, Table 2).

demonstrates

a suprahepatic

a circumcaval ring at the infrahepatic reveals no calcification.

circumcaval

caval

ring

anastomosis.

(arrowhead).

(b) CT

(c) CT scan

scan

obtained

May

at a

1992

Cl)

z

Figure

4.

CT scan

obtained

liver transplantation prahepatic circumcaval

2

weeks

demonstrates ring (arrow).

after faint

su-

Figure

6.

patients

Amount of blood products without rings, striped bars

the standard

error

transfused =

patients

during

with

liver

rings.

transplantation.

Horizontal

lines

Black

bars

at asterisks

=

indicate

of the mean.

E

controls

ctrcumcaval

ring

Figure 5. Mean serum phosphate levels after liver transplantation in patients with and without circumcaval ring. Standard errors of the mean (horizontal lines at asterisks) were 0.313 and 0.390 for patients with and without circumcaval ring, respectively. The difference was not significant. Black bar = patients without rings, shaded bar = patients with rings.

30

25

20 01

E 15

10

Figure rings.

7. Functional Black bars =

at asterisks

moses

of the

new

liven

are

usually

done in the following order: (a) suprahepatic vena cava, (b) infrahepatic vena cava, (c) portal vein, (d) hepatic artery, and (e) biliary system (3). Most vascular complications occur at the hepatic arterial and portal venous anastomoses.

Achieving mosis

of the

formidable Volume

the

suprahepatic

inferior

technical 183

Number

#{149}

vena

anastocava

challenge 2

indicate

status

of transplanted

livers

Difficulties in dissection and vascular control during hepatectorny are encountered because the caval segment between the liver and diaphragm is very short. Obesity, narrow costal margin, perihepatic adhesions, and a large liven may further restrict exposure required for careful dissection and creation of the anastomosis. Despite the difficulty in creating

is a

this

(4).

on thrombosis

anastomosis,

for

patients without rings, striped bars the standard error of the mean.

occlusion,

of the

stenosis,

suprahepatic

in-

patients with and without circumcaval = patients with rings. Horizontal lines

ferior vena cava appears to be uncommon (5). Dalen et al (1) reported five cases of inferior vena caval thrombosis in 98 liven grafts, two of which de-

veloped after either aortic on portal thrombosis. Lerut et al (6) reported a 0.8% frequency of vena caval thrombosis

in 393

orthotopic

liver

grafts.

These thromboses were almost exclusively seen in pediatric patients. The negligible frequency of vena caval complications in adults is probably Radiology

547

#{149}

Figure 8. suprahepatic

(a) CT scan

of the

region

caval anastomosis after liver transplantation

weeks

strates a faint (arrowheads).

but definite (b) Inferior

of the

obtained demon-

7

circumcaval ring vena cavogram of

the same patient demonstrates stenoses of both the suprahepatic and infrahepatic anastomoses (arrows) but no evidence of thrombosis. (c) Pathologic soft tissue of same sin stain; original

onstrates

specimen of pericaval patient (hematoxylin-eomagnification, x80) dem-

calcification

(arrowhead).

The

(arrow) caval

and

endothelium

fibrosis is not

seen on this image but was normal at autopsy, with no evidence of thrombosis.

due to relatively high caval blood flow and continued improvement in surgical techniques. There was no evidence of vena caval thrombosis in our patients. However, 20 of our 37 patients had a highattenuation ring at the level of the suprahepatic inferior vena caval anastomosis on CT scans. The presence of high-attenuation rings around the vena cava after liven transplantation has been attributed to intravascular thrombosis (7). There was no evidence of this complication in our patients. The rings tended to occur and progress with no relation to liven graft function. Our experience suggests that the suprahepatic circumcaval ring is a common finding that should not be confused with other caval complications. Calcification is a likely cause of this high-attenuation ring. This was confirmed at autopsy in one of our cases (Fig 8). The calcification was not within the inferior vena caval wall but in circurncaval fibrotic tissue. Calcification of the inferior vena cava has been previously reported and attnbuted to thrombosis (8,9). Two cases of suprahepatic inferior vena cava calcification were confirmed to be in a caval membrane causing primary BuddChiari evidence

syndrome (10). There of vascular thrombi

was no or Budd-

Chiari syndrome in our patients. Ectopic soft-tissue calcium deposition after liver transplantation has been documented (11). The cause of such calcification is unknown, but potential pathogenic factors include the large quantities of calcium administened during and after surgery, renal failure, acid-base changes, and citrate administered in fresh-frozen plasma and platelets. It has been proposed that local tissue injury and adrninistration of large amounts of exogenous calcium in liver transplant recipients results in metastatic soft-tissue calciurn deposition (11). In our study, the patients with suprahepatic circumcaval rings had received larger amounts of blood prod548

Radiology

#{149}

a.

c. ucts

b. during

surgery

than

those

without rings. Sodium citrate is present in relatively large amounts in fresh-frozen plasma, packed red blood cells, and platelets. High plasma citrate concentrations in this setting may lead to metabolic alkabosis and hypocalcemia by chelation of ionized calcium. As a result, release of parathyroid hormone is triggered, causing secondary hyperparathyroidism (11). This may paradoxically lead to high serum calcium levels and elevated calcium phosphate product, as were found in our patients who developed the suprahepatic caval ring. It is uncertain why calcium deposition has a tendency to occur at the suprahepatic inferior vena cava. It is documented that creation of the suprahepatic vena caval anastomosis is difficult to perform (4). Ischernic changes resulting from local trauma may have a propensity to occur at this site. The clamp used to control the suprahepatic vena cava exerts tremendous force on the tissues as it transverses the diaphragm and presumably causes substantial tissue injury. Dystrophic soft-tissue calcification may occur as a sequelae of local tissue injury. The finding of a suprahepatic cmcurncaval ring on CT scans is not uncommon after orthotopic liver transplantation and has uncertain pathologic importance in a functioning liver graft. Surgeons, however, should be aware of this finding if nepeat transplantation is considered.

Calcification motic site gery

more

may

at a potential anastomake subsequent

difficult.

sun-

U

Acknowledgments: The authors thank Lisa Massanova, Ann Hunter, Gloria Crumbley, and Sandra del Buono for their word processing assistance and Sharon Westerberg, BA, for expert technical assistance.

References 1.

2.

3.

4.

5.

of

Dalen K, Day DL, Ascher NL, et al. Imaging vascular complications after hepatic transplantation. AJR 1988; 150:1285-1290. Davis PL, Van Thiel DH, Zajko AB, Campbell WL, Sumkin JH, Rothschild MA. Imaging in hepatic transplantation. Semin Liver Dis 1989; 9:90-101. Iwatsukz 5, Shaw BW Jr, Starzl TG. Current status of hepatic transplantation. Semin Liver Dis 1983; 3:173-179. Raju S, Pidlake R. Suprahepatic vena caval cuff in liver transplantation. Transplantation 1984; 37:110. Zajko AB, Campbell WL, Bron KM. Schade RR, Koneru B, Van Thiel DH. Diagnostic and interventional radiology in liver transplantation. Gastroenterol

6.

7.

Clin

North

Am

Lerut J, Tzakis AG, Bron K, et tions of venous reconstruction thotopic liver transplantation. 205:404-414. Letourneau JG, Day DL, Maile Ascher NL, Frick MP. Liver plantation: postoperative CT

1988;

17:105-143.

al. Complicain human orAnn Surg 1987; CW, Crass JR. allograft transfindings. AJR

1987; 148:1(199-1103. 8.

Singleton EB, Rosenberg HS. Intraluminal calcifications of the inferior vena cava. AJR 1961; 86:556-560.

9. 10.

11.

Gammill SL, Nice CM Jr. Calcification in the inferior vena cava. Radiology 1%9; 92:1288-1290. Kobayashi A, Matsui 0, Takashima T. Calcification in caval membrane causing primary Budd-Chiari syndrome: CT demonstration. Comput Assist Tomogr 1988; 12:401-404. Munoz Sj, Nagelberg SB, Green PJ, et al. Ectopic soft tissue calcium deposition following liver transplantation. Hepatology 1988; 8:476-483.

May 1992

Suprahepatic circumcaval ring: CT finding after orthotopic liver transplantation.

A suprahepatic circumcaval ring or arc was noted on computed tomographic (CT) scans in 20 of 37 patients who had undergone 42 orthotopic liver transpl...
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