Systemic venous enhancement patterns during dynamic abdominal CT

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SYSTEMIC V E N O U S E N H A N C E M E N T P A T T E R N S D U R I N G D Y N A M I C A B D O M I N A L CT DAVID S. MENDELSON, MD, KEITH M. STERLING, MD, ROBERT S. SHAPIRO, MD, AGATA STANCATO-PASIK, MD, KATHLEEN P. HALTON, MD, AND GENNADY KOGAN

In 25 patients we assessed the enhancement of abdominal venous structures during dynamic computed tomography (CT). The degree of venous enhancement demonstrated great variation. In six instances (out of 250 observations) a vessel was visually perceived as not enhancing and potentially thrombosed, including three gonadal veins. CT measurements were helpful in identifying enhancement, but were occasionally low enough that thrombosis remained a radiological consideration. The great variation in venous enhancement makes the diagnosis of thrombosis suspect, based on CT alone. Corroboration of this finding is suggested, when clinically relevant.

structures enhance poorly, and their enhancement properties are the subject of our current investigation (1, 7). The poor enhancement of venous structures has been noted in the radiology literature. Radiologists are familiar with the so-called pseudothrombus (8), often noted in the inferior vena cava (IVC). Recently two reports described thrombosis of gonadal vessels, usually as an incidental finding, on contrast-enhanced CT scans (9, 10). The question arose as to whether any of the cases reported could in fact have represented pseudothrombosis. Here we described the enhancement pattern of the major systemic venous structures in the abdomen, during routine dynamic CT of the abdomen.

KEY WORDS:

C o m p u t e d t o m o g r a p h y ; Veins; C o n t r a s t ; A b d o m e n ;

Thrombosis

INTRODUCTION During the last decade the means of administering intravenous contrast material during computed tomographic (CT) scanning have evolved to address particular problems (1-6). Currently, the predominant technique is some form of dynamic CT, with the rapid infusion of a contrast agent over a 1- to 2-minute period. Though optimized to provide good enhancement of certain organs, a variety of problems with this relatively standard technique have been recognized. Venous From the Department of Radiology, The Mount Sinai School of Medicine of the City University of New York, New York, New York. Address reprint requests to: David S. Mendelson, MD, Department of Radiology- Box 1234, One Gustave L. Levy Place, New York, NY 10029-6574. Received June 1, 1994; revised November 10, 1994; accepted November 20, 1994.

CLINICAL IMAGING 1996;20:103-111 © Elsevier Science Inc., 1996 655 Avenue of the Americas, New York, NY 10010

MATERIALS AND METHODS Dynamic contrast-enhanced CT scanning of the abdomen was performed on 25 randomly selected patients in a prospective fashion. All scans were performed on a General Electric (GE) 9800 scanner (GE Medical Systems, Milwaukee, WI). Between 36 and 45 g of iodinated contrast material in a 150-mL formulation (Omnipaque 240, 300 Sanofi-Winthrop, New York, NY; or Conray 60, Mallinckrodt, St. Louis, MO) was infused into an antecubital vein as a rapid bolus at 1.0 mL/sec for 45 seconds, followed by 0.6 mL/sec for the remainder of the injection. All studies were performed by the same diagnostic radiology resident. Serial transaxial sections as 10-ram contiguous scans were obtained from the lung bases through the superior margin of the iliac crests. Dynamic scanning was programmed to commence following a 45-second delay (corresponding to the initial-45-second injection) to allow a bolus of contrast agent to be infused. The scans were of 2 seconds' duration with a 6-second interscan delay. The

0899-7071/96/$15.00 SSDI 0899-7071(95)00001-7

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A

FIGURE 1. (A) 0 - n o enhancement. This image demonstrates the right gonadal vein larrow), which was perceived as being unenhanced despite a CT number of 80. Of note is the fact that most of the venous structures enhanced greatly, with CT numbers ranging from 102 to 164. This relative difference may account for an illusory effect of no enhancement. (B) This inferior vena cava (IVC) was again perceived as nonenhancing larrow). Is it thrombosed? The CT number was 68.8, suggesting that it is patent but perceived as nonenhanced.

zero time of the study was r e c o r d e d at the time of the first axial scan. All scans were filmed with a w i n d o w of 500 H o u n s f i e l d units (HU) at a level of + 50 HU, and viewed at other settings w h e n d e e m e d necessary. Specific slices were selected to evaluate certain venous structures. These i n c l u d e d (1) the IVC at 1.0 cm c a u d a d to the level of the right atrium, w h e r e approximately 50% of the IVC is b o r d e r e d by the heart; (2) the intrahepatic portion of the IVC at the c o n f l u e n c e of the right, middle, and left hepatic veins; (3) the IVC at 2.0 cm c a u d a d to a point at w h i c h approximately 50% of the IVC is b o r d e r e d by the liver; (4) the IVC at the level of the m a i n left renal vein; (5) the IVC at the level of the main right renal vein; (6) the proximal m a i n left

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FIGURE 2. P-partial enhancement. This image was obtained at the level of the infrarenal IVC. The IVC (arrow) was perceived as being poorly enhanced with a CT number of 82.

renal vein; (7) the proximal m a i n right renal vein; (8) the IVC at 2.0 cm c a u d a d to the level of the m o r e inferior renal vein insertion; (9) the left gonadal vein at the most craniad level it c o u l d be identified; and (10) the right gonadal vein at the most craniad level it could be identified (11). The raw times of the scans were recorded as the time the section was imaged after the c o m p l e t i o n of the 45-mL rapid bolus infusion. The IVC at all of the selected levels was assigned a CT n u m b e r in Hounsfield units with a nine-pixel region-of-interest samples. The main renal veins and gonadal veins were similarly assigned CT n u m b e r s with a 1-pixel region-of-interest sample, c h o s e n because of the small caliber of these vessels. In the case of a heterogeneous vessel, the regions of interest were selected at several portions of

FIGURE 3. M--heterogeneous enhancement. This image depicts a heterogeneous appearance of enhancement at the infrahepatic IVC (arrow). This pattern, believed secondary to mixing of nonopacified blood with enhanced blood, is generally not confused with thrombosis.

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FIGURE 4. 1 - strong homogeneous enhancement. This image demonstrates typical strong enhancement of the IVC and both renal veins. This is the pattern of venous enhancement consistently identified as normal flow, with no question of thrombosis. CT numbers on this image ranged from 126.2 to 135.0. the vessel l u m e n and averaged. This mean n u m b e r was t h e n utilized as the value for the given heterogeneous vessel. All of the a f o r e m e n t i o n e d vessels were t h e n subjectively assigned an appearance based on the characteristic e n h a n c e m e n t . T h e s e were as follows: no enh a n c e m e n t (0; Figure 1); partial (poor) h o m o g e n e o u s e n h a n c e m e n t (P; Figure 2), heterogeneous or mixed e n h a n c e m e n t (M; Figure 3), or u n i f o r m strong homogeneous e n h a n c e m e n t (1; Figure 4). This subjective visual characterization was a c c o m p l i s h e d by the consensus of four imagers e x p e r i e n c e d in cross-sectional imaging. A variety of statistical tests were a p p l i e d to the data collected. Student's t test (z test) was utilized to determ i n e if there was a statistically significant difference a m o n g the subjectively determined groups (0, P, M, 1). The probability of a specific CT n u m b e r being visually

TABLE 1. Vessel Opacification: Visual Interpretation" 1.evel IV(: at heart 1VC at hepatic vein IVC infrahepatic 1VC at left renal vein IV(; at right renal vein Left renal vein Right renal vein Infrarena] IVC Left gonadal vein Right gonadal vein

0

1'

lt'/31 2/65 1~'/2{i 11/79 3/64 2/68 5/87 2/71 2/60 1/59 8/77 3/70 3/67 2/78

" N~. of patients/average CT ml. f' Same patienl Obscured by arlifact.

M 16/86 6/77 11/81 10/88 8/80 1/133 1/74 2/92 1/99 1/76

1 6/100 6/91 11/1{}4 13/99 12/94 22/104 22/106 14/94 20/98 13/89

Not seen 1~

1 6

105

FIGURE 5. ?-Thrombosed right gonadal vein (arrow). This image is of one of the three patients perceived as having no enhancement of the right gonadal vein. This patient also demonstrated an enhancing rim, another criteria for determining thrombosis. assigned to any specific group (0, P, M, 1) was also analyzed. RESULTS The e n h a n c e m e n t characteristics of the vessels evaluated are s u m m a r i z e d in Table 1. M e a s u r e d CT n u m bers ranged from 26 to 164 HU. No venous structure demonstrated h o m o g e n e o u s e n h a n c e m e n t in all 25 patients. T h e r e were 250 venous sties evaluated, but only 242 were actually identified (see Table 1}. T h e r e was a p e r c e p t i o n of no e n h a n c e m e n t at six sites (2.4 %). Of particular note are three patients in w h o m the right gonadal vein was not p e r c e i v e d by visual inspection as being e n h a n c e d (Figure 5}. The other instances of no e n h a n c e m e n t were in the infrarenal IVC in one patient, and the IVC at both the levels of the heart and the hepatic veins in another patient. Of these five patients two had a history of heart disease; the other three did not. For patients w i t h o u t e n h a n c e m e n t of the right gonadal vein the time from initiation of scanning (45 seconds after contrast bolus injection commenced) and the CT n u m b e r of the vessels were, respectively, 119 seconds and 80 HU, 262 seconds and 51 HU, and 450 seconds and 48 HU; for the patient w i t h o u t enhancement of the IVC, 82 seconds and 68.8 HU. T h e total injection time i n c l u d i n g the initial bolus w i t h delay s h o u l d have been 3 minutes. Thus at least two of these levels were r e a c h e d after cessation of the injection. Variations in the time at w h i c h the gonadal veins are m e a s u r e d are a c c o u n t e d for by variations in both the b o d y habitus of i n d i v i d u a l patients and the ability of the observers to reliably identify the veins. The most craniad level at w h i c h the veins were detected w i t h c o n f i d e n c e varied greatly from patient to patient. In

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TABLE 2. Vein Statistics Vein no. 1 2 3 4 5 6 7 8 9 10

Vein

Number of measurements

Percentageof total measurementsmade

IVC at heart IVC at hepatic vein IVC infrahepatic IVC at left renal vein IVC at right renal vein Left renal vein Right renal vein Infrarenal IVC Left gonadal vein Right gonadal vein

25 24 25 25 25 25 25 25 24 19

10.33 9.92 10.33 10.33 10.33 10.33 10.33 10.33 9.92 7.85

one of these patients the right gonadal vein was believed to be dilated with a rim of enhancement. In the other patients lack of enhancement was the only abnormality. Regarding the four sites below the hepatic IVC, all observers thought that thrombosis of the vessel was a serious diagnostic concern on the basis of the CT findings. These cases were reviewed well after the CTs were performed and this finding was not pursued in any of the patients. However, review of the patients' charts did not reveal venous thrombosis to be a clinical concern. Table 2 and Figure 6 summarize the measured CT numbers at each venous site. The mean measurement at each site as well as the standard deviation were calculated. There were statistically significant differences (p < 0.01) between sites: IVC at heart versus left renal vein, IVC at hepatic veins versus left renal vein, IVC at hepatic veins versus right renal vein, IVC at hepatic veins versus left gonadal vein, IVC infrahepatic versus left renal vein, IVC at right renal vein versus left renal vein, infrarenal IVC versus left renal vein, and right gonadal vein versus left renal vein. The subjective categories of 0, P, M, and I were analyzed regarding the CT numbers falling into each category (Figure 7). Graphically one can see that there is great overlap in CT numbers between groups. Figure 8 gives the probability that a given CT measurement will be visually categorized into a particular category. Generally as noted above, there is great overlap, except at the extremes of enhancement. For example, a CT measurement of 110 HU has a probability of 0.861 of being perceived as belonging to category 1. Also, it should be noted that any vessel with a CT number lower than 50 is perceived as belonging to group 0. In fact three vessels perceived as belonging to group 0 fell below the 95% borders for measurements belonging to group P, M, or 1. Application of Student's t test {z test) to these four groups demonstrated a statistically significant difference between the means in several cases. Group 0 was

Mean 85.20 79.67 89.24 92.44 87.92 105.76 100.60 87.16 94.50 83.58

Deviation 23.55 16.92 20.85 18.70 15.70 20.60 22.35 15.21 18.58 20.68

95% Confidencelimits 38.10-132.30 45.84-113.50 47.53-130.95 55.05-129.83 56.53-119.31 64.55-146.97 55.89-145.31 56.75-117.57 57.33-131.67 42.22-124.94

significantly different from group 1 (p < 0.01) and different from the combination of groups P, M, and 1 (p < 0.01). Similarly there was a significant difference (p < 0.01) when group P was compared individually to groups M and 1, and when group M was compared to group 1. We lastly evaluated whether a history of heart disease influenced CT enhancement. The mean CT numbers, for all vessels, were 79.78 for 76 measurements made in patients with heart disease, and 95.68 for 166 measurements made in patients without heart disease. This was a significant difference (p < 0.01). DISCUSSION Current CT techniques are generally tailored to the enhancement of particular organs or arterial structures. The liver is often the target of dynamic CT, with the rapid infusion of 40 to 50 g of iodine in a 100- to 150-mL formation over 1 to 2 minutes (2, 3). A well-recognized limitation of these techniques is the relatively poor enhancement of venous structures (1, 4, 7). Our investigation was designed to examine the degree and consistency of enhancement of major systemic venous structures during routine abdominal CT scanning. This subject is important for several reasons. Firstly, suspected venous thrombosis is commonly reported as an incidental finding (9, 10). However, pseudothrombus is described in the IVC and might occur in any venous structure (8). The accuracy of this finding, thrombosis, should be known. Secondly, poorly enhanced venous structures may be confused with lymph nodes and result in the misstaging of patients with neoplasms (7). Our results suggest that standard dynamic CT techniques result in inconsistent and often poor-to-undetectable enhancement of systemic venous structures. We suspect that most radiologists visually assume that this is artifactual in origin and exclude this information. However, the recent reports regarding un-

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suspected gonadal vein thrombosis (9, 10) detected on CT imply that a second more objective look at venous structures is warranted. In three of 25 patients we found CT evidence of right gonadal vein thrombosis. We do not have corroboration of this finding, though such was not actively sought in these patients during their hospitalization. In two other patients, portions of the IVC were perceived as unenhanced with relatively low CT numbers. They had no clinical evidence to substantiate this finding. It is our belief that these findings are likely to have been artifactually created by the injection technique employed. The incidental finding of deep venous thrombosis in 20% of patients examined is certainly suspect. The remainder of our data points to the very inconsistent enhancement pattern of venous structures of the abdomen when a fairly standard contrast injection protocol is used. Our data represent the assessment of 250 venous sites, 242 actually identified. A frequent assumption is that all veins enhance to a similar extent. In fact this was not true. Our subjective division of venous enhancement was statistically significant when analyzed regarding CT number in a population of patients selected at random. Hence for a variety of reasons (some unknown), venous enhancement is not uniform. The presence of heart disease appears to be one factor resulting in lower CT numbers of venous structures. Great care must be employed when assessing venous structures. Assumptions and expectations regarding their enhancement must be carefully considered both in diagnosing thrombosis and when distinguishing veins from other structures, particularly lymph nodes. Clearly, one cannot assume that veins will be uniformly, obviously enhancing structures. Our data suggest that when vessels enhance with CT numbers greater than 90, there is generally uniform perception among radiologists of enhancement. The visual perception of enhancement becomes less consistent below this degree of enhancement, until the opposite extreme is reached. The ability to measure CT

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numbers is both simple and obvious as an adjunct in confirming whether there is in fact enhancement. Note that in several cases perceived as having no enhancement, it is likely that there was some. To further complicate this situation is that injection protocols continue to evolve, particularly to accommodate the newer technique of spiral CT. We should not have preconceived notions as to how venous structures will appear when we change the volume and timing of contrast administration as substantial changes of injection protocols are introduced. An awareness of the vagaries of venous enhancement can help prevent the misinterpretation of CT studies. REFERENCES 1. Platt JF, Glazer GM. IV contrast material for abdominal CT: comparison of three methods of administration. AJR 1988;151: 275-277. 2. Foley DW. Dynamic hepatic CT. Radiology 1989;170:617-622. 3. Berland LL, Lee JY. Comparison of contrast media injection rotes and volume for hepatic dynamic incremented computed tomography. Invest Radiol 1988;23:918-922. 4. Young SW, Noon MA, Marincek B. Dynamic computed tomogmpby time-density study of normal human tissue after intravenous contrast administration. Invest Radiol 1981;16:36-39. 5. Baker ME, Cohan R, Cooper C, Dunnick R. Dynamic incremental computed tomogmphy using a high heat detector and automated injector. Potential in body imaging. Clin Imag 1989;13:189-194. 6. Kormano M, Partanen K, Soimakallro S, Kivimaki T. Dynamic contrast enhancement of the upper abdomen: effect of contrast medium and body weight. Invest Radiol 1983;18:364-367. 7. Teefey SA, Baron RL, Schulte SJ, Shuman WP. Differentiating pelvic veins and enlarged lymph nodes: optimal CT techniques. Radiology 1990;175:683-685. 8. Makai J, Chen P. The inferior vena caval pseudothrombus sign: diagnostically dynamic CT after arm vein injection. J Assoc Can Radiol 1985;36:250-253. 9. Jain KA, Jeffrey RB Jr. Gonadal vein thrombosis with acute gastrointestinal inflammation: diagnosis with CT. Radiology 1991: 180:111-113. 10. Jacoby WT, Cohan RH, Baker ME, Leder RA, Nadel SN, Dunnick NR. Ovarian vein thrombosis in oncology patients: CT detection and clinical significance. AJR 1990;155:291-294. 11. Rebner M, Gross GH, Korobkin M, Ruiz J. CT appearance of right gonadal vein. J Comput Assist Tomogr 1989;13:460-462.