J Clin Ultrasound 20:433-438, September 1992 0 1992 by John Wiley &, Sons, Inc. CCC 0091-2751/92/070433-06 $04.00

Color Doppler Imaging of the Cystic Artery Frank P. McGrath, MB, Stephen H. Lee, MB, and Robert G. Gibney, M B

Abstract: Color Doppler ultrasonography was used to examine the gallbladder vascular supply in 30 volunteers and in 30 biliary lithotripsy patients pre- and 2 hours posttreatment. A preliminary study of 1 0 cases of acute cholecystitis was also performed. A cystic artery waveform was obtained in 24 of the volunteers, 18 pre- and postlithotripsy patients, and in 1 of 10 patients with acute cholecystitis. The mean pulsatility indices obtained were 1.04 in the volunteers, 0.98 pre- and 1.02 postlithotripsy ( p > 0.1).This study shows that the normal gallbladder blood supply can be consistently identified using color Doppler flow imaging and that there is no appreciable difference in the cystic artery pulsatility index following medium-energy shock-wave extracorporeal lithotripsy. Preliminary results in acute cholecystitis suggest that flow is decreased below the sensitivity of the color Doppler imaging system used in this investigation. Indexing Words: Ultrasound * Color Doppler Cystic artery * Gallbladder * Biliary lithotripsy . Cholecystitis

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Prior to the advent of high-resolution color Doppler flow imaging (CDFI), the blood supply to small parts could only be accurately assessed with angiography. CDFI has provided an accurate noninvasive means of assessing the blood supply in the normal testis, infant brain, and orb i t ~ . ' - Other ~ studies have evaluated the role of CDFI in disease states, including acute thyroidi~ tis4 and carcinoma of the b r e a ~ t .Gallbladder wall changes following extracorporeal lithotripsy (BL) in animal studies have shown focal vascular and soft tissue damage causing small hemorrhages that have also been found in the lung and liver parenchyma.6 Human studies have also r'eported vascular dilatation and petechial hemorrhages on microscopic examination of surgically excised gallbladders within 6 hours of BL.7 The aims of this study were to establish the normal appearance of the cystic artery wave form using CDFI and to evaluate the cystic artery waveform in conditions where alteration in flow to the gallbladder might reasonably be expected. For this purpose the immediate postbiliary lithotripsy period was selected as reports

From the Department of Radiology, University of British Columbia and Vancouver General Hospital, Vancouver, BC, Canada. For reprints contact F. P. McGrath, MB, Department of Radiology, McMaster University Hospital, 1200 Main Street West, Hamilton, Ontario, Canada L8N 325.

have suggested a microscopic increase in vessel diameter within the gallbladder wall following BL. A preliminary investigation of its potential role in acute cholecystitis was also evaluated. MATERIALS AND METHODS

The gallbladders of 30 asymptomatic volunteers between the ages of 23 years and 35 years (mean: 26 years) were studied using an Acuson 128 (Mountain View, CA) with color Doppler capability. All volunteers were examined following an overnight fast. None of the volunteers had any previous history attributable to the biliary tract. A further 30 patients with symptomatic gallbladder calculi were then studied in the fasting state and 2 hours after a session of biliary lithotripsy, age range 38 years to 64 years (mean: 51 years). All patients were treated in the left posterior oblique (LPO) position and targeted with the overhead module of a secondgeneration Lithostar Plus (Siemens, Erlangen, Germany). This produces medium-energy shock waves from an electromagnetic generator that does not require the use of general or epidural analgesia. Each BL patient received between 1700 and 4000 shocks (mean 3276) at 60% to 70% of the maximum power level. In addition, a preliminary study of 10 patients presenting with the typical clinical and sonographic signs of acute cholecystitis was also performed at the 433

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time of acute presentation. All 10 patients subsequently had cholecystectomies performed on an acute basis and pathological confirmation was obtained. The gallbladder blood supply was determined using the combined B-mode and range-gated color Doppler ultrasound system. Examinations were performed using a 3.5-MHz phased array 6 3 2 8 ) and a 5-MHz (L538) linear array transducer for the more superficially located gallbladder. The color Doppler flow threshold was set at a low level (0.09 to 0.16) to increase the sensitivity for identifying flow in small-caliber vessels such as the cystic artery. The sampling volume was maintained at a minimum level by keeping the sampling gate as small as possible (1.5 mm) in order to obtain a more accurate waveform. A redhlue color shading was assigned to blood flow depending on the direction of flow relative to the transducer head. The cystic artery was best visualized using an oblique plane through the long axis of the gallbladder in the supine and LPO positions (Figure 1). The main right hepatic artery as it passes between the cystic duct anteriorly and the right

branch of the portal vein posteriorly was initially identified (Figure 2). On identification of the right hepatic artery, the cystic artery, and its deep branches using the color Doppler mode, point spectral analysis was performed. Initially, the CDFI examinations took approximately 40 minutes to 45 minutes and proved moderately difficult to perform, but later in the study the examination time was reduced to 25 minutes to 30 minutes. In general, it was difficult to image sufficient segments of the cystic artery to apply the angle-correct cursor, thereby invalidating systolic and diastolic velocity measurements. The pulsatility index ({maximum velocity - minimum velocity} + mean velocity) was used. This index rules out error in velocity measurements attributable to lack of angle correction, and has been used in preference to the resistive index in obstetrical and abdominal Doppler examinations.' It takes into account the average velocity change with time and is therefore considered a more sensitive index for assessing alteration in waveforms. The difference in pulsatility indices (PIS) between the right hepatic artery and the main cys-

common hepatic duct

right hepatic artery

\

cystic duct artery common bile duct

artery

FIGURE 2. (A) Schematic diagram of normal vascular and biliary anatomy of the gallbladder fossa. Note the point of origin of the cystic artery from the right hepatic artery reported to occur in 95% of patients (6) (arrows). (B) (Opposite page) Color flow image correlating with schematic diagram in 2(A). JOURNAL OF CLINICAL ULTRASOUND

FIGURE 1. Oblique image through the gallbladder fossa demonstrating the color Doppler image of the cystic artery (straight arrow). Also illustrated are the right hepatic artery (curved arrow) and right branch of portal vein (thick arrow).

FIGURE 4. Sagittal color flow image of acute cholecystitis. Note some of the typical ultrasound features: thick-walled gallbladder, pericholecystic fluid, and echogenic bile. A segment of cystic artery is visualized (arrow), its waveform was of low impedance similar t o that in Figure 3.

FIGURE 28 VOL. 20. NO. 7, SEPTEMBER 1992

FIGURE 4

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tic artery in the volunteer group and for those cystic artery waveforms obtained in the pre- and postlithotripsy group was assessed using Student’s t test. RESULTS

The cystic artery was identified and a consistent waveform obtained in 21 (70%) of the 30 volunteers examined. The waveforms were of low impedance and characteristic of blood supply to a low resistance bed (Figure 3). In 3 of the 9 cases in whom a main cystic artery was not visualized, flow was identified in the region of the hepatic surface of the gallbladder. The right hepatic artery was identified and a waveform obtained in 26 volunteers. A deep gallbladder wall branch was identified in 3 patients (10%). Analysis of the cystic artery waveforms obtained using the pulsatility indices revealed a range of 0.54 to 1.8 (mean: 1.04) and for the right hepatic artery 0.61 to 1.36 (mean: 0.98; Table 1). This difference was not statistically significant ( t = 0.081, p > 0.5). A cystic vein was seen in 2 volunteer subjects. This was visualized in the gallbladder mesentery approximating the site of the cystic artery as it branches off the right main

hepatic artery. A cystic vein waveform was obtained from the hepatic surface of the gallbladder. The cystic artery was identified before and after treatment in 18 of 30 (60%) lithotripsy patients, spectral analysis of these vessels revealed a pretreatment PI range of 0.81 to 1.17 (mean: 0.95), and posttreatment of 0.75 to 1.36 (mean: 1.02). This difference was not statistically significant (t = 1.79, p > 0.1). Cystic artery flow could not be visualized in 9 of the 10 patients with acute cholecystitis examined. The single patient with identifiable flow in the cystic artery (Figure 4) had a similar waveform to that identified in the volunteer group. DISCUSSION

Mapping of the normal gallbladder blood supply and carrying out waveform analysis using highresolution color Doppler ultrasonography may have a role to play in gallbladder disease processes. It is possible that, as in the thyroid inferno found in Graves’ disease: a similar increase in gallbladder blood supply would be expected in the early stages of the gallbladder wall’s inflammatory response to repeated minor trauma, as in

FIGURE 3. Normal cystic artery waveform characteristic of blood supply to a low resistance bed. JOURNAL OF CLINICAL ULTRASOUND

COLOR DOPPLER OF CYSTIC ARTERY TABLE 1 Cystic Artery Pulsatility indices Obtained PI Values n (30) Volunteers Pre-BL Post-BL

21 18 18

Mean

Range

1.04 0.95 1.02

0.54- 1.80 0.81-1.17 0.75- 1.36

PI: pulsatility index = (peak systolic - end diastolichne average velocity; BL: extracorporeal biliary lithotripsy.

shock-wave lithotripsy or in established gallbladder wall disease, such as in acute cholecystitis. In an attempt to investigate this hypothesis, CDFI was used, first, to establish if the normal cystic artery could be identified and Doppler waveform information obtained using current state-of-the art equipment. Second, having established the normal cystic artery waveform appearance, this information was used to examine the gallbladders of patients undergoing extracorporeal gallstone lithotripsy. A preliminary investigation of patients with the classical clinical and sonographic criteria of acute cholecystitis was also carried out. Anatomical studies show that in 95% of cases the cystic artery branches from the main right hepatic artery and courses around the neck of the gallbladder before dividing into superficial and deep branches supplying the hepatic and peritoneal surfaces of the gallbladder.g CDFI consistently demonstrated this anatomy in 21 of our 30 (70%)volunteers, and in 18 of 30 (60%)of patients examined before and after lithotripsy. In 3 volunteers, variation in cystic artery blood supply was seen and in the remaining 6, no cystic artery flow could be demonstrated. The cystic artery waveforms obtained in both the volunteer and the BL groups were consistent in appearance, had high diastolic flows in keeping with the blood supply to a low impedance vascular bed, and were similar to the right hepatic artery waveforms. The PI allows quantitative data to be obtained when the beam angle is difficult to align with the long axis of the vessel. This index is more sensitive in detecting alterations in the waveform. It takes into account the mean velocity in contrast to the resistive index, which uses the peak velocity as the denominator.' The mean PI for the right hepatic artery in our study was 0.98 and for the cystic artery was 1.04. This difference was not statistically significant and although one might expect the smaller diameter cystic artery PI to increase relative to the larger right hepatic artery, this was not substantiated VOL. 20, NO. 7, SEPTEMBER 1992

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and may be a reflection of the different distal branching network of the two systems. Similarly, no significant difference in the cystic artery PI was identified following lithotripsy. Biliary lithotripsy is a recognized form of nonoperative treatment for gallbladder stones. There are currently 11 manufacturers of secondgeneration lithotripsy machines. These produce shock-waves from three major energy sources: electromagnetic generator, piezoelectric crystals, or underwater electrostatic spark discharge. The safety and efficacy of biliary lithotripsy using these different machines remains under evaluation. There have been several studies demonstrating both macro- and microscopic hepatic and gallbladder wall hematomas following extracorporeal shockwave administration with a variety of l i t h o t r i p t e r ~ . l ~ -These '~ changes tend to be found in the early postlithotripsy treatment period and have largely resolved by one week. The preliminary results of the 10 acute cholecystitis patients would suggest that the cystic artery flow was decreased to a level below the sensitivity of the CDFI unit used. This was apparent in all except 1 individual, whose cystic artery waveform was similar to that of the volunteer group. One further patient had an apparent increased blood flow to the gallbladder wall. This was a subjective impression based on the normal appearances established in the control group. The inability to identify flow in the remainder may reflect the degree of anatomical distortion and compression of the gallbladder blood supply caused by wall thickening and surrounding fluid. It is reasonable to speculate that at some point in the evolution of the inflammatory process, the cystic artery blood supply would have a more resistive pattern indicating greater peripheral resistance distally. This may occur at a subclinical stage of the inflammatory process and represent an early stage in disease progression. Clearly, the number of patients studied to date is not sufficient to draw any firm conclusions. However, it appears that CDFI has limited application in acute calculous cholecystitis where the real-time sonographic appearances are typical. These results support the findings of Freimanis et al., who reported a lack of sensitivity of CDFI in detecting the vascular changes in 7 patients with acute ch01ecystitis.l~It may be interesting to study serially obtained cystic artery waveforms of in-hospital patients at risk for developing acute acalculous cholecystitis to look for a possible early predictor of the underlying disease process. Technically, although we were aware of the

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gallbladder blood supply in anatomical terms, in the early phase of the volunteer study, demonstration of flow in the cystic artery was difficult to elucidate with examinations lasting up to 45 minutes. This was resolved somewhat by setting the color Doppler flow threshold as low as possible (0.09 to 0.16), allowing the sensitivity of the system for identifying flow in small caliber vessels to be increased. The cine loop facility also proved helpful in obtaining good-quality color flow images of the cystic artery and helped to reduce the examination times to the order of 25 minutes to 30 minutes. It became evident that patients were best imaged in the LPO position with the transducer positioned obliquely in the sagittal plane angling through the long axis of the gallbladder toward the right shoulder.

ACKNOWLEDGMENT We thank Betty Fowler for her help in the preparation of the manuscript.

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JA, Sinnet HD: Color Doppler in breast disease. Radiology 173(P):361, 1989. 6. Delius M, Brendel W: Mechanisms of action in extracorporeal shock wave lithotripsy: Experimental studies, in Biliary Lithotripsy, Ferrucci JT, Delius M, Burhenne H J (eds). Year Book Medical Publishers, Chicago, 1989, pp 31-42. 7. Stephenson TJ, Johnson AG, Ross B: Short term effects of extracorporeal shock wave lithotripsy on the human gallbladder. J Pathol 158:239- 246, 1989. 8. Nelson TR, Pretorius DH: The Doppler signal: Where does it come from and what does it mean? A J R 151:439-447, 1988. 9. Schwartz SI. Gallbladder and extrahepatic biliary system, in Principles of Surgery (Vol 2, ed 5) Schwartz SI, Shires GT, Spencer FC (eds). 1989, McGraw-Hill, New York. pp 1381-1412. 10. Malone DE, Rawat B, Fache JS, Quenville NF, Burhenne HJ: The intercostal pathway for biliary extracorporeal shockwave lithotripsy. Radiology 174:349-351, 1990. 11. Becker CD, Blake-Gilks C, Burhenne HJ: Biological effects of biliary shockwave lithotripsy in swine. Invest Radiol 24:366-370, 1989. 12. Malone DE, Becker CD, Reich KD, Quenville NF, Burhenne HJ: Soft tissue effects of biliary extracorporeal shockwave lithotripsy in swine. Br J Radiol 62:843-848, 1989. 13. Chapman WC, Kaufman AJ, Parish KL, Stephens WH, Price RR, Williams LF Jr: Preliminary biliary studies with an ultrasonic extracorporeal lithotripter, in Biliary Lithotripsy II, Burhenne HJ, Paumgartner G, Ferrucci J T (eds). Chicago: Year Book Medical Publishers, 1990, pp 29-36. 14. Ell CH, Kerzel W, Heyder N, et al: Tissue reactions under piezoelectric shockwave application for the fragmentation of biliary calculi. Gut 30:680-685, 1989. 15. Freimanis MG, Bohm-Velez M: Color and duplex Doppler Ultrasound of the gallbladder in acute cholecystitis. J Ultrasound Med 9:S26, 1990.

JOURNAL OF CLINICAL ULTRASOUND

Color Doppler imaging of the cystic artery.

Color Doppler ultrasonography was used to examine the gallbladder vascular supply in 30 volunteers and in 30 biliary lithotripsy patients pre- and 2 h...
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