Chronic mesenteric arterial occlusive disease

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1 Duplex Doppler Sonography of Celiac Trunk and Superior Mesenteric Artery: Comparison with Intra-arterial Angiography Reinhold Mallek, MD, Gerhard H Mostbeck, MD, Reinhard M Walter, MD, Andreas Stumpflen, MD, Thomas Helbich, MD, Dimiter Tscholakoff, MD DDS was compared to intra-arterial angiography for the diagnosis of significant (> 50%) stenoses of the celiac trunk and the SMA in 38 consecutive patients referred for angiographic evaluation of peripheral arterial occlusive disease Celiac trunk occlusion was correctly identified by DDS in three of three patients In patients with significant celiac trunk stenoses, mean peak systolic velocity was 246 (± 154) cm/sec and differed significantly (P < 005) from the peak systolic velocity (101 ± 22 cm/sec) of 22 patients with no angiographic evidence of significant stenosis Five false-negative DDS examinations in patients with >50% celiac trunk stenoses were noted Using a peak systolic velocity of > 160 cm/sec (mean value in normal vessels plus 3 standard deviations) to diagnose >50% celiac trunk stenosis, sensitivity of DDS was 57% and specificity was 100% However, considering celiac trunk stenoses and occlusions as a single group, the sensitivity rate of DDS in diagnosing significant stenosis and occlusion of celiac trunk was 70% KEY WORDS: Ultrasound, Doppler studies; Ultrasound, comparative studies; Arteries, mesenteric Chronic mesenteric arterial occlusive disease frequently has unspecific abdominal symptoms as its presenting feature Because of the lack of characteristic clinical signs, diagnosis is diffi- ABBREVIATIONS DDS, Duplex Doppler sonography; SMA, Superior mesenteric artery; RI, Resistive index; CHA, Common hepatic artery; RR, Blood pressure; SD, Standard deviation Received July 30, 1992, from the Departments of Radiology (RM, GHM, RMW, TH, DT) and Angiology (AS), University of Vienna, Vienna, Austria Revised manuscript accepted for publication December 28, 1992 Address correspondence and reprint requests to Doz, Dr Gerhard Mostbeck, Univ Klinik fuer Radiodiagnostik, Waehringer Guertel 18-20, A-1090 Vienna, Austria Acknowledgment: This study was supported by a grant from the Ludwig Boltzmann-Institute for Radiologic Tumor Research, Uni~ versity of Vienna, Vienna, Austria cult Invasive procedures, such as angiography, gen erally are not part of the initial evaluation Thus, diagnosis of this rare disease often is delayed tj The application of duplex technology has been extended to intra-abdominal imaging Numerous studies document the value of DDS in assessing the visceral hemodynamics and quantitating the hemodynamic response to physiologic and pharmacologic stimuli both in volunteers and in patients 4-12 Case reports describing the application of DDS for the detection of mesenteric arterial occlusive lesions suggested that ODS might be an effective screening modality to select patients for invasive angiography 2,J, 13-l!i Two retrospective studies evaluated DDS criteria for the diagnosis of splanchnic artery stenoses and compared DDS with angiography The authors of both reports recommend DDS as a screening test for the diagnosis of significant mesenteric artery stenoses1611 However, no prospective studies have compared 1993 by the American Institute of Ultrasound in Medicine J Ultrasound Med 12: , /931$350

2 338 CELIAC TRUNK AND SMA J Ultrasound Med 12: , 1993 the diagnostic capability of DDS with angiography The present study attempts to (1) establish normal values for our laboratory for peak systolic velocity measured in the celiac trunk and the SMA by DDS, and (2) evaluate how DDS compared to intra-arterial angiography in the detection and grading of splanch nic artery stenoses PATIENTS AND METHODS The study population consisted of 38 consecutive patients (13 female, 25 male; mean age, 65 years; range, 32 to 82 years) referred to our department for angiographic evaluation of arteriosclerotic peripheral vascular disease After informed consent was obtained, all patients were studied with DDS immediately before intraarterial angiography with an ATL MK 600 unit (ATL, Bothell, WA) using a 35 MHz mechanical sector transducer equipped with a 30 MHz pulsed Doppler probe All patients were scanned after an overnight fast by one radiologist experienced in Doppler techniques (RM) DDS examinations were performed with the pa tient in the supine position In sagittal and transverse planes, the following DDS data were obtained: peak systolic velocity and RI (defined by A - BIA, where A is the peak systolic frequency shift and B the enddiastolic frequency shift) within 2 cm of the origin of the celiac trunk Multiple measurements were performed within this vessel, and careful attention was paid to detect the highest frequency shift in that area If Doppler spectral analysis demonstrated signs of stenosis, the two highest velocity values were documented and consecutively averaged for statistical analysis Our rationale for selection of this site for measurement relied on the characteristic location of celiac trunk stenoses Averaging series of measurements for data analysis might reduce the operatordependent variability of obtained velocities, as accurate angle correction near the origin of the curved vessel is difficult Peak systolic velocity and RI of the SMA were measured at its origin and 3 cm distally within the straight segment of the mainstem (Fig 1) Selection of these sampling sites was based on technical considerations as well as on the idea of correlating changes in velocity and pulsatility parameters within the proximal portion of the SMA's mainstem to collateral blood flow in cases of celiac axis occlusion The Doppler angle was less than 60 degrees, and peak systolic velocity readings were obtajned by angle correction Range gate length was 3 to 5 mm DDS studies were interpreted without knowledge of the intra-arterial angiographic results B-mode im Figure 1 Sagittal scan 0 the abdominal aorta DDS sample volume in the center of the celiac trunk at its origin (open arrow) The proximal SMA is indicated by a curved arrow ages were evaluated to identify possible anatomic variants of the mesenteric vasculature and to rule out aneurysmal dilation of the abdominal aorta at the origin of the visceral arteries Occlusion was diagnosed if, in the absence of anatomic variants, no Doppler signals were obtained from the visible celiac trunk Additionally, flow direction was assessed in the CHA Retrograde flow in the common hepatic artery due to collateral circulation was interpreted as a sign of celiac trunk occlusion Intra-arterial digital subtraction angiography was performed via the femoral route with a 5 Fr pigtail catheter Fifteen milliliters of a low osmolar nonionic contrast medium Oopamiro 300, Gerot, Vienna, Austria), diluted to 30 ml with saline solution, was injected at a rate of 15 ml/sec with the pigtail catheter positioned slightly above the origin of the celiac trunk Anteroposterior and lateral views of the upper abdominal aorta, celiac trunk, and SMA were obtained, followed by the study of the lower extremity arteries, Angiographic studies of the visceral arteries were interpreted by consensus opinion of two experienced radiologists (RW, DT) blinded to the results of DDS The following scoring system was used: 0 = normal finding; 1 = vessel wall irregularities; 2 = < = 50% reduction of vessel diameter; 3 = >50% reduction of vessel diameter-significant stenosis; 4 = occlusion of vessel AJI patients were evaluated by the referring angiologists for the presence of an epigastric bruit, arterial hypertension, and cardiac insufficiency None of the

3 ] Ultrasound Med 12: , 1993 MALLEK ET AL 339 Table 1: Intra-arterial Angiography Scores: Peak Systolic Velocity and RI in Celiac Trunk and SMA Score Celiac Trunk Origin 3 cm Distally CHA SMA n PSV RI n PSV RI PSV RI n flow c1779r 074 (005) (3528) 088 (005) (4073) 092 (006) c282w 073 (007) (268) o89 coosr (6737) 092 (006) 28 Antegrade (30 99) 078 (001) (15378} 073 (009) 4 3 (3) (106) 092 (005) 1870 (97) 077 (019) 3 Retrograde Data are expressed as mean peak systolic velocity (± 1 SD) in cm/sec Each asterisk indicates one technically unsuccessful DDS examination n "' Number of observations in each score group SMA, Superior mesenteric artery; CHA, common hepatic artery; PSV, peak systolic velocity; RI, Resistive index patients suffered from symptoms common to mesenteric ischemia, such as colicky abdominal pain postprandially or cachexia, nor did any of them have clinical evidence of malabsorption An epigastric bruit was diagnosed in two of nine patients with significant celiac trunk stenosis Two patients suf fered from cardiac congestion, and another 11 patients experienced arterial hypertension (RR > 140/90 mm Hg) Differences in peak systolic velocity and RI in the five groups of angiographic scores were tested for statistical significance using the Kruskal Wallis test A P value < 005 was considered statistically significant Results are presented as means ± 1 SD RESULTS Angiographic Results The results of the visceral intra-arterial angiography are summarized in Table 1 for our patient group Of nine significant stenoses of the celiac trunk, eight were classified as intrinsic and one as extrinsic None of the 38 patients was found to have aneurysmal dilation of the abdominal aorta at the origin of the visceral arteries with either intra-arterial angiography or DDS One patient revealed a hepatomesenteric trunk No significant stenoses of the SMA were diagnosed Sonographic Results, Including Duplex Doppler Results Results of DDS examinations are summarized in Table 1 In six patients (16%) the celiac trunk and in five patients (13%) the SMA were not sufficiently visualized to obtain a Doppler signal In three patients (8%) neither vessel could be imaged by DDS DDS correctly identified the patient with the hepatomesen teric trunk, as well as three patients with occlusions of the celiac trunk In these three patients, retrograde perfusion of the common hepatic artery was noted (Fig 2A and B; Table 1) In celiac trunk DDS, a statistically significant difference (P < 005) was seen in the peak systolic velocity of patients with signifi cant stenosis (score 3) versus the normal group (score 0) or patients with no angiographic evidence of sig nificant stenosis (scores 1 and 2) (Fig 3) Using a threshold peak systolic velocity value of 160 cm/sec (the mean value in patients without angiographic evidence (score O] of arteriosclerotic lesions plus 3 SD) to diagnose a significant stenosis of the celiac trunk, the sensitivity rate was 31 % when the six technical failures are considered false-negative examinations However, for patients with good visualization of the celiac trunk, the sensitivity rate for diagnosing a significant stenosis was 57% Considering stenoses and occlusions of the celiac trunk as a single data group, DDS yielded a sensitivity of 70% With no falsepositive DDS examinations, the specificity rate was 100% The RI obtained in the celiac trunk was lower than the RI obtained at both locations of the SMA (Table 1) No significant difference was found between the RI values obtained in different score groups of arteriosclerosis in the celiac trunk or the SMA (Table 1) DISCUSSION Stenoses of the celiac and mesenteric arteries are common in patients with atherosclerotic disease that affects the peripheral vascular system tj, 1s19 Therefore, consecutive patients referred for angiographic evaluation of their lower limb arteries formed a good cohort for this prospective study comparing the abilities of DDS and intra-arterial angiography to detect and diagnose significant stenoses of the visceral arteries As indicated in our study, only a minority of patients with stenoses of the celiac trunk and SMA initially have clinical symptoms of chronic mesenteric

4 340 CELIAC TRUNK AND SMA A B Figure 2 A, Transverse scan of upper abdomen in a patient with celiac trunk occlusion Sample volume in the center of the common hepatic artery (arrow) The splenic artery is indicated by a curved arrow B, Corresponding Doppler spectrum above zero line indicates retrograde perfusion of the common hepatic artery ischemia 12)it19 However, even in symptomatic patients, clinical findings are nonspecific, often leading to a delayed diagnosis -3ic; On the other hand, symptoms of intestinal angina have been reported to precede the catastrophic event of bowel infarction due to mesenteric vessel thrombosis1i Thus, the clinical problem of patient selection for invasive diagnostic procedures arises Angiography can establish a definitive diagnosis of mesenteric arterial occlusive disease and identify patients who might benefit from optional percutaneous transluminal angioplasty or J Ultrasound Med 12: , 1993 surgical revascularization1 However, a noninvasive modality like DDS, with a high sensitivity and specificity, could diagnose occlusive lesions of mesenteric arteries, reduce the prevalence of missed diagnosis, and help to avoid unnecessary angiography16,11 DDS and color Doppler ultrasonography with measurement of peak systolic velocity have become the standard modality to diagnose noninvasively and grade arterial occlusive disease of the extracranial carotid arteriesjo The origin of the visceral arteries from the ventral abdominal aorta, as well as the characteristic location of stenotic lesions at the vessels' origin and mainstems, might be factors facilitating a DDS examination15,21 Case reports on visceral artery DDS describe high systolic velocities as characteristic signs of stenoses Furthermore, two retrospective studies comparing DDS to intra-arterial angiography found a high sensitivity for DDS in the diagnosis of visceral artery stenoses16,17 The results of our prospective study confirm the diagnostic value of DDS in cases of adequate sonographic visibility of the mesenteric arteries but revealed several limitations of the DDS technique in the application to the mesenteric vasculature Velocity measurements in the celiac trunk in the group without angiographic evidence of atherosclerotic changes ranged from 78 to 145 cm/sec, yielding a mean of 104 (± 18) cm/sec This is consistent with values reported in previous studies for fasting volunteersis17 Therefore, a peak systolic velocity within this range might be considered a normal value for the fasting state A significant stenosis of the celiac trunk was demonstrated by intra arterial angiography in nine of 38 patients Peak systolic velocity obtained by DDS in seven of these nine patients ranged from 99 to 542 cm/sec (Fig 3) Although the mean peak systolic velocity in patients with significant stenoses (246 ± 154 cm/sec) differs significantly (P < 005) from that in patients without significant lumen narrowing (101 ± 22 cmlsec), there was some overlap of data One patient with a peak systolic velocity of 99 cm/sec was thought to have a ligamentous compression with an extrinsic stenosis of the celiac trunk demonstrated by intra-arterial angiography Lower extremity angiography did not show any evidence of atherosclerotic lesion but did demonstrate a single stenosis of the left popliteal artery, later confirmed as cystic adventitial degeneration at surgery Intra-arterial angiography of the visceral arteries is performed during deep expiration, thus accentuating vessel compression by the median arcuate ligament 22 In contrast, DDS was performed during deep inspiration and might therefore have missed this type of stenosis In a second patient, with a peak systolic

5 J Ultrasound Med 12; , 1993 MALLEK ET AL 341 PSV cm/sa: 4SO 400 3SO WO ISO 1fNI 0 " SCOREO -! f SCORE I f -- * I~ SCORE2 SCORE J Figure 3 Scattergram and mean values ( ± 1 SD) of peak systolic velocity (PSV) by DDS versus intra ~arterial angiography score Asterisk indicates a statistically significant difference (P < 005) peak systolic velocity in group 3 compared to score groups 0, 1, and 2 velocity of 119 cm/sec, a significant, short eccentric stenosis demonstrated by angiography was missed by DDS Using a peak systolic velocity of 160 cm/sec as the threshold value, a specificity rate of 100% and a sensitivity rate of 31 % for diagnosis of significant stenoses of the celiac trunk was established when nonvisualization of the celiac trunk was considered a falsenegative examination However, excluding technical failures would result in a sensitivity rate of 57% for DDS for diagnosis of significant celiac trunk stenosis As significant stenoses and occlusions are thought to have the same clinical implications, both of these could be considered as a single group in data analysis17 Therefore, the sensitivity of DDS in the diagnosis of significant celiac trunk stenosis and occlusion was 70% Moneta and colleagues17 proposed a peak systolic velocity of > 200 cm/sec as the threshold velocity for diagnosing a high grade (>70%) stenosis of the celiac trunk Using this criterion, a sensitivity rate of 75% for the diagnosis of high-grade stenosis has been reported17 However, this was a retrospective study and technically unsatisfactory DDS examinations were excluded Furthermore, occlusions and highgrade stenoses were considered a single group for data analysis Their data compare favorably compare with our results Celiac trunk occlusion was diagnosed by DDS in our study in three of three patients and verified by intra-arterial angiography In addition to absent Doppler signals from the ultrasonographically visible trunk, evaluation of flow direction in the common hepatic artery proved to be another diagnostic criterion of celiac trunk occlusion, as has been demonstrated by Bowersox and colleagues in two of three patients16 Collateral circulation leads to a retrograde perfusion of the common hepatic artery, easily depicted by DDS 19 This might be of specific value in patients without ultrasonic visualization of the celiac trunk Peak systolic velocity in the SMA of these three patients was higher than in patients without occlusion and increased within the proximal portion of the vessel This increase in peak systolic velocity was accompanied by a decrease in RI (Table 1) Although not statistically significant and limited to only three observations, this finding of collateral perfusion might be of additional value in the diagnosis of celiac axis occlusion The capability of DDS using peak systolic velocity to diagnose SMA stenoses was not definitely established by our study because no significant stenosis was demonstrated by intra-arterial angiography Due to nonvisualizauon of the SMA in five patients, up to five false-negative results could have been possible using DDS in comparison to angiography A mean peak systolic velocity of 140 (±43) cm/sec at the origin of the SMA is in agreement with observations reported previously 1o1s-11 A slight decrease in peak systolic velocity to 123 (±56 cm/sec) more distally was accompanied by an increase in RI from 088 to 092 (Table 1) These results correspond to previously published data indicating a high vascular impedance of the SMA in the fasting state23 The uniformity of RI values in all score groups precludes using this parameter as a discriminatory feature in the diagnosis of vessel stenosis This is in accordance with the results of a recent study demonstrating that semiquantitative DDS parameters are not useful in predicting significant mesenteric vessel stenoses17 Mean RI values in the score 0 group compare favorably with data in the literature detailing low resistance in the vasculature of the liver and the spleen 9 Our results indicate that DDS of the celiac trunk is valuable for the diagnosis of significant vessel stenosis However, several factors limit the use of DDS in the evaluation of mesenteric vessels: 1 Visualization of these vessels may be compromised owing to obesity or overlying bowel gas, thus decreasing sensitivity in comparison to angiography In our study, as a result of nonvisualization of the celiac trunk, two of nine significant stenoses were missed by DDS Previous studies document adequate ultrasonographic visualization of the celiac axis and

6 342 CELIAC TRUNK AND SMA J Ultrasound Med 12: , 1993 proximal SMA in up to 90% of patients 24 These data are comparable to our results In regard to missing six of 12 stenotic celiac arteries in their study, Bowersox and coworkers stated that the inability to visuajize the stenotic vessel precluded the application of numeric accuracy methods16 Therefore, nonvisualization of the mesenteric arteries remains a significant limitation of DDS 2 Limited examination of the entire vessel with conventional DDS might be another reason for its imperfect sensitivity As a result of determining peak systolic velocity near the vessel's origin, where stenoses most likely occur, two significant stenoses located more distally were missed Deep location, small size, and anatomic variability of the mesenteric vasculature25 are drawbacks in real-time imaging and contribute to the limited sensitivity of conventional DDS Alternatively, it has been speculated that collateral circulation providing adequate inflow pressure from the SMA could result in the absence of increased velocity across a significant celiac stenosis16 In support of this concept, we observed reversed flow in the CHA in all patients with celiac trunk occlusion In conclusion, our results suggest the use of DDS as first-line study in the evaluation of suspected mesenteric artery stenosis and occlusion A peak systolic velocity of > 160 cm/sec is a highly specific indicator of a significant celiac trunk stenosis and implies the need for invasive angiography in the symptomatic patient Real-time visualization of the celiac trunk without detectable Doppler signals, combined with a decreased RI of the SMA and retrograde perfusion of the common hepatic artery, are characteristic DDS findings in patients with celiac trunk occlusion Thus, provided that there is good sonographk visualization, DDS is a valuable tool in the diagnosis of stenoses and occlusions of the celiac trunk REFERENCES 1 Chronic intestinal ischaemia (editorial) Lancet 2:1332, Nicholls StC, Kohler TA, Martin RL, et al: Use of hemodynamic parameters in the diagnosis of mesenteric insufficiency J Vase Surg 3:507, Yedlicka JW, Hunter DW: Evaluation of suspected chronic mesenteric ischemia with Duplex sonography Semin Intervent Radio! 7:39, Qamar Ml, Read AE, Skidmore R, et al: Transcutane ous Dopper ultrasound measurement of celiac axis blood flow in man Br J Surg 72:391, Qamar MI, Read AE, Skidmore R, et al: TranscutaneT ous Doppler ultrasound measurement of superior mes enteric artery blood flow in man Gut 27:100, Van Bel F, Van Zwieten PHT, Guit GL, et al: Superior mesenteric artery blood flow velocity and estimated volume flow; Duplex Doppler US study of preterm and term neonates Radiology 174:165, Qamar MI, Read AE, Skidmore R, et al: Pulsatility index of superior mesenteric artery blood velocity waveforms Ultrasound Med Biol 12:773, Taylor KJW, Burns PN: Duplex Doppler scannjng in the pelvic and abdomen Ultrasound Med Biol 11:643, Taylor KJW, Burns PN, Woodcock JP, et al: Blood flow in deep abdominal and pelvic vessels: Ultrasonic pulsed Doppler analysis Radiology 154:487, Jager K, Bollinger A, Valli C, et al; Measurement of mesenteric blood flow by Duplex scanning J Vase Surg 3:462, Aldoori Ml, Qamar MI, Read AE, et al: Increased flow in the superior mesenteric artery in dumping syn drome Br J Surg 72:389, Best IM, Pitzele A, Green A, et al: Mesenteric blood flow in patients with diabetic neuropathy J Vase Surg 13:84, Jager KA, Fortner GS, Thiele BL, et al: Noninvasive diagnosis of intestinal angina J Clio Ultrasound 12:588, Kaude JV, Wright PG: Ultrasonic demonstration of celiac artery stenosis ROFO 135:108, Flinn WR, Rizzo RJ, Park JS, et al: Duplex scanning for assessment of mesenteric ischemia Surg Clin North Am 70:99, Bowersox JC, Zwolak RM, Walsh DB, et al: Duplex ultrasonography in the diagnosis of celiac and mesenteric artery occlusive disease J Vase Surg 14:780, Moneta CL, Yeager RA, Dalman R, et al: Duplex ultrasound criteria for diagnosis of splanchnic artery stenosis of occlusion J Vase Surg 14:511, Reiner L, Jimenez FA, Rodriguez FL: Atherosclerosis in the mesenteric circulation Observations and correlations with aortic and coronary atherosclerosis Am Heart J 66:200, Bron KM, Redman HC: Splanchnic artery stenosis and occlusion Incidence; arteriographic and clinical manifestations Radiology 92:323, Cardoso TJ, Middleton WO: Duplex and color Doppler ultrasound of the carotid arteries Semin Intervent Ra diol 7:1, Derrick JR, Pollard HS, Moore RM: The pattern of arteriosderotic narrowing of the celiac and superior mesenteric arteries Ann Surg 149:684, Reuter SR: Accentuation of celiac compression by the median arcuate ligament of the diaphragm during deep expiration Radiology 98:561, Grant EG, White EM: Duplex Sonography New York Springer-Verlag, 1988, p Muller JE, Niederau CL, Fritsch WP: Real time Sonographie der Arterien und Venen im Oberbauch Deutsch Med Wschr 107:809, Dunbar JD, Molnar W, Beman FF, et al: Compression of the celiac trunk and abdominal angina AJR 95:731, 1965

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