Duplex Scanning for Assessment of Mesenteric Ischemia

Noninvasive Diagnosis of Vascular Diseases

0039-6109/90

$0.00+ .20

Duplex Scanning for Assessment of Mesenteric Ischemia William R. Flinn, MD, * Robert]. Rizzo, MD, t lang Sang Park, MD, PhD;t. and Gail P. Sandager, RN, RVT§

Mesenteric arterial occlusive disease is rare, and the diagnosis is frequently delayed until other causes of visceral pathology have been investigated or until intestinal infarction has occurred, at which point the outcome frequently may be fatal. Occlusive lesions of splanchnic vessels can be visualized by arteriography, but no reliable, less-invasive diagnostic examination has previously been available. Further, radiographic images offer no objective physiologic data, which is of particular importance in cases of chronic visceral ischemia. Dye-dilution techniques have been used to measure splanchic blood flow in man but have not achieved widespread acceptance owing to their complexity and invasive nature. Duplex scanning (real-time B-mode ultrasound imaging and Doppler frequency spectral analysis) has become the standard noninvasive diagnostic examination for the evaluation of extracranial carotid artery occlusive disease. More recently, this technique has been described for the detection of abnormalities in peripheral arteries and the aorta and its major branches. The mesenteric vessels (celiac and superior mesenteric arteries) seemed particularly suitable for deep abdominal duplex examination owing to their predictable ventral origins off the aorta and the characteristic ostial'location of most occlusive lesions. The initial experience with mesenteric duplex scanning has produced preliminary observations of interest to the investigation of splanchnic blood flow. Clinical cases of mesenteric arterial occlusive disease are rare, so the clinical evaluation of this technique would be difficult were one to examine only patients with significant disease. Also, acute mesenteric ischemia frequently produces an associated ileus with distended bowel loops, making ultrasound scanning unreliable. Thus, the initial evaluation of mesenteric duplex scanning has largely involved three major areas of investigation: (1)

*Associate Professor of Surgery,

Division of Vascular Surgery, Department of Surgery, Northwestern University Medical School, Chicago, Illinois tChiefResident in Thoracic Surgery, Brigham and Women's Hospital, Boston, Massachusetts *Assistant Professor, Department of Surgery, Catholic Medical College, Seoul, Korea §Technical Director, Vascular Laboratory, Columbus Hospital, Chicago, Illipois This article was supported in part by the Feinberg Cardiovascular Research Institute.

Surgical Clinics of North America-Vol. 70, No.1, February 1990

99

100

WILLIAM

R.

FLINN ET AL.

Figure 1. A sagittal B-mode scan of the abdominal aorta (patient's head is to the left) demonstrating the easily identifiable celiac artery and superior mesenteric arteries (SMA) in a normal subject. (From Flinn WR, Lilly MP, Sandager GP, et al: Measurement of mesenteric blood flow using duplex scan. In Bernstein EF (ed): Recent Advances in Noninvasive Diagnostic Techniques in Vascular Disease, 3rd ed. St. Louis, CV Mosby, 1989; with permission.)

assessment of splanchnic blood Bow in normal subjects, (2) Bow responses to physiologic and pharmacologic stimuli, and (3) evaluation of mesenteric revascularization procedures. Discussion of these areas follows a brief description of the basic technique employed for mesenteric arterial duplex scanning.

TECHNIQUE FOR MESENTERIC DUPLEX SCANNING Oral intake is withheld from patients overnight prior to initial mesenteric arterial duplex scanning because intestinal gas will obviously compromise B-mode imaging, and food ingested prior to any examination may compromise the physiologic accuracy of results. Scans are performed with the patient supine and the head elevated 20 to 30 degrees. Sagittal B-mode imaging of the abdominal aorta is performed using a 3-MHz medium-focus probe to identify the celiac and superior mesenteric arteries near their char!lcteristic ventral origins from the aorta (Fig. 1). A 3-MHz pulsed Doppler transducer is used to record Bow velocities in these vessels approximately 1 to 3 cm from the origins of the vessel. The significant parameters for assessment (as will be evident from the studies outlined below) appear to be peak systolic velocity, diastolic velocity, and, in the superior mesenteric artery (SMA), the presence of diastolic reverse Bow. Most currently available duplex scanners allow a direct output of Bow velocity from the microprocessor unit. In all cases, this represents an onboard calculation from the frequency shift detected by the pulsed Doppler; thus, to an extent, it is dependent upon the angle of insonation. Measurements of Bow velocity may be less dependent upon the precise angle of insonation than changes in frequency shift; therefore, it is more useful for assessment of visceral arteries whose course may be difficult to follow precisely within the abdomen. Nevertheless, it must be recognized that variation in the angle of pulsed Doppler sampling will introduce error into individual measurements (especially at angles in excess of 70 degrees), and attention must be paid to this parameter during the course of the ex-

DUPLEX SCANNING FOR MESENTERIC ISCHEMIA

101

Figure 2. The SMA How-velocity waveform in a normal fasting volunteer shows a triphasic configuration that is reminiscent of higher-resistance peripheral arteries.

amination. We have observed 60 to 70 per cent increases in measured peak systolic velocities and mean velocities in the SMA when the angle of insonation exceeded 70 degrees. As will be seen in the following section, recognition of this source of sampling error is critical to the analysis of clinical data. DUPLEX-SCAN EVALUATION OF NORMAL SPLANCHNIC BLOOD FLOW

The normal SMA spectral pattern demonstrates organized flow throughout the cardiac cycle and, in the fasting state, characteristically has flow reversal in early diastole (Fig. 2). This is similar to the higher-resistance outflow vessels in the periphery. Normal celiac artery velocity waveform demonstrates organized flow in systole and somewhat disorganized diastolic flow with continuous forward flow throughout diastole and no diastolic flow reversal (Fig. 3). These waveforms are reminiscent of the low-outflow-resistance system seen in the internal carotid artery. Fasting peak systolic velocities (PSVs) in the SMA of normal healthy volunteers have ranged from 103 to 196 cm per second in currently reported clinical studies.2-4,6,7 Diastolic velocities observed in the SMA have ranged from 15.8 to 55 cm per second. Celiac artery PSVs in normal fasting volunteers have been reported from 118 to 163.6 cm per second, and diastolic velocities of 33 to 73.8 cm per second have been observed in these celiac arteries. 2,4,6,7 The substantial variations in some of these observed fasting

102

WILLIAM

R.

FLINN ET AL.

Figure 3. The characteristic normal fasting celiac artery How-velocity waveform demonstrating continuous forward How throughout diastole (horizontal arrow).

flow velocities have not been well explained to date, but certainly some consideration must be given to anatomic variation of the deep abdominal vessels as well as control of the angle of insonation. At the present time, however, the absolute value of the fasting flow velocities in these visceral vessels may not be as important as observations made about the changes produced by a variety of physiologic and pharmacologic stimuli to splanchic perfusion. QuamarlO,ll used the average fasting flow velocities measured by duplex scan from the celiac and SMA and the B-mode ultrasound image to measure vessel diameter and thus calculate volume flow in these vessels (flow velocity X cross-sectional area), This was in an attempt to approximate noninvasively previous studies that used invasive flow-measurement techniques. 8,g Mean fasting SMA flow (SMABF) in normal subjects was calculated to be just over 500 ml per minute, with a range of 250 to 890 ml per minute; this was similar to measurements made using invasive dye-dilution techniques,8,g Fasting celiac flow was approximately 700 ml per minute in 42 normal subjects, The relative shortcomings of this method include the fact that measurement of vessel diameter requires mechanical placement of cursor points on the B-mode image and the assumption that the vessel diameter sampled is circular. Also, few duplex units have on-board capabilities to calculate mean velocity throughout the cardiac cycle, which requires integration of the Doppler spectral curve. Perhaps most importantly, frequency or velocity analyses have been demonstrated to be more accurate than volume-flow measurements for the detection of arterial occlusive lesions, 7

DUPLEX SCANNING FOR MESENTERIC ISCHEMIA

103

FLOW RESPONSES TO PHYSIOLOGIC AND PHARMACOLOGIC STIMULI Jager and colleagues3 measured postprandial flow velocities in the SMAs of 20 normal subjects after a 1000-calorie test meal. The most striking observations were recognizable changes in the systolic and diastolic flow components in the velocity waveforms. Within 15 minutes after eating, a significant increase in peak systolic SMA flow velocity was observed. This reached a maximum of almost double the baseline flow velocity 45 minutes after eating and returned to normal levels by 90 minutes. During this same period, diastolic velocity increased to almost three times fasting levels. This dramatic postprandial increase in diastolic velocity appeared to be the most predictable spectral change in the SMA velocity waveforms. Nicholls and associates 7 used duplex scanning to assess flow-velocity changes in the celiac and SMA that occurred in 15 normal subjects 1 hour postprandially. No significant changes in postprandial celiac velocities were observed in this study, but systolic velocity in the SMA increased postprandially (182.6 IE 203 cm per second). The most dramatic change was an almost complete disappearance of diastolic flow reversal in the SMA after eating, with a concomitant significant increase in diastolic flow velocity (42.78.6 cm per second; P < 0.01). Quamar and colleagues l l measured celiac artery blood flow (CABF) at intervals after a 405-calorie liquid meal. Postprandial CABF increased by 38 per cent (P < 0.05) almost immediately after the meal. This significant increase was very transient, however, and flow returned to normal levels within 30 minutes after eating. Moneta and coworkers6 measured celiac and SMA flow velocities in normal subjects after the ingestion of a series of different dietary components with variable caloric contents and osmolarities. These all were prepared as 300-cc volumes and included a mixed meal, carbohydrate, fat, protein, mannitol, and water. Serial scans were performed in each subject 10 to 90 minutes postprandially. There were 20 to 24 per cent increases in celiac systolic and diastolic flow velocities after the mixed meal, but no statistically significant changes in celiac artery flow parameters were observed after any of the test meals. In contrast, SMA flow velocities increased significantly after all of the test meals except water. Flow-velocity changes appeared to occur earlier after the carbohydrate meal, but the fat and mixed meals produced the maximal increases in duplex parameters. These studies seemed to demonstrate that mesenteric duplex scans can be performed relatively easily in normal individuals with minimal preparation. Trained vascular technologists with a knowledge of visceral arterial anatomy can perform scans expeditiously without undue technical difficulties in most cases. There were recognizable differences in fasting flow-velocity waveforms in the celiac and SMA, and there appeared to be characteristic changes in the postprandial flow velocities in these vessels that might be related to composition of the meal and of the examination.

EXPERIENCE AT NORTHWESTERN UNIVERSITY A preliminary study was done in 39 normal subjects who had mesenteric duplex scans 30 minutes after the ingestion of 240 cc of an elemental diet

104

WILLIAM

R.

FLINN ET AL.

that contained 14 per cent protein, 32 per cent fat, and 53 per cent carbohydrates and totaled 355 calories (Ensure Plus). Postprandial arterial flow velocities were then compared with those observed before eating. No qualitative changes in the celiac spectral pattern were observed postprandially in this study. Fasting mean peak systolic flow velocity in the celiac artery was 143.2 cm per second and mean diastolic flow was 39.3 cm per second. Postprandially, mean peak systolic velocity was observed to be 160 cm per second and diastolic velocity was 50.4 cm per second. The apparent increases in celiac flow velocities in this initial phase were not statistically significant. Fasting mean systolic flow velocity in the SMAs of these normal individuals was 102.9 cm per second, and mean diastolic flow was 23.7 cm per second. After eating, the characteristic diastolic flow reversal in the SMA waveform was essentially eliminated and a significant increase in diastolic flow velocity was noted. Postprandially, peak systolic flow velocity in the SMA was 137.4 cm per second, and end-diastolic flow in the SMA increased significantly to a mean of 48.5 cm per second (P < 0.01) in the normal arteries tested. A follow-up study4 was performed using nine healthy volunteers. Each subject had a baseline fasting mesenteric scan and then one of three treatments: (1) 480 cc of the liquid nutritional supplement containing 710 kcal (double the volume and caloric content of the original study), (2) intravenous glucagon at a continuous infusion rate of 40 f.1g per minute, and (3) intravenous arginine-vasopressin at an infusion rate of 0.2 unit per minute (Fig. 4). Among its other effects, glucagon produces intestinal-smooth-muscle relaxation and splanchnic vasodilatation, and it has been shown in the canine model to increase celiac and SMA blood flow significantly. Vasopressin is a well-known splanchnic vasoconstrictor. This second study was designed to assess the effect of a variable test meal as well as to determine normal responses to different hormonal stimuli. Post-treatment scans were performed at 20, 40, and 60 minutes after the meal and 20 minutes after the hormone infusions to determine the possible impact of the timing of the examination on previously observed velocities. Significant increases in peak systolic flow velocities were observed in both the celiac and SMA following ingestion of this higher-calorie test meal. Maximal systolic velocity changes in the celiac artery were seen most often approximately 20 minutes after eating, whereas maximal systolic velocity changes in the SMA occurred later, about 40 minutes after the meal. Once again, diastolic reverse flow in the SMA characteristically disappeared postprandially, and diastolic forward flow increased significantly. Significant increases in peak systolic velocities were also noted in both the celiac and SMA following glucagon infusion and were essentially indistinguishable from those observed after the test meal. Glucagon also produced a disappearance of diastolic reversed flow in the SMA velocity waveform of most subjects and produced increased diastolic velocities in both visceral vessels, although this latter effect was not as marked as after the meal. Arginine-vasopressin infusion produced some abdominal cramping in most subjects, but no untoward effects on cardiac rate or rhythm or blood pressure were observed. Marked decreases in celiac and SMA systolic flow velocities were produced by the vasopressin infusion. Diastolic velocities were reduced in both vessels, although this was only Significant in the celiac

105

DUPLEX SCANNING FOR MESENTERIC ISCHEMIA

CELIAC ARTERY 140

,..

I-

e:;

0 ....

~

'
~ == ><

~

<.>

60

~

40 20 0

l:l ~

·20

"'==" Figure 4. Maximum changes in systolic and diastolic How velocity in the celiac artery (a) and SMA (b) induced by a test meal, glucagon, or arginine-vasopressin infusion. The asterisk (*) denotes values that are statistically significantly different from measured fasting velocities (P < 0.05). (From Lilly MP, Harward TRS, Flinn WR, et al: Duplex ultrasound measurement of changes in mesenteric How velocity with pharmacologic and physiologic alteration of intestinal blood How in man. J Vasc Surg 9:18-25, 1989; with permission.)

120 100 80

·40

·60 SYSTOLIC

A

DIASTOLIC

SUPERIOR MESENTERIC ARTERY 100

,..

80

l-

e:;

0

.... ~

'
;::, ==

~ "'=="

B

60

..

~

<.>

40

'"

20

~

0

~

·20 ·40 ·60 SYSTOLIC

DIASTOLIC

artery. In fact, several subjects developed diastolic flow reversal in the celiac waveform, which is characteristic of increased outflow resistance, after vasopressin infusion. These latter observations would suggest that flow parameters in the visceral vessels accessible by duplex scan are characteristic but variable, depending upon the stimulus employed and perhaps the timing of serial examinations. These observations and those of others outlined previously indicate that we are developing a good understanding of the "normal" splanchnic arterial response to physiologic and pharmacologic stimuli.

MESENTERIC REVASCULARIZATION When mesenteric ischemia requires surgical intervention, bypass grafting from the aorta to the mesenteric arteries is frequently employed. The clinical success of these procedures is well documented, but it depends primarily upon graft patency. Improved arterial perfusion after lower-extremity bypass has been easy to document using standard noninvasive techniques; in the past, however, the patency of visceral bypass grafts could only be confirmed by angiography. This may be a significant clinical problem because failure of mesenteric bypass grafts has been observed in 18 per cent of cases studied by McCollum and coworkers 5 with postoperative arterio-

106

WILLIAM

R.

FLINN ET AL.

grams. Mesenteric duplex scanning may provide an improved, noninvasive technique for objective assessment of postoperative graft patency as well as a method for long-term follow-up of these arterial reconstructive procedures,12 Five patients studied at Northwestern University had revascularization of 10 mesenteric arteries (eight bypass grafts, two arterial replantations). Early postoperative patency of eight reconstructions was documented by duplex scanning in the four patients studied before discharge from the hospital. Results of duplex scanning in these four cases were confirmed by contrast studies. Repeat examination 1 year postoperatively in one member of this group documented asymptomatic occlusion in an aorta-SMA vein graft. The remaining patient had duplex scanning 2 years after celiac and SMA vein bypasses. This examination revealed occlusion of the SMA graft (confirmed by angiography), but the celiac graft remained patent. Increased How velocity in the celiac graft in response to a test meal suggested satisfactory physiologic compensation in this patient. Although the initial experience is limited, it suggests that duplex scanning will be a clinically effective technique for the evaluation of visceral arterial reconstructive procedures both immediately postoperatively and for late follow-up examination. It is critical for the success of these examinations that the surgeon transmit detailed information about the technical conduct of the revascularization technique employed (bypass versus endarterectomy, infrarenal graft origin versus supraceliac, and so forth) to the technologist performing the examination.

CONCLUSIONS Mesenteric duplex scanning represents a noninvasive technique for anatomic and physiologic assessment of visceral vessels. It may have a significant impact upon the standard diagnostic evaluation of patients with suspected disorders of splanchnic How. In the past, visceral angiography to confirm mesenteric ischemic symptoms was often delayed. Often, barium or other enteric contrast had been administered, thus compromising the accuracy of arteriography. Mesenteric duplex scanning may provide a rapid, accurate, and noninvasive method for the evaluation of the patency of the major splanchnic vessels. This will aid in the selection of patients for arteriography and allow rational selection of alternative diagnostic studies. This article documents the need for standardization in several important areas before the full impact of these studies will be realized. The characteristic postprandial How changes in the celiac and SMA may be modified to an as yet undetermined degree by the volume, caloric value, or basic distribution (lipid, protein, carbohydrate) of the ingested meal. Similarly, the timing of the postprandial examination may be critical because there appears to be an orderly, evolving set of How changes in these vessels. The similarity of How responses to glucagon and to the test meal is intriguing. It is possible that such a technique could be employed as an alternative physiologic "stress test" in patients with suspected intestinal ischemia in

DUPLEX SCANNING FOR MESENTERIC ISCHEMIA

107

whom a standard test meal was not tolerated or in whom postprandial bloating compromised the conduct of the examination. Finally, substantially more clinical experience must be documented in patients with angiographically proven arterial occlusive lesions to determine precisely what may constitute a pathologic response to any visceral stimulus in the form of enteral ingeStion or parenteral infusion. As these areas become more standardized, it is likely that objective physiologic observations will help to clarify the clinical manifestations of visceral arterial occlusive disease.

REFERENCES 1. Buchardt Hansen HJ, Engell HC, Ring-Larsen H, et al: Splanchnic blood How in patients with abdominal angina before and after arterial reconstruction. Ann Surg 186:216-220, 1977 2. Flinn WR, Sandager GP, Lilly MP, et al: Duplex scan of mesenteric and celiac arteries. In Bergan JJ, Yao JST (eds): Arterial Surgery: New Diagnostic and Operative Techniques. Orlando, Grune & Stratton, 1988, pp 367-375 3. Jager K, Bollinger A, Valli C, et al: Measurement of mesenteric blood How by duplex scan. J Vasc Surg 3:462-469, 1986 4. Lilly MP, Harward TRS, Flinn WR, et al: Duplex ultrasound measurement of changes in mesenteric How velocity with pharmacologic and physiologic alteration of intestinal blood How in man. J Vasc Surg 9:18-25, 1989 5. McCollum CH, Graham JM, DeBakey ME: Chronic mesenteric arterial insufficiency: Results of revascularization in 33 patientS. South Med J 69: 1266-1273, 1976 6. Moneta GL, Taylor DC, Helton WS, et al: Duplex ultrasound measurement of postprandial intestinal blood How: Effect of meal composition. Gastroenterology 95:1294-1301, 1988 7. Nicholls SC, Kohler TR, Martin RS, et al: Use of hemodynamic parameters in the diagnosis of mesenteric insufficiency. J Vasc Surg 3:507-510, 1986 8. Norryd C, Dencker H, Lunderquist A, et al: Superior mesenteric blood flow during digestion in man. Acta Chir Scand 141:197-202, 1975 9. Norryd C, Dencker H, Lunderquist A, et al: Superior meseniric blood How in man studied with a dye-dilution technique. Acta Chit Scand 141:109-118, 1975 10. Quamar MI, Read AE, Skidmore R, et al: Transcutaneous Doppler ultrasound measurement of superior mesentertic artery blood How in man. Gut 27:100-105, 1986 11. Quamar MI, Read AE, Skidmore R, et al: Transcutaneous Doppler ultrasound measurement of coeliac axis blood How in man. Br J Surg 72:391-393, 1985 12. Sandager G, Flinn WR, McCarthy WJ, et al: Assessment of visceral arterial reconstruction using duplex scan. J Vasc Technol11:13-16, 1987 Address reprint requests to: William R. Flinn, MD Division of Vascular Surgery Department of Surgery Northwestern University Medical School 251 East Chicago Avenue Suite 628 Chicago, IL 60611 "