EXPERIMENTAL STUDIES OF THE SPLANCHNIC CIRCULATION OF THE RABBIT AFTER LIGATION OF THE SUPERIOR MESENTERIC ARTERY*

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1 AUGUST, 1969 EXPERIMENTAL STUDIES OF THE SPLANCHNIC CIRCULATION OF THE RABBIT AFTER LIGATION OF THE SUPERIOR MESENTERIC ARTERY* II: RADIONUCLIDE TRACER STUDIES By FREDERICK J. BONTE, M.D., ROBERT W. PARKEY1 M.D., and GEORGE C. CURRY, M.D.t I N EARLIER reports 2 we described studies of the angiographic and physiologic aspects of the splanchnic circulation of the rabbit after ligation of the superior mesenteric artery. Briefly, collateral circulation at an aortographically demonstrable level was established almost immediately after ligation, but mesenteric arterial flow waned steadily and disappeared before the death of the animal 8 hours later. Diminution of blood flow did not seem to DALLAS, be the result of clotting, for heparinization failed to affect survival of experimental animals. Certain evidence, reviewed in detail in an earlier publication,2 suggested that the mechanism ofbowel-ischemic death might involve the opening of splanchnic arteriovenous shunts. In support of this contention were the rise in portal venous blood oxygen saturations after ligation, and, of equal importance, a high incidence of contrast material opacification of the portal vein after ligation. Opacification did not appear to be the result of repeated administration of contrast material, when comparison was made with suitable control animals. Roentgen aortography and selective superior mesenteric arteriography promise to be of great value in the early diagnosis of bowel ischemic states, but some simpler test is required to select appropriate patients for contrast studies. It was our feeling that sufficient alteration might occur in the distribution of the splanchnic blood pool, * Presented at the Sixty-ninth Annual Meeting of the American Roentgen Ray Society, New Orleans, Louisiana, October 5-4, From the Department of Radiology, The University of Texas Southwestern Medical School at Dallas and Parkland Memorial Hospital, Dallas, Texas. This work was supported in part by Grant HE-og s8 i and Training Grant CA-oS 136 from the National Institutes of Health, USPHS; in part by a grant from the Southwestern Medical Foundation, Dallas, Texas t Clinical Fellow of the American Cancer Society, Inc. TEXAS after interruption of mesenteric arterial flow, to be detectable by the technique of radionuclide blood pool scanning. Accordingly, the following laboratory experiments were carried out. MATERIAL AND METHODS SCANNING OF THE ABDOMINAL BLOOD POOL The experimental subjects were mature albino laboratory rabbits of either sex. Eight animals were used for this phase of the study. The aortographic technique we have previously outlined2 was followed, and preoperative aortograms of the celiac and splanchnic circulation of each nembutalanesthetized rabbit were made so that each animal might serve as his own control. The superior mesenteric artery was then ligated, and aortograms were made at irregular intervals from immediate postligation to the premortem state, at about 6 to 8 hours after ligation. These studies were used to demonstrate the establishment of collateral circulation, opacification of the portal vein and similar findings of roentgenologic interest. Before ligation, and either before or after the preligation aortogram, an intravenous dose of 2.0 mc I s HSA (human serum albumin) was injected intravenously into a marginal ear vein. Scanning of the abdomen was carried out with a dual-probe, high-speed rectilinear scanner with two 5 inch Tl-activated Nal crystals and mediumenergy focusing collimators. Additional rectilinear blood pool scans were made im- 8o8

2 VOL. xo6,no.4 Splanchnic Circulation of the Rabbit 809 mediately after ligation and at hourly intervals until death. RADIONUCLIDE SCINTIPHOTOGRA PHY OF THE ISOLATED SPLANCHNIC BLOOD POOL Under nembutal anesthesia the abdomens of 5 rabbits were opened and tiny polyethylene catheters were inserted near the origin of the superior mesenteric artery in such a fashion as not to occlude splanchnic blood flow. A i.o mc dose of Tc99m HSA was injected slowly through the catheter and serial exposures were made during injection, and for 3 second intervals thereafter, with a commercial I I inch crystal scintillation camera of the Anger type. A low-energy grid collimator was used. In 7 additional rabbits the superior mesenteric artery was catheterized and the artery was ligated proximal to the catheterization site. Through the catheter was injected a dose of mc TcS9m HSA, and serial scintiphotographs were made with an Anger camera during, and at 3 second intervals after, the injection of the bolus. An attempt was made to keep the tracer bolus small in size by using very high specific activity pertechnetate (i mc/ml.) in the synthesis of the labeled serum albumin; 2.0 mc boluses could be kept within the volume of ml. RESULTS SCANNING OF THE ABDOMINAL BLOOD POOL Figure I, 1-D represents a group of rectilinear scans of the abdomen of a rabbit made at intervals after the intravenous injection of 2.0 mc I s HSA. The first scan (Fig. i1) was made under control circumstances on an anesthetized animal and shows the blood pools of the liver (H), the right kidney, and the left kidney (K). Tracer radionuclide may be seen in the midline superimposed within great vessels and low in the pelvis within the bladder. The remainder of the pattern represents the splanchnic blood pool and the superimposed blood pools of the anterior and posterior abdominal walls. The second scan (Fig. ib) was made immediately after ligation of the superior mesenteric artery and shows an augmented blood pool in theleft lower quadrant, thought to be due to transfer of blood to the inferior mesenteric arterial circulation in an attempt to establish collateral flow. The scan in Figure I C was made 2 hours after ligation and showed an increase in the counting rate over both lower quadrants and over the right upper quadrant as well, thought to be reflections of collateral flow to the superior mesenteric system. The pattern has changed but little on the fourth scan (Fig. ID), made at 6 hours,just before the death of the animal. This sequence is representative of scans obtained in all 8 animals. On the basis of this experience, abdominal blood pool pattern promises little of value in the selection of patients who may have splanchnic vascular flow abnormalities. However, since patterns in humans may differ from those observed in rabbits, an attempt is being made to evaluate the human abdominal blood pool. RADIONUCLIDE SCINTIPHOTOGRAPHY OF THE ISOLATED SPLANCHNIC BLOOD POOL Figure 2, zi, B and C represents Anger camera scintiphotographs of the isolated splanchnic blood pool under normal flow circumstances. The first frame (Fig. 2i1) was made dui ing injection, the second (Fig. 2B) at 3 seconds after injection, and the third (Fig. 2C) at 6 seconds. In Figure LI, C represents the escape of TcS9m HSA at the site of insertion of the catheter into the superior mesenteric artery. The bi-lobed pattern beneath it (Fig. 2B) represents the distribution of blood in the ileocecocolic (R) and left intestinal (L) segments of the superior mesenteric arterial circulation. In Figure 2C, H is thought to represent tracer entering the liver by way of the portal vein. When TcS9m HSA was injected through a catheter inserted into the superior mesenteric artery distal to a point of ligation, a much different sequence of scintiphotographs was produced (Fig. 3, ii, B and C). Figure 3z1, made during injection, again shows the escape of tracer at C, and early

3 8io lt-ederick j. Bonte, Robert \V. Parke- and George C. Curry (.t 1, 1969 A B C 0 11G. 1. (1) Rectilinear scan ofthe abdomen and pelvis ofa rabbit made after injection of2.o mc ofl 3 HSA. H represents the blood pool of the liver superimposing that of the right kidney. K is the blood pool of the left kidney. In the left upper and in both lower quadrants may be seen the normal splanchnic blood pool. Note tracer in great vessels in the abdominal midline and pelvis. (B) Rectilinear scan of the abdomen and pelvis of the same rabbit as in 1, obtained immediately after ligation of the superior mesenteric artery. Note increased radioactivity in the left lower quadrant, possibly representing the blood pool of the inferior mesenteric artery and its branches. (C) Rectilinear scan of same animal made 2 hours after ligation of the superior mesenteric artery. There is now increased activity in both lower quadrants. The collateral flow through the abdominal wall may account for part of this, as may leakage of labeled protein through walls of the damaged splanchnic vessels. (D) Rectilinear scan, made 6 hours after ligation of the superior mesenteric artery and just before the death of the animal, shows little change in pattern in the. hours since the scan seen in C. spread of tracer through the proximal mesenteric circulation is thought to be responsible for the island of activity caudad to this point. Of great interest, however, is the appearance of tracer in what appears to be a channel leading cephalad (P in Fig. 3//) toward the liver. Within 3 seconds after injection (Fig. 3B) this channel is well defined and the liver (H) is anatomically recognizable. At 6 seconds blood has entered the right heart (HE in Fig. 3C). Confirmation is offered b\- the experiment in Figure 4. Once again, the individual frames (Fig. 4, zl B and C) were made respectively during, and at 3 and 6 seconds after, injection of a 2.0 mc bolus of Tc #{176} HSA. Again there is escape of tracer at the site of insertion of a catheter distal to the point of ligation of the superior mesenteric artery. While very little tracer enters the general splanchnic blood pool, there is immediate flow through a channel, P (Fig. 4/1), in the direction of the rabbit s left upper quadrant. At 3 seconds (Fig. 4B) the channel is even better visualized and the outline of a structure resembling the liver is flow visible above, and to the left of, the injection site. After conclusion of scmtiphotograph-, the animal was killed and the abdomen was opened widely. An anomalous left-sided liver was present, and the channel corresponding to P in Figure 4z1 was unequivocally the portal vein. CONCLUSIONS It is disappointing, but not surprising, to find that blood pool scanning of the whole abdomen does not yield much useful information about changes in the superior mesenteric arterial blood flow. Even though

4 Voi. io6, No. Splanchnic Circulation of the Rabbit 81 FIG. 2. (1) Anger camera scintiphotograph made after injection of 2.0 mc Tc99m HSA through a tiny catheter in place in the unobstructed superior mesenteric artery of a rabbit. C is thought to represent escape of tracer at the catheter insertion site. The catheter was shielded with a small lead tunnel. (B) Scintiphotograph made 3 seconds after the scan in ii. The isolated splanchnic blood pool is seen to greater advantage and assumes a bi-lobed appearance. R is thought to correspond to the ileocecocolic segment and L to the left intestinal segment of the mesenteric arterial circulation. (C) Scintiphotograph made seconds after that in B. Normal splanchnic blood pool is seen to maximum advantage and tracer is now thought to have entered the liver (H) by way ofmesenteric and portal veins. there is evidence on whole-abdomen scan- superior mesenteric artery, it is not thought fling which suggests the transfer of blood to likely that patterns of this sort would be collateral pathways after obstruction of the sufficiently obvious in the human to make FIG. 3. (1) Anger camera scintiphotograph of the abdomen of a rabbit made during injection of 2.0 mc Tc99m HSA. The catheter is in place in the superior mesenteric artery distal to a point of ligation. C represents tracer escaping at catheter insertion site. P is thought to represent the portal vein. (B) Scintiphotograph made 3 seconds after that in 4. Note spread of tracer through proximal aspect of mesenteric circulation and better delineation of the portal vein. Tracer now outlines the liver (H). Note residual tracer in syringe at right of photo. The intervening catheter was shielded by small lead tunnel. (C) Scintiphotograph made 3 seconds after B shows tracer now entering heart (HE).

5 812 Frederick J. Bonte, Robert W. Parkey and George C. Curry AUGUST, 5969 I #{149} TI -. #{149}1..,-, FIG.. (4) Anger camera scintiphotograph of the abdomen of a rabbit made during injection of 2.0 mc HSA through a catheter in place in the superior mesenteric artery distal to a point of ligation. Once again, tracer is thought to be escaping at catheter insertion site, but there is early demonstration of what appears to be a portal vein (P) anomalously directed into the rabbit s left upper quadrant. (B) Scintiphotograph made 3 seconds after 4 shows better definition of portal vein and early outlining of the liver. (C) Scintiphotograph made 3 seconds after B shows more complete outlining of a structure which was found at autopsy to represent an anomalous left-sided liver. abdominal blood pool scanning a useful screening test to designate patients for Selective superior mesenteric arteriography. We believe that the camera studies described above, showing more immediate entry of undiluted tracer radionuclide into the portal vein, supply another bit of confirmatory evidence for the opening of arteriovenous shunts after ligation of the superior mesenteric artery. It is possible that changes in circulatory dynamics which are the result of altered mesenteric arterial blood flow might be detectable by means of radionuclide tracer flow studies done with a multiple probe system, which would afford a detailed analysis of flow patterns in the regions of the superior mesenteric artery, the celiac axis and the portal vein. Pilot experiments of this sort are now underway in our labora tory. Frederick J. Bonte, M.D. Department of Radiology The University of Texas Southwestern Medical School at Dallas 5323 Harry Hines Boulevard Dallas, Texas The authors wish to acknowledge the excellent technical assistance of J. G. Moore, R.T., P. R. Tribble, R.T., C. P. Bonte, and K. D. Graham, R.T., in these studies. RE FERENCES i. BONTE, F. J., PARKEY, R. \V., and CURRY, G. C. Splanchnic blood-pool scanning in occlusive disease of superior mesenteric artery: an experimental study. 7. Nuclear Med., 1968, 9, BONTE, F. J.,CURRY, G. C., and PARKEY, R. W. Experimental studies of splanchnic circulation of rabbit after ligation of superior mesenteric artery. I. Angiographic and physiologic studies. AM. J. ROENTGENOL., RAD. THERAPY & Nu- CLEAR MED., 3969, zo#{243},