Pancreaticoduodenectomy and the Celiac Artery Compression Syndrome Ted R. Kohler, MD, Haite Debas, MD, Miles Crames, BS, D.E. Strandness Jr, MD, Seattle, Washington
Celiac compression is usually a benign condition, but when surgery necessitates division of collaterals from the superior mesenteric artery, it may cause lifethreatening gut ischemia. We report a case of cholangiocarcinoma necessitating pancreaticoduodenectomy in a patient with celiac artery compression by the median arcuate ligament. Preoperative duplex scanning confirmed the celiac stenosis and revealed retrograde flow through collaterals from the superior mesenteric artery. Intraoperative continuous wave Doppler examination revealed that gastric blood flow disappeared with compression of the superior mesenteric artery. This maneuver no longer affected gastric flow after transection of the compressing structures at the celiac origin. Preoperative identification of celiac artery stenosis is crucial to prevent small bowel ischemia and possible anastomotic breakdown or liver failure. Duplex scanning can provide important insight about collateral circulation, and intraoperative Doppler testing can assess the adequacy of revascularization. (Ann Vasc Surg 1990; 4:77-80) KEY WORDS: Celiac axis; median arcuate ligament; celiac compression syndrome; pancreaticoduodenectomy; duplex scanning; Doppler; bile duct tumor; cholangiocarcinoma.
noninvasive vascular testing in preoperative evaluation and intraoperative decision making.
Because celiac artery occlusive disease increases the rate of anastomotic leak associated with pancrea t i c o d u o d e n e c t o m y (Whipple procedure), preoperative assessment of mesenteric blood flow is essential [1]. Patients who have celiac artery stenosis require some form of revascularization to prevent midgut ischemia when the pancreaticoduodenal arteries are sacrificed. The most c o m m o n lesion is a proximal atherosclerotic stenosis, which can be treated with bypass from the superior mesenteric artery or aorta to the celiac axis. The following case describes an unusual association of a bile duct tumor with compression of the celiac artery by the median arcuate ligament. It demonstrates the use of
CASE REPORT A 52-year-old man presented at another institution with steatorrhea and hyperbilirubinemia. Work-up included an abdominal ultrasound study, CT scan, arteriogram, and percutaneous transhepatic cholangiogram. Imaging studies showed a mass obstructing the distal common bile duct. Arteriography demonstrated a significant stenosis at the origin of the celiac axis (Fig. 1) with collaterals from the superior mesenteric artery supplying both the hepatic and gastric arteries (Fig. 2). Exploration revealed a localized cholangiocarcinoma of the distal common bile duct with no evidence of nodal metastases by biopsy. The surgeon did not perform a pancreaticoduodenectomy due to concern that the celiac artery stenosis would compromise blood flow and increase the risk of anastomotic leak. Instead. a choledochoduodenostomy and gastrojejunostomy were constructed.
From the Department of Surgetw, University of Washington, Seattle, Washington. Reprint requests: Ted R. Kohler, MD, Department of Surgery (l 12), Veterans Administration Hospital, 1660 S. Columbian Way, Seattle, Washington 98108. 77
78
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Fig. 1. Lateral aortogram demonstrating stenosis at origin of celiac axis (arrow). Three months later the patient sought a second opinion at the University of Washington Medical Center regarding the operability of his tumor. Repeated computerized tomography revealed no evidence of metastasis, and arteriography again demonstrated an extrinsic appearing,
ANNALS OF VASCULAR SURGERY
high-grade stenosis at the origin of the celiac axis. Duplex scanning confirmed the celiac stenosis (Fig. 3) and revealed retrograde flow through collaterals from the superior mesenteric artery filling the hepatic and gastric arteries. Balloon dilatation of the celiac lesion was attempted because it carried little risk. If successful, it would have assured adequate, prograde celiac blood flow and eliminated the possibility of needing to perform a vascular anastomosis in a potentially contaminated field. Although the lesion dilated with the Gruntzig balloon, it immediately returned to its former diameter with deflation of the balloon in a manner consistent with extrinsic compression. At reexploration a small mass was palpable in the head of the pancreas. After assuring that the superior mesenteric vein and portal vein were free of tumor, the origin of the celiac artery was identified in the lesser sac where aberrant diaphragmatic muscle and the median arcuate ligament were observed to compress the vessel. A continuous-wave, 7.5 mHz Doppler instrument* was used for intraoperative assessment of the celiac artery stenosis and evaluation of the collateral circulation. Doppler signals over the stomach disappeared with compression of the superior mesenteric artery. With transection of the compressing muscular and ligamentous structures at the celiac origin, the Doppler signal in the celiac artery improved, and compression of the superior mesenteric artery no longer affected the gastric flow pattern. Pancreaticoduodenectomy was then performed, and recovery was uncomplicated. The patient was doing well one year after surgery.
DISCUSSION
Fig. 2. Selective injection of superior mesenteric artery demonstrating filling of hepatic artery and celiac axis by means of pancreaticoduodenal branches from superior mesenteric artery (arrow).
In the past, p a n c r e a t i c o d u o d e n e c t o m y was associated with a perioperative mortality rate of up to 25%, with most o f the morbidity resulting from b r e a k d o w n of the pancreaticojejunal anastomosis [1]. While perioperative mortality of one to three percent has been reported more recently with pyloric sphincter-preserving p a n c r e a t e c t o m y [2-4], it is still critical to assure the adequacy of the blood supply to the bowel a n a s t o m o s e s . Selective celiac and superior mesenteric arteriography is recommended to: (1) help distinguish inflammatory from neoplastic lesions and islet cell from exocrine lesions; (2) determine resectability; (3) detect hepatic metastases; and (4) identify aberrant visceral arteries and significant stenoses [1]. The incidence of high grade celiac stenosis in one large series was 10.5%, with most cases caused by atherosclerotic disease [1]. Although successful Whipple procedures have been reported without revascularization in patients with total occlusion of the celiac axis [5], revascularization at the time o f t u m o r resection should be considered when such lesions are found. High-grade stenoses of the superior mesenteric or celiac arteries can c o m p r o m i s e midgut circulation
*Medasonics Inc., Mountain View, California.
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Fig. 3. Duplex study: B-mode inset shows celiac axis stenosis. Spectral waveforms demonstrate marked increase in frequency and spectral broadening in this region,
when the pancreaticoduodenal arcade connecting the superior mesenteric and celiac artery branches is divided during the Whipple procedure. This may increase the risk of anastomotic leak or hepatic failure. We have used duplex scanning to identify significant stenoses in the celiac and superior mesenteric arteries [6]. In the case presented, duplex scanning detected the direction of flow in the hepatic and gastric arteries, confirming that collaterals from the superior mesenteric artery supplied the branches of the celiac axis. The arteriogram of the celiac lesion was consistent with an extrinsic lesion. Although the role of celiac compression in the pathophysiology of mesenteric insufficiency is widely debated [7-9], it is well known that the median arcuate ligament often causes an extrinsic compression at the origin of the celiac axis. When this lesion is present and collateral vessels that normally supply the celiac branches are sacrificed during tumor resection, significant mesenteric ischemia can result.
Although balloon angioplasty cannot correct extrinsic lesions, it has been used successfully to dilate atherosclerotic lesion in mesenteric arteries [10--12] and recurrent celiac artery stenosis after surgery for median arcuate ligament syndrome [13]. We attempted balloon angioplasty in this case because of our reluctance to perform vascular anastomoses in conjunction with pancreatic and small bowel surgery. The observation that the balloon catheter temporarily dilated the celiac narrowing with immediate restenosis on deflation was further evidence of the extrinsic nature of this lesion. The operative approach to the celiac axis is through the lesser omental bursa. The constricting branches of the diaphragmatic crura should be cut and the origin of the celiac artery and the adjacent aorta should be dissected free as widely as possible to ensure adequate decompression. In the more usual case of celiac axis occlusion due to atherosclerosis, successful revascularization of this vessel has been accomplished at the time of pancreaticoduodenectomy by constructing an anastomosis
ANNALS OF VASCULAR SURGERY
CELIAC ARTER Y COMPRESSION
80
between the divided end of the splenic artery and the side of the superior mesenteric artery or by constructing bypass grafts using saphenous vein or polytetrafluoroethylene [1]. In our case intraoperatire Doppler studies confirmed that gastric blood flow was dependent on collaterals from the superior mesenteric artery. Following division of the ligament compressing the celiac axis, Doppler examination confirmed improved flow in this artery and demonstrated that gastric blood flow was no longer dependent on collaterals. This knowledge allowed the surgical team to proceed with resection of the tumor.
CONCLUSION
We have presented a case of celiac artery compression complicating pancreaticoduodenectomy for a cholangiocarcinoma. Although celiac compression is usually a benign condition, it may cause life-threatening gut ischemia when surgery necessitates division of collaterals from the superior ruesenteric artery. Revascularization is necessary to prevent anastomotic breakdown or liver failure. Therefore, preoperative identification of celiac artery stenosis is crucial. Duplex scanning can provide important information about collateral circulation, and intraoperative Doppler testing can assess the adequacy of revascularization. In this case, division of a constricting median arcuate ligament increased celiac blood flow and allowed safe tumor resection.
n u n
REFERENCES 1. T H O M P S O N N W , E C K H A U S E R FE, T A L P O S G, C H O KJ. Pancreaticoduodenectomy and celiac occlusive disease. A n n Surg 1981:193:399~,06. 2. B R A A S C H JW, D E Z I E L DJ, ROSSI RL, W O T K I N S E Jr, W I N T E R PF. Pyloric and gastric preserving pancreatic resection. Experience with 87 patients. Ann Surg 1986: 204:411~-18. 3. B E G E R HG. B U C H L E R M, B I T T N E R RR, O E T T I N G E R W, ROSCHER R. Duodenum-preserving resection of the head of the pancreas in severe chronic pancreatitis. Early and late results. A n n Sur~, 1989:209:273-278. 4. G R A C E PA, PITT HA, T O M P K I N S R K , D E N B E S T E N L, L O N G M I R E W O Jr. Decreased morbidity and mortality after pancreaticoduodenectomy. A m J Surg 1986:151:141149. 5. T R E D E M. The surgical treatment of pancreatic carcinoma. Sur~,,eo' 1985:97:28-35. 6. N I C H O L L S SC, K O H L E R TR, M A R T I N RL, S T R A N D NESS DE Jr. The use of hemodynamic parameters in the diagnosis of mesenteric ischemia. J Vase Stlrg 1986;3:507510. 7. K E R N O H A N RM, B A R R O S D ' S A AA, C R A N L E Y B, J O H N S T O N HM. Further evidence supporting the existence of the celiac artery compression syndrome. Arch Sttrg 1985"120:1072-1076. 8. G U T N I K LM. Celiac artery compression syndrome. A m J M e d 1984:76:334-336. 9. P L A T E G, E K L O F B, V A N G J. The celiac compression syndrome. Myth or reality'? Acta Chir S t a n d 1981;147: 201-203. 10. R O B E R T S L Jr, W E R T M A N DA Jr, M I L L S SR, M O O R E AV Jr, H E A S T O N DK. Transluminal angioplasty of the superior mesenteric artery: an alternative to surgical revascularization. A J R 1983:141:1039-1042. I1. O D U R N Y A, S N I D E R M A N K W , C O L A P 1 N T O RF. Intestinal angina: percutaneous transluminal angioplasty of the celiac and superior mesenteric arteries. Radiology 1988: 167:59~62. 12. L E V Y PJ, H A S K E L L L, G O R D O N RL. Percutaneous transluminal angioplasty of splanchnic arteries: an alternative method to elective revascularization in chronic visceral ischaemia. Eur J Radiol 1987:7:239-242. 13. S A D D E N K N I S, S N I D E R M A N K W , H I L T O N S, SOS TA. Percutaneous transluminal angioplasty of nonatherosclerotic lesions. A J R 1980:135:975-982.
Celiac compression is usually a benign condition, but when surgery necessitates division of collaterals from the superior mesenteric artery, it may cause lifethreatening gut ischemia. We report a case of cholangiocarcinoma necessitating pancreaticoduodenectomy in a patient with celiac artery compression by the median arcuate ligament. Preoperative duplex scanning confirmed the celiac stenosis and revealed retrograde flow through collaterals from the superior mesenteric artery. Intraoperative continuous wave Doppler examination revealed that gastric blood flow disappeared with compression of the superior mesenteric artery. This maneuver no longer affected gastric flow after transection of the compressing structures at the celiac origin. Preoperative identification of celiac artery stenosis is crucial to prevent small bowel ischemia and possible anastomotic breakdown or liver failure. Duplex scanning can provide important insight about collateral circulation, and intraoperative Doppler testing can assess the adequacy of revascularization. (Ann Vasc Surg 1990; 4:77-80) KEY WORDS: Celiac axis; median arcuate ligament; celiac compression syndrome; pancreaticoduodenectomy; duplex scanning; Doppler; bile duct tumor; cholangiocarcinoma.
noninvasive vascular testing in preoperative evaluation and intraoperative decision making.
Because celiac artery occlusive disease increases the rate of anastomotic leak associated with pancrea t i c o d u o d e n e c t o m y (Whipple procedure), preoperative assessment of mesenteric blood flow is essential [1]. Patients who have celiac artery stenosis require some form of revascularization to prevent midgut ischemia when the pancreaticoduodenal arteries are sacrificed. The most c o m m o n lesion is a proximal atherosclerotic stenosis, which can be treated with bypass from the superior mesenteric artery or aorta to the celiac axis. The following case describes an unusual association of a bile duct tumor with compression of the celiac artery by the median arcuate ligament. It demonstrates the use of
CASE REPORT A 52-year-old man presented at another institution with steatorrhea and hyperbilirubinemia. Work-up included an abdominal ultrasound study, CT scan, arteriogram, and percutaneous transhepatic cholangiogram. Imaging studies showed a mass obstructing the distal common bile duct. Arteriography demonstrated a significant stenosis at the origin of the celiac axis (Fig. 1) with collaterals from the superior mesenteric artery supplying both the hepatic and gastric arteries (Fig. 2). Exploration revealed a localized cholangiocarcinoma of the distal common bile duct with no evidence of nodal metastases by biopsy. The surgeon did not perform a pancreaticoduodenectomy due to concern that the celiac artery stenosis would compromise blood flow and increase the risk of anastomotic leak. Instead. a choledochoduodenostomy and gastrojejunostomy were constructed.
From the Department of Surgetw, University of Washington, Seattle, Washington. Reprint requests: Ted R. Kohler, MD, Department of Surgery (l 12), Veterans Administration Hospital, 1660 S. Columbian Way, Seattle, Washington 98108. 77
78
CELIAC ARTERY COMPRESSION
Fig. 1. Lateral aortogram demonstrating stenosis at origin of celiac axis (arrow). Three months later the patient sought a second opinion at the University of Washington Medical Center regarding the operability of his tumor. Repeated computerized tomography revealed no evidence of metastasis, and arteriography again demonstrated an extrinsic appearing,
ANNALS OF VASCULAR SURGERY
high-grade stenosis at the origin of the celiac axis. Duplex scanning confirmed the celiac stenosis (Fig. 3) and revealed retrograde flow through collaterals from the superior mesenteric artery filling the hepatic and gastric arteries. Balloon dilatation of the celiac lesion was attempted because it carried little risk. If successful, it would have assured adequate, prograde celiac blood flow and eliminated the possibility of needing to perform a vascular anastomosis in a potentially contaminated field. Although the lesion dilated with the Gruntzig balloon, it immediately returned to its former diameter with deflation of the balloon in a manner consistent with extrinsic compression. At reexploration a small mass was palpable in the head of the pancreas. After assuring that the superior mesenteric vein and portal vein were free of tumor, the origin of the celiac artery was identified in the lesser sac where aberrant diaphragmatic muscle and the median arcuate ligament were observed to compress the vessel. A continuous-wave, 7.5 mHz Doppler instrument* was used for intraoperative assessment of the celiac artery stenosis and evaluation of the collateral circulation. Doppler signals over the stomach disappeared with compression of the superior mesenteric artery. With transection of the compressing muscular and ligamentous structures at the celiac origin, the Doppler signal in the celiac artery improved, and compression of the superior mesenteric artery no longer affected the gastric flow pattern. Pancreaticoduodenectomy was then performed, and recovery was uncomplicated. The patient was doing well one year after surgery.
DISCUSSION
Fig. 2. Selective injection of superior mesenteric artery demonstrating filling of hepatic artery and celiac axis by means of pancreaticoduodenal branches from superior mesenteric artery (arrow).
In the past, p a n c r e a t i c o d u o d e n e c t o m y was associated with a perioperative mortality rate of up to 25%, with most o f the morbidity resulting from b r e a k d o w n of the pancreaticojejunal anastomosis [1]. While perioperative mortality of one to three percent has been reported more recently with pyloric sphincter-preserving p a n c r e a t e c t o m y [2-4], it is still critical to assure the adequacy of the blood supply to the bowel a n a s t o m o s e s . Selective celiac and superior mesenteric arteriography is recommended to: (1) help distinguish inflammatory from neoplastic lesions and islet cell from exocrine lesions; (2) determine resectability; (3) detect hepatic metastases; and (4) identify aberrant visceral arteries and significant stenoses [1]. The incidence of high grade celiac stenosis in one large series was 10.5%, with most cases caused by atherosclerotic disease [1]. Although successful Whipple procedures have been reported without revascularization in patients with total occlusion of the celiac axis [5], revascularization at the time o f t u m o r resection should be considered when such lesions are found. High-grade stenoses of the superior mesenteric or celiac arteries can c o m p r o m i s e midgut circulation
*Medasonics Inc., Mountain View, California.
VOLUME 4 NO I - 1990
CELIAC A R T E R Y C O M P R E S S I O N
79
Fig. 3. Duplex study: B-mode inset shows celiac axis stenosis. Spectral waveforms demonstrate marked increase in frequency and spectral broadening in this region,
when the pancreaticoduodenal arcade connecting the superior mesenteric and celiac artery branches is divided during the Whipple procedure. This may increase the risk of anastomotic leak or hepatic failure. We have used duplex scanning to identify significant stenoses in the celiac and superior mesenteric arteries [6]. In the case presented, duplex scanning detected the direction of flow in the hepatic and gastric arteries, confirming that collaterals from the superior mesenteric artery supplied the branches of the celiac axis. The arteriogram of the celiac lesion was consistent with an extrinsic lesion. Although the role of celiac compression in the pathophysiology of mesenteric insufficiency is widely debated [7-9], it is well known that the median arcuate ligament often causes an extrinsic compression at the origin of the celiac axis. When this lesion is present and collateral vessels that normally supply the celiac branches are sacrificed during tumor resection, significant mesenteric ischemia can result.
Although balloon angioplasty cannot correct extrinsic lesions, it has been used successfully to dilate atherosclerotic lesion in mesenteric arteries [10--12] and recurrent celiac artery stenosis after surgery for median arcuate ligament syndrome [13]. We attempted balloon angioplasty in this case because of our reluctance to perform vascular anastomoses in conjunction with pancreatic and small bowel surgery. The observation that the balloon catheter temporarily dilated the celiac narrowing with immediate restenosis on deflation was further evidence of the extrinsic nature of this lesion. The operative approach to the celiac axis is through the lesser omental bursa. The constricting branches of the diaphragmatic crura should be cut and the origin of the celiac artery and the adjacent aorta should be dissected free as widely as possible to ensure adequate decompression. In the more usual case of celiac axis occlusion due to atherosclerosis, successful revascularization of this vessel has been accomplished at the time of pancreaticoduodenectomy by constructing an anastomosis
ANNALS OF VASCULAR SURGERY
CELIAC ARTER Y COMPRESSION
80
between the divided end of the splenic artery and the side of the superior mesenteric artery or by constructing bypass grafts using saphenous vein or polytetrafluoroethylene [1]. In our case intraoperatire Doppler studies confirmed that gastric blood flow was dependent on collaterals from the superior mesenteric artery. Following division of the ligament compressing the celiac axis, Doppler examination confirmed improved flow in this artery and demonstrated that gastric blood flow was no longer dependent on collaterals. This knowledge allowed the surgical team to proceed with resection of the tumor.
CONCLUSION
We have presented a case of celiac artery compression complicating pancreaticoduodenectomy for a cholangiocarcinoma. Although celiac compression is usually a benign condition, it may cause life-threatening gut ischemia when surgery necessitates division of collaterals from the superior ruesenteric artery. Revascularization is necessary to prevent anastomotic breakdown or liver failure. Therefore, preoperative identification of celiac artery stenosis is crucial. Duplex scanning can provide important information about collateral circulation, and intraoperative Doppler testing can assess the adequacy of revascularization. In this case, division of a constricting median arcuate ligament increased celiac blood flow and allowed safe tumor resection.
n u n
REFERENCES 1. T H O M P S O N N W , E C K H A U S E R FE, T A L P O S G, C H O KJ. Pancreaticoduodenectomy and celiac occlusive disease. A n n Surg 1981:193:399~,06. 2. B R A A S C H JW, D E Z I E L DJ, ROSSI RL, W O T K I N S E Jr, W I N T E R PF. Pyloric and gastric preserving pancreatic resection. Experience with 87 patients. Ann Surg 1986: 204:411~-18. 3. B E G E R HG. B U C H L E R M, B I T T N E R RR, O E T T I N G E R W, ROSCHER R. Duodenum-preserving resection of the head of the pancreas in severe chronic pancreatitis. Early and late results. A n n Sur~, 1989:209:273-278. 4. G R A C E PA, PITT HA, T O M P K I N S R K , D E N B E S T E N L, L O N G M I R E W O Jr. Decreased morbidity and mortality after pancreaticoduodenectomy. A m J Surg 1986:151:141149. 5. T R E D E M. The surgical treatment of pancreatic carcinoma. Sur~,,eo' 1985:97:28-35. 6. N I C H O L L S SC, K O H L E R TR, M A R T I N RL, S T R A N D NESS DE Jr. The use of hemodynamic parameters in the diagnosis of mesenteric ischemia. J Vase Stlrg 1986;3:507510. 7. K E R N O H A N RM, B A R R O S D ' S A AA, C R A N L E Y B, J O H N S T O N HM. Further evidence supporting the existence of the celiac artery compression syndrome. Arch Sttrg 1985"120:1072-1076. 8. G U T N I K LM. Celiac artery compression syndrome. A m J M e d 1984:76:334-336. 9. P L A T E G, E K L O F B, V A N G J. The celiac compression syndrome. Myth or reality'? Acta Chir S t a n d 1981;147: 201-203. 10. R O B E R T S L Jr, W E R T M A N DA Jr, M I L L S SR, M O O R E AV Jr, H E A S T O N DK. Transluminal angioplasty of the superior mesenteric artery: an alternative to surgical revascularization. A J R 1983:141:1039-1042. I1. O D U R N Y A, S N I D E R M A N K W , C O L A P 1 N T O RF. Intestinal angina: percutaneous transluminal angioplasty of the celiac and superior mesenteric arteries. Radiology 1988: 167:59~62. 12. L E V Y PJ, H A S K E L L L, G O R D O N RL. Percutaneous transluminal angioplasty of splanchnic arteries: an alternative method to elective revascularization in chronic visceral ischaemia. Eur J Radiol 1987:7:239-242. 13. S A D D E N K N I S, S N I D E R M A N K W , H I L T O N S, SOS TA. Percutaneous transluminal angioplasty of nonatherosclerotic lesions. A J R 1980:135:975-982.
