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Pancreatic head resections in the setting of celiac axis stenosis: Case report and review of literature


Resekce hlavy pankreatu v terénu stenózy truncus coeliacus: kazuistika a přehled literatury

Úvod: Ischemické komplikace jsou významnou příčinou morbidity u pacientů po resekcích hlavy pankreatu. Stenóza truncus coealiacus představovala tradičně kontraindikaci pankreatoduodenektomie.

Kazuistika: Prezentujeme pacientku s adenokarcinomem hlavy pankreatu indikovanou k pankreatoduodenektomii dle Whippla při současné hemodynamicky významné stenóze truncus coealiacus. Navzdory uvolnění tepny z komprese ligamentum arcuatum medianum byla první pooperační den zaznamenaná elevace jaterních testů. Endovaskulární angioplastika vedla k výraznému zlepšení radiologického nálezu a rychlé normalizaci laboratorních hodnot. Další pooperační průběh byl bez komplikací.

Závěr: Časné rozpoznání ischemických komplikací po resekci hlavy pankreatu je zásadní. I pooperačně může být endovaskulární intervence efektivní léčbební metodou významné stenózy truncus coeliacus u selektovaných pacientů po pankreatoduodenektomii.

Klíčová slova:

pancreatoduodenektomie − stenóza truncus coealiacus − endovaskulární angioplastika − ligamentum arcuatum medianum


Authors: T. Kocisova 1;  A. Nikov 1;  P. Záruba 1;  T. Tuma 2;  J. Lacman 2;  R. Pohnán 1
Authors place of work: Department of Surgery, 2nd Faculty of Medicine of the Charles University and the Military University Hospital Prague 1;  Department of Radiology, Military University Hospital Prague 2
Published in the journal: Rozhl. Chir., 2021, roč. 100, č. 5, s. 239-242.
Category: case report
doi: https://doi.org/10.33699/PIS.2021.100.5.242–245

Summary

Introduction: Ischemic complications are a notable cause of morbidity in patients after pancreatic head resections. Stenosis of celiac axis in patients undergoing pancreatoduodenectomy requires further perioperative attention.

Case report: We present a patient with pancreatic head malignancy scheduled for Whipple procedure in the setting of hemodynamically significant celiac axis stenosis. Despite release of the artery from compression by median arcuate ligament, elevation of liver function tests on the first postoperative day was noted. Endovascular stenting was performed on the same day with significant radiological improvement and subsequent normalization of laboratory values. The patient had no further postoperative complications.

Conclusion: Fast recognition of ischemic complications after pancreatic head resection is crucial. Even postoperatively, endovascular intervention might be a feasible treatment modality of celiac axis stenosis in selected patients who undergo pancreatoduodenectomy.

Keywords:

celiac axis stenosis – pancreatoduodenectomy − endovascular stenting − median arcuate ligament release

INTRODUCTION

Unrecognized vascular anomalies, vascular pathology or intraoperative vascular injury may lead to ischemic complications with possibly fatal consequences in hepatobiliary surgery [1]. Celiac axis stenosis (CAS) is reported in 4−11% of patients who undergo pancretoduodenectomy (PD) [1, 2]. Compression by the median arcuate ligament (MAL) is the most common cause followed by atherosclerosis. They account for nearly 90% of all cases, fibrosis due to chronic pancreatitis or lymph node metastasis are amongst the others [3, 4]. Ligation of collateral circulation between celiac artery (CA) and superior mesenteric artery (SMA), i.e. gastroduodenal artery (GDA), pancreaticoduodenal arcades and Arch of Buhler is obligatory during PD. In the setting of significant CAS, this leads to ischemic complications such as liver failure, liver abscesses or anastomotic insufficien cy [1,4,5]. Preoperative computed tomography (CT) scans and intraoperative GDA clamping test are used to diagnose hemodynamically significant stenosis [1,5]. Endovascular stenting, intraoperative median arcuate ligament release or vascular reconstructions may be utilized to safely perform PD.

We report a patient who underwent PD in the setting of hemodynamically significant celiac axis stenosis. Intraoperative MAL division was followed by stent insertion on the first postoperative day due to suspected liver ischemia.

CASE REPORT

A 68year old female patient was referred to our department with pancreatic head adenocarcinoma. The CT scan showed a borderline resectable tumor due to contact with 1/3 of circumference of superior mesenteric artery (SMA), therefore, neoadjuvant chemotherapy was initially administered. After 6 cycles of FOLFORINOX, partial response according to RECIST was noted and the patient was scheduled for PD. Synchronous finding on preoperative CT scan was a celiac axis stenosis most likely due to external MAL compression (Image I.). The short stenosis followed proximal non-stenotic segment and no calcifications were visible on the CT around the stenosis. Retrograde filling of the common hepatic artery (CHA) via GDA of 4.5mm in diameter was suspected (Image II.). According to the classification proposed by Sugae T. et al, the stenosis would be classified as B/C with more than 80% stenosis in diameter and less than 4mm in length [3]. The division of MAL with complete liberation of celiac axis from surrounding tissues was performed at the beginning of the surgery. After GDA clamping, the faint pulse of the common hepatic artery did not alter, and the liver showed no signs of ischemia. The subtotal stomach preserving PD with standard lymphadenectomy was performed. There was a minimal elevation of transaminases two hours after the surgery (ALT 1.52 μkat/l, AST 1.97 μkat/l). However, gradual increase in lactate and a significant elevation of liver function tests (LFTs) with maximal values of ALT 14.3 μkat/l, AST 19.5 μkat/l was noted on the first postoperative day. Considering the initial diagnosis of stenotic celiac axis, endovascular angioplasty using a multi-link 4/8 stent was performed from the right femoral artery on the same day. This led to immediate angiographic improvement (Image III.) and prompt normalization of LFTs and lactate. Further postoperative course was uneventful. Pathological analysis found pancreatic ductal adenocarcinoma, pT2N1, negative margin resection was achieved, and the patient was discharged on 13th postoperative day.

Fig. 1: Preoperative CT finding of CA stenosis in arterial
phase, sagittal view
Fig. 1: Preoperative CT finding of CA stenosis in arterial phase, sagittal view

Fig. 2: Hepatic artery and well-developed gastroduodenal
artery, coronal CT scan in arterial phase
Fig. 2: Hepatic artery and well-developed gastroduodenal artery, coronal CT scan in arterial phase

Fig. 3: Celiac axis, findings before − 3A and after − 3B;
stent insertion
Fig. 3: Celiac axis, findings before − 3A and after − 3B; stent insertion

DISCUSSION

Careful attention to preservation of a sufficient arterial blood flow to the liver is of a paramount importance in hepatobiliary surgery. Detailed preoperative planning is necessary, which is why the diagnosis of CAS should be included in the radiological report. Additionaly, a proven correlation between the diameter of GDA and the degree of CA stenosis could be used in the assessment of hemodynamic significance of the stenosis [6]. Characteristics for MAL compression is the hook-shape appearance of the artery on sagittal images and stenotic lesions located at least 5mm from aorta with a short nonstenotic segment in between. On the contrary, calcified stenosis imminent to aorta without any deviation is specific for atherosclerosis [1,3,7]. Smith et al found no association between CAS <60% in diameter and increased postoperative morbidity [8]. To establish the severity of stenosis and the supposed extent of needed intervention, Sugae T. et al proposed a classification of the CAS owing to MAL compression according to preoperative CT scans as follows: type A represents a stenosis of less than 50% in diameter and 3mm in length, where no intervention is necessary. Type B is stenosis of 50−80%, 3−8mm in length, where MAL division should establish a sufficient HA blood flow. Type C is stenosis of more than 80% in diameter, 8mm or more in length with visibly well-developed collateral circulation and a high probability of the need of arterial reconstruction [3].

In case of a known stenosis with non-conclusive GDA clamping test, intraoperative doppler ultrasound is commonly used by many hepatobiliary surgeons. To date, there is no consensus on the threshold to necessitate further intervention in PD. However, tardus-parvus pattern waveform with acceleration time greater than 80ms and resistive index (RI) less than 0.5 on intraoperative ultrasound indicate insufficient HA blood flow in the setting of liver transplant surgery [9].

The prevalence of hemodynamically significant arterial stenosis in patients undergoing PD is reported in up to 5% [1]. In the most common setting, CAS is caused by MAL compression and division of the ligament is sufficient to restore CHA blood flow in up to 87% of these cases [1]. Complete liberation of celiac artery from surrounding tissues should be achieved, sometimes necessitating ligation of the inferior phrenic artery [10,11]. Several complications have been reported, such as bleeding, chylous ascites, pleural effusion, pneumothorax, aortic injury and wound infection [12−14]. Multiple studies on median arcuate ligament syndrome demonstrated that endovascular angioplasty alone is insufficient due to sustained extrinsic pressure of intact MAL on celiac axis [7,15]. However, PTA has proved to be an effective adjunctive therapy to surgical MAL division [15].

Preoperative stenting of significant CAS should be considered especially in atherosclerotic occlusions. Complications include thrombosis, restenosis and dislocation of the stent, partially preventable with anticoagulation therapy and waiting period of at least 3 weeks [16]. Sufficient waiting period in patients with pancreatic head malignancy is potentially achievable in patients scheduled for neoadjuvant treatment. All three patients with atherosclerotic arterial stenosis reported by Gajoux et al. treated with endovascular stenting before PD reported no procedural complications and uneventful postoperative recovery [1]. Arterial reconstructions represent the last treatment modality possibly used in patients with celiac axis stenosis to safely perform PD. Several vascular reconstruction have been described [17]. The use of autologous grafts is desirable, given the potential risk of intraoperative contamination by gastrointestinal tract and the leakage of pancreatic fluid around the anastomosis in case of postoperative pancreatic fistula (POPF) development [3]. Similarly, the vascular anastomosis located aside of pancreaticojejunal anastomosis, e.g. graft between the iliac and the splenic artery is of advantage in case of POPF development [17,18].

Predicting which patient will develop a clinically relevant ischemia following PD is challenging given the highly variable nature of collateral circulation [16]. Compensating mechanisms for postoperative highgrade stenosis include the development of additional collaterals from SMA, inferior phrenic artery, lumbar arteries or splenic artery [19]. Nonetheless, most patients with liver ischemia develop superinfection favored by contamination through biliodigestive anastomosis, which not uncommonly limits further oncological treatment.

In the case of our patient, preoperative radiological findings revealed CAS due to the external compression. MAL division alone was not a sufficient intervention. This was quickly recognized and treated with postoperative endovascular stent insertion. We acknowledge the possible risks of addressing CAS partly postoperatively. Nevertheless, the endovascular stenting after intraoperative division of MAL represented a sufficient treatment modality in this case. Furthermore, this case report highlights the need of a high quality interdisciplinary cooperation in tertiary surgical centers. The constantly present interventional radiologist is able to promtly react to vascular complications, which is crucialy important in hepatobiliary surgery.

CONCLUSION

Ischemic complications after pancreatoduodenectomy are not to be neglected. Delayed diagnosis is related to poor patient prognosis and therefore attention should be paid to any sign of visceral ischemia on first postoperative days [1]. Preoperative planning, early diagnosis and adequate treatment is crucial to limit ischemic complications.

Notes:

acceleration time − the interval from the end of diastole to the first systolic peak the measure of the rapidity of upstroke

RI                         − resistive index − peak systolic velocity end diastolic velocity/ peak systolic velocity

Supported by The grant IP MO 1012

Conflict of interests

The authors declare that they have not conflict of interest in connection with this paper and that the article has not been published in any other journal, except congress abstracts and clinical guidelines.

MUDr. Tereza Kočišová

Chirurgická klinika 2. LF UK a ÚVN, Praha

U vojenské nemocnice 1200

160 00 Praha 6

e-mail: t.kocisova@gmail.com


Zdroje

1. Gaujoux S, Sauvanet A, Vulliermeet MP, al. Ischemic complications after pancreaticoduodenectomy: incidence, prevention, and management Ann Surg. 2009 Jan;249(1):111−117. doi: 10.1097/ SLA.0b013e3181930249.

2. McCracken E, Turley R, Cox M, et al., Leveraging aberrant vasculature in celiac artery stenosis: The arc of buhler in pancreaticoduodenectomy. J Pancreat Cancer 2018 Jan 1;4(1):4−6. doi: 10.1089/ pancan.2017.0020.

3. Sugae T, Fujii T, Kodera Y, et al., Classification of the celiac axis stenosis owing to median arcuate ligament compression, based on severity of the stenosis with subsequent proposals for management during pancreatoduodenectomy. Surgery 2012 Apr;151(4):543-9. doi: 10.1016/j.surg.2011.08.012. Epub 2011 Oct 14.

4. Yamamoto M, Itamoto T, Oshita A, et al., Celiac axis stenosis due to median arcuate ligament compression in a patient who underwent pancreatoduodenectomy; intraoperative assessment of hepatic arterial flow using Doppler ultrasonography: a case report. J Med Case Rep. 2018 Apr 11;12(1):92. doi: 10.1186/s13256- 018-1614-2.

5. Bull DA, HunterGC, Crabtree TG, et al. Hepatic ischemia, caused by celiac axis compression, complicating pancreaticoduodenectomy Ann Surg. 1993 Mar;217(3):244−247. doi: 10.1097/00000658-199303000-00005.

6. Haquin A, Sigovan M, Si-Mohamed S, et al. Phase-contrast MRI evaluation of haemodynamic changes induces by a coeliac axis stenosis in the gastroduodenal artery. Br J Radiol. 2017;90(1072). doi: 10.1259/bjr.20160802.

7. Delis KT, Gloviczki P, Altuwaijri M, et al. Median arcuate ligament syndrome: open celiac artery reconstruction and ligament division after endovascular failure. J Vasc Surg. 2007 Oct;46(4):799−802. doi: 10.1016/j.jvs.2007.05.049.

8. Smith SL, Rae D, Sinclair M, et al. Does moderate celiac axis stenosis identified on preoperative multidetector computed tomographic angiography predict an increased risk of complications after pancreaticoduodenectomy for malignant pancreatic tumors? Pancreas 2007 Jan;34(1):80−84. doi:10.1097/01. mpa.0000240607.49183.7e.

9. Sanyal R, Zarzour JG, Ganeshanet DM, et al. Postoperative doppler evaluation of liver transplants. Indian J Radiol Imaging 2014 Oct-Dec; 24(4): 360–366. doi: 10.4103/0971-3026.143898.

10. Brody F, Richards NG. Median arcuate ligament release. J Am Coll Surg. 2014. 219(4):e45−50.

11. Berard X, Cau J, Déglise S,et al. Laparoscopic surgery for coeliac artery compression syndrome: current management and technical aspects. Eur J Vasc Endovasc Surg. 2012 Jan;43(1):38−42. doi: 10.1016/j.ejvs.2011.09.023. Epub 2011 Oct 15.

12. Riess KP, Serck L, Gundersen SB, et al. Seconds from disaster: lessons learned from laparoscopic release of the median arcuate ligament. Surg Endosc. 2009 May;23(5):1121−1124. doi: 10.1007/ s00464-008-0256-7. Epub 2009 Mar.

13. Duran M, Simon F, Ertas N, et al. Open vascular treatment of median arcuate ligament syndrome. BMC Surg. 2017 Aug 29;17(1):95. doi: 10.1186/s12893-017- 0289-8.

14. Jimenez JC, Harlander-Locke M, Dutson EP. Open and laparoscopic treatment of median arcuate ligament syndrome. J Vasc Surg. 2012 Sep;56(3):869-73. doi: 10.1016/j. jvs.2012.04.057. Epub 2012 Jun 27.

15. Kim EN, Lamb K, Relleset D, et al. Median arcuate ligament syndrome-review of this rare disease. JAMA Surg. 2016 May 1;151(5):471−477. doi: 10.1001/jamasurg. 2016.0002.

16. Sakorafas GH, Sarr MG, Peros G. Celiac artery stenosis: an underappreciated and unpleasant surprise in patients undergoing pancreaticoduodenectomy. J Am Coll Surg. 2008 Feb;206(2):349−356. doi: 10.1016/j.jamcollsurg.2007.09.002. Epub 2007 Oct.

17. Beane JD, Schwarz RE. Vascular challenges from pancreatoduodenectomy in the setting of coeliac artery stenosis. BMJ Case Rep. 2017 Mar 16;2017:bcr2016217943. doi: 10.1136/bcr-2016-217943.

18. Okamoto H, Suminaga Y, Toyama N, et al. Autogenous vein graft from iliac artery to splenic artery for celiac occlusion in pancreaticoduodenectomy. J Hepatobiliary Pancreat Surg. 2003;10(1):109−112. doi: 10.1007/s10534-002-0831-7.

19. Pfeiffenberger J, Adam U, Drognitz O, et al. Celiac axis stenosis in pancreatic head resection for chronic pancreatitis. Langenbecks Arch Surg. 2002 Oct;387(5−6):210−215. doi: 10.1007/ s00423-002-0310-1.

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