Abstract
Purpose
Risk factors of ischemic gastropathy (IG) following distal pancreatectomy with en bloc celiac axis resection (DP-CAR) remain unclear.
Methods
Fifty consecutive patients with pancreatic cancer who underwent DP-CAR were retrospectively reviewed for possible risk factors for IG. This study was registered on the UMIN Clinical Trials Registry (UMIN 000028732).
Results
Complications higher than grade 3 were observed in 21 patients (42%) and mortality in 4 (8%). Left gastric artery (LGA) resection (P = 0.046) and a combination of left inferior phrenic artery (IPA) with LGA resection (P = 0.012) were risk factors of IG, and an elevated creatine kinase (CK) value ≥ 1005 IU/L (P = 0.025) was associated with IG. Among prognostic factors, IG (OR, 5.997; 95% CI, 1.543–23.309; P = 0.010), completion of adjuvant chemotherapy (OR, 0.282; 95% CI, 0.121–0.654; P = 0.003), longer operative time (OR, 2.261; 95% CI, 1.084–4.714; P = 0.030), and higher age (OR, 2.212; 95% CI, 1.081–4.524; P = 0.030) remained independent predictors of survival. Comparison at 2 and 3 months postoperatively showed nutritional values were higher in patients who underwent LGA-preserving DP-CAR than those with LGA-resecting DP-CAR: total protein (7.17 ± 0.56 vs 6.65 ± 0.66 g/dl, P = 0.007), albumin (4.04 ± 0.45 vs 3.43 ± 0.43 g/dl, P < 0.001), and total cholesterol (162.3 ± 34.7 vs 141.6 ± 27.2 mg/dl, P = 0.044).
Conclusions
The poorer prognosis in patients who undergo DP-CAR may be related to more advanced tumors. A combination of left IPA and LGA resection was a significant risk factor for IG. IG, completion of adjuvant chemotherapy, longer operative time, and higher age remain good independent predictors of survival.
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References
Rahib L, Smith BD, Aizenberg R, Rosenzweig AB, Fleshman JM, Matrisian L (2014) Projecting cancer incidence and deaths to 2030: the unexpected burden of thyroid, liver, and pancreas cancers in the United States. Cancer Res 74:2913–2921
Valle JW, Palmer D, Jackson R, Cox T, Neoptolemos JP, Ghaneh P, Rawcliffe CL, Bassi C, Stocken DD, Cunningham D, O'Reilly D, Goldstein D, Robinson BA, Karapetis C, Scarfe A, Lacaine F, Sand J, Izbicki JR, Mayerle J, Dervenis C, Oláh A, Butturini G, Lind PA, Middleton MR, Anthoney A, Sumpter K, Carter R, Büchler MW (2014) Optimal duration and timing of adjuvant chemotherapy after definitive surgery for ductal adenocarcinoma of the pancreas: ongoing lessons from the ESPAC-3 study. J Clin Oncol 32:504–512
Katz MH, Shi Q, Ahmad SA, Herman JM, Marsh Rde W, Collisson E, Schwartz L, Frankel W, Martin R, Conway W, Truty M, Kindler H, Lowy AM, Bekaii-Saab T, Philip P, Talamonti M, Cardin D, LoConte N, Shen P, Hoffman JP, Venook AP (2016) Preoperative modified FOLFIRINOX treatment followed by capecitabine-based chemoradiation for borderline resectable pancreatic cancer: alliance for clinical trials in oncology trial A021101. JAMA Surg 151:e161137
Fortner JG, Kim DK, Cubilla A, Turnbull A, Pahnke LD, Shils ME (1977) Regional pancreatectomy: en bloc pancreatic, portal vein and lymph node resection. Ann Surg 186:42–50
Appleby LH (1953) The coeliac axis in the expansion of the operation for gastric carcinoma. Cancer 6:704–707
Kondo S, Katoh H, Hirano S, Ambo Y, Tanaka E, Okushiba S, Morikawa T (2003) Results of radical distal pancreatectomy with en bloc resection of the celiac artery for locally advanced cancer of the pancreatic body. Langenbeck's Arch Surg 388:101–106
Hishinuma S, Ogata Y, Tomikawa M, Ozawa I (2007) Stomach-preserving distal pancreatectomy with combined resection of the celiac artery: radical procedure for locally advanced cancer of the pancreatic body. J Gastrointest Surg 11:743–749
Hirano S, Kondo S, Hara T, Ambo Y, Tanaka E, Shichinohe T, Suzuki O, Hazama K (2007) Distal pancreatectomy with en bloc celiac axis resection for locally advanced pancreatic body cancer: long-term results. Ann Surg 246:46–51
Okada K, Kawai M, Tani M, Hirono S, Miyazawa M, Shimizu A, Kitahata Y, Yamaue H (2013) Surgical strategy for patients with pancreatic body/tail carcinoma: who should undergo distal pancreatectomy with en-bloc celiac axis resection? Surgery 153:365–372
Kawai M, Hirono S, Okada K, Sho M, Nakajima Y, Eguchi H, Nagano H, Ikoma H, Morimura R, Takeda Y, Nakahira S, Suzumura K, Fujimoto J, Yamaue H (2016) Randomized controlled trial of pancreaticojejunostomy versus stapler closure of the pancreatic stump during distal pancreatectomy to reduce pancreatic fistula. Ann Surg 264:180–187
Okada K, Kawai M, Tani M, Hirono S, Miyazawa M, Shimizu A, Kitahata Y, Yamaue H (2014) Isolated Roux-en-Y anastomosis of the pancreatic stump in a duct-to-mucosa fashion in patients with distal pancreatectomy with en-bloc celiac axis resection. J Hepatobiliary Pancreat Sci 21:193–198
Klompmaker S, de Rooij T, Korteweg JJ, van Dieren S, van Lienden KP, van Gulik TM, Busch OR, Besselink MG (2016) Systematic review of outcomes after distal pancreatectomy with coeliac axis resection for locally advanced pancreatic cancer. Br J Surg 103:941–949
Okada K, Kawai M, Tani M, Hirono S, Miyazawa M, Shimizu A, Kitahata Y, Yamaue H (2014) Preservation of the left gastric artery on the basis of anatomical features in patients undergoing distal pancreatectomy with celiac axis en-bloc resection (DP-CAR). World J Surg 38:2980–2985
Sobin LH, Gospodarowicz MK, Witterkind C (2009) TNM classification of malignant tumors, 7th edn. Wiley, New York
Menon KV, Gomez D, Smith AM, Anthoney A, Verbeke CS (2009) Impact of margin status on survival following pancreatoduodenectomy for cancer: the Leeds Pathology Protocol (LEEPP). HPB (Oxford) 11:18–24
National Comprehensive Cancer Network. NCCN practice guidelines for pancreatic cancer, version 2. 2015 Available at: http://www.nccn.org/professionals/physician_gls/PDF/pancreatic.pdf. Accessed 15 Jan 2016
Abo D, Hasegawa Y, Sakuhara Y, Terae S, Shimizu T, Tha KK, Tanaka E, Hirano S, Kondo S, Shirato H (2012) Feasibility of a dual microcatheter-dual interlocking detachable coil technique in preoperative embolization in preparation for distal pancreatectomy with en bloc celiac axis resection for locally advanced pancreatic body cancer. J Hepatobiliary Pancreat Sci 19:431–437
Hirono S, Kawai M, Okada KI, Miyazawa M, Shimizu A, Kitahata Y, Ueno M, Yamaue H (2016) Treatment strategy for borderline resectable pancreatic cancer with radiographic artery involvement. Pancreas 45:1438–1446
Okada K, Kawai M, Hirono S, Satoi S, Yanagimoto H, Ioka T, Miyazawa M, Shimizu A, Kitahata Y, Yamaue H (2016) Impact of treatment duration of neoadjuvant FIRINOX in patients with borderline resectable pancreatic cancer: a pilot trial. Cancer Chemother Pharmacol 78:719–726
Okada KI, Hirono S, Kawai M, Miyazawa M, Shimizu A, Kitahata Y, Ueno M, Hayami S, Yamaue H (2017) Phase I study of Nab-paclitaxel plus gemcitabine as neoadjuvant therapy for borderline resectable pancreatic cancer. Anticancer Res 37:853–858
Oettle H, Post S, Neuhaus P, Gellert K, Langrehr J, Ridwelski K, Schramm H, Fahlke J, Zuelke C, Burkart C, Gutberlet K, Kettner E, Schmalenberg H, Weigang-Koehler K, Bechstein WO, Niedergethmann M, Schmidt-Wolf I, Roll L, Doerken B, Riess H (2007) Adjuvant chemotherapy with gemcitabine vs observation in patients undergoing curative-intent resection of pancreatic cancer: a randomized controlled trial. JAMA 297:267–277
Yamaue H, Satoi S, Kanbe T, Miyazawa M, Tani M, Kawai M, Hirono S, Okada K, Yanagimoto H, Kwon AH, Mukouyama T, Tsunoda H, Chijiiwa K, Ohuchida J, Kato J, Ueda K, Yamaguchi T, Egawa S, Hayashi K, Shirasaka T (2014) Phase II clinical study of alternate-day oral therapy with S-1 as first-line chemotherapy for locally advanced and metastatic pancreatic cancer. Cancer Chemother Pharmacol 73:97–102
Uesaka K, Boku N, Fukutomi A, Okamura Y, Konishi M, Matsumoto I, Kaneoka Y, Shimizu Y, Nakamori S, Sakamoto H, Morinaga S, Kainuma O, Imai K, Sata N, Hishinuma S, Ojima H, Yamaguchi R, Hirano S, Sudo T, Ohashi Y, JASPAC 01 Study Group (2016) Adjuvant chemotherapy of S-1 versus gemcitabine for resected pancreatic cancer: a phase 3, open-label, randomised, non-inferiority trial (JASPAC 01). Lancet 388:248–257
Marco-Clement I, Martinez-Barco A, Ahumada N, Simon C, Valderrama JM, Sanudo J, Arrazola J (2016) Anatomical variations of the celiac trunk: cadaveric and radiological study. Surg Radiol Anat 38:501–510
Aslaner R, Pekcevik Y, Sahin H, Toka O (2017) Variations in the origin of inferior phrenic arteries and their relationship to celiac axis variations on CT angiography. Korean J Radiol 18:336–344
Wente MN, Bassi C, Dervenis C, Fingerhut A, Gouma DJ, Izbicki JR, Neoptolemos JP, Padbury RT, Sarr MG, Traverso LW, Yeo CJ, Büchler MW (2007) Delayed gastric emptying (DGE) after pancreatic surgery: a suggested definition by the International Study Group of Pancreatic Surgery (ISGPS). Surgery 142:761–768
Bassi C, Marchegiani G, Dervenis C, Sarr M, Abu Hilal M, Adham M, Allen P, Andersson R, Asbun HJ, Besselink MG, Conlon K, Del Chiaro M, Falconi M, Fernandez-Cruz L, Fernandez-Del Castillo C, Fingerhut A, Friess H, Gouma DJ, Hackert T, Izbicki J, Lillemoe KD, Neoptolemos JP, Olah A, Schulick R, Shrikhande SV, Takada T, Takaori K, Traverso W, Vollmer CR, Wolfgang CL, Yeo CJ, Salvia R, Buchler M, International Study Group on Pancreatic Surgery (ISGPS) (2017) The 2016 update of the International Dtudy Group (ISGPS) definition and grading of postoperative pancreatic fistula: 11 years after. Surgery 161:584–591
Wente MN, Veit JA, Bassi C, Dervenis C, Fingerhut A, Gouma DJ, Izbicki JR, Neoptolemos JP, Padbury RT, Sarr MG, Yeo CJ, Büchler MW (2007) Postpancreatectomy hemorrhage (PPH): an International Study Group of Pancreatic Surgery (ISGPS) definition. Surgery 142:20–25
Sato T, Saiura A, Inoue Y, Takahashi Y, Arita J, Takemura N (2016) Distal pancreatectomy with en bloc resection of the celiac axis with preservation or reconstruction of the left gastric artery in patients with pancreatic body cancer. World J Surg 40:2245–2253
Okada KI, Hirono S, Kawai M, Hayami S, Asamura S, Wada Y, Ueno M, Miyazawa M, Shimizu A, Kitahata Y, Yamaue H (2017) Left gastric artery reconstruction after distal pancreatectomy with celiac axis en-bloc resection: how we do it. Gastrointest Tumors 4:28–35
van der Voort PH, Westra B, Wester JP, Bosman RJ, van Stijn I, Haagen IA, Loupatty FJ, Rijkenberg S (2014) Can serum L-lactate, D-lactate, creatine kinase and I-FABP be used as diagnostic markers in critically ill patients suspected for bowel ischemia. BMC Anesthesiol 14:111
Matsumoto S, Sekine K, Funaoka H, Yamazaki M, Shimizu M, Hayashida K, Kitano M (2014) Diagnostic performance of plasma biomarkers in patients with acute intestinal ischaemia. Br J Surg 101:232–238
Palmerini T, Mehran R, Dangas G, Nikolsky E, Witzenbichler B, Guagliumi G, Dudek D, Genereux P, Caixeta A, Rabbani L, Weisz G, Parise H, Fahy M, Xu K, Brodie B, Lansky A, Stone GW (2011) Impact of leukocyte count on mortality and bleeding in patients with myocardial infarction undergoing primary percutaneous coronary interventions: analysis from the Harmonizing Outcome with Revascularization and Stent in Acute Myocardial Infarction trial. Circulation 123:2829–2837
Nakamura T, Hirano S, Noji T, Asano T, Okamura K, Tsuchikawa T, Murakami S, Kurashima Y, Ebihara Y, Nakanishi Y, Tanaka K, Shichinohe T (2016) Distal pancreatectomy with en bloc celiac Axis resection (modified Appleby procedure) for locally advanced pancreatic body cancer: a single-center review of 80 consecutive patients. Ann Surg Oncol 23(Suppl 5):969–975
Sadot E, Doussot A, O'Reilly EM, Lowery MA, Goodman KA, Do RK, Tang LH, Gönen M, D'Angelica MI, DeMatteo RP, Kingham TP, Jarnagin WR, Allen PJ (2015) FOLFIRINOX induction therapy for stage 3 pancreatic adenocarcinoma. Ann Surg Oncol 22:3512–3521
Crippa S, Partelli S, Zamboni G, Barugola G, Capelli P, Inama M, Bassi C, Pederzoli P, Falconi M (2012) Poorly differentiated resectable pancreatic cancer: is upfront resection worthwhile? Surgery 152:S112–S119
Strobel O, Hinz U, Gluth A, Hank T, Hackert T, Bergmann F, Werner J, Büchler MW (2015) Pancreatic adenocarcinoma: number of positive nodes allows to distinguish several N categories. Ann Surg 261:961–969
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We would like to thank the Clinical Research Center, Wakayama Medical University, for proofreading and editing the manuscript.
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KO drafted the manuscript. MK and SH helped to draft the manuscript. MM, YK, MU, and SH supported acquisition of data. HY helped in the revision of the article. TS supervised statistical analysis.
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All procedures performed were in accordance with the ethical standards of the institutional and national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
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Informed consent was obtained from all individual participants included in the study.
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Okada, Ki., Kawai, M., Hirono, S. et al. Ischemic gastropathy after distal pancreatectomy with en bloc celiac axis resection for pancreatic body cancer. Langenbecks Arch Surg 403, 561–571 (2018). https://doi.org/10.1007/s00423-018-1692-z
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DOI: https://doi.org/10.1007/s00423-018-1692-z