Abstracts
Purpose
The first reports of hepatic steatosis following pancreaticoduodenectomy (PD) were published several years ago; however, clear risk factors remain to be identified. Therefore, the aim of this study was to identify the risk factors for hepatic steatosis post-PD.
Methods
We studied 90 patients who had undergone PD between September 2005 and January 2015. The inclusion criteria were as follows: available unenhanced CT within one month before PD and at least one unenhanced CT acquisition between PD and chemotherapy initiation. Using scanners, we studied the liver and spleen density as well as the surface areas of visceral (VF) and subcutaneous fat (SCF). These variables were previously identified by univariate and multivariate analyses.
Results
Hepatic steatosis occurred in 25.6% of patients at 45.2 days, on average, post-PD. Among the patients with hepatic steatosis, the average liver density was 52 HU before PD and 15.1 HU post-PD (p < 0.001). The Patients with hepatic steatosis lost more VF (mean, 28 vs. 11 cm2) and SCF (28.8 vs. 13.7 cm2) (p < 0.01 and p = 0.01, respectively). Portal vein resection and extensive lymph node dissection were independent risk factors in the multivariate analysis (odds ratio [OR] 5.29, p = 0.009; OR 3.38, p = 0.04, respectively).
Conclusion
Portal vein resection and extensive lymph node dissection are independent risk factors for post-PD hepatic steatosis.
Similar content being viewed by others
References
Lundstedt C, Andrén-Sandberg A (1991) CT of liver steatosis after subtotal pancreatectomy. Acta Radiol 32:30–33. doi:10.3109/02841859109177502
Yeo CJ, Cameron JL, Lillemoe KD, et al. (2002) Pancreaticoduodenectomy with or without distal gastrectomy and extended retroperitoneal lymphadenectomy for periampullary adenocarcinoma, part 2: randomized controlled trial evaluating survival, morbidity, and mortality. Ann Surg 236:355–368. doi:10.1097/01.SLA.0000027272.08464.0B
Cameron JL, Riall TS, Coleman J, Belcher KA (2006) One thousand consecutive pancreaticoduodenectomies. Ann Surg 244:10–15. doi:10.1097/01.sla.0000217673.04165.ea
Neoptolemos JP, Russell RC, Bramhall S, Theis B (1997) Low mortality following resection for pancreatic and periampullary tumours in 1026 patients: UK survey of specialist pancreatic units. UK Pancreatic Cancer Group. Br J Surg 84:1370–1376
Richter A, Niedergethmann M, Sturm JW, et al. (2003) Long-term results of partial pancreaticoduodenectomy for ductal adenocarcinoma of the pancreatic head: 25-year experience. World J Surg 27:324–329. doi:10.1007/s00268-002-6659-z
Kooby DA, Gillespie T, Bentrem D, et al. (2008) Left-sided pancreatectomy: a multicenter comparison of laparoscopic and open approaches. Ann Surg 248:438–446. doi:10.1097/SLA.0b013e318185a990
Lillemoe KD, Kaushal S, Cameron JL, et al. (1999) Distal pancreatectomy: indications and outcomes in 235 patients. Ann Surg 229:693–698. doi:10.1097/00000658-199905000-00012
Nomura R, Ishizaki Y, Suzuki K, Kawasaki S (2007) Development of hepatic steatosis after pancreatoduodenectomy. Am J Roentgenol 189:1484–1489. doi:10.2214/AJR.07.2809
Reichler B, Hofmann-Preiss K, Tomandl B, Zirngibl H, Beyer R (1992) Results of computerized tomography after Whipple operation of chronic pancreatitis. Bildgebung 59:72–75
Okamura Y, Sugimoto H, Yamada S, et al. (2012) Risk factors for hepatic steatosis after pancreatectomy: a retrospective observational cohort study of the importance of nutritional management. Pancreas 41:1067–1072. doi:10.1097/MPA.0b013e31824c10ab
Krawczyk M, Bonfrate L, Portincasa P (2010) Nonalcoholic fatty liver disease. Best Pract Res Clin Gastroenterol 24:695–708. doi:10.1016/j.bpg.2010.08.005
Caldwell SH, Oelsner DH, Iezzoni JC, et al. (1999) Cryptogenic cirrhosis: clinical characterization and risk factors for underlying disease. Hepatology 29:664–669. doi:10.1002/hep.510290347
Miura H, Ijichi M, Ando Y, et al. (2013) A rapidly progressive and fatal case of nonalcoholic steatohepatitis following pancreaticoduodenectomy. Clin J Gastroenterol 6:470–475
Zein CO, Unalp A, Colvin R, et al. (2011) Smoking and severity of hepatic fibrosis in nonalcoholic fatty liver disease. J Hepatol 54:753–759. doi:10.1016/j.jhep.2010.07.040
Seufferlein T, Bachet JB, Van Cutsem E, Rougier P on behalf of the ESMO Guidelines Working (2012) Pancreatic adenocarcinoma: ESMO-ESDO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol 23:vii33–vii40. doi:10.1093/annonc/mds224
Niedergethmann M, Hildenbrand R, Wostbrock B, et al. (2002) High expression of vascular endothelial growth factor predicts early recurrence and poor prognosis after curative resection for ductal adenocarcinoma of the pancreas. Pancreas 25:122–129. doi:10.1097/00006676-200208000-00002
Festi D, Schiumerini R, Marzi L, et al. (2013) Review article: the diagnosis of non-alcoholic fatty liver disease—availability and accuracy of non-invasive methods. Aliment Pharmacol Ther 37:392–400. doi:10.1111/apt.12186
Betzel B, Drenth JP (2014) A new noninvasive technique for estimating hepatic triglyceride: will liver biopsy become redundant in diagnosing non-alcoholic fatty liver disease? BMC Med 12:152. doi:10.1186/s12916-014-0152-z
Kawamoto S, Soyer PA, Fishman EK, Bluemke DA (1998) Nonneoplastic liver disease: evaluation with CT and MR imaging. RadioGraphics 18:827–848. doi:10.1148/radiographics.18.4.9672968
Park SH, Kim PN, Kim KW, et al. (2006) Macrovesicular hepatic steatosis in living liver donors: use of CT for quantitative and qualitative assessment. Radiology 239:105–112. doi:10.1148/radiol.2391050361
Tokunaga K, Matsuzawa Y, Ishikawa K, Tarui S (1983) A novel technique for the determination of body fat by computed tomography. Int J Obes 7:437–445
Irlbeck T, Massaro JM, Bamberg F, et al. (2010) Association between single-slice measurements of visceral and abdominal subcutaneous adipose tissue with volumetric measurements: the Framingham heart study. Int J Obes (Lond) 34:781–787. doi:10.1038/ijo.2009.279
Yoshizumi T, Nakamura T, Yamane M, et al. (1999) Abdominal fat: standardized technique for measurement at CT. Radiology 211:283–286. doi:10.1148/radiology.211.1.r99ap15283
Kvist H, Chowdhury B, Grangård U, Tylén U, Sjöstrom L (1988) Total and visceral adipose-tissue volumes derived from measurements with computed tomography in adult men and women: predictive equations. Am J Clin Nutr 48:1351–1361
Berry AJ (2013) Pancreatic surgery: indications, complications, and implications for nutrition intervention. Nutr Clin Pract 28:330–357. doi:10.1177/0884533612470845
Buscemi S, Damiano G, Palumbo VD, et al. (2015) Enteral nutrition in pancreaticoduodenectomy: a literature review. Nutrients 7:3154–3165. doi:10.3390/nu7053154
Yu HH, Shan YS, Lin PW (2010) Effect of pancreaticoduodenectomy on the course of hepatic steatosis. World J Surg 34:2122–2127. doi:10.1007/s00268-010-0636-8
Zorzi D, Laurent A, Pawlik TM, et al. (2007) Chemotherapy-associated hepatotoxicity and surgery for colorectal liver metastases. Br J Surg 94:274–286. doi:10.1002/bjs.5719
Song SC, Choi SH, Choi DW, et al. (2011) Potential risk factors for nonalcoholic steatohepatitis related to pancreatic secretions following pancreaticoduodenectomy. World J Gastroenterol 17:3716–3723. doi:10.3748/wjg.v17.i32.3716
Tanaka N, Horiuchi A, Yokoyama T, et al. (2011) Clinical characteristics of de novo nonalcoholic fatty liver disease following pancreaticoduodenectomy. J Gastroenterol 46:758–768. doi:10.1007/s00535-011-0370-5
Kato H, Isaji S, Azumi Y, et al. (2010) Development of nonalcoholic fatty liver disease (NAFLD) and nonalcoholic steatohepatitis (Nash) after pancreaticoduodenectomy: proposal of a postoperative NAFLD scoring system. J Hepato Biliary Pancreat Sci 17:296–304. doi:10.1007/s00534-009-0187-2
Ito Y, Kenmochi T, Shibutani S, et al. (2014) Evaluation of predictive factors in patients with nonalcoholic fatty liver disease after pancreaticoduodenectomy. Am Surg 80:500–504
Ivanics T, Sanjeevi S, Ansorge C, Andren-Sandberg A (2015) Hepatic Steatosis following pancreatic surgery: a Swedish Centers experience with demographics, risks and outcome. J Pancreas 16:527–532
Nakagawa N, Murakami Y, Uemura K, et al. (2014) Nonalcoholic fatty liver disease after pancreatoduodenectomy is closely associated with postoperative pancreatic exocrine insufficiency. J Surg Oncol 110:720–726. doi:10.1002/jso.23693
Hasselmann M, Kummerlen C (2006) Nutrition des patients en insuffisance respiratoire aiguë. Nutr Clin Metab 20:208–214. doi:10.1016/j.nupar.2006.10.186
Parikh AA, Gentner B, Wu TT, et al. (2003) Perioperative complications in patients undergoing major liver resection with or without neoadjuvant chemotherapy. J Gastrointest Surg 7:1082–1088. doi:10.1016/j.gassur.2003.08.005
Abildgaard A, Kolmannskog F, Mathisen O, Bergan A (1990) Computed tomography after modified Whipple procedure with pancreatic duct occlusion. Acta Radiol 31:579–584. doi:10.1080/02841859009173101
Slezak LA, Andersen DK (2001) Pancreatic resection: effects on glucose metabolism. World J Surg 25:452–460. doi:10.1007/s002680020337
Kontis E, Prassas E, Srinivasan P, Prachalias AA (2016) Extended lymphadenectomy and “mesopancreas” excision during pancreatoduodenectomy for cancer; is it worth it? Review of current evidence. J Pancreas 17:149–153
Brennan MF, Moccia RD, Klimstra D (1996) Management of adenocarcinoma of the body and tail of the pancreas. Ann Surg 223:506–512. doi:10.1097/00000658-199605000-00006
Johnson PT, Curry CA, Urban BA, Fishman EK (2002) Spiral CT following the Whipple procedure: distinguishing normal postoperative findings from complications. J Comput Assist Tomogr 26:956–961. doi:10.1097/00004728-200211000-00018
Mortelé KJ, Lemmerling M, de Hemptinne B, et al. (2000) Postoperative findings following the Whipple procedure: determination of prevalence and morphologic abdominal CT features. Eur Radiol 10:123–128. doi:10.1007/s003300050017
Rupp CC, Linehan DC (2009) Extended lymphadenectomy in the surgery of pancreatic adenocarcinoma and its relation to quality improvement issues. J Surg Oncol 99:207–214. doi:10.1002/jso.21210
Iqbal J, Hussain MM (2009) Intestinal lipid absorption. Am J Physiol Endocrinol Metab 296:E1183–E1194. doi:10.1152/ajpendo.90899.2008
Brasaemle DL, Rubin B, Harten IA, et al. (2000) Perilipin A increases triacylglycerol storage by decreasing the rate of triacylglycerol hydrolysis. J Biol Chem 275:38486–38493. doi:10.1074/jbc.M007322200
Bastard JP, Bruno F (2012) Physiologie et physiopatholigie du tissus adipeux. Paris: Springer
Parks EJ, Hellerstein MK (2000) Carbohydrate-induced hypertriacylglycerolemia: historical perspective and review of biological mechanisms. Am J Clin Nutr 71:412–433
Vuarnesson H, Lupinacci RM, Semoun O, et al. (2013) Number of examined lymph nodes and nodal status assessment in pancreaticoduodenectomy for pancreatic adenocarcinoma. Eur J Surg Oncol 39:1116–1121. doi:10.1016/j.ejso.2013.07.089
Sato T (ed) (1997) Color atlas of applied anatomy of lymphatics anatomical basis for cancer operation. Tokyo: Nankoudou
Arrivé L, Azizi L, Lewin M, et al. (2007) DIV-WP-7 Lymphographie par resonance magnetique: imagerie abdominale et retroperitoneale. J Radiol 88:1542. doi:10.1016/S0221-0363(07)81747-1
Yamada Y, Mori H, Matsumoto S, et al. (2015) Lymphatic pathway around the pancreatic head and extrahepatic bile duct: evaluation using MR imaging at 3.0-T. Abdom Imaging 40:1617–1628. doi:10.1007/s00261-014-0346-z
Ahmed M, Rubio IT, Kovacs T, Klimberg VS, Douek M (2016) Systematic review of axillary reverse mapping in breast cancer. Br J Surg 103:170–178. doi:10.1002/bjs.10041
Geppert B, Persson J (2015) Robotic infrarenal paraaortic and pelvic nodal staging for endometrial cancer: feasibility and lymphatic complications. Acta Obstet Gynecol Scand 94:1074–1081. doi:10.1111/aogs.12712
Solmaz U, Turan V, Mat E, et al. (2015) Chylous ascites following retroperitoneal lymphadenectomy in gynecologic malignancies: incidence, risk factors and management. Int J Surg 16:88–93. doi:10.1016/j.ijsu.2015.02.020
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Funding
No funding was received for this study.
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval and Informed consent
The authors' ethics committee did not require specific authorization for obtaining and processing patient data in an observational retrospective study.
Rights and permissions
About this article
Cite this article
Mignot, A., Ayav, A., Quillot, D. et al. Extensive lymph node dissection during pancreaticoduodenectomy: a risk factor for hepatic steatosis?. Abdom Radiol 42, 1880–1887 (2017). https://doi.org/10.1007/s00261-017-1087-6
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00261-017-1087-6