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Extensive lymph node dissection during pancreaticoduodenectomy: a risk factor for hepatic steatosis?

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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.

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References

  1. Lundstedt C, Andrén-Sandberg A (1991) CT of liver steatosis after subtotal pancreatectomy. Acta Radiol 32:30–33. doi:10.3109/02841859109177502

    Article  CAS  PubMed  Google Scholar 

  2. 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

    Article  PubMed  PubMed Central  Google Scholar 

  3. 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

    Article  PubMed  PubMed Central  Google Scholar 

  4. 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

    Article  CAS  PubMed  Google Scholar 

  5. 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

    Article  PubMed  Google Scholar 

  6. 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

    PubMed  Google Scholar 

  7. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. 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

    Article  Google Scholar 

  9. 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

    CAS  PubMed  Google Scholar 

  10. 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

    Article  PubMed  Google Scholar 

  11. 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

    Article  CAS  PubMed  Google Scholar 

  12. 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

    Article  CAS  PubMed  Google Scholar 

  13. 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

    Article  PubMed  Google Scholar 

  14. 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

    Article  CAS  PubMed  Google Scholar 

  15. 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

  16. 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

    Article  PubMed  Google Scholar 

  17. 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

    Article  CAS  PubMed  Google Scholar 

  18. 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

    Article  PubMed  PubMed Central  Google Scholar 

  19. 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

    Article  CAS  PubMed  Google Scholar 

  20. 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

    Article  PubMed  Google Scholar 

  21. 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

    CAS  PubMed  Google Scholar 

  22. 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

    Article  CAS  Google Scholar 

  23. 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

    Article  CAS  PubMed  Google Scholar 

  24. 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

    CAS  PubMed  Google Scholar 

  25. Berry AJ (2013) Pancreatic surgery: indications, complications, and implications for nutrition intervention. Nutr Clin Pract 28:330–357. doi:10.1177/0884533612470845

    Article  PubMed  Google Scholar 

  26. Buscemi S, Damiano G, Palumbo VD, et al. (2015) Enteral nutrition in pancreaticoduodenectomy: a literature review. Nutrients 7:3154–3165. doi:10.3390/nu7053154

    Article  PubMed  PubMed Central  Google Scholar 

  27. 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

    Article  PubMed  Google Scholar 

  28. 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

    Article  CAS  PubMed  Google Scholar 

  29. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. 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

    Article  CAS  PubMed  Google Scholar 

  31. 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

    Article  Google Scholar 

  32. 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

    PubMed  Google Scholar 

  33. 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

    Google Scholar 

  34. 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

    Article  CAS  PubMed  Google Scholar 

  35. 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

    Article  Google Scholar 

  36. 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

    Article  PubMed  Google Scholar 

  37. 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

    Article  CAS  PubMed  Google Scholar 

  38. Slezak LA, Andersen DK (2001) Pancreatic resection: effects on glucose metabolism. World J Surg 25:452–460. doi:10.1007/s002680020337

    Article  CAS  PubMed  Google Scholar 

  39. 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

    Google Scholar 

  40. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. 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

    Article  PubMed  Google Scholar 

  42. 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

    Article  PubMed  Google Scholar 

  43. 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

    Article  PubMed  Google Scholar 

  44. Iqbal J, Hussain MM (2009) Intestinal lipid absorption. Am J Physiol Endocrinol Metab 296:E1183–E1194. doi:10.1152/ajpendo.90899.2008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. 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

    Article  CAS  PubMed  Google Scholar 

  46. Bastard JP, Bruno F (2012) Physiologie et physiopatholigie du tissus adipeux. Paris: Springer

    Google Scholar 

  47. Parks EJ, Hellerstein MK (2000) Carbohydrate-induced hypertriacylglycerolemia: historical perspective and review of biological mechanisms. Am J Clin Nutr 71:412–433

    CAS  PubMed  Google Scholar 

  48. 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

    Article  CAS  PubMed  Google Scholar 

  49. Sato T (ed) (1997) Color atlas of applied anatomy of lymphatics anatomical basis for cancer operation. Tokyo: Nankoudou

    Google Scholar 

  50. 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

    Article  Google Scholar 

  51. 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

    Article  PubMed  Google Scholar 

  52. 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

    Article  CAS  PubMed  Google Scholar 

  53. 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

    Article  PubMed  Google Scholar 

  54. 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

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Radiology, CHU Nancy Brabois, Vandœuvre-lès-Nancy, 54500, France

    A. Mignot, I. Petit & V. Laurent

  2. Department of Hepato-Pancreato-Biliary Surgery, CHU Nancy Brabois, Vandœuvre-lès-Nancy, 54500, France

    A. Ayav

  3. Department of Diabetes and Nutrition, CHU Nancy Brabois, Vandœuvre-lès-Nancy, 54500, France

    D. Quillot & A. Malgras

  4. Department of Cardiovascular Medicine, CHU Nancy Brabois, Vandœuvre-lès-Nancy, 54500, France

    S. Zuily

  5. Department of PARC, ESPRI-BIOBASE, Pôle S, CHU Nancy Brabois, Vandœuvre-lès-Nancy, 54500, France

    P. L. Nguyen-Thi

  6. 6 rue Jean XXIII Résidence Haut Rivage, 54130, Saint Max, France

    A. Mignot

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  1. A. Mignot
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  2. A. Ayav
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Correspondence to A. Mignot.

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The authors declare that they have no conflict of interest.

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The authors' ethics committee did not require specific authorization for obtaining and processing patient data in an observational retrospective study.

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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

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