Association Between Preoperative Muscle Mass and Intraoperative Bacterial Translocation in Patients Undergoing Hepatectomy, Pancreatoduodenectomy, and Esophagectomy

  • Kumiko Akashi
  • Yukihiro YokoyamaEmail author
  • Takashi Mizuno
  • Tetsuya Abe
  • Masahide Fukaya
  • Takashi Asahara
  • Masato Nagino
Translational Research and Biomarkers



This study investigated the correlation between the fecal profile and muscle mass, which has not been elucidated before.


This study included patients who underwent hepatectomy, pancreatoduodenectomy, or esophagectomy and had fecal samples collected preoperatively and mesenteric lymph nodes (MLNs) harvested intraoperatively to determine the fecal profile and presence of bacteria in the MLNs. Total psoas area (TPA) was measured at the third lumbar vertebra using preoperative computed tomography images. TPA was standardized by body surface area (BSA) using the following equation: standardized TPA (mm2/m2) (stTPA) = TPA (mm2)/BSA (m2). The fecal concentrations of representative microorganisms and organic acids also were measured.


A total of 127 patients undergoing hepatectomy (n = 48), pancreatoduodenectomy (n = 44), and esophagectomy (n = 35) were included. The fecal levels of predominant obligate anaerobes showed a positive correlation with stTPA, whereas that of pathogenic microorganisms showed a negative correlation with stTPA. The fecal concentrations of total short chain fatty acids (the sum of acetic acid, propionic acid, and butyric acid) also showed a positive correlation with stTPA. The stTPA was significantly lower in patients with positive microorganisms in the MLNs (patients with bacterial translocation) compared to those without microorganisms in the MLNs (p = 0.047).


This study was the first to demonstrate the association between muscle mass and the fecal profile, as well as their association with bacterial translocation.



The authors thank Eiji Nishigaki and Takashi Miyake, who dedicatedly collected the samples. The authors also thank Yukiko Kado and Akira Takahashi for their technical assistance in analyzing fecal and MLN samples.


The authors affirm that they have no financial or personal affiliations (including research funding) or other involvement with any commercial organization that has a direct financial interest in any matter included in this manuscript.

Supplementary material

10434_2019_7707_MOESM1_ESM.docx (13 kb)
Supplementary material 1 (DOCX 13 kb)


  1. 1.
    Kawai M, Kondo S, Yamaue H, et al. Predictive risk factors for clinically relevant pancreatic fistula analyzed in 1,239 patients with pancreaticoduodenectomy: multicenter data collection as a project study of pancreatic surgery by the Japanese Society of Hepato-Biliary-Pancreatic Surgery. J Hepatobiliary Pancreat Sci. 2011;18:601–8.CrossRefGoogle Scholar
  2. 2.
    Ebata T, Mizuno T, Yokoyama Y, et al. Surgical resection for Bismuth type IV perihilar cholangiocarcinoma. Br J Surg. 2018;105:829–38.CrossRefGoogle Scholar
  3. 3.
    Yokoyama Y, Mizuno T, Sugawara G, et al. Profile of preoperative fecal organic acids closely predicts the incidence of postoperative infectious complications after major hepatectomy with extrahepatic bile duct resection: importance of fecal acetic acid plus butyric acid minus lactic acid gap. Surgery. 2017;162:928–36.CrossRefGoogle Scholar
  4. 4.
    Yokoyama Y, Nishigaki E, Abe T, et al. Randomized clinical trial of the effect of perioperative synbiotics versus no synbiotics on bacterial translocation after oesophagectomy. Br J Surg. 2014;101:189–99.CrossRefGoogle Scholar
  5. 5.
    Sugawara G, Nagino M, Nishio H, et al. Perioperative synbiotic treatment to prevent postoperative infectious complications in biliary cancer surgery: a randomized controlled trial. Ann Surg. 2006;244:706–14.CrossRefGoogle Scholar
  6. 6.
    Kanazawa H, Nagino M, Kamiya S, et al. Synbiotics reduce postoperative infectious complications: a randomized controlled trial in biliary cancer patients undergoing hepatectomy. Langenbecks Arch Surg. 2005;390:104–13.CrossRefGoogle Scholar
  7. 7.
    Nishigaki E, Abe T, Yokoyama Y, et al. The detection of intraoperative bacterial translocation in the mesenteric lymph nodes is useful in predicting patients at high risk for postoperative infectious complications after esophagectomy. Ann Surg. 2014;259:477–84.CrossRefGoogle Scholar
  8. 8.
    Otsuji H, Yokoyama Y, Ebata T, et al. Preoperative sarcopenia negatively impacts postoperative outcomes following major hepatectomy with extrahepatic bile duct resection. World J Surg. 2015;39:1494–500.CrossRefGoogle Scholar
  9. 9.
    Peng P, Hyder O, Firoozmand A, et al. Impact of sarcopenia on outcomes following resection of pancreatic adenocarcinoma. J Gastrointest Surg. 2012;16:1478–86.CrossRefGoogle Scholar
  10. 10.
    Tamandl D, Paireder M, Asari R, et al. Markers of sarcopenia quantified by computed tomography predict adverse long-term outcome in patients with resected oesophageal or gastro-oesophageal junction cancer. Eur Radiol. 2016;26:1359–67.CrossRefGoogle Scholar
  11. 11.
    Hayashi K, Yokoyama Y, Nakajima H, et al. Preoperative 6-minute walk distance accurately predicts postoperative complications after operations for hepato-pancreato-biliary cancer. Surgery. 2017;161:525–32.CrossRefGoogle Scholar
  12. 12.
    Mizuno T, Yokoyama Y, Nishio H, et al. Intraoperative bacterial translocation detected by bacterium-specific ribosomal rna-targeted reverse-transcriptase polymerase chain reaction for the mesenteric lymph node strongly predicts postoperative infectious complications after major hepatectomy for biliary malignancies. Ann Surg. 2010;252:1013–9.CrossRefGoogle Scholar
  13. 13.
    Yokoyama Y, Miyake T, Kokuryo T, et al. Effect of perioperative synbiotic treatment on bacterial translocation and postoperative infectious complications after pancreatoduodenectomy. Dig Surg. 2016;33:220–9.CrossRefGoogle Scholar
  14. 14.
    Otsuji H, Yokoyama Y, Ebata T, et al. Surgery-related muscle loss and its association with postoperative complications after major hepatectomy with extrahepatic bile duct resection. World J Surg. 2017;41:498–507.CrossRefGoogle Scholar
  15. 15.
    Baumgartner RN, Koehler KM, Gallagher D, et al. Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol. 1998;147:755–63.CrossRefGoogle Scholar
  16. 16.
    Mourtzakis M, Prado CM, Lieffers JR, et al. A practical and precise approach to quantification of body composition in cancer patients using computed tomography images acquired during routine care. Appl Physiol Nutr Metab. 2008;33:997–1006.CrossRefGoogle Scholar
  17. 17.
    Du Bois D, Du Bois EF. A formula to estimate the approximate surface area if height and weight be known. 1916. Nutrition. 1989;5:303–11; discussion 312–3.Google Scholar
  18. 18.
    Matsuda K, Tsuji H, Asahara T, et al. Sensitive quantitative detection of commensal bacteria by rRNA-targeted reverse transcription-PCR. Appl Environ Microbiol. 2007;73:32–9.CrossRefGoogle Scholar
  19. 19.
    Matsuda K, Tsuji H, Asahara T, et al. Establishment of an analytical system for the human fecal microbiota, based on reverse transcription-quantitative PCR targeting of multicopy rRNA molecules. Appl Environ Microbiol. 2009;75:1961–9.CrossRefGoogle Scholar
  20. 20.
    Sakaguchi S, Saito M, Tsuji H, et al. Bacterial rRNA-targeted reverse transcription-PCR used to identify pathogens responsible for fever with neutropenia. J Clin Microbiol. 2010;48:1624–8.CrossRefGoogle Scholar
  21. 21.
    Sugawara G, Ebata T, Yokoyama Y, et al. The effect of preoperative biliary drainage on infectious complications after hepatobiliary resection with cholangiojejunostomy. Surgery. 2013;153:200–10.CrossRefGoogle Scholar
  22. 22.
    Asahara T, Takahashi A, Yuki N, et al. Protective effect of a synbiotic against multidrug-resistant Acinetobacter baumannii in a murine infection model. Antimicrob Agents Chemother. 2016;60:3041–50.CrossRefGoogle Scholar
  23. 23.
    Asaoka T, Miyamoto A, Maeda S, et al. Prognostic impact of preoperative NLR and CA19-9 in pancreatic cancer. Pancreatology. 2016;16:434–40.CrossRefGoogle Scholar
  24. 24.
    Han-Geurts IJ, Hop WC, Tran TC, Tilanus HW. Nutritional status as a risk factor in esophageal surgery. Dig Surg. 2006;23:159–63.CrossRefGoogle Scholar
  25. 25.
    Okamura Y, Ashida R, Ito T, et al. Preoperative neutrophil to lymphocyte ratio and prognostic nutritional index predict overall survival after hepatectomy for hepatocellular carcinoma. World J Surg. 2015;39:1501–9.CrossRefGoogle Scholar
  26. 26.
    Roy LB, Edwards PA, Barr LH. The value of nutritional assessment in the surgical patient. JPEN J Parenter Enteral Nutr. 1985;9:170–2.CrossRefGoogle Scholar
  27. 27.
    Bassi C, Dervenis C, Butturini G, et al. Postoperative pancreatic fistula: an international study group (ISGPF) definition. Surgery. 2005;138:8–13.CrossRefGoogle Scholar
  28. 28.
    Wente MN, Bassi C, Dervenis C, et al. Delayed gastric emptying (DGE) after pancreatic surgery: a suggested definition by the International Study Group of Pancreatic Surgery (ISGPS). Surgery. 2007;142:761–8.CrossRefGoogle Scholar
  29. 29.
    Rahbari NN, Garden OJ, Padbury R, et al. Posthepatectomy liver failure: a definition and grading by the International Study Group of Liver Surgery (ISGLS). Surgery. 2011;149:713–24.CrossRefGoogle Scholar
  30. 30.
    Koch M, Garden OJ, Padbury R, et al. Bile leakage after hepatobiliary and pancreatic surgery: a definition and grading of severity by the International Study Group of Liver Surgery. Surgery. 2011;149:680–8.CrossRefGoogle Scholar
  31. 31.
    Navarro MA, McClane BA, Uzal FA. Mechanisms of action and cell death associated with Clostridium perfringens toxins. Toxins (Basel). 2018;10.Google Scholar
  32. 32.
    Takehara M, Takagishi T, Seike S, et al. Clostridium perfringens alpha-toxin impairs innate immunity via inhibition of neutrophil differentiation. Sci Rep. 2016;6:28192.CrossRefGoogle Scholar
  33. 33.
    Nakajima H, Yokoyama Y, Inoue T, et al. Clinical benefit of preoperative exercise and nutritional therapy for patients undergoing hepato-pancreato-biliary surgeries for malignancy. Ann Surg Oncol. 2019;26:264–72.CrossRefGoogle Scholar

Copyright information

© Society of Surgical Oncology 2019

Authors and Affiliations

  • Kumiko Akashi
    • 1
  • Yukihiro Yokoyama
    • 1
    • 2
    Email author
  • Takashi Mizuno
    • 1
  • Tetsuya Abe
    • 3
  • Masahide Fukaya
    • 1
  • Takashi Asahara
    • 4
  • Masato Nagino
    • 1
  1. 1.Division of Surgical Oncology, Department of SurgeryNagoya University Graduate School of MedicineNagoyaJapan
  2. 2.Department of Perioperative MedicineNagoya University Graduate School of MedicineNagoyaJapan
  3. 3.Department of Gastroenterological SurgeryAichi Cancer CenterNagoyaJapan
  4. 4.Yakult Central InstituteTokyoJapan

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