Skip to main content
SpringerLink
Log in

Preoperative Bile Replacement Improves Immune Function for Jaundiced Patients Treated with External Biliary Drainage

  • Original Article
  • Published:
Journal of Gastrointestinal Surgery Aims and scope

Abstract

Background

Although preoperative biliary drainage in jaundiced patients is controversial, external biliary drainage (EBD) is beneficial for infection control in patients with biliary cancers. When EBD is performed, additional bile replacement (BR) has the benefit of improving impaired intestinal barrier function, but the detailed mechanism remains unknown. We examined the effect of bile replacement on immune functions over the duration of BR in jaundiced patients.

Methods

Fifteen patients were enrolled into this prospective study. BR was started soon after the total serum bilirubin concentration reached 5.0 mg/dl and was continued for 14 days. Drained bile was given two times orally (2 × 100 ml/day). Concanavalin A (Con A)- and phytohemagglutinin (PHA)-stimulated lymphocyte proliferation and serum diamine oxidase (DAO) activity were measured before starting and during BR. Twenty patients with EBD and no BR were analyzed as a control group.

Results

Serum liver enzymes, prothrombin time–international normalized ratio (PT-INR), and responses to Con A and PHA gradually improved over the 14 days of BR, but percentages of lymphocytes and DAO levels did not. PT-INR, and Con A and PHA responses did not improve during EBD in the control group. PT-INR significantly decreased in patients with a greater fraction of their drained bile replaced.

Conclusions

Our results indicate that preoperative BR using as large a quantity of bile as possible is useful for improving blood coagulability and cellular immunity in patients with EBD.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Garcea G, Chee W, Ong SL, Maddern GJ. Preoperative biliary drainage for distal obstruction: the case against revisited. Pancreas 2010;39:119–26.

    Article  PubMed  Google Scholar 

  2. Iacono C, Ruzzenente A, Campagnaro T, Bortolasi L, Valdegamberi A, Guglielmi A. Role of preoperative biliary drainage in jaundiced patients who are candidates for pancreatoduodenectomy or hepatic resection: highlights and drawbacks. Ann Surgery 2013;257:191–204.

    Article  Google Scholar 

  3. Smith RC, Pooley M, George CR, Faithful GR. Preoperative percutaneous transhepatic internal drainage in obstructive jaundice: a randomized, controlled trial examining renal function. Surgery 1985;97:641–8.

    CAS  PubMed  Google Scholar 

  4. Denning DA, Ellison EC, Carey LC. Preoperative percutaneous transhepatic biliary decompression lowers operative morbidity in patients with obstructive jaundice. Am J Surg 1981;141:61–5.

    Article  CAS  PubMed  Google Scholar 

  5. Srivastava S, Sikora SS, Kumar A, Saxena R, Kapoor VK. Outcome following pancreaticoduodenectomy in patients undergoing preoperative biliary drainage. Dig Surg 2001;18:381–7.

    Article  CAS  PubMed  Google Scholar 

  6. Sewnath ME, Karsten TM, Prins MH, Rauws EJ, Obertop H, Gouma DJ. A meta-analysis on the efficacy of preoperative biliary drainage for tumors causing obstructive jaundice. Ann Surg 2002;236:17–27.

    Article  PubMed Central  PubMed  Google Scholar 

  7. van der Gaag NA, Rauws EA, van Eijck CH, Bruno MJ, van der Harst E, Kubben FJ, Gerritsen JJ, Greve JW, Gerhards MF, de Hingh IH, Klinkenbijl JH, Nio CY, de Castro SM, Busch OR, van Gulik TM, Bossuyt PM, Gouma DJ. Preoperative biliary drainage for cancer of the head of the pancreas. N Engl J Med 2010;362:129–37.

    Article  PubMed  Google Scholar 

  8. Sugiura T, Uesaka K, Ohmagari N, Kanemoto H, Mizuno T. Risk factor of surgical site infection after pancreaticoduodenectomy. World J Surg 2012;36:2888–94.

    Article  PubMed  Google Scholar 

  9. Nagino M, Takada T, Miyazaki M, Miyakawa S, Tsukada K, Kondo S, Furuse J, Saito H, Tsuyuguchi T, Yoshikawa T, Ohta T, Kimura F, Yoshitomi H, Nozawa S, Yoshida M, Wada K, Amano H, Miura F. Preoperative biliary drainage for biliary tract and ampullary carcinomas. J Hepatobiliary Pancreat Surg 2008;15:25–30.

    Article  PubMed Central  PubMed  Google Scholar 

  10. Rerknimitr R, Attasaranya S, Kladchareon N, Mahachai V, Kullavanijaya P. Feasibility and complications of endoscopic biliary drainage in patients with malignant biliary obstruction at King Chulalongkorn Memorial Hospital. J Med Assoc Thai 2002;85 Suppl 1:S48-53.

    PubMed  Google Scholar 

  11. Kawakami H, Kuwatani M, Onodera M, Haba S, Eto K, Ehira N, Yamato H, Kudo T, Tanaka E, Hirano S, Kondo S, Asaka M. Endoscopic nasobiliary drainage is the most suitable preoperative biliary drainage method in the management of patients with hilar cholangiocarcinoma. J Gastroenterol 2011;46:242–8.

    Article  PubMed  Google Scholar 

  12. Seyama Y, Makuuchi M. Current surgical treatment for bile duct cancer. World J Gastroenterol 2007;13:1505–15.

    Article  PubMed Central  PubMed  Google Scholar 

  13. Nimura Y. Preoperative biliary drainage before resection for cholangiocarcinoma (Pro). HPB (Oxford) 2008;10:130–3.

    Article  CAS  Google Scholar 

  14. Sano T, Ajiki T, Takeyama Y, Kuroda Y. Internal biliary drainage improves decreased number of gut mucosal T lymphocytes and MAdCAM-1 expression in jaundiced rats. Surgery 2004;136:693–9.

    Article  PubMed  Google Scholar 

  15. Matsumoto T, Ajiki T, Kajiwara E, Mita Y, Fujita T, Morimoto H, Miyazawa M, Ku Y. Decreased expression of intestinal chemokine TECK/CCL25 in experimental obstructive jaundice and its reversal following internal biliary drainage. J Gastroenterol 2008;43:390–6.

    Article  CAS  PubMed  Google Scholar 

  16. Saiki S, Chijiiwa K, Komura M, Yamaguchi K, Kuroki S, Tanaka M. Preoperative internal biliary drainage is superior to external biliary drainage in liver regeneration and function after hepatectomy in obstructive jaundiced rats. Ann Surg 1999;230:655–62.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  17. Suzuki H, Iyomasa S, Nimura Y, Yoshida S. Internal biliary drainage, unlike external drainage, does not suppress the regeneration of cholestatic rat liver after partial hepatectomy. Hepatology 1994;20:1318–22.

    Article  CAS  PubMed  Google Scholar 

  18. Kamiya S, Nagino M, Kanazawa H, Komatsu S, Mayumi T, Takagi K, Asahara T, Nomoto K, Tanaka R, Nimura Y. The value of bile replacement during external biliary drainage: an analysis of intestinal permeability, integrity, and microflora. Ann Surg 2004;239:510–7.

    Article  PubMed Central  PubMed  Google Scholar 

  19. Suzuki D, Furukawa K, Kimura F, Shimizu H, Yoshidome H, Ohtsuka M, Kato A, Yoshitomi H, Miyazaki M. Effects of perioperative immunonutrition on cell-mediated immunity, T helper type 1 (Th1)/Th2 differentiation, and Th17 response after pancreaticoduodenectomy. Surgery 2010;148:573–81.

    Article  PubMed  Google Scholar 

  20. Takagi K, Nakao M, Ogura Y, Nabeshima T, Kunii A. Sensitive colorimetric assay of serum diamine oxidase. Clin Chim Acta 1994;226:67–75.

    Article  CAS  PubMed  Google Scholar 

  21. Tanaka Y, Mizote H, Asakawa T, Kobayashi H, Otani M, Tanikawa K, Nakamizo H, Kawaguchi C, Asagiri K, Akiyoshi K, Hikida S, Nakamura T. Clinical significance of plasma diamine oxidase activity in pediatric patients: influence of nutritional therapy and chemotherapy. Kurume Med J 2003;50:131–7.

    Article  CAS  PubMed  Google Scholar 

  22. Hamada Y, Shinohara Y, Yano M, Yamamoto M, Yoshio M, Satake K, Toda A, Hirai M, Usami M. Effect of the menstrual cycle on serum diamine oxidase levels in healthy women. Clin Biochem 2013;46:99–102

    Article  CAS  PubMed  Google Scholar 

  23. Kiriyama S, Takada T, Strasberg SM, Solomkin JS, Mayumi T, Pitt HA, Gouma DJ, Garden OJ, Büchler MW, Yokoe M, Kimura Y, Tsuyuguchi T, Itoi T, Yoshida M, Miura F, Yamashita Y, Okamoto K, Gabata T, Hata J, Higuchi R, Windsor JA, Bornman PC, Fan ST, Singh H, de Santibanes E, Gomi H, Kusachi S, Murata A, Chen XP, Jagannath P, Lee S, Padbury R, Chen MF, Dervenis C, Chan AC, Supe AN, Liau KH, Kim MH, Kim SW; Tokyo Guidelines Revision Committee. TG13 guidelines for diagnosis and severity grading of acute cholangitis (with videos). J Hepatobiliary Pancreat Sci 2013;20:24–34.

    Article  PubMed  Google Scholar 

  24. Thompson RL, Hoper M, Diamond T, Rowlands BJ. Development and reversibility of T lymphocyte dysfunction in experimental obstructive jaundice. Br J Surg 1990;77:1229–32.

    Article  CAS  PubMed  Google Scholar 

  25. Dwyer JM, Johnson C. The use of concanavalin A to study the immunoregulation of human T cells. Clinical and experimental immunology 1981;46:237–49.

    CAS  PubMed Central  PubMed  Google Scholar 

  26. Confer BD, Lopez R, Zein NN. CD4+ T-cell function and the risk for developing spontaneous bacterial peritonitis in patients with cirrhosis. J Clin Gastroenterol 2013;47:807–13.

    Article  CAS  PubMed  Google Scholar 

  27. Christou NV, Tellado-Rodriguez J, Chartrand L, Giannas B, Kapadia B, Meakins J, Rode H, Gordon J. Estimating mortality risk in preoperative patients using immunologic, nutritional, and acute-phase response variables. Ann Surg 1989;210:69–77.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  28. Fukuoka K, Ajiki T, Miyazawa M, Takeyama Y, Onoyama H, Kuroda Y. Changes in the number of gut mucosal T-lymphocytes and macrophages in patients treated by external biliary drainage. Eur J Surg 2001;167:684–8.

    Article  CAS  PubMed  Google Scholar 

  29. Aida T, Furukawa K, Suzuki D, Shimizu H, Yoshidome H, Ohtsuka M, Kato A, Yoshitomi H, Miyazaki M. Preoperative immunonutrition decreases postoperative complications by modulating prostaglandin E2 production and T-cell differentiation in patients undergoing pancreatoduodenectomy. Surgery 2014;155:124–33.

    Article  PubMed  Google Scholar 

  30. Schwartz SI. Principles of surgery. McGraw-Hill, Health Professions Division, 1999.

  31. Bemelmans MH, Gouma DJ, Greve JW, Buurman WA. Cytokines tumor necrosis factor and interleukin-6 in experimental biliary obstruction in mice. Hepatology 1992;15:1132–6.

    Article  CAS  PubMed  Google Scholar 

  32. Hirazawa K, Hazama S, Oka M. Depressed cytotoxic activity of hepatic nonparenchymal cells in rats with obstructive jaundice. Surgery 1999;126:900–7.

    Article  CAS  PubMed  Google Scholar 

  33. Parks RW, Clements DB, Smye MG, Pope C, Rowlands BJ, Diamond T. Intestinal barrier dysfunction in clinical and experimental obstructive jaundice and its reversal by internal biliary drainage. Br J Surg 1996;83:1345–9.

    Article  CAS  PubMed  Google Scholar 

  34. Shoda J, Kano M, Oda K, Kamiya J, Nimura Y, Suzuki H, Sugiyama Y, Miyazaki H, Todoroki T, Stengelin S, Kramer W, Matsuzaki Y, Tanaka N. The expression levels of plasma membrane transporters in the cholestatic liver of patients undergoing biliary drainage and their association with the impairment of biliary secretory function. Am J Gastroenterol 2001;96:3368–78.

    Article  CAS  PubMed  Google Scholar 

  35. Yamada T, Arai T, Nagino M, Oda K, Shoda J, Suzuki H, Sugiyama Y, Nimura Y. Impaired expression of hepatic multidrug resistance protein 2 is associated with posthepatectomy hyperbilirubinemia in patients with biliary cancer. Langenbeck’s Arc Surg 2005;390:421–9.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Hepato-Biliary-Pancreatic Surgery, Department of Surgery, Kobe University Graduate School of Medicine, 7-5-1 Kusunoki-cho, Chuo-ku, Kobe, 650-0017, Japan

    Yuko Yoshida, Tetsuo Ajiki, Kimihiko Ueno, Kenta Shinozaki, Sae Murakami, Taro Okazaki, Taku Matsumoto, Ippei Matsumoto, Takumi Fukumoto & Yonson Ku

  2. Division of Nutrition and Metabolism, Department of Biophysics, Kobe University Graduate School of Health Sciences, 7-10-2 Tomogaoka, Suma-ku, Kobe, 654-0102, Japan

    Makoto Usami

Authors
  1. Yuko Yoshida
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tetsuo Ajiki
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kimihiko Ueno
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kenta Shinozaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sae Murakami
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Taro Okazaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Taku Matsumoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ippei Matsumoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Takumi Fukumoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Makoto Usami
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Yonson Ku
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tetsuo Ajiki.

Additional information

No grant support was provided for this study.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yoshida, Y., Ajiki, T., Ueno, K. et al. Preoperative Bile Replacement Improves Immune Function for Jaundiced Patients Treated with External Biliary Drainage. J Gastrointest Surg 18, 2095–2104 (2014). https://doi.org/10.1007/s11605-014-2674-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11605-014-2674-2

Keywords

Search

Navigation