Comparative Clinical Pathology

, Volume 28, Issue 4, pp 1031–1036 | Cite as

Spilt bile and gallstones effect during laparoscopic cholecystectomy: an experimental study for adhesion formation

  • Sedigheh Tahmasebi
  • Shahram Jamshidi
  • Nader Tanideh
  • Mohammad Yasin KaramiEmail author
Original Article


Laparoscopic cholecystectomy (LC) is recognized as the standard treatment for symptomatic gallstone disease. In comparison with open techniques, LC results in a higher rate of iatrogenic biliary tract damage and spillage of bile and stones. The present study was designed to compare intraperitoneal adhesion formation following LC due to the bile and stone spillage. In this randomized experimental study, 15 dogs were randomly allocated to three groups. Each group contained five dogs. The control group underwent LC, while in the group of bile and stone spillage (BS), 5 cc of a mixture of dog bile and a sterile ground human gallstone was placed in the bed of the gallbladder following LC. The bile spillage (B) group underwent LC, followed by adding 5 cc of the bile in the bed of the gallbladder. Postsurgical adhesion formation was measured, using Nair and Zühlke classifications for inflammation, fibrosis, and neovascularization. Adhesion formation was noted in one dog from the control and B groups, whereas all animals in group 2 were found to develop high-grade adhesion. Bile cultures were negative for the control group and group B with adhesion. Based on the findings, bile spillage, as well as gallbladder stone spillage, is related to a significant increase in adhesion formation after LC. Therefore, it is necessary to avoid the bile and stone spillage.


Laparoscopic Cholecystectomy Adhesion Stone Bile 



We express our gratitude to Shiraz University of Medical Sciences, as well as the Center for Clinical Research Development of Nemazee Hospital. We also thank Dr. Nasrin Shokrpour for her editorial assistance. This study was extracted from a thesis by Dr. Shahram Jamshidi.

Funding information

This study was funded by Shiraz University of Medical Sciences (No. 90-02-012-2352).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. The ethics committee of Shiraz University of Medical Sciences approved the study protocols (IR.SUMS.REC.1390.2352).


  1. Agalar F, Sayek I, Agalar C, Cakmakci M, Hayran M, Kavuklu B (1997) Factors that may increase morbidity in a model of intra-abdominal contamination caused by gallstones lost in the peritoneal cavity. Eur J Surg 163:909–914PubMedGoogle Scholar
  2. Aytekin FO, Tekin K, Kabay B, Erdem E, Erbis H, Ozden A (2004) Role of a hyaluronic-acid derivative in preventing surgical adhesions and abscesses related to dropped bile and gallstones in an experimental model. Am J Surg 188:288–293CrossRefPubMedGoogle Scholar
  3. Behar J (2013) Physiology and pathophysiology of the biliary tract: the gallbladder and sphincter of Oddi—a review. ISRN Physiol 2013Google Scholar
  4. Bernhoft R, Pellegrini C, Broderick W, Way L (1983) Pigment sludge and stone formation in the acutely ligated dog gallbladder. Gastroenterology 85:1166–1171PubMedGoogle Scholar
  5. Csikesz NG, Singla A, Murphy MM, Tseng JF, Shah SA (2010) Surgeon volume metrics in laparoscopic cholecystectomy. Dig Dis Sci 55:2398–2405CrossRefPubMedGoogle Scholar
  6. Diez J, Arozamena C, Ferraina P, Franci J, Ferreres A, Lardies J, Gutierrez V (1996) Relation between postoperative infections and gallbladder bile leakage during laparoscopic cholecystectomies. Surg Endosc 10:529–532CrossRefPubMedGoogle Scholar
  7. Helme S, Samdani T, Sinha P (2009) Complications of spilled gallstones following laparoscopic cholecystectomy: a case report and literature overview. J Med Case Rep 3:8626CrossRefPubMedPubMedCentralGoogle Scholar
  8. Jaffey J et al (2018) Gallbladder mucocele: variables associated with outcome and the utility of ultrasonography to identify gallbladder rupture in 219 dogs (2007–2016). J Vet Intern Med 32:195–200CrossRefPubMedGoogle Scholar
  9. Johansson M, Thune A, Nelvin L, Stiernstam M, Westman B, Lundell L (2005) Randomized clinical trial of open versus laparoscopic cholecystectomy in the treatment of acute cholecystitis. Br J Surg 92:44–49CrossRefPubMedGoogle Scholar
  10. Johnston S, O’Malley K, McEntee G, Grace P, Smyth E, Bouchier-Hayes D (1994) The need to retrieve the dropped stone during laparoscopic cholecystectomy. Am J Surg 167:608–610CrossRefPubMedGoogle Scholar
  11. Khan MH, Howard TJ, Fogel EL, Sherman S, McHenry L, Watkins JL, Canal DF, Lehman GA (2007) Frequency of biliary complications after laparoscopic cholecystectomy detected by ERCP: experience at a large tertiary referral center. Gastrointest Endosc 65:247–252CrossRefPubMedGoogle Scholar
  12. Kim B-S, Joo S-H, Kim H-C (2016) Spilled gallstones mimicking a retroperitoneal sarcoma following laparoscopic cholecystectomy. World J Gastroenterol 22:4421–4426CrossRefPubMedPubMedCentralGoogle Scholar
  13. Mayhew PD, Mehler SJ, Radhakrishnan A (2008) Laparoscopic cholecystectomy for management of uncomplicated gall bladder mucocele in six dogs. Vet Surg 37:625–630CrossRefPubMedGoogle Scholar
  14. Nair SK, Bhat IK, Aurora AL (1974) Role of proteolytic enzyme in the prevention of postoperative intraperitoneal adhesions. Arch Surg 108:849–853CrossRefPubMedGoogle Scholar
  15. Sathesh-Kumar T, Saklani A, Vinayagam R, Blackett R (2004) Spilled gall stones during laparoscopic cholecystectomy: a review of the literature. Postgrad Med J 80:77–79CrossRefPubMedPubMedCentralGoogle Scholar
  16. Schnüriger B, Barmparas G, Branco BC, Lustenberger T, Inaba K, Demetriades D (2011) Prevention of postoperative peritoneal adhesions: a review of the literature. Am J Surg 201:111–121CrossRefPubMedGoogle Scholar
  17. Scott J, Singh A, Mayhew PD, Brad Case J, Runge JJ, Gatineau M, Kilkenny J (2016) Perioperative complications and outcome of laparoscopic cholecystectomy in 20 dogs. Vet Surg 45:O49–O59CrossRefPubMedGoogle Scholar
  18. Soybir G, Köksoy F, Polat C, Özşeker A, Yalçln O, Aker Y, Topuzlu C (1997) The effects of sterile or infected bile and dropped gallstones in abdominal adhesions and abscess formation. Surg Endosc 11:711–713CrossRefPubMedGoogle Scholar
  19. Vollmer CM, Callery MP (2007) Biliary injury following laparoscopic cholecystectomy: why still a problem? Gastroenterology 133:1039–1041CrossRefPubMedGoogle Scholar
  20. Wiesen SM, Unger SW, Barkin JS, Edelman D, Scott J, Unger H (1993) Laparoscopic cholecystectomy: the procedure of choice for acute cholecystitis. Am J Gastroenterol 88:334–337PubMedGoogle Scholar
  21. Willis R, Lawson W, Hoare E, Kingston R, Sykes P (1984) Are bile bacteria relevant to septic complications following biliary surgery? Br J Surg 71:845–849CrossRefPubMedGoogle Scholar
  22. Woodfield J, Rodgers M, Windsor J (2004) Peritoneal gallstones following laparoscopic cholecystectomy. Surg Endosc 18:1200–1207CrossRefPubMedGoogle Scholar
  23. Yamashita Y, Takada T, Kawarada Y, Nimura Y, Hirota M, Miura F, Mayumi T, Yoshida M, Strasberg S, Pitt HA, de Santibanes E, Belghiti J, Büchler MW, Gouma DJ, Fan ST, Hilvano SC, Lau JWY, Kim SW, Belli G, Windsor JA, Liau KH, Sachakul V (2007) Surgical treatment of patients with acute cholecystitis: Tokyo Guidelines. J Hepato-Biliary-Pancreat Surg 14:91–97CrossRefGoogle Scholar
  24. Yerdel MA et al (1997) The fate of intraperitoneally retained gallstones with different morphologic and microbiologic characteristics: an experimental study. J Laparoendosc Adv Surg Tech A 7:87–94CrossRefPubMedGoogle Scholar
  25. Zekavat O, Amanat A, Karami M, Paydar S, Gramizadeh B, Zareian-Jahromi M (2016) Wound healing studies using Punica granatum Peel: an animal experimental study. Adv Skin Wound Care 29:217–225CrossRefPubMedGoogle Scholar
  26. Zorluoğlu A, Özgüç H, Yilmazlar T, Güney N (1997) Is it necessary to retrieve dropped gallstones during laparoscopic cholecystectomy? Surg Endosc 11:64–66CrossRefPubMedGoogle Scholar
  27. Zühlke H, Lorenz E, Straub E-M, Savvas V (1990) Pathophysiologie und klassifikation von adhäsionen. In: Deutsche Gesellschaft für Chirurgie. Springer, Berlin, pp 1009–1016CrossRefGoogle Scholar

Copyright information

© Springer-Verlag London Ltd., part of Springer Nature 2019

Authors and Affiliations

  1. 1.Breast Diseases Research Center, Department of Surgery, School of MedicineShiraz University of Medical SciencesShirazIran
  2. 2.Department of Plastic and Reconstructive Surgery, School of MedicineIran University of Medical SciencesTehranIran
  3. 3.Stem Cell and Transgenic Technology Research Center, School of MedicineShiraz University of Medical SciencesShirazIran

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