Bacterial Translocation from the Biliary Tract to Blood and Lymph in Rats with Obstructive Jaundice

doi:10.1006/jsre.1997.5192

Journal of Surgical Research

Volume 74, Issue 2, 1 February 1998, Pages 125-130

https://doi.org/10.1006/jsre.1997.5192 Get rights and content

Abstract

Background.The disruption of the hepatocyte tight junctions observed in biliary obstruction suggests altered permeability of the blood–bile barrier. In this study the role of biliary obstruction and increased biliary pressure on the translocation of bacteria from biliary tract to bloodstream and lymphatic system were evaluated.Materials and Methods.Rats underwent distal bile duct ligation (BDL,n= 33) for two weeks or a sham celiotomy (n= 21). Seventeen of the 33 BDL rats underwent subsequent biliary decompression by a choledochojejunostomy (CJ). Two weeks after the final operation, a laparotomy was performed again and the CBD, the thoracic duct, and the caval vein were canulated. Next, a suspension containing 10⁸Escherichia coli/ml was retrogradely infused in the CBD for 5 min at 5 or 20 cm H₂O above the secretory biliary pressure.Results.A higher biliary infusion pressure resulted in a significant increase of cfuE.coliper milliliter of blood in all the three groups (Sham, BDL, CJ). BDL rats showed significantly more bacterial translocation to the bloodstream than the shams. After biliary decompression, translocation normalized to the control levels. At 5 cm H₂O infusion pressure only one lymph culture was positive (CJ group). At 20 cm H₂O overpressure, nine lymph cultures wereE.colipositive (P= 0.03). These were found mainly in groups with a nonobstructed bile duct (Sham and CJ 40% vs BDL 10%).Conclusion.Translocation of bacteria from biliary tract to bloodstream increased at higher intrabiliary pressures. Longstanding bile duct obstruction was an independent determinant for cholangiovenous reflux. Bacterial translocation to the lymphatic system did not parallel translocation to the bloodstream, although in the nonobstructed biliary tract, increased bacterial translocation to the lymphatic system was pressure related.

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However, the procedure itself can lead to translocation of bacteria or secreted endotoxin from the infected bile ducts into the bloodstream with subsequent bacteremia and septic shock [2]. The mechanism is thought to involve increased biliary pressure causing cholangiovenous reflux [3-5]. To prevent this complication, when performing ERCP in patients with cholangitis, it is recommended to use the wire-guided technique for cannulation, to aspirate bile during the procedure so as to decrease biliary pressure, to minimize the injection of contrast, and especially to avoid occlusion cholangiography [6].
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In short, the presence of bacteria in bile implies a carrier state, not an infection. Bacteremia in acute cholangitis is caused by a combination of colonized bile and increased bile duct pressure that favours the translocation of bacteria from the biliary tract to systemic circulation [18–20]. The dissemination of microbes and endotoxins via the blood stream activates a systemic inflammatory response and leads to septicemia and clinical features of cholangitis with chills and fever [21].
Bile is normally sterile, but the presence of organisms in the bile does not necessarily imply an active infection. We wonder what the significance of bile culture results on antibiotics choice in cholangitis with negative blood culture. The aim of this study was to compare organisms cultured from bile with those from blood in bacteremic biliary tract infection and to evaluate factors associated with concordance between blood and bile isolates.
Between 2000 and 2010, 266 positive blood cultures with concomitant bile culture in bacteremic biliary tract infection were identified. Follow-up bile specimens obtained after negative conversion of blood culture and clinical recovery from acute infection were collected for supplementary analysis.
Of the 266 events, 258 showed positive bile culture. Of the 258 bile samples, 80 yielded the same organisms with blood, 129 showed partial agreement and 49 yielded completely different organisms with blood. Only the number of organism was found to be independently associated with concordance. Of the 529 organisms isolated from bile, 227 were found in blood and gram-negative organisms showed higher rate of coincidence than gram-positive organisms. Of the 84 follow-up bile sample, 94% showed persistent positive culture and higher rate of antibiotics resistance than initial bile culture.
More than half of the organisms isolated from bile, especially gram-positive organisms, are not likely to be true pathogens. But single organism cultured from bile has clinical significance. Routine follow-up bile culture in patients showing clinical improvement is not necessary.
Restoration of hepatocytes function following decompression therapy in extrahepatic biliary obstructed patients: Metabolite profiling of bile by NMR
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Adequate palliation is desirable as prolonged obstruction causes jaundice, pruritis and progressive hepatocellular dysfunction with alteration in host defence system due to retention of bile [8,9]. This follows altered permeability of blood–bile barrier allowing regurgitation of biliary constituents into blood circulation and endotoxemia [10–15]. Biliary drainage via PTBD alleviates icterus, resolves infection, restores most of the changes of the liver parenchyma and recovery of tight junction of hepatocytes and immune function [5–7,16,17].
Prolonged biliary obstruction and infection cause retention of biliary constituents in liver followed by hepatocyte dysfunction. Decompression therapy is important for both management and prognostic reasons and restores hepatocyte function. Quantitative metabolite profiling of bile using NMR spectroscopy at the time of obstruction and serially following decompression therapy using percutaneous transhepatic biliary drainage (PTBD) from nineteen patients with extrahepatic malignant biliary obstruction are presented. Based on detailed history, clinical condition, total leucocyte counts (TLC) and microbiological cultures of bile, patients were classified in two groups depending upon absence or presence of cholangitis. Statistical analysis was performed for comparison within each group using Wilcoxan sign square rank test. TLC and liver function tests indicated a trend towards recovery following decompression by one week. While on day 0 biliary constituents were undetectable in both the groups of patients, they increased significantly following one week of drainage with better recovery in patients with cholangitis compared to without. Free amino acids’ signals were detected in all specimens starting from day 1 after decompression. This indicates disruption of blood–bile barrier during cholestasis and slow restoration of tight junction of hepatocytes following decompression leading to the appearance of biliary constituents in bile. Decompression therapy tends to restore biliary constituents with a prompt recovery in patients with cholangitis further supports such therapy for clinical management and outcome. To our knowledge this is the first report on the detection of amino acids in bile taken from common bile duct though they have been reported in hepatic bile.
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In most settings of acute cholangitis it is unclear exactly how bacteria enter an obstructed biliary. Some studies showed that the incidence of bacteremia or appearance of endotoxemia was related directly to the pressure within the biliary system [18–22]. Recent research has demonstrated that biliary obstruction is associated with increased intestinal permeability and disruption of intestinal integrity, which leads to an increased likelihood that bacteria enter the blood or lymphatic system [23–25].
The effect of immunonutrition on bacterial translocation, and intestinal villus atrophy in experimental obstructive jaundice
2003, Clinical Nutrition
Background & aims: Spontaneous bacterial infection and septicemia due to increased bacterial translocation (BT) in patients with obstructive jaundice result in significant morbidity and mortality. The present study evaluates the effects of enteral nutrition with immune enhancing feeds on BT and intestinal villus histopathology promoted by obstructive jaundice.
Methods: Fifty male Wistar-albino rats weighing 250–300 g were assigned into five equal groups of 10. Animals in Groups I, II, and III were fed with standard chow, those in Group IV were given glutamine 1 g/kg/day and the remaining 10 animals in Group V were fed with an arginine, ω-3 fatty acids, and RNA-supplemented enteral diet for (1 g/kg/day amino acid and 230 kcal/kg) 7 days preoperatively. Group I underwent sham operation and the remaining animals in all other groups underwent common bile duct ligation. After operation, Group I had standard chow, Groups II and IV had glutamine, Groups III and V had an arginine ω-3 fatty acids, and RNA-supplemented enteral diet for 7 days. All animals were sacrificed on the 8th postoperative day and evaluated both biochemically and histopathologically. Samples from blood, liver, mesenteric lymph nodes and spleen were cultured under aerobic conditions.
Results: Significantly less BT was observed in groups fed with an arginine, ω-3 fatty acids, and RNA-supplemented enteral diet or glutamine in pre-and postoperative periods as compared to others (P<0.001). Histologic evaluation also showed significant reduction in villus atrophy in these groups.
Conclusions: Enteral immunonutrition using glutamine or arginine, ω-3 fatty acids, and RNA-supplemented enteral diet during both pre-and postoperative periods seems to reduce BT and decrease atrophy of intestinal mucosal villi in rats with obstructive jaundice.
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: Paper presented at the 2nd World Congress of the IHPBA, Bologna, Italy, June 2–6, 1996.

: McSween, R. N. M.Anthony, P. P.Scheuer, P. J.

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Regular ArticleBacterial Translocation from the Biliary Tract to Blood and Lymph in Rats with Obstructive Jaundice

Abstract

Am. J. Surg.

J. Surg. Res.

Lancet

J. Pediatr. Surg.

Am. J. Surg.

The significance of biliary pressure in cholangitis

Arch. Surg.

Experimental studies on biliary regurgitation during cholangiography

Gastroenterology

Cholangiovenous reflux. An experimental study

Acta Chir. Scand.

Relationship of biliary pressure to cholangiovenous reflux during endoscopic retrograde ballon catheter cholangiography

Dig. Dis. Sci.

Cholestasis: extrahepatic obstruction and secondary biliary cirrhosis

Pathology of the Liver