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 Table of Contents  
ORIGINAL ARTICLE
Year : 2018  |  Volume : 14  |  Issue : 7  |  Page : 1503-1508

Multifactorial analysis of biliary infection after percutaneous transhepatic biliary drainage treatment of malignant biliary obstruction


1 Department of Interventional Therapy, Tianjin Medical University Cancer Institute and Hospital, National Clinical Research Center for Cancer, Tianjin's Clinical Research Center for Cancer, Tianjin, China
2 Capital Medical University Cancer Center, Capital Medicine University, Beijing Shijitan Hospital, Beijing, China

Date of Web Publication19-Dec-2018

Correspondence Address:
Haipeng Yu
Department of Interventional Therapy, Tianjin Medical University Cancer Institute and Hospital, National Clinical Research Center for Cancer, Tianjin's Clinical Research Center for Cancer, Tianjin 300060
China
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jcrt.JCRT_256_18

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 > Abstract 


Background: The symptoms of patients with malignant biliary obstruction (MBO) could be effectively alleviated with percutaneous transhepatic biliary drainage (PTBD). Postoperative infections were considered as challenging issues for clinicians. In this study, the risk factors of biliary infection in patients after PTBD were analyzed.
Methods: From July 2003 to September 2010, 694 patients with MBO received PTBD treatment. Bile specimens were also collected during PTBD. All relevant information and results were collected, including gender, age, obstruction time, types of primary tumor, sites of obstruction, drainage style, tumor stage, hemoglobin, phenotype of peripheral blood monocyte (Treg), total bilirubin, direct bilirubin, albumin, Child–Pugh score, and results of bile bacterial culture.
Results: For the 694 patients involved in this study, 485 were male and 209 were female, with a mean age of 62 years (ranged 38–78 years). For the bile culture, 57.1% patients (396/649) were negative and 42.9% patients showed positive (298/694), and then 342 strains of microorganism were identified. The risk factors of biliary system infection after PTBD included: age (χ2 = 4.621, P = 0.032), site of obstruction (χ2 = 17.450, P < 0.001), drainage style (χ2 = 14.452, P < 0.001), tumor stage (χ2 = 4.741, P = 0.029), hemoglobin (χ2 = 3.914, P = 0.048), Child–Pugh score (χ2 = 5.491, P = 0.019), phenotype of peripheral blood monocyte (Treg) (χ2 = 5.015, P = 0.025), and results of bile bacterial culture (χ2 = 65.381, P < 0.001). Multivariate analysis suggested that high-risk factors were drainage style, Child–Pugh score, and results of bile culture.
Conclusions: The risk factors of biliary infection after PTBD included: age, site of obstruction, drainage style, tumor stage, hemoglobin, Child–Pugh score, phenotype of peripheral blood monocyte (Treg), and results of bile culture. It was further concluded that drainage style, Child–Pugh score, and results of bile culture were independent risk factors.

Keywords: Biliary infection, malignant biliary obstruction, percutaneous transhepatic biliary drainage


How to cite this article:
Yu H, Yuanyuan S, Guo Z, Xing W, Si T, Guo X, Liu F. Multifactorial analysis of biliary infection after percutaneous transhepatic biliary drainage treatment of malignant biliary obstruction. J Can Res Ther 2018;14:1503-8

How to cite this URL:
Yu H, Yuanyuan S, Guo Z, Xing W, Si T, Guo X, Liu F. Multifactorial analysis of biliary infection after percutaneous transhepatic biliary drainage treatment of malignant biliary obstruction. J Can Res Ther [serial online] 2018 [cited 2019 Jan 24];14:1503-8. Available from: http://www.cancerjournal.net/text.asp?2018/14/7/1503/247717




 > Introduction Top


Malignant biliary obstruction (MBO) is a common complication of several malignancies, including cholangiocarcinoma, pancreatic cancer, gallbladder cancer, and gastric cancer. Moreover, it was a potential risk factor for poor outcomes of these patients.[1],[2] Many studies showed that surgery for severe biliary obstruction with concurrent infections led to higher perioperative mortality and morbidity, compared to that of without infections.[3] On the one hand, if there was obstruction combined with biliary infection, the quality of life could be seriously affected, as well as clinical outcomes.[4] The Tokyo Guidelines [5],[6] for the management of acute cholangitis and cholecystitis have been published in 2007, which have been widely applied for guiding therapy for biliary obstructions. However, the guidelines were primarily based on data obtained from studies on benign biliary obstruction.[7] Moreover, medical centers, at this moment in time, usually provided antimicrobial therapy on the basis of culture and susceptibility data.[8] On the other hand, there were a few published articles regarding risk factors of biliary infection after percutaneous transhepatic biliary drainage (PTBD) treatment of MBO or anti-infection strategies specific to MBO.[9],[10] It was a clinical challenge for oncologists. Therefore, investigations were performed on the causal relationship between preoperative factors and biliary infection, by multifactorial analysis using more objective clinical information and multiple statistical methods. The results would provide valuable evidence for judging high-risk factors associated with biliary infection after PTBD and antimicrobial therapy.

In our previously published study, PTBD was applied to collect bile samples from patients with MBO for culture and susceptibility testing.[11] Our research showed that the results of bile culture in MBO were different from those described in the Tokyo Guidelines and other studies on benign biliary obstruction. It indicated that a different antibacterial therapy should be applied.

On the previous basis, we would like to provide great and considerable information, which was required by managing biliary infection after MBO treated with PTBD therapy. For this purpose, a single-center, retrospective study was conducted to identify the risk factors of biliary infection after PTBD treatment for MBO.


 > Methods Top


Clinical data

A total of 694 patients with MBO included in this study received PTBD during July 2003 and September 2010. There were no additional inclusion criteria. This study was reviewed and approved by the Institutional Review Board of Tianjin Medical University Cancer Hospital and Institute. Informed consent was obtained from all individual participants included in the study. The registration identifier of this study was NCT01073614. In this study, all procedures received by the human participants were in accordance with the ethical standards of the institutional research committee, 1964 Helsinki declaration and its later amendments, or comparable ethical standards. All the patients in this study were diagnosed as malignant tumors by means of laboratory examination, medical imaging, and pathologic examination. The patients who had received antibacterial therapy 1 month before receiving PTBD were excluded in this analysis, as well as those diagnosed with infections in respiratory system or urinary system. Detailed information on the participants included in this study was collected from our institution. This information was obtained by computer searches, including age, sex, type of primary tumor, body temperature, white blood cell count, percentage of neutrophilic granulocytes, and results of bile cultures. A total of 694 patients were included in the study, 485 men and 209 women, with the mean age of 62 years (ranged 38–78 years) at the time of diagnosis. Of these 694 patients, there were 159 (22.9%) cases of cholangiocellular carcinoma, 131 (18.9%) cases of pancreatic carcinoma, 117 (16.9%) cases of hepatocellular carcinoma, 68 (9.8%) cases of gastric cancer, 49 (7.1%) cases of gallbladder carcinoma, and 170 (24.5%) cases of metastatic carcinomas.

Instrumentation and reagents

PTBD was performed with a Logic-5 ultrasound machine (General Electric, Wauke-sha, WI) and a digital fluoroscopy system with a digital subtraction function (DFP-2000A, Toshiba, Japan). Furthermore, bile culture and susceptibility testing were performed with a CO2 gas incubator (Sanyo, Japan), VITEK-2 compact microorganism-analysis system (bioMe´rieux, Marcy l'Etoile, France) and a BACTEC-9050 automatic hemoculture machine (Becton-Dickinson, Franklin Lakes, NJ). In addition, VITEK identification cards (bioMe´rieux, Marcy l'Etoile, France) were applied, including a VITEK-2 GN card for the identification of Gram-negative bacteria and a VITEK-2 GP card for Gram-positive bacteria. The applied susceptibility cards included AST-GN08 (22007) and AST-GN09 (22008) for Gram-negative bacteria and AST-P534 (22066) and AST-P535 (22067) for Gram-positive bacteria, respectively.

Procedure of percutaneous transhepatic biliary drainage and collection of bile specimens

All patients received PTBD after providing informed consent. The procedures were guided by ultrasound and digital fluoroscopy. The bile duct was punctured with a 22-gauge Chiba needle under local anesthesia, and the extension sheath was exchanged. A 20-ml bile sample was collected with a 10-ml syringe through the extension sheath. Two 10-ml bile samples were, respectively, collected into anaerobic and aerobic culture bottles (Becton Dickinson, San Jose, CA). Then, the bottles were taken to the laboratory department to avoid the damage of anaerobes. All patients received routine antibiotics therapy after the PTBD procedure.

Observatory parameters

To compare the impacts of different factors on biliary infection during the operation, all patients with MBO had received the examinations before PTBD, including routine blood test, liver function, blood clotting tests, and Treg (CD4+CD25+cells) detection. Information was collected as part of research parameters, including gender, age, time, types of primary tumors, site of obstruction, tumor stage, drainage ways, hemoglobin, phenotype of peripheral blood monocyte (Treg), total bilirubin, direct bilirubin, albumin, Child–-Pugh scores, and bile bacteria culture results.

Determination of postoperative infection of percutaneous transhepatic biliary drainage and parameter criteria

A clinical diagnosis of biliary infection with MBO was made based on both the physical signs and the laboratory results,[10] such as a body temperature higher than 38.5°C, a white blood cell counts >10 × 109/L, and a percentage of neutrophilic granulocytes in white blood cells of >70%. All these conditions were in accordance with the incidence of infections.

According to our research data and statistic processing requirements, primary tumors were divided into bile duct carcinomas, pancreatic carcinomas, hepatocellular carcinomas, and other tumors. According to Bismuth–Corlette classification, the obstruction site was classified into high obstruction, with the violation of forked or branched common hepatic duct and low obstruction, with the violation of common bile duct. Based on the initial treatment, drainage methods were divided into external drainage and internal and external drainage. According to TNM staging established by UICC, cancer staging was determined as I/II or III/IV stage. According to the results of bile bacterial culture from interventional treatment, it was deemed to be positive or negative. Following results were in accordance with the results of laboratory test: routine complete blood test, liver function, blood clotting tests, Treg (CD4+ CD25+ cells), within 1–3 days before PTBD, records of hemoglobin (≥90 g/L and <90 g/L), peripheral blood mononuclear cells with Treg phenotype (≥15% and <15%) and total bilirubin (≥300 μmol/L and <300 μmol/L), bilirubin (≥200 μmol/L and <200 μmol/L), and albumin (<35 g/L and >35 g/L), Child–Pugh score (<11 points and ≥11 points).

Statistical analysis

The statistical analysis was performed with SPSS for Windows software, version 11.5 (Chicago, IL, USA). Pearson's Chi-square test was applied for the performing the correlation analysis. A two-tailed Pearson's Chi-square test with P < 0.05 was considered statistically significant.


 > Results Top


For the 694 patients with MBO, the success rate of PTBD was 100%. Simple drainage was applied in 210 cases, while internal and external drainage was applied in 484 cases. The average of preoperative total bilirubin was 456.2 ± 103.7 μmol/L and the postoperative average of total bilirubin was 238.3 ± 132.2 μmol/L.

The incidence of percutaneous transhepatic biliary drainage complicated with biliary infection

Based on clinical symptoms, routine blood tests, and peripheral blood culture results, the number of patients with biliary infection was 156 and the rate was approximately 22.4% (156/694).

Univariate analysis for percutaneous transhepatic biliary drainage complicated with biliary infection

Univariate analysis was performed on gender, age, obstruction time (<2 week, and ≥ 2 week), original sent tumor species (bile duct carcinoma, pancreatic carcinoma, hepatocellular carcinoma, and other tumors), obstruction sites (high and low obstruction), drainage way (external and both internal and external drainage), tumor staging (I/II period and III/IV period), hemoglobin (≥90 g/L and <90 g/L), phenotype of peripheral blood monocyte with Treg (≥15% and <15%), total bilirubin (≥300 μmol/L and <300 μmol/L), bilirubin (≥200 μmol/L and <200 μmol/L), albumin (<35 g/L and >35 g/L), Child–Pugh score (<11 points and ≥11 points), and bile bacteria culture (positive or negative), where (P < 0.05) was considered to be statistically significant. Factors related to biliary infection were screened [Table 1]: Age (χ2 = 4.621, P = 0.032), obstruction parts (χ2 = 17.450, P < 0.001), drainage (χ2 = 14.452, P < 0.001), clinical stage (χ2 = 4.741, P = 0.029), hemoglobin (χ2 = 3.914, P = 0.048), hepatic Child–Pugh score (χ2 = 5.491, P = 0.019), phenotype of peripheral blood monocyte with Treg (χ2 = 5.015, P = 0.025), and bile bacteria culture-positive (χ2 = 65.381, P < 0.001), suggesting that these risk factors may be responsible for PTBD complicated with perioperative biliary infection.
Table 1: Univariate analysis for percutaneous transhepatic biliary drainage peri-surgical period complicated with biliary infection

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Multivariate analysis of percutaneous transhepatic biliary drainage complicated with biliary infection

Above-mentioned risk factors were analyzed with logistic regression model and multivariate variance analysis was performed [Table 2]. Results demonstrated that drainage, liver function, Child–Pugh score, and positive bacterial culture of bile were all independent risk factor for perioperative biliary infection after PTBD.
Table 2: Multivariate analysis for percutaneous transhepatic biliary drainage peri-surgical period complicated with biliary infection

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 > Discussion Top


The significance of identifying the preoperative risk factors related to percutaneous transhepatic biliary drainage complicated with biliary infection

MBO was one of the common complications in patients with advanced tumors,[12] with the main treatments of surgery, ERCP and PTBD.[13],[14] Since the majority of patients were in a late-stage of malignancy, the eligible time for radiotherapy has been missed. Thus, PTBD has become one of the leading and favorable strategies for the treatment of MBO.[12],[15] Biliary infection has been one of the most common and serious complications of MBO, during PTBD preoperatively.[16] The incidence of infection could be 30%~50% in MBO, directly affecting the clinical curative effects of PTBD, as well as the patient' quality of life. The infection has also been one of the main causes of death after 30 days of PTBD treatment.[12] For the clinical presentation, the main symptoms were characterized by fever, abdominal pain, and jaundice. In severe cases, blood pressure and neuronal functions would also be affected. The results of laboratory test showed increased white blood cells; diagnostic gold standard demonstrated pathogenic microorganisms in blood or bile culture. Clinically, there was not a bacterial culture and antibiotic sensitivity test highly specific to biliary infection symptoms, which was valuable for the laboratory test-based diagnosis. However, the results of laboratory tests were only available as early as 72 h after the collection of samples.

Therefore, a more accurate assessment of high-risk factors during PTBD perioperative period can be helpful for patients with MBO, which may prevent infection before surgery. A more accurate assessment of high-risk factors would also be considered significant in the scientific and rational applications of antibiotics, which could reduce perioperative infection-related deaths and other postoperative relevant serious complications. However, there was currently no systematic studies focusing on high-risk factors for perioperative infections of the biliary tract system in PTBD. This was one of the unresolved problems in the treatment of patients with MBO.

Analysis of risk factors related to biliary infection after percutaneous transhepatic biliary drainage

Our studies demonstrated that the high-risk factors related to biliary infection included old age, obstruction, III/IV stage tumors, internal and external drainage, Child–Pugh score ≥11 points, hemoglobin <90 g/L, albumin <30 g/L, peripheral blood mononuclear cells (Treg) in patients ≥15%, and positive bile bacterial culture. Studies have indicated that aging,[16] late stage,[17] generally poor conditions (anemia and hypoproteinemia),[18] and low immunity [19] were considered as high-risk factors, responsible for the infection of benign and malignant lesions in patients with malignant tumors. By multivariate analysis, drainage, liver Child–Pugh score (≥11 points), and a positive result for bile bacterial culture were independent risk factors contributing to postoperative biliary infection of PTBD.

Drainage

Major internal and external drainage may be through the duodenal ampulla, which would lead to the dysfunction of the sphincter of the ampulla. Therefore, bile duct drainage ways were considered as independent risk factors for MBO, complicated with biliary infection. Especially, when the obstruction was removed, the balance between gut pressure and bile duct pressure would be altered, and consequently, bacteria-containing intestinal contents would be moved into the bile duct in a retrograde manner. It became a predisposing factor for a biliary infection. Our previous study [11] had suggested that the vast majority of pathogenic bacteria in malignant biliary infection were gut bacteria. This was consistent with the findings in this study.

Child–Pugh score of liver function

In the practice of interventional therapy for liver tumors, Child–Pugh score of liver function has become an important indicator for preoperative evaluation of prognosis, confirmed by the large number of transcatheter arterial chemoembolization (TACE)-oriented evidence-based medical information.[20] However, there has been no uniform understanding of Child–Pugh score during PTBD treatment.[19] Our studies have shown that bilirubin (total bilirubin and direct bilirubin) was not correlated with biliary infection (P > 0.05). Furthermore, preoperative hepatic Child–Pugh score that directly represented the state of albumin was associated with other risk factors such as hemoglobin. Moreover, immune functions may be completed rely on various proteins synthesized by the liver. Therefore, to some extent, Child–Pugh score of liver function was representative of some infection-associated factors, such as albumin, hemoglobin, and immune functions. It would become more convenient indicator for evaluating risk factors of biliary infection before PTBD.

Bile bacterial culture

In terms of pathogenic detection, blood culture and bile bacterial culture were closely related to infection assessment. The blood culture was the gold standard for the diagnosis of infection; however, its detection rate was significantly lower than that of bile bacterial culture.[20],[21],[22] Thus, it would be feasible to collect bile specimens intraoperatively and perform bacterial culture to increase the diagnostic accuracy of infections. In addition, some scholars [23] suggested that bile samples should be collected in regular intervals, during the diagnosis and treatment. In 2010, the Society of Interventional Radiology Clinical Standards Committee published a set of guidelines for intervention operations.[24] Noncompulsory collection of bile samples for bacterial culture in PTBD has been mentioned in the operation guidance of PTBD. Experts in the field of interventional therapy not only considered the issues from intervention techniques aspects but also from clinical practices, involved in the developmental issues as a whole.

The prevention and therapeutic strategies for biliary infection after percutaneous transhepatic biliary drainage

According to our research results, specific strategies should be taken for patients with dangerous factors, especially for drainage way, Child–Pugh score of liver function, and positive bile bacterial culture. These specific strategies included the correction of hypoproteinemia or anemia, protection of liver function, improvement of cellular immune functions, collection of bile samples for bacterial culture, and necessary adjustment of current therapy strategy. The possibility of postoperative infection in patients with MBO could be alleviated with all these strategies. Patients should be fully assessed before surgery, focusing on the Child–Pugh score. If the Child–Pugh score was >11 points, strategies including liver protection, protein supplement, and symptomatic treatment should be preferentially taken to reduce the possibilities of biliary infection after operation. In addition, it should note that a simple elevated level of bilirubin could not be considered as a high-risk factor related to biliary infection. Therefore, the increase of Child–Pugh score caused by hyperbilirubinemia would not be considered as the preoperative risk factor for infection.

According to our results, drainage was an independent perioperative risk factor of PTBD complicated with biliary infection. It was also one of the most important adjustable interventions. Thus, the risk could be reduced through proper changes of drainage. As the results of this study showed, although age was not an independent risk factor, univariate analysis showed that age was associated with infections. Moreover, elderly patients were also characterized with atypical symptoms of infection, low rate of early diagnosis, severe infection, high mortality, and complications with other disorders. Consistent with their own central data, Clark et al.[22] proposed that age was associated with biliary tract microorganism infection and more special attentions should be paid to elderly patients >65 years old. Furthermore, based on our findings, external drainage may be selected to treat senior patients with low-level obstructive jaundice or other high-risk factors. Then, the risk of biliary infection after PTBD could be reduced. In addition to routine operation attentions, bile bacteria culture should also be involved as an important part of routine operation procedures. According to the results of bacterial culture, postoperative anti-infection therapy should be adjusted and developed. Moreover, if severe postoperative biliary infection occurred after PTBD, once obstruction was removed, active treatment specific for infection-associated factors should be performed in addition to conventional antibiotic treatment. These treatments included enough supplementation of albumin and hemoglobin as well as liver protection. This should be one of the main differences between benign lesions with biliary infection and MBO with biliary infection. In addition, the limitation of our study was that the data were just from our single center. It would be better if more data from other centers could be collected, analyzed, and compared.


 > Conclusion Top


In conclusion, the high-risk factors of biliary infection included senile (age ≥65 age), low obstruction, late-stage tumor (III/IV), high Child–Pugh score (≥11 points), low level of hemoglobin (<90 g/L) and albumin (<35 g/L), phenotype of peripheral blood monocyte (Treg ≥15%), and positive bile bacterial culture. Meanwhile, both internal and external drainage, Child–Pugh score of liver function (≥11 points), and positive bile bacterial culture were also independent preoperative risk factors for PTBD complicated with biliary infection. The prevention and therapeutic strategies should be developed and improved according to the related risk factors.

Acknowledgments

We thank all participants participated in this study.

Financial support and sponsorship

This research was partially supported by Key Project of Tianjin Science and Technology Support Program (15ZCZDSY00890), National Natural Science Foundation of China (81471761, 81501568), and National Science and Technology Support Program of China (2012BAI15B06). The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Conflicts of interest

There are no conflicts of interest.



 
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