|Year : 2021 | Volume
| Issue : 3 | Page : 726-732
Comparative analysis of bile culture and blood culture in patients with malignant biliary obstruction complicated with biliary infection
Chengli Wang1, Haipeng Yu1, Ji'an He2, Mei Li3, Lei Zhang1, Yan Xu1, Wei Gao1, Xueling Yang1, Xiuying Guo1, Zhi Guo1
1 Department of Intervention, National Clinical Research Center for Cancer, Tianjin's Clinical Research Center for Cancer, Key Laboratory of Cancer Prevention and Therapy, Tianjin Medical University Cancer Institute and Hospital, Tianjin, Hebei Province, China
2 Department of Intervention, National Clinical Research Center for Cancer, Tianjin's Clinical Research Center for Cancer, Key Laboratory of Cancer Prevention and Therapy, Tianjin Medical University Cancer Institute and Hospital; General Surgery, Tianjin Beichen Traditional Chinese Medicine Hospital, Tianjin, Hebei Province, China
3 Department of Intervention, National Clinical Research Center for Cancer, Tianjin's Clinical Research Center for Cancer, Key Laboratory of Cancer Prevention and Therapy, Tianjin Medical University Cancer Institute and Hospital, Tianjin; Department of Interventional Radiology and Vascular Surgery, The Affiliated Hospital of Hebei University, Baoding, Hebei Province, China
|Date of Submission||26-Nov-2020|
|Date of Decision||04-Feb-2021|
|Date of Acceptance||27-Mar-2021|
|Date of Web Publication||9-Jul-2021|
Department of Intervention, National Clinical Research Center for Cancer, Tianjin's Clinical Research Center for Cancer, Key Laboratory of Cancer Prevention and Therapy, Tianjin Medical University Cancer Institute and Hospital, Tianjin
Source of Support: None, Conflict of Interest: None
Objective: This study is aimed to provide a clinical basis for the identification and treatment of patients with malignant biliary obstruction (MBO) complicated with biliary infection by comparing pathogenic bacteria detected in bile and blood cultures from these patients.
Materials and Methods: A total of 380 patients with MBO who received percutaneous transhepatic cholangic drainage from January 2004 to January 2019 were included in the study. A total of 90 patients were diagnosed with having MBO complicated with biliary infection, and bile and blood culture were simultaneously performed on these patients. The patients included 58 men and 32 women, ranging in age from 33 to 86 years old, with a mean age of 60.69 years.
Results: The detection rate using bile bacterial culture in patients with MBO complicated with biliary infection was significantly higher than that using blood culture, and there were significant differences in the two kinds of bacterial culture found positive bile and blood cultures from the same patients. Gram-positive cocci were dominant in the bile cultures and Gram-negative bacilli were dominant in the blood cultures. Therefore, it is necessary to conduct simultaneous bile bacterial culture and blood culture for patients with MBO complicated with biliary infection, especially those with severe or critical diseases.
Conclusions: It is vital to enable simultaneous bile bacterial culture and blood culture in patients with MBO complicated with biliary infection. Existing guidelines for the diagnosis and treatment of benign biliary infection are not applicable to patients with MBO complicated with biliary infection.
Keywords: Bile bacterial culture, biliary infection, blood culture, malignant biliary obstruction, percutaneous transhepatic cholangic drainage
|How to cite this article:|
Wang C, Yu H, He J, Li M, Zhang L, Xu Y, Gao W, Yang X, Guo X, Guo Z. Comparative analysis of bile culture and blood culture in patients with malignant biliary obstruction complicated with biliary infection. J Can Res Ther 2021;17:726-32
|How to cite this URL:|
Wang C, Yu H, He J, Li M, Zhang L, Xu Y, Gao W, Yang X, Guo X, Guo Z. Comparative analysis of bile culture and blood culture in patients with malignant biliary obstruction complicated with biliary infection. J Can Res Ther [serial online] 2021 [cited 2021 Jul 29];17:726-32. Available from: https://www.cancerjournal.net/text.asp?2021/17/3/726/321017
| > Introduction|| |
Malignant biliary obstruction (MBO) is a common complication of malignant tumors, and it can cause severe liver function damage, which can be a potential risk factor for poor prognosis., Biliary infection is a common and severe complication of MBO. The mortality rate of patients with biliary tract infection is significantly higher than that of noninfected patients and that of patients with benign biliary obstruction, making the clinical diagnosis and treatment of biliary tract infection essential.,
At present, when obstructive jaundice is complicated with biliary infection, more and more clinical experts believe that bile culture and blood culture should be used to formulate anti-infective treatment, and they emphasize the importance of related bacterial culture and drug sensitivity tests. Recently, there have been reports about the characteristics of the bacterial spectrum in the bile culture of MBO complicated with biliary infection., However, as it is difficult to simultaneously collect bile and blood samples from patients with MBO complicated with biliary infection for further bacterial culture, there is no reported research on whether there is any difference in the detection rate, pathogen composition, and drug sensitivity between bile bacterial culture and blood culture. To date, there are no relevant clinical guidelines for malignant biliary infection, which is an urgent problem that needs to be solved in the field of biliary infection.
In this study, patients with MBO complicated with biliary infection underwent simultaneous bile bacterial culture and blood culture. Then, the positive rate, pathogen distribution, and drug sensitivity of two different samples were compared and analyzed. By comparing the differences of bacterial culture and drug sensitivity in bile and blood, the purpose of this study is to provide reference for clinical selection of appropriate antibiotics in the treatment of biliary tract infection.
| > Materials and Methods|| |
A total of 380 patients with MBO who received percutaneous transhepatic cholangic drainage (PTCD) in our hospital from January 2004 to January 2019 were considered for the study. This study included patients with MBO complicated with biliary infection that had been subjected to simultaneous bile bacterial culture and blood culture. This analysis excluded patients who had received antimicrobial therapy 1 month before PTCD treatment and patients diagnosed with other systemic infections. A total of 90 patients met the inclusion and exclusion criteria, including 58 males and 32 females, with an average age of 60.69 years (33–86 years) at the time of diagnosis. All patients were pathologically confirmed as having malignant tumors, including 39 cases of cholangiocarcinoma (41.33%), 19 cases of pancreatic cancer (21.11%), 18 cases of liver cancer (20.0%), 5 cases of gallbladder cancer (5.56%), and 9 cases of other metastases (10.0%).
Instrumentation and reagents
A digital fluoroscopy system with a digital subtraction function (DFP-2000A, Toshiba, Japan) was used for conducting PTCD. Further, a VITEK-2 compact microorganism-analysis system (bioMerieux, Marcy l'Etoile, France), a BACTEC-9050 automatic hemoculture machine (Becton Dickinson, Franklin Lakes, NJ), and a CO2 gas incubator (Sanyo, Japan) were used for bile culture, blood culture, and susceptibility testing. VITEK identification cards (bioMerieux, Marcy l'Etoile, France), including a VITEK-2 GN card for the identification of Gram-negative bacteria and a VITEK-2 GP card for Gram-positive bacteria, were used. The susceptibility cards included AST-GN08 (22007) and AST-GN09 (22008) for Gram-negative bacteria and AST-P534 (22066) and ASTP535 (22067) for Gram-positive bacteria. In addition, a Vitek2YST card was used for the identification of fungi and the AST-YS01 (22108) susceptibility card for fungi.
Percutaneous transhepatic cholangic drainage procedure and collection of bile and blood specimens
Bile sample collection
All patients were subjected to PTCD after giving informed consent. The procedures were guided by angiography. The patient was placed in the supine position, the right costal part and xiphoid process were routinely disinfected, and towels were placed. After local anesthesia at the 8–9th intercostal intersection of the right midaxillary line, a 22-G Chiba needle was inserted, and the extension sheath was exchanged after successfully puncturing the intrahepatic bile duct. Bile samples were collected through the extended sheath using a 10 ml syringe. Before taking the sample, 10 ml of bile was drained and discarded to prevent contamination. Then, 20 ml of bile was taken as the specimen for examination. Two bile samples of 10 ml were injected into anaerobe and aerobe culture bottles, respectively (Becton Dickinson, San Jose, CA) and sent to the laboratory immediately to prevent the samples from being damaged by anaerobes.
Blood sample collection
When the patients had symptoms of high fever and chills before operation, 10 ml of venous blood were taken for the culture of pathogenic bacteria. All patients were examined simultaneously using blood culture.
Bacterial identification and susceptibility testing
All bile samples were processed in the laboratory department of our hospital. A microorganism-analysis system was used to identify the bacteria. VITEK-2 (version VT2-R4.01) software was used for analysis. Subsequently, bacteria-producing β-lactamase and extended-spectrum β-lactamase (ESBL) were identified using the double paper-disk method. The M02-A10 performance standards were used to conduct the antimicrobial disk susceptibility tests.
Criteria for biliary infection with malignant biliary obstruction
According to the guidelines related to biliary infection,,, the diagnostic criteria of MBO with biliary infection are as follows: (a) local inflammatory symptoms: 1 – positive murphy sign and 2 – pain and discomfort in the right upper abdomen; (b) systemic inflammation: 1 – fever and body temperature >38.0°C; 2 – C-reactive protein >1 mg/dL; and 3 – white blood cell count >10 × 109/L or <4 × 109/L; (c) imaging features of acute biliary infection; and (d) in addition, patients with respiratory, urinary, and other systemic infection symptoms or clearly diagnosed with having other systemic infections were excluded. Satisfying any of the above criteria from each of a and b and c and d lead to the diagnosis of MBO complicated with biliary infection.
SPSS for Windows software, version 21.0 (Chicago, IL, USA), was used to conduct statistical analyses. Pearson's Chi-squared test was used to conduct correlation analysis on the samples. A two-tailed Pearson's Chi-squared test with P < 0.05 was considered as statistically significant.
| > Results|| |
Comparison of positive rate of bile bacterial culture and blood culture
When the bile and blood samples from all the patients underwent simultaneous bile bacterial culture and blood culture, the detection rate of pathogenic bacteria in bile culture (75.56%) was found to be significantly higher than that in blood culture [53.33%; χ2 =12.764, P < 0.01, [Table 1]].
Distribution of pathogens with positive results in bile culture and blood culture
Among the matched samples in this study, 29 patients (32.22%) showed pathogenic bacteria in both bile culture and blood culture. A total of 37 strains of microorganisms, including 17 species of bacteria and 1 species of fungi (Candida albicans), were isolated from 29 bile samples. In addition, 27.59% (8 of 29) of patients were infected with two or more pathogens. Among them, there were 17 strains of Gram-positive bacteria (45.96%), 16 strains of Gram-negative bacteria (43.24%), and 4 strains of fungi (10.81%). No anaerobes were cultured in this group of bile samples. The primary pathogens were 11 strains of Enterococcus (29.73%), 6 strains of Klebsiella (16.22%), 4 strains of Staphylococcus (10.81%), 4 strains of Escherichia coli (10.81%), 3 strains of Enterobacter (8.11%), 4 strains of C. albicans (10.81%), and 5 other strains (13.51%).
A total of 38 strains of microorganisms, including 16 species of bacteria and 2 species of fungi (C. albicans and Cryptococcus laurentii), were isolated from 29 blood samples, and 20.69% (6 of 29) of them were infected with two or more pathogens. Among them, there were 22 strains of Gram-negative bacteria (57.89%), 14 strains of Gram-positive bacteria (36.84%), and 2 strains of fungi (5.26%). No anaerobes were cultured in this group of blood samples. The primary pathogens were 14 strains of E. coli (36.84%), 7 strains of Enterococcus (18.42%), 6 strains of Staphylococcus (15.80%), 4 strains of Klebsiella (10.53%), 2 strains of fungi (5.26%), and 5 strains of other fungi (13.16%). There were significant differences in the pathogens identified in the bile and blood samples [Table 2].
|Table 2: Comparison of the distribution of pathogenic bacteria between bile culture and blood culture in 29 patients|
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Comparison of pathogenic bacteria between the bile and blood samples
Among the 29 patients with positive bile and blood cultures, the pathogens identified from the two samples were completely different in 62.07% of cases (18 of 29 patients) and completely consistent in 20.69% of cases (6 of 29). In addition, a single strain was cultured for all the patients with the same pathogens, and the etiological results showed Staphylococcus wallichii, Staphylococcus maltophilia, E. faecalis, E. coli, and C. albicans. Among these, E. coli accounted for two cases. The etiological results of the bile and blood cultures showed that one kind of bacteria was the same (17.24%, 5 of 29 patients). The distribution of specific pathogens is as follows [Table 3].
|Table 3: 29 cases of positive etiological composition of bile culture and blood culture|
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Note: No. 19–23 have a common pathogen between the bile and blood cultures in [Table 3], and the pathogenic bacteria in bile culture No. 24–29 were completely consistent.
Antimicrobial susceptibilities in 29 bile and blood cultures
Sensitivity tests were conducted on both bile and blood samples to determine effective drugs for patients with biliary tract infection. A total of two ESBL-producing strains and two β-lactamase-producing strains were detected in this group of bile samples, and ESBL-producing strains accounted for 12.50% of Gram-negative bacteria (2 of 16 patients). Among Gram-positive bacteria, β-lactamase-producing strains accounted for 11.76% (2 of 17 patients). A total of two strains producing ESBL and one strain producing β-lactamase were detected in blood samples. 9.09% (2 of 22 patients) of Gram-negative bacteria produced ESBL. The β-lactamase production rates of Gram-positive bacteria and E. coli were 7.14% (1 of 14 patients) and 14.29% (2 of 14 patients), respectively.
The results of the drug sensitivity tests of the bile and blood samples showed that E. faecium and E. faecalis were 100% sensitive to tigecycline and vancomycin and E. coli and Streptococcus were 100% sensitive to imipenem, meropenem, ertapenem, and doripenem. Staphylococci were 100% sensitive to ciprofloxacin and nitrofurantoin, and fungal strains were 100% sensitive to fluconazole, itraconazole, and voriconazole. In addition, aminoglycoside antibiotics and vancomycin-resistant strains were not detected in the bile and blood samples.
| > Discussion|| |
Biliary tract infection is the most common severe complication of MBO. The incidence of secondary biliary tract infection in all patients is 20%–40%, and it is one of the primary causes of death in patients with MBO. The results of the bile bacterial culture is the “gold standard” for the diagnosis of biliary infection and guides the use of antibiotics., In addition, some studies speculate that the detection of pathogenic bacteria in bile bacterial cultures from patients with MBO is closely related to biliary infection.,
Similar to the secretions of liver cells, the human gallbladder and bile should be aseptic. The hepatobiliary system can prevent bacterial invasion through strong immune defense mechanisms (Kupffer cells and bile IgA) and anatomical barriers (tight junctions), physical barriers (bile flow, mucus), and chemical barriers (bile acids). However, some studies have found that when biliary obstruction occurs, the infection rate of bile bacteria increases significantly. In principle, bacteria can invade the biliary tract by ascending from the duodenum or through blood from the hepatic portal vein. In humans, hepatic sinusoids may be periodically exposed to enterogenic bacteria during enterohepatic circulation, and portal bacteremia has been proved in healthy dogs.
All the patients in this study were evidently diagnosed as MBO complicated with biliary infection, and bile bacterial culture and blood culture were performed simultaneously. The results showed that the incidence of pathogenic bacteria in bile culture was significantly different from that in blood culture. It has been reported before that pathogenic bacteria are not detected in all patients with biliary infection, and the rate of detection is about 40%–60%. However, to date, there have been no studies on blood culture in patients with MBO complicated with biliary infection.
Blood culture is still the gold standard and first-line tool for the diagnosis of bacteremia and sepsis pathogens. However, the identification of pathogenic bacteria in blood cultures from patients with bacteremia depends on the patient's body temperature, skin preparation, blood collection, and other related factors. Recently, related articles have shown that the detection rate of bacterial pathogens in blood culture is only 8%–12%.,
The results of this study showed that the detection rate of pathogenic bacteria in the blood cultures of patients with MBO complicated with biliary infection was significantly lower than that in bile culture. The reasons for this result could be threefold: (1) it takes a certain amount of time for the biliary tract bacteria in patients with MBO complicated with biliary infection to translocate to the blood and grow and reproduce to cause bacteremia and further aggravate the disease. Therefore, it could be inferred that the patients with negative results for the blood culture had not developed bacteremia when the blood samples were taken. (2) Positive results for blood culture are closely related to the body temperature of patients when blood is taken. Studies have shown that the best time to collect blood culture samples for pathogen culture is during shivering or 1 h before fever. Therefore, the reason for the low positive rate of blood culture in this group could be that the blood samples were not collected at the best time to detect pathogens. (3) For patients with bacteremia, the positive rate of blood culture is only 8%–12%, and the blood culture of patients with bacteremia in this group could also be negative, which could also be one of the reasons why pathogenic bacteria were detected less frequently in blood culture than bile culture.
Interestingly, in addition to finding a significant difference in the detection rate, we also found a difference in the distribution of pathogens. The primary bacterial culture in the bile samples was Gram-positive bacteria (45.71%), while the blood cultures primarily showed Gram-negative bacteria (57.89%). The bacteria cultured in the bile and blood samples of the same patient accounted for 62.07% (18 of 29). Staphylococcus epidermidis was not found in the culture results in this group, which can rule out the positive results caused by sample contamination. The occurrence of pathogenic bacteria in the bile bacterial cultures we found is in agreement with that of related articles in recent years., In addition, some literature shows that the distribution of pathogens in bacteremia caused by other diseases is primarily Gram-negative bacilli, which is consistent with the results of this study.
Intestinal flora is known as the “second organ” of the human body. Under a healthy physiological state, the intestinal flora maintains the dynamic balance of the intestinal ecological environment and plays an important role in maintaining the stability of the intestinal tract and the body. The intestinal flora is primarily composed of Bacteroides, true Bacilli, Bifidobacteria, Clostridium, and digestive Streptococcus. Under pathological conditions, the intestinal flora is disordered and maladjusted, which impairs the immune function of the body and leads to the occurrence and development of disease., When the intestinal flora is maladjusted, it is generally characterized by a decrease in beneficial symbiotic flora and an increase in harmful flora, such as enterotoxin-producing Bacteroides fragilis, E. coli, and Clostridium difficile., As a complex disease, malignant tumors are closely related to immunity, metabolism, and other life activities, and they are often accompanied by an intestinal flora imbalance. Recently, the relationship between intestinal flora and the occurrence, development, and therapeutic effect of malignant tumors has become a focus of tumor research.
The decline of autoimmunity in patients with malignant tumors can lead to the gradual transformation of colonized bacteria in the biliary system into pathogenic bacteria. When complicated with biliary infection, the pathogens primarily originate from the intestinal tract. When the biliary tract obstruction is blocked, the intestinal pathogenic microorganisms can enter the biliary tract through three pathways to induce biliary infection: ascending the ampulla, through blood flow, and through the lymphatic duct. Bile acid is the primary organic solute in human bile. A decrease in bile acid concentration can disrupt the healthy intestinal microflora, lead to diarrhea, mucosal inflammation, or activate harmful drugs and carcinogens in intestinal contents. Some studies have shown that bile acid concentrations in patients with primary sclerosing cholangitis are decreased, leading to an increase in the number of Enterococcus in the bile duct.
Therefore, Enterococcus is the primary bacterial culture in the bile of patients with MBO complicated with biliary infection in this study, which could be related to the decrease in bile acid concentration or content in bile. In addition, patients with bacteremia primarily show Gram-negative bacteria., This could be the result of the drug resistance of Gram-negative bacteria, leading to blood cultures dominated by Gram-negative bacteria., However, more clinical data and evidence are needed to support the specific reasons for the differences between bile culture and blood culture in the same patient with MBO complicated with biliary infection.
No anaerobic strains were isolated in this study. However, previous studies have shown that anaerobes are an important pathogen in biliary tract infections, which are why some anti-anaerobic drugs are recommended. In a report of 65 cases of biliary tract, anaerobic bacteria and anaerobic plus aerobic bacteria were isolated from 7.7% (4 of 65 patients) of biliary tract surgeries. Considering the potentially high production of anaerobes, simultaneous anaerobic culture during biliary drainage is recommended.
A recent study shows that the results of blood culture in patients with biliary infection are consistent with the distribution of microorganisms found in routine bile specimens. This study showed that the consistency between blood and bile isolates and the use of appropriate decisive antibiotics for bile isolates did not affect mortality, but the study found that the use of appropriate decisive antibiotics for blood isolates had a significant effect on mortality. More than half of the microorganisms isolated from bile, especially Gram-positive bacteria and multibacterial growth bacteria, may not be real pathogens, meaning that there is no need to use antibiotics against all microbes in bile. However, some studies have shown that the detection of pathogens in bile culture is related to the detection of pathogens in blood culture for patients with cholangitis, and blood and bile culture data can effectively guide the selection of antibiotics., Due to the lack of relevant literature on improving bile culture and blood culture in patients with MBO complicated with biliary infection, more clinical evidence is still needed to inform the selection and use of antibiotics.
Through this study, it can be concluded that it is very necessary to conduct both bile bacterial culture and blood culture for patients with MBO complicated with biliary infection, especially for those with severe or critical diseases. However, further research is required to determine what antibiotics should be administered when there are differences between the pathogens identified in bile and blood cultures in the same patient.
However, the results of the drug sensitivity test showed that when the type of bacterial infection was determined, enterococcal infection could be directly treated with vancomycin or tigecycline. Imipenem or meropenem can be used as a suitable choice for Gram-negative bacterial infection or severe/refractory infection. It has been suggested that the guidance of BOJ anti-infection guidelines is not applicable to the treatment of MBO patients with biliary infection.
There are some limitations to our research. The number of cases enrolled in this study was relatively small, and the results could be accidental and restrictive. Therefore, it is necessary to further supplement the number of cases to prove the conclusions of this study. In addition, the data did not include changes in the inflammatory indices and symptoms before and after antibiotic treatment, but it indicated what kind of bacteria should be used in anti-infective treatment for such patients. Considering inflammatory indices and symptoms will be the direction and theme of our next research. In addition, there has been no statistical analysis of the risk factors of bacterial antibiotic resistance to avoid the widespread use of related advanced antibiotics and further increase the rate of drug resistance, increasing the difficulty of clinical treatment for patients with MBO complicated with biliary infection.
To sum up, the detection of pathogenic bacteria in the cultured bile samples from patients with MBO complicated with biliary infection was significantly higher than that in the cultured blood samples, and the types of bacteria found in the two types of culture were significantly different. Further research is required to determine the cause of this result. Meanwhile, the choice of follow-up antibiotics and the formulation of treatment plans for such patients will be our next area of research.
The authors would like to thank all the patients, their families, the investigators, comedical staffs, and all others who participated in the present study.
Financial support and sponsorship
This study was financially supported by Cancer Interventional Research Fund of China Health Promotion Foundation, Tianjin, Fund number: XM-2018-011-0006-01.
Conflicts of interest
There are no conflicts of interest.
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[Table 1], [Table 2], [Table 3]