Role of Interventional Radiology in the Management of Acute Cholangitis

Address for correspondence Ahsun Riaz, MD Division of Interventional Radiology, Department of Radiology, Northwestern University, 676 N. St. Clair, Suite 800, Chicago, IL 60611, ude.nretsewhtron@zair-nusha

Abstract

Acute cholangitis presents with a wide severity spectrum and can rapidly deteriorate from local infection to multiorgan failure and fatal sepsis. The pathophysiology, diagnosis, and general management principles will be discussed in this review article. The focus of this article will be on the role of biliary drainage performed by interventional radiology to manage acute cholangitis. There are specific scenarios where percutaneous drainage should be preferred over endoscopic drainage. Percutaneous transhepatic and transjejunal biliary drainage are both options available to interventional radiology. Additionally, interventional radiology is now able to manage these patients beyond providing acute biliary drainage including cholangioplasty, stenting, and percutaneous cholangioscopy/biopsy.

Acute cholangitis (AC) presents with a wide severity spectrum and can rapidly deteriorate from local infection to fatal sepsis and multiorgan failure. 1 2 Before the systemic use of antibiotics and advances in critical care, this disease had a high mortality rate. 3 With the introduction of biliary drainage as a mainstay of the treatment, mortality rates have significantly decreased. 1 4 Yet, the disease can be highly life-threatening without timely management.

In a study conducted by Khashab et al, delayed biliary drainage (>72 hours after admission) by endoscopic retrograde cholangiopancreatography (ERCP) was significantly associated with increased death, persistent organ failure, and prolonged intensive care unit stay. 5 In another study on 331 patients with AC, urgent biliary drainage (within 24 hours) significantly reduced hospital stay compared with early biliary drainage (24–48 hours), regardless of cholangitis severity. Also, success or failure of biliary drainage was remarkably related to mortality in those patients. 6 These findings emphasize the significance of early reliable diagnosis, severity assessment, and properly timed treatment. There are different approaches for biliary drainage in AC patients including endoscopic, percutaneous, and open methods, with differences in their indications, effectiveness, and morbidity. 3 This article provides a review of AC and role of interventional radiology in the management of AC using percutaneous approaches.

Pathophysiology of Acute Cholangitis

Two main factors are required for the development of AC 1 : biliary obstruction 2 and bacterial growth in stagnant bile. 7 Biliary obstruction impairs bile flow, resulting in elevated intraductal pressure and subsequent translocation of microorganisms from infected bile into systemic circulation. 8 The etiologies of AC are presented in Table 1 . Choledocholithiasis is considered the most common reason for biliary obstruction leading to cholangitis, followed by malignant stenosis, postoperative stricture, and biliary instrumentation. 7 8 9 The most common strains isolated from bile cultures are Escherichia coli , Klebsiella species, Enterococcus species, and Pseudomonas species. 10 The same bacterial strains account for the most common microorganisms isolated from blood culture in patients with bacteremic biliary tract infection. 10

Table 1

Abbreviations: AIDS, acquired immunodeficiency syndrome; ERCP, endoscopic retrograde cholangiopancreatography.

Diagnosis

AC can manifest with a wide variety of clinical presentations including fever, abdominal pain, nausea and vomiting, jaundice, or altered consciousness. 11 Despite the need for prompt diagnosis, there has been a lack of consensus regarding standard diagnostic criteria for the disease.

Traditionally, Charcot triad (jaundice, right upper quadrant pain, fever) was widely used to establish a diagnosis of AC based on clinical findings. 12 Despite a high specificity, low sensitivity of the Charcot triad, reported mainly between 50 and 70% by multiple studies, was the primary weakness limiting its diagnostic efficacy for AC. 7 9 12 13 In a study conducted by Kiriyama et al on 6,063 patients diagnosed with cholangitis, the diagnosis rate of Charcot triad was reported as low as 21.2%. 14 In another analysis of 1,432 patients with biliary tract disease, it was demonstrated that Charcot triad has a sensitivity of 26.4% and a specificity of 95.9% for AC. 1 To overcome these limitations, the first diagnostic criteria called Tokyo guidelines 2007 (TG07) was introduced that considered clinical manifestation, laboratory data, and imaging findings in the diagnosis of AC. 2 Due to assessments that demonstrated lack of sensitivity in TG07 to detect severe cases and to improve the application of TG07 in clinical settings, TG13 was presented which improved the sensitivity from 82.8 to 91.8% without remarkably changing the specificity (79.8% in TG07 to 77.7% in TG13). 1 4 In a validation of TG13 conducted by Kiriyama et al, TG13 yielded a diagnosis rate of 90% in patients with suspected AC, in comparison to the diagnosis rate of 79.4% based on TG07 in the same population. 14 In 2018, it was suggested to adopt TG13 in TG18 and to implement it as standard diagnostic criteria in clinical practice. 15 Table 2 outlines the TG18/TG13 diagnostic criteria for AC.

Table 2

Abbreviation: ULN, upper limit of normal value.

Another way to classify AC is (1) uncomplicated and (2) complicated. Complicated AC due to any cause could be due to complications such as local complications (liver abscess, acute cholecystitis, portal vein thrombosis, and biliary pancreatitis) or systemic complications (sepsis, multisystem organ failure).

Laboratory Evaluation

Studies and guidelines recommend that white blood cell count, bilirubin, alkaline phosphatase (Alp), alanine aminotransferase, and aspartate aminotransferase should be routinely assessed in patients with suspected cholangitis. 2 9 13 15 Alp is considered as the most consistently elevated marker in patients with AC. 16 In a study on patients with malignant obstructive jaundice, it was demonstrated that Alp levels show faster decline patterns following biliary drainage, when compared with other liver function test markers. 17 Recently investigated, a procalcitonin level greater than 2.2 ng/mL was shown to predict severe AC cases better than traditional biomarkers. 18 This can be used as a promising predictor of rapid progression to sepsis and signify patients who would benefit from urgent biliary drainage at the time of admission. 19

Generally, routine blood cultures are not recommended in the management of community-acquired intra-abdominal infections, including AC, as they do not provide any additional information that impacts the course of treatment. 20 Furthermore, in a study conducted on patients in emergency departments, it was stated that only 1.6% of obtained blood culture samples altered patient management. 21

Imaging

To this date, there is no radiological sign that aids in directly diagnosing AC. However, imaging studies can provide findings that indirectly support the diagnosis including bile duct dilatation, predisposing factor, and complications. 4 22 With its low cost, wide availability, and noninvasiveness, transabdominal ultrasound (US) is usually the first-line imaging study used in patients suspected for AC. 15 Yet, there are many limitations including a major impact of operator expertise on diagnostic accuracy of US in detecting bile stones. 23 Studies have reported sensitivity of US for detecting choledocholithiasis as low as 22%. 24 In a meta-analysis conducted by Abboud et al, US showed promising specificity of 100% (95% confidence interval [CI]: 99–100%) but lacked sufficient sensitivity (38%. 95% CI: 27–49%) in detecting common bile duct stones. 25 Computed tomography (CT) has a higher sensitivity in detecting biliary stones, compared with US. Lee et al assessed the efficacy of combined unenhanced and contrast-enhanced CT scan for the diagnosis of biliary stones and reported a sensitivity and specificity rates of 73 and 98%, respectively, in intrahepatic stones and a sensitivity and specificity rates of 71 and 97%, respectively, in common duct stones. 26

Among different imaging studies, endoscopic ultrasonography (EUS) and magnetic resonance cholangiopancreatography (MRCP) are considered the most accurate modalities in the diagnosis of biliary stones. EUS was reported to have sensitivity of 100%, specificity of 95.4%, and accuracy of 96.9% in the diagnosis of choledocholithiasis. 27 The corresponding values for MRCP were 100, 72.7, and 82.2%, respectively. 27 However, MRCP sensitivity in detecting biliary stones smaller than 6 mm is particularly low. 28

General Management Principles

The mainstay of management in AC is focused on the treatment of principal components causing the disease: biliary infection and biliary obstruction. Early management of the disease includes administering intravenous fluid therapy and correcting any coagulopathy or electrolyte abnormalities. 29 Empirical intravenous antibiotic therapy should be administered as soon as AC is suspected. 30 Initial antibiotics should cover both gram-negative and anaerobic organisms. The choice of antibiotic depends on multiple factors such as the severity of the infection, morbidities of the patient, hepatic and renal functions, and drug allergies. Penicillin/β-lactamase inhibitors are one of the most frequently used antibiotics in empirical management of cholangitis. 31 A randomized clinical trial conducted by Sung et al demonstrated that ciprofloxacin alone can be adequate empirical therapy for patients with AC. 32 Biliary drainage is another cornerstone of AC management, as elevated intraductal pressure can diminish the biliary secretion of antibiotics and render them ineffective. 33 Efficient biliary drainage can reduce the duration of antibiotics therapy and, hence, shorten the duration of associated side effects. Although the traditionally recommended duration of antimicrobial treatment is 4 to 7 days, it was recently demonstrated that antibiotic use of up to 3 days can be sufficient, if accompanied by adequate biliary drainage. 34 Over time, different modalities for establishing biliary drainage have been developed including open surgical drainage, endoscopic transpapillary biliary drainage (divided into two types: first, external drainage by endoscopic nasobiliary drainage; second, internal drainage by endoscopic biliary stenting), percutaneous transhepatic biliary drainage (PTBD), and EUS-guided drainage. 35 PTBD is discussed in further details below.

Percutaneous Transhepatic and Transjejunal Biliary Drainage

Success Rate and Indications

PTBD success rate is favorably high (94–100%) in reported studies. 36 37 38 39 Although some studies propose that absence of bile duct dilatation can reduce the success rate of the procedure, other studies have not found such relation. 39 40 PTBD is mostly considered when endoscopic procedures fail to provide successful drainage. Also in situations like intrasegmental cholangitis and altered biliary anatomy (such as Roux-en-Y anastomosis), PTBD is superior to other approaches in the management of cholangitis. 41 Furthermore, in the treatment of recurrent pyogenic cholangitis caused by intrahepatic stones, PTBD can be employed to assist percutaneous transhepatic cholangioscopy and lithotripsy for stone extraction. 42 In a study on 248,942 patients with ascending cholangitis, multivariate analysis on 10,486 patients who underwent percutaneous drainage showed that PTBD was more often performed in older patients, malignant obstruction, and Charlson Comorbidity Index (CCI) score ≥3. 43

Preprocedural Evaluation

Coagulation profile and liver function tests should be evaluated for the patient. Recent imaging by CT or MRCP is crucial in terms of planning the procedure, revealing the cause and level of obstruction, and assessing the most appropriate approach for procedure. The level of cystic duct insertion is defined as the border between “low” and “high” level of bile duct obstruction. Low bile duct obstruction is best managed with endoscopic approach, and drainage can be successfully achieved by a single catheter or stent. However, percutaneous approach is best for high bile duct obstruction, as it provides the greatest chance to access the target bile duct. 44 Imaging can also be highly valuable in cases of liver malignant involvement to assess the functional liver parenchyma as drainage of nonfunctional parenchyma will not result in improved liver function. Functional areas of liver parenchyma are defined as tumor-free areas with intact blood supply by portal vein. 44 Patients should also be administered prophylactic antibiotics such as (1) 1 g ceftriaxone intravenous (IV); (2) 1.5 to 3 g ampicillin/sulbactam IV; (3) 1 g cefotetan IV plus 4 g mezlocillin IV; and (4) 2 g ampicillin IV plus 1.5 mg/kg gentamicin IV. Vancomycin can be used in cases of penicillin allergy. 45

General Technique

Percutaneous Transhepatic Drainage

An 18- to 22-gauge hollow needle is used to puncture the bile duct. It is safer to use needles with a smaller gauge in patients with nondilated bile ducts. 35 This procedure is performed under fluoroscopic and US guidance. 38 46 After confirming the backflow of the bile (which may not happen in all cases), contrast is injected to opacify the target duct. Peripheral puncture access is more desirable than central access, as it is associated with lower risk of bleeding and inadequate drainage. 44 In the next step, after inserting a 0.018-inch guide wire into the bile duct, the needle is exchanged for a coaxial introducer set to pass a 0.035-inch access guide wire into the bile duct. Then, with the aid of a 7- to 10-Fr catheter, the guide wire can be exchanged for a stiff wire to further dilate the biliary tract. Finally, a biliary drainage catheter (either external or internal–external) is inserted and secured to the skin. 47 External drains are less stable, more prone to dislodgment, and carry a risk of fluid loss (dehydration). 48 Hence, internal–external drains are more desirable unless the stricture is so severe that cannot be crossed. In these situations, external drains are placed to drain bile for a few days and, after the local inflammation has subsided, drain internalization can be attempted. 49

Biliary Drainage in the Presence of Metal Biliary Stents

As metal stents become more commonly used by gastroenterologists (GIs) and interventional radiologists (IRs) for malignant biliary disease to manage benign and malignant biliary strictures, there are more and more cases of stent occlusions. Sometimes, these stents cover branches of segmental or lobar biliary ducts leading to segmental or lobar cholangitis ( Fig. 1 ). Alternatively, the stent itself can get occluded and lead to upstream cholangitis. It is difficult for IR and GI to manage patients with preexisting stents, as crossing the stent interstices is difficult. Usually, these patients end up with lifelong biliary drains.

Diagrammatic representation of a stent occluding a branch (arrow) with upstream stasis which can lead to cholangitis (thick arrow).

Percutaneous Transjejunal Drainage

Hutson et al first introduced retrograde biliary cannulation by creating a stoma in the anterior abdominal wall of the antecolic Roux-en-Y limb. This was introduced in 1984 for repeat biliary interventions in patients with primary sclerosing cholangitis. 50 There were significant patient lifestyle limitations in having a stoma (Hutson loop). Hence, surgical affixation of the biliary (afferent/Roux) limb of the Roux-en-Y anatomy to the anterior abdominal wall (without a stoma) was performed. This has been termed the “modified Hutson loop.” The surgical affixation to the anterior abdominal wall increased the procedure's safety. 51 The modified Hutson loop allowed jejunal entry through the skin using radiographic markers and subsequent catheterization of the hepaticojejunostomy followed by cholangiography and biliary interventions as indicated. 52 Modified Hutson loops are created in patients with hepaticojejunostomies due to malignant biliary diseases as well. 52 IRs have also performed percutaneous transjejunal approach without surgical affixation. 53 The percutaneous transjejunal approach in patients with modified Hutson loops limits injury to the liver and provides IRs with another avenue to manage biliary disease. 54

Postprocedural Management

Patient's vital signs and clinical conditions should be frequently monitored after the procedure. Catheter output and laboratory evaluations (such as liver function tests and white blood cell counts) should be regularly examined to assess adequate biliary drainage. Routine interventional radiology follow-ups for drain checks and exchanges should be scheduled as well.

Percutaneous Transhepatic Biliary Drainage versus Surgery

Open surgical decompression of the bile duct is no longer performed routinely for cholangitis management, as it carries higher morbidity and mortality rates, compared with other biliary drainage techniques. 55 It has been shown that conditions such as underlying medical diseases, thrombocytopenia, serum albumin less than 3 g/L, serum PH less than 7.40, and total bilirubin levels ≥90 µmol/L can considerably increase mortality rates up to 55%. 56 Studies have recommended PTBD over emergency surgery for the management of an acute episode of cholangitis, as it can provide decompression to prepare patient for elective surgical intervention, once the patient's clinical condition is more stable. 57

PTBD versus Endoscopic Transpapillary Biliary Drainage

ERCP is considered superior to PTBD for drainage in cholangitis, as it is associated with less pain and discomfort (such as cosmetic issues and skin inflammation) and a significantly lower rate of adverse events especially for the elderly patients. 35 55 Duration of hospitalization is significantly lower in endoscopic drainage. 55 However, PTBD is the treatment of choice in cases of difficult biliary cannulation, upper gastrointestinal adhesions, altered biliary anatomy, intrahepatic stones, or high biliary obstruction. 22 35 38 41 Despite PTBD, success or failure of endoscopic biliary drainage (EBD) is independent of bile duct dilatation and hence, it can be highly effective in decompressing the biliary tree in cholangitis patients with nondilated bile ducts. 58 Yet, in patients with underlying malignant stricture, EBD can face multiple challenges. Several meta-analysis studies have compared PTBD and EBD in preoperative biliary drainage in patients with malignant biliary obstruction like cholangiocarcinoma. They demonstrated that PTBD is associated with similar or better success rates than EBD in such patients and although these procedures carry similar rates of overall complications, PTBD is associated with a lower risk of immediate procedural complications, especially postprocedure cholangitis and pancreatitis. 59 60

PTBD versus EUS-Guided Drainage

Both PTBD and EUS-guided drainage (EUS-GD) have been utilized for biliary drainage in patients with failed ERCP. However, there is a lack of consensus regarding the best alternative procedure in these cases. Most studies mention the same technical success rates between PTBD and EUS-guided drainage. Yet, clinical success and complications rates appear to be lower in patients undergoing EUS-GD. Tables 3 and ​ and4 , 4 , respectively, outline reported success rates and outcome differences between these two approaches by different studies. In a meta-analysis conducted by Sharaiha et al, there were no differences in technical success rate and hospitalization duration between both procedures. However, clinical success of EUS-guided biliary drainage was higher, as it was associated with lower rates of complications, reinterventions, and total cost for patients. 61 Another meta-analysis conducted by Baniya et al demonstrated no differences between the technical and clinical success rates and mild complication rates for both procedures. However, the rates of total complications and moderate-to-severe complications were higher in PTBD. 62 Of note, Baniya et al included fewer studies in their meta-analysis. In a survey conducted on patients undergoing ERCP, patients were informed about PTBD and EUS-GD as alternative procedures, in cases of ERCP failure, and were instructed about procedure techniques, complications, and outcomes. 80.2% of the patients preferred EUS-GD over PTBD as their alternative procedure. As reported, reasons for selecting EUS-GD were noted as less physical discomfort and the ability to be performed with ERCP simultaneously. On the other hand, patients who preferred PTBD cited higher technical safety, shorter duration of procedure, and cost-effectiveness as their rationale. 63 Despite the lower complication rate of EUS-GD, studies have reported varied technical success rates and some studies mention technical challenges in performing the procedure. 64 Therefore, it is proposed to use EUS-GD as the alternative procedure only if an expert operator is available. Otherwise, PTBD should be considered for biliary drainage, in patients with failed ERCP. 35

Table 3

Abbreviations: EUS, endoscopic ultrasonography; N/A, not available; PTBD, percutaneous transhepatic biliary drainage; SD, standard deviation.

Table 4

Abbreviations: EUS, endoscopic ultrasonography; PTBD, percutaneous transhepatic biliary drainage.

Contraindications and Complications

The reported complication rates of PTBD vary greatly between studies (ranging from 9 to 45.6% of patients for acute complications) and depend on many factors such as underlying diagnosis, patient's clinical status, and operator's expertise. 36 37 39 40 65 66 Major complications, however, are reported only in nearly 4% of the patients. 36 39 Different complications can be developed such as catheter-related problems (e.g., occlusion, dislocation), bleeding, sepsis, and cholangitis. Several risk factors have been suggested for the development of drain occlusion and postprocedure cholangitis including malignant stricture of biliary tree, bilateral approach for drainage, and catheter size ≥16 CH. 65 In a study on 97 patients, 14.4 and 17.5% of patients developed immediate (within 24 hours) and delayed (after 24 hours) fever, respectively, after the procedure. They found a significant relationship between low international normalized ratio (INR) and absence of intrahepatic bile duct dilatation with developing immediate fever. Furthermore, delayed fever development was associated with inadequate biliary drainage during the procedure. 67 Regarding the type of drainage, external drainage, compared with internal–external drainage, carries a lower risk of procedure-related infection and is associated with a better rate of infection control and prognosis. 68 Patel et al reported that the presence of ascites, especially diffuse type, significantly elevates the risk of sepsis and hemorrhagic complications associated with PTBD. 69 The presence of nondilated intrahepatic ducts was suggested to be significantly associated with higher risk of developing complications following PTBD. 39 It has also been highlighted that patients with underlying malignant biliary disease are at higher risk of developing PTBD-related complications. 66

Due to the complex and dense vascular supply of the liver, PTBD carries a high risk of bleeding, reported between 1.9 and 3% by different studies. 36 37 70 71 Therefore, the procedure should be avoided in patients with coagulopathy. In a study on 23,735 patients undergoing PTBD, 2.5% experienced severe bleeding requiring red blood cell transfusion. They demonstrated that continuation of antiplatelet agents considerably increases the risk of severe bleeding in patients who undergo PTBD; however, the impact of continuing anticoagulant agents on bleeding was insignificant. They also found age ≥73 years, chronic renal failure, and liver cirrhosis as major risk factors for severe bleeding following PTBD. 71 A study reviewing 3,780 PTBD procedures proved left-sided PTBD approach to be an independent risk factor for hepatic arterial injury and bleeding in patients. 70 Some measures are suggested to lower the risk of PTBD-related bleeding such as avoiding central bile ducts and using lower border of intercostal space for needle and drain insertion. A maximum INR of 1.4 and 1.6 and a minimum platelet count of 70,000 and 50,000/mm 3 in elective and emergent cases, respectively, are recommended for safe practice of the procedure. 72 Considering all factors, it is proposed to prefer endoscopic transpapillary biliary drainage over PTBD in patients with cholangitis who have coagulopathy or consume antithrombotic agents. 35

Role of Interventional Radiology beyond Drainage

Interventional radiology has seen significant advancements in imaging modalities and available devices. US has significantly improved in its resolution. Fluoroscopy machines are now able to perform three-dimensional imaging. There are combination fluoroscopy–CT rooms that can increase safety and reduce procedure duration significantly. In addition to all the advancements in imaging, there has been great progress in the devices.

Wires, catheters, balloons, and stents (plastic and metal) are now very safe to use and easily deliverable through a percutaneous approach. Hence, once percutaneous access to the biliary system is obtained, many interventions historically performed by GIs can now be performed by IRs. A collaborative environment between gastroenterology and interventional radiology can lead to safe and effective patient management. This also allows for appropriate treatment allocation and for combined procedures performed by interventional radiologist and GI.

The LithoVue and SpyGlass Discover (Boston Scientific, Marlborough, MA) are less than 11 Fr (outer diameter) single-use scopes which can be introduced through a sheath equal to or greater than 11 Fr. These scopes provide a 3.6-Fr working channel that can be used for flushing and advancement of wires, catheters, and devices (such as lithotripsy probes and forceps). This gives IRs another tool to assist in the management of biliary pathologies. Once AC resolves and patient's clinical status improves, IR can perform definitive treatment for a lot of etiologies of AC.

Conclusion

Acute cholangitis is a fatal disease that requires immediate medical attention and effective treatment. Biliary drainage is an essential component of the management. Although endoscopic approach is regarded as the treatment of choice, it is not safe and feasible in some cases such as patients with altered biliary anatomy, underlying malignancy, or severe biliary strictures. Percutaneous transhepatic and transjejunal biliary drainage performed by IRs is a well-established, promising alternative in these patients with a considerable impact on management and overall prognosis.

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