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Cholangitis

Causes, Diagnosis, and Management

a a,b,
Jesse K. Sulzer, MD, PhD , Lee M. Ocuin, MD *

KEYWORDS
 Acute cholangitis  Biliary obstruction  Choledocholithiasis  Biliary infection

KEY POINTS
 Improvements in endoscopic management and critical care have decreased mortality
from acute cholangitis but the disease remains lethal.
 Knowledge of advancements in drainage techniques being used in biliary drainage during
acute cholangitis can improve care.
 Modern diagnostic schemes and treatment algorithms can reduce mortality from acute
cholangitis.

INTRODUCTION

Acute cholangitis has long been recognized as a potentially lethal medical emergency
characterized by obstruction and subsequent infection of the biliary tree.1 Before
recent advancements in critical care, diagnostic modalities and strategies, and expan-
sion of less invasive means by which to decompress the bile duct system, mortality
was reported to be more than 50% for acute cholangitis.2,3 Utilization of these new
tools in the diagnosis and care of patients with acute cholangitis have contributed
to a significant decrease in mortality from this disease. The significant decrease in
mortality emphasizes the importance of early and accurate diagnosis and proper se-
lection and timing of interventions when needed. A working knowledge of common eti-
ologies and updated diagnostic criteria can enable the practitioner to not only make
this critical diagnosis early but appropriately assess the severity of the disease pro-
cess and thus the urgency and scope of interventions.

Disclosures: The authors have nothing to disclose.


a
Division of Hepatopancreatobiliary Surgery, Department of Surgery, Atrium Health/Carolinas
Medical Center, Charlotte, NC, USA; b Division of Hepatopancreatobiliary Surgery, Atrium
Health/Carolinas Medical Center – Northeast, 200 Medical Park Drive, Suite 430, Concord, NC
28025, USA
* Corresponding author. Division of Hepatopancreatobiliary Surgery, Atrium Health/Carolinas
Medical Center – Northeast, 200 Medical Park Drive, Suite 430, Concord, NC 28025.
E-mail address: lee.ocuin@atriumhealth.org

Surg Clin N Am 99 (2019) 175–184


https://doi.org/10.1016/j.suc.2018.11.002 surgical.theclinics.com
0039-6109/19/ª 2018 Elsevier Inc. All rights reserved.

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176 Sulzer & Ocuin

CAUSES
Pathophysiology
Partial or complete obstruction of the bile duct and subsequent infection is the key fac-
tor in the development of acute cholangitis.4 Under normal circumstances, the contin-
uous flow of bile and immunologic defenses of the biliary epithelial cells keep the
biliary tree sterile. Obstruction and the resulting increase in bile duct pressure to
greater than 25 cm H2O can lead to a breakdown of these defenses and subsequent
infection and septicemia from bacterial translocation into the bloodstream.5,6 Seeding
of the biliary tree can occur via retrograde entry of bacteria from the gastrointestinal
track or the portal vein.7 The impact of retrograde infection of the biliary tree is evi-
denced by the fact that higher positive bile duct culture rates are observed in cases
of partial obstruction when compared with complete obstruction.8 Gram-negative
bacteria, including Escherichia coli and Klebsiella pneumoniae, are the most
commonly identified bacteria in acute cholangitis.9 In patients with indwelling stents,
Enterococcus species are the most commonly detected bacteria, and high rates of
Candida species are also reported.10

Etiology of Obstruction
There are multiple disease processes that can result in biliary obstruction with resul-
tant cholangitis (Box 1). Benign etiologies include stone-related disease and resultant
complications, and strictures related to chronic pancreatitis, prior biliary surgery, and
primary sclerosing cholangitis. Biliary obstruction most commonly occurs from chol-
edocholithiasis, representing roughly half of cases.11 Mirizzi syndrome, defined by
obstruction of the extrahepatic bile ducts by a gallstone in the neck of the gallbladder
or cystic duct, has also been reported as a cause of acute cholangitis.12 Malignant eti-
ologies include biliary strictures related to periampullary cancers, hilar cholangiocar-
cinoma, or gallbladder cancers. Acute cholangitis resulting from malignant
obstruction accounts for 10% to 30% of cases.8 Endoluminal or percutaneous instru-
mentation of the biliary tree is another known risk factor for development of acute chol-
angitis. Complications have decreased significantly following endoscopic biliary
procedures, and acute cholangitis following these procedures represents 0.5% to

Box 1
Causes of acute cholangitis

 Benign
 Choledocholithiasis
 Benign biliary stricture
 Congenital abnormalities
 Postoperative stricture
 Pancreatitis
 Malignant
 Bile duct cancer
 Gallbladder cancer
 Pancreatic cancer
 Ampullary cancer
 Duodenal cancer
 Other
 Autoimmune/inflammatory disease
 External compression (Mirizzi/Lemel syndromes)
 Sump syndrome

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Cholangitis 177

2.4% of cases.13 Infrequent causes of obstruction and cholangitis include duodenal


diverticula, which can cause mechanical obstruction of the common bile duct (Lemmel
syndrome),14,15 parasitic infections, acquired immunodeficiency syndrome cholangi-
opathy, and autoimmune/immunoglobulin G4–associated cholangitis.16

DIAGNOSIS
Diagnostic Criteria
Numerous definitions and diagnostic criteria exist to establish a diagnosis of acute
cholangitis. These range from purely clinical approaches encompassing the Charcot
triad (fever, right upper quadrant pain, and jaundice), to greater focus on documenta-
tion of biliary obstruction.17 The Tokyo Guidelines have attempted to establish a com-
mon definition and diagnostic criteria consisting of a mix of clinical, laboratory, and
imaging findings (Box 2).18
Clinical Presentation
Fever and right upper quadrant pain are the most common presenting symptoms and
occur in patients 80% of the time.19 Jaundice, the third component of the traditionally
taught Charcot triad, is observed in 60% to 70% of cases.17,19 The Charcot triad has
been reported to have high specificity (95.9%) but lacks sensitivity (26.4%) for acute
cholangitis.17,20 A 2017 study by Kiriyama and colleagues21 that included more than
6000 patients with acute cholangitis found the Charcot triad to be positive only
21.2% of the time. Likewise, the Reynold pentad (Charcot triad plus septic shock
and mental status changes) has been reported to be found in only 4% to 8% of pa-
tients with severe cholangitis.17 The Tokyo Guidelines (see Box 2), originally published
in 2007 and revised in 2013 and 2018, have attempted to provide an additional data-
driven diagnostic framework for the clinical diagnosis of acute cholangitis.21,22 The
Tokyo Guidelines retain the presence of the Charcot triad as a definitive diagnostic cri-
terion. However, given the variable presentation of this clinical constellation, the
guidelines incorporate the addition of laboratory and imaging findings consistent
with biliary obstruction in the diagnostic criteria.8,22 The Tokyo Guidelines have
been shown to provide accurate diagnosis on 90% of cases.21

Box 2
Diagnostic criteria

A. Systemic inflammation

- A-1. Fever higher than 38
- A-2. Laboratory evidence of inflammation (white blood cell count <4 or >10, C-reactive
protein >1)
B. Cholestasis
- B-1. Jaundice (Total bilirubin >2 mg/dL)
- B-2. Abnormal liver function tests (elevation > 1.5  Standard deviation of alkaline
phosphatase, glutamate pyruvate transaminase, aspartate aminotransferase, or alanine
aminotransferase )
C. Imaging
- C-1. Biliary dilation
- C-2. Evidence of etiology of obstruction

Suspected diagnosis: One item in A 1 1 item in either B or C.


Definite diagnosis: One item in A, 1 item in B, and 1 item in C.
From Kiriyama S, Takada T, Strasberg SM, et al. TG13 guidelines for diagnosis and severity
grading of acute cholangitis (with videos). J Hepatobiliary Pancreat Sci 2013;20:28; with
permission.

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178 Sulzer & Ocuin

Laboratory Findings
Laboratory tests consistently associated with acute cholangitis include white blood
cell count greater than 10  109/L and elevated blood levels of bilirubin, alkaline phos-
phatase, aspartate aminotransferase and alanine aminotransferase, and these tests
should be routinely sent in all suspected cases.11,17,19 Alkaline phosphatase is the
most consistently elevated marker, with elevations found in 74% to 93% of cases
of acute cholangitis. Alkaline phosphatase also exhibits a quicker recovery pattern
following successful drainage than other markers of obstruction, such as bilirubin,
and may provide a more accurate early indicator of adequate drainage.23 Other labo-
ratory findings, such as elevated amylase and prothrombin time, have been more var-
iable.19 The tumor marker carbohydrate antigen 19-9 (CA19-9) has been reported with
a broad range of both frequency and values,24–26 and high levels (>9000 IU/mL) have
been observed in confirmed cases of cholangitis with rapid resolution following suc-
cessful treatment.26 We do not recommend routine analysis of amylase, prothrombin
time, or CA19-9 in context of workup and management of acute cholangitis. Elevation
of additional markers of inflammation/infection, including C-reactive protein and pro-
calcitonin, are regularly observed and values can provide additional guidance on
choice of therapeutic interventions and for prognosis. Procalcitonin has recently
received much attention in the diagnosis of and management of sepsis. In cases of
acute cholangitis, procalcitonin has been shown to be a more accurate predictor of
severe disease than conventional biomarkers.27 Furthermore, high procalcitonin levels
have the potential to expose the need to perform emergency decompression in cases
that may otherwise not be classified as severe based on other clinical data.28–30
Blood cultures are often collected as part of the initial investigation in patients with
suspected infection. Positive blood cultures in acute cholangitis have been reported
over a range from 21% to 71% of cases.22 However, these positive cultures most
often do not provide additional clinically relevant information in routine cases of
community-acquired intra-abdominal infection.31 A study of the impact of blood cul-
tures taken in the emergency department for patients with suspected infection found
that positive cultures resulted in changes to clinical management in a small minority of
cases.32 Thus, both the Tokyo Guidelines and the Guidelines by the Surgical Infection
Society/Infectious Diseases Society of America do not routinely recommend blood
cultures.31,33 An exception to this is the toxic or immunocompromised patient or in
high-severity infections when culture results may change therapy or guide duration.

Imaging
Initial radiographic studies rely on indirect findings of bile duct obstruction in support
of the diagnosis of acute cholangitis. Transabdominal ultrasound is often a first-line
diagnostic study, given its ready availability and low cost. Findings of biliary ductal
dilation can support the diagnosis, but sensitivity for detection of common bile duct
stones is less than 30%.20 Contrast-enhanced computed tomography (CT) scan
also can provide indirect support for the diagnosis of cholangitis in suspected cases,
including findings of biliary stones, ductal dilation, hepatic abscess, or pneumobilia.18
The ability of CT to detect stones in the biliary tree has been reported at 42%.5 Hepatic
parenchymal changes have been noted as a more specific finding of acute cholangitis.
Inhomogeneous hepatic parenchymal enhancement caused by a decrease in portal
blood flow is observed in acute cholangitis.34 In addition, CT allows for evaluation of
the entire liver, enabling diagnosis of complications of cholangitis, such as liver ab-
scesses. MRI/magnetic resonance cholangiopancreatography (MRCP) provides
another noninvasive diagnostic method. MRCP has been demonstrated to reveal

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Cholangitis 179

ductal pathology in acute cholangitis in more than 80% of cases but is limited in its
sensitivity to detect stones smaller than 6 mm.5
Endoscopic ultrasound (EUS) and endoscopic retrograde cholangiopancreatography
(ERCP) are invasive tests that can provide additional diagnostic information. ERCP has
the additional advantage of allowing for therapeutic intervention. EUS has a sensitivity
approaching 100% and a specificity of more than 90%, with an overall accuracy of
96.9% for the detection of bile duct stones.35,36 EUS has the advantage of portability
and the possibility of performing ERCP during the same session.37 Purulence emanating
from the major papilla encountered on ERCP remains the gold standard for diagnosis of
acute cholangitis.20 Furthermore, ERCP may elucidate additional information regarding
the etiology of the episode and allows for therapeutic intervention.5
Grading
The Tokyo Guidelines divide acute cholangitis into 3 grades (Box 3): mild (grade I),
moderate (grade II), and severe (grade III). The grades are defined by initial response
to medical treatment and associated organ dysfunction. Grade I acute cholangitis is
defined by response to initial medical treatment. Grade II acute cholangitis does not
respond to initial medical treatment but is not associated with additional organ
dysfunction. Grade III acute cholangitis is associated with organ dysfunction. Accu-
rate diagnosis and grading can assist with prognosis and help guide management.
Mortality has been demonstrated to increase significantly with rising severity staging
ranging from 1% in grade I to 5% or more in grade III.17,18

MANAGEMENT
Antibiotics
Aggressive resuscitation and early antibiotic administration remain the initial therapeu-
tic steps in cases of suspected or confirmed acute cholangitis.38,39 Antibiotics are
administered to limit systemic sepsis and local inflammation as well as complications
associated with acute cholangitis, such as intrahepatic abscess formation.33 Current
guidelines recommend initial treatment with a penicillin/beta-lactamase inhibitor,
third-generation cephalosporin, or carbapenem.33,38 Regional variations in the micro-
biology profile and drug-resistance patterns can further guide antibiotic selection. In
patients with indwelling biliary stents or with other potential for hospital-acquired
infection, it is reasonable to add antifungal coverage, and bile culture with Gram stain
should be obtained when possible to guide the antimicrobial regimen.9,33

Box 3
Severity grading

 Grade I
 Responds to initial medical management
 Grade II
 Does not respond to initial medical treatment but without evidence of organ dysfunction
 Grade III
 Acute cholangitis associated with evidence of organ dysfunction defined as follows:
- Hypotension requiring pressor use
- Altered mental status
- PaO2/FiO2 ratio less than 300
- Acute kidney injury
- Prothrombin time–international normalized ratio greater than 1.5
- Thrombocytopenia

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180 Sulzer & Ocuin

Drainage Procedures
Biliary drainage is recommended for all but the mildest cases of acute cholangitis that
respond effectively to antibiotics and supportive care. Drainage can be accomplished
endoscopically, percutaneously, or surgically. In addition to improvements in care of
the septic patient, advances in endoscopic biliary drainage have been credited with
the decrease in mortality from acute cholangitis.40

Endoscopic Retrograde Cholangiopancreatography


Endoscopic transpapillary biliary drainage should be first-line therapy for decompres-
sion in acute cholangitis. This can be accomplished by endoscopic biliary stenting or
placement of a nasobiliary tube. Several studies have demonstrated clinical equiva-
lence between these 2 techniques but increased patient discomfort and greater elec-
trolyte abnormalities in patients who underwent nasobiliary drainage.41,42 Advantages
of the nasobiliary approach include continued monitoring of bile output and ability for
flushing of purulent bile. Endoscopic biliary stenting involves placement of a 7-Fr to
10-Fr plastic stent after selective biliary cannulation to provide internal drainage.
This can be performed alone as a drainage procedure or with other interventions to
clear the bile duct of stones in cases of choledocholithiasis.40
Endoscopic sphincterotomy, commonly performed for stone extraction, can be
used as an adjunct to stent placement. When performed before large-bore stent
placement, sphincterotomy can possibly prevent occlusion of the pancreatic duct
and had been suggested to help prevent post-ERCP pancreatitis. Studies have failed
to demonstrate any difference unless multiple stents are required; however, with post-
ERCP pancreatitis rates of 3% to 4% following ERCP whether sphincterotomy was
performed or not.43 Sphincterotomy when performed at the time of biliary drainage
can decrease the duration of symptoms and hospital stay.44 A major concern with per-
forming endoscopic sphincterotomy is bleeding. The combination of severe sepsis,
biliary obstruction, and hepatic dysfunction in acute cholangitis can lead to increased
rates of hemorrhage following sphincterotomy.45 This increased risk has been demon-
strated in the absence of any associated coagulopathy.46 The Tokyo Guidelines
recommend against sphincterotomy in severe acute cholangitis, reserving sphincter-
otomy and stone extraction combined with biliary drainage for patients with mild or
moderate disease.40
Percutaneous transhepatic cholangiography
Percutaneous transhepatic cholangiography (PTC) is an additional safe and effective
technique for biliary drainage. It is currently considered second-line therapy after
failed ERCP, in the setting of surgically altered anatomy, or when a therapeutic endo-
scopist is not available.47 Procedural success has been reported at 95% with dilated
hepatic ducts and at 70% with nondilated ducts. Internal drainage and stone removal
have technical success rates of 90% following successful cannulation.48 Complica-
tions of PTC, including sepsis, hemorrhage, peritonitis, and pancreatitis, have been re-
ported in 1.2% to 2.5% of patients.49

Endoscopic Ultrasound–Guided Biliary Drainage


In cases when endoscopic access to the ampulla is not possible, either from altered
surgical anatomy or failed cannulation, an alternative to ERCP is endoscopic
ultrasound–guided biliary drainage (EUS-BD). This approach has been used to
attempt to limit the potential complications associated with PTC. EUS-BD can be
accomplished in several ways, including transgastric or transjejunal intrahepatic biliary
drainage, transduodenal or transgastric extrahepatic biliary drainage, or EUS-guided

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Cholangitis 181

antegrade stenting. The multiple approaches can be tailored to the patient’s pathol-
ogy. Meta-analysis of EUS-BD studies demonstrates a high technical and functional
success rate. Importantly, a success rate of more than 90% was achieved in high-
volume centers following failed ERCP.50 The procedure is associated with an adverse
event rate of 25%, with hemorrhage and bile leak being the most common morbidities.
Other serious complications have been reported, including perforation and sepsis. It is
therefore recommended to reserve EUS-BD for cases in which ERCP has failed, and it
should be performed only by a therapeutic endoscopist trained in the technique.20,40

Surgical Drainage
Open surgical drainage was once the mainstay of treatment of biliary obstruction and
cholangitis, but currently has no role in the treatment of severe acute cholangitis. A
randomized trial by Lai and colleagues51 that compared ERCP with surgical decom-
pression demonstrated a significantly higher rate of complications (66% vs 34%)
and mortality (32% vs 10%) in the surgical drainage group. Endoscopic and percuta-
neous biliary drainage have since remained first-line and second-line therapeutic
choices, with open surgical drainage as a last resort. Recently there has been an
increased interest in early laparoscopic common duct exploration with cholecystec-
tomy.52 Studies have demonstrated feasibility of this approach, although current rec-
ommendations reserve this approach only for nonsevere acute cholangitis.53

Drainage in the Setting of Surgically Altered Anatomy


Patients with surgically altered anatomy, such as after a Roux-en-Y gastric bypass,
present a unique challenge for nonsurgical drainage of the biliary tree. Several ap-
proaches have been devised to circumvent the altered anatomy, including balloon
enteroscopy–assisted ERCP, EUS-BD, and transgastric ERCP. Balloon
enteroscopy–assisted ERCP is the first-line recommendation in the Tokyo Guide-
lines.40 PTC, EUS-BD, and laparoscopic common bile duct exploration can provide
additional techniques when there is no available therapeutic endoscopist or when
balloon enteroscopy–assisted ERCP fails.

SUMMARY

A thorough understanding of the etiology and pathophysiology of acute cholangitis


coupled with utilization of modern diagnostic schema can assist the practitioner in
making this urgent diagnosis in an accurate and timely fashion. Furthermore, evolving
methods of biliary drainage add to the armamentarium available to prevent mortality in
this potentially lethal disease. Further ongoing refinements of these diagnostic and
prognostic criteria will continue to aid in targeted intervention and reduction in patient
morbidity and mortality.

REFERENCES

1. Lipsett PA, Pitt HA. Acute cholangitis. Front Biosci 2003;8:s1229–39.


2. Andrew DJ, Johnson SE. Acute suppurative cholangitis, a medical and surgical
emergency. A review of ten years experience emphasizing early recognition.
Am J Gastroenterol 1970;54(2):141–54.
3. Shimada H, Nakagawara G, Kobayashi M, et al. Pathogenesis and clinical fea-
tures of acute cholangitis accompanied by shock. Jpn J Surg 1984;14(4):269–77.
4. Reynolds BM, Dargan EL. Acute obstructive cholangitis; a distinct clinical syn-
drome. Ann Surg 1959;150(2):299–303.

Descargado para TISAL S.A. (bibliotecamedica@tisal.cl) en Information Technology in Health SA de ClinicalKey.es por Elsevier en
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182 Sulzer & Ocuin

5. Buyukasik K, Toros AB, Bektas H, et al. Diagnostic and therapeutic value of ERCP
in acute cholangitis. ISRN Gastroenterol 2013;2013:191729.
6. Leung JW, Ling TK, Chan RC, et al. Antibiotics, biliary sepsis, and bile duct
stones. Gastrointest Endosc 1994;40(6):716–21.
7. Ahmed M. Acute cholangitis - an update. World J Gastrointest Pathophysiol 2018;
9(1):1–7.
8. Kimura Y, Takada T, Kawarada Y, et al. Definitions, pathophysiology, and epide-
miology of acute cholangitis and cholecystitis: Tokyo Guidelines.
J Hepatobiliary Pancreat Surg 2007;14(1):15–26.
9. Reuken PA, Torres D, Baier M, et al. Risk factors for multi-drug resistant patho-
gens and failure of empiric first-line therapy in acute cholangitis. PLoS One
2017;12(1):e0169900.
10. Lübbert C, Wendt K, Feisthammel J, et al. Epidemiology and resistance patterns
of bacterial and fungal colonization of biliary plastic stents: a prospective cohort
study. PLoS One 2016;11(5):e0155479.
11. Gigot JF, Leese T, Dereme T, et al. Acute cholangitis. Multivariate analysis of risk
factors. Ann Surg 1989;209(4):435–8.
12. Beltrán MA. Mirizzi syndrome: history, current knowledge and proposal of a
simplified classification. World J Gastroenterol 2012;18(34):4639–50.
13. Kimura Y, Takada T, Strasberg SM, et al. TG13 current terminology, etiology, and
epidemiology of acute cholangitis and cholecystitis. J Hepatobiliary Pancreat Sci
2013;20(1):8–23.
14. Desai K, Wermers JD, Beteselassie N. Lemmel syndrome secondary to duodenal
diverticulitis: a case report. Cureus 2017;9(3):e1066.
15. Kang HS, Hyun JJ, Kim SY, et al. Lemmel’s syndrome, an unusual cause of
abdominal pain and jaundice by impacted intradiverticular enterolith: case
report. J Korean Med Sci 2014;29(6):874–8.
16. Lim JH. Liver flukes: the malady neglected. Korean J Radiol 2011;12(3):269–79.
17. Wada K, Takada T, Kawarada Y, et al. Diagnostic criteria and severity assessment
of acute cholangitis: Tokyo guidelines. J Hepatobiliary Pancreat Surg 2007;14(1):
52–8.
18. Kiriyama S, Kozaka K, Takada T, et al. Tokyo guidelines 2018: diagnostic criteria
and severity grading of acute cholangitis (with videos). J Hepatobiliary Pancreat
Sci 2018;25(1):17–30.
19. Boey JH, Way LW. Acute cholangitis. Ann Surg 1980;191(3):264–70.
20. Ramchandani M, Pal P, Reddy DN. Endoscopic management of acute cholangitis
as a result of common bile duct stones. Dig Endosc 2017;29(Suppl 2):78–87.
21. Kiriyama S, Takada T, Hwang TL, et al. Clinical application and verification of the
TG13 diagnostic and severity grading criteria for acute cholangitis: an interna-
tional multicenter observational study. J Hepatobiliary Pancreat Sci 2017;24(6):
329–37.
22. Takada T, Strasberg SM, Solomkin JS, et al. TG13: updated Tokyo guidelines for
the management of acute cholangitis and cholecystitis. J Hepatobiliary Pancreat
Sci 2013;20(1):1–7.
23. Watanapa P. Recovery patterns of liver function after complete and partial surgi-
cal biliary decompression. Am J Surg 1996;171(2):230–4.
24. Ker CG, Chen JS, Lee KT, et al. Assessment of serum and bile levels of CA19-9
and CA125 in cholangitis and bile duct carcinoma. J Gastroenterol Hepatol 1991;
6(5):505–8.
25. Albert MB, Steinberg WM, Henry JP. Elevated serum levels of tumor marker
CA19-9 in acute cholangitis. Dig Dis Sci 1988;33(10):1223–5.

Descargado para TISAL S.A. (bibliotecamedica@tisal.cl) en Information Technology in Health SA de ClinicalKey.es por Elsevier en
septiembre 17, 2019. Para uso personal exclusivamente. No se permiten otros usos sin autorización. Copyright ©2019. Elsevier Inc.
Todos los derechos reservados.
Cholangitis 183

26. Korkmaz M, Ünal H, Selçuk H, et al. Extraordinarily elevated serum levels of CA


19-9 and rapid decrease after successful therapy: a case report and review of
literature. Turk J Gastroenterol 2010;21(4):461–3.
27. Umefune G, Kogure H, Hamada T, et al. Procalcitonin is a useful biomarker to pre-
dict severe acute cholangitis: a single-center prospective study. J Gastroenterol
2017;52(6):734–45.
28. Shinya S, Sasaki T, Yamashita Y, et al. Procalcitonin as a useful biomarker for
determining the need to perform emergency biliary drainage in cases of acute
cholangitis. J Hepatobiliary Pancreat Sci 2014;21(10):777–85.
29. Shah T, Zfass A. Predicting cholangitis with procalcitonin: procrastinate or pro-
cedure? Dig Dis Sci 2018. https://doi.org/10.1007/s10620-018-5098-0.
30. Lee YS, Cho KB, Park KS, et al. Procalcitonin as a decision-supporting marker of
urgent biliary decompression in acute cholangitis. Dig Dis Sci 2018;63(9):
2474–9.
31. Solomkin JS, Mazuski JE, Bradley JS, et al. Diagnosis and management of
complicated intra-abdominal infection in adults and children: guidelines by the
Surgical Infection Society and the Infectious Diseases Society of America. Clin
Infect Dis 2010;50(2):133–64.
32. Kelly AM. Clinical impact of blood cultures taken in the emergency department.
J Accid Emerg Med 1998;15(4):254–6.
33. Gomi H, Solomkin JS, Schlossberg D, et al. Tokyo guidelines 2018: antimicrobial
therapy for acute cholangitis and cholecystitis. J Hepatobiliary Pancreat Sci
2018;25(1):3–16.
34. Arai K, Kawai K, Kohda W, et al. Dynamic CT of acute cholangitis: early inhomo-
geneous enhancement of the liver. AJR Am J Roentgenol 2003;181(1):115–8.
35. Meeralam Y, Al-Shammari K, Yaghoobi M. Diagnostic accuracy of EUS compared
with MRCP in detecting choledocholithiasis: a meta-analysis of diagnostic test
accuracy in head-to-head studies. Gastrointest Endosc 2017;86(6):986–93.
36. de Lédinghen V, Lecesne R, Raymond JM, et al. Diagnosis of choledocholithiasis:
EUS or magnetic resonance cholangiography? A prospective controlled study.
Gastrointest Endosc 1999;49(1):26–31.
37. Chen YI, Martel M, Barkun AN. Choledocholithiasis: should EUS replace MRCP in
patients at intermediate risk? Gastrointest Endosc 2017;86(6):994–6.
38. Okamoto K, Takada T, Strasberg SM, et al. TG13 management bundles for acute
cholangitis and cholecystitis. J Hepatobiliary Pancreat Sci 2013;20(1):55–9.
39. Mayumi T, Okamoto K, Takada T, et al. Tokyo guidelines 2018: management bun-
dles for acute cholangitis and cholecystitis. J Hepatobiliary Pancreat Sci 2018;
25(1):96–100.
40. Mukai S, Itoi T, Baron TH, et al. Indications and techniques of biliary drainage for
acute cholangitis in updated Tokyo guidelines 2018. J Hepatobiliary Pancreat Sci
2017;24(10):537–49.
41. Lee DW, Chan AC, Lam YH, et al. Biliary decompression by nasobiliary catheter
or biliary stent in acute suppurative cholangitis: a prospective randomized trial.
Gastrointest Endosc 2002;56(3):361–5.
42. Park SY, Park CH, Cho SB, et al. The safety and effectiveness of endoscopic
biliary decompression by plastic stent placement in acute suppurative cholangi-
tis compared with nasobiliary drainage. Gastrointest Endosc 2008;68(6):
1076–80.
43. Tarnasky PR, Cunningham JT, Hawes RH, et al. Transpapillary stenting of prox-
imal biliary strictures: does biliary sphincterotomy reduce the risk of postproce-
dure pancreatitis? Gastrointest Endosc 1997;45(1):46–51.

Descargado para TISAL S.A. (bibliotecamedica@tisal.cl) en Information Technology in Health SA de ClinicalKey.es por Elsevier en
septiembre 17, 2019. Para uso personal exclusivamente. No se permiten otros usos sin autorización. Copyright ©2019. Elsevier Inc.
Todos los derechos reservados.
184 Sulzer & Ocuin

44. Hui CK, Lai KC, Wong WM, et al. A randomised controlled trial of endoscopic
sphincterotomy in acute cholangitis without common bile duct stones. Gut
2002;51(2):245–7.
45. Lee MH, Tsou YK, Lin CH, et al. Predictors of re-bleeding after endoscopic hemo-
stasis for delayed post-endoscopic sphincterotomy bleeding. World J Gastroen-
terol 2016;22(11):3196–201.
46. Freeman ML. Complications of endoscopic retrograde cholangiopancreatogra-
phy: avoidance and management. Gastrointest Endosc Clin N Am 2012;22(3):
567–86.
47. Itoi T, Tsuyuguchi T, Takada T, et al. TG13 indications and techniques for biliary
drainage in acute cholangitis (with videos). J Hepatobiliary Pancreat Sci 2013;
20(1):71–80.
48. Saad WE, Wallace MJ, Wojak JC, et al. Quality improvement guidelines for percu-
taneous transhepatic cholangiography, biliary drainage, and percutaneous chol-
ecystostomy. J Vasc Interv Radiol 2010;21(6):789–95.
49. Burke DR, Lewis CA, Cardella JF, et al. Quality improvement guidelines for percu-
taneous transhepatic cholangiography and biliary drainage. J Vasc Interv Radiol
2003;14(9 Pt 2):S243–6.
50. Wang K, Zhu J, Xing L, et al. Assessment of efficacy and safety of EUS-guided
biliary drainage: a systematic review. Gastrointest Endosc 2016;83(6):1218–27.
51. Lai EC, Mok FP, Tan ES, et al. Endoscopic biliary drainage for severe acute chol-
angitis. N Engl J Med 1992;326(24):1582–6.
52. Sun Z, Zhu Y, Zhu B, et al. Controversy and progress for treatment of acute chol-
angitis after Tokyo Guidelines (TG13). Biosci Trends 2016;10(1):22–6.
53. Atstupens K, Plaudis H, Fokins V, et al. Safe laparoscopic clearance of the com-
mon bile duct in emergently admitted patients with choledocholithiasis and chol-
angitis. Korean J Hepatobiliary Pancreat Surg 2016;20(2):53–60.

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septiembre 17, 2019. Para uso personal exclusivamente. No se permiten otros usos sin autorización. Copyright ©2019. Elsevier Inc.
Todos los derechos reservados.

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