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Canadian Association of Radiologists Journal xx (2013) 1e6

www.carjonline.org

Abdominal Imaging / Imagerie abdominale

Dilatation of the Bile Duct in Patients After Cholecystectomy:


A Retrospective Study
David Landry, MD, B Enga, An Tang, MD, FRCPCa, Jessica Murphy-Lavallee, MD, FRCPCa,*,
Luigi Lepanto, MD, FRCPCa, Jean-Sebastien Billiard, MDa, Damien Olivie, MDa,
Marie-Pierre Sylvestre, PhDb
a
Department of Radiology, University of Montreal and CRCHUM, H^opital Saint-Luc, Montreal, Quebec, Canada
b
Biostatistics Services, University of Montreal Hospital Research Center (CRCHUM), Centre de recherche du CHUM, Montreal, Quebec, Canada

Abstract

Purpose: Retrospective assessment of impact of cholecystectomy, age, and sex on bile duct (BD) diameter.
Materials and Methods: We retrospectively reviewed abdominal contrast-enhanced multidetector computed tomography and laboratory
reports of 290 consecutive patients (119 men; mean age, 55.9 years) who presented without cholestasis to the emergency department of our
institution between June 2009 and August 2010. BD diameters were measured in 3 locations, by 2 independent observers, twice, at 1-month
intervals. Reproducibility and agreement were evaluated by intraclass correlation coefficients and Bland-Altman analyses. The effects of
cholecystectomy, age, and sex on BD diameter were analysed with linear mixed models.
Results: BD diameter inter-reader reproducibility and agreement were excellent at the level of the right hepatic artery (intraclass correlation
coefficient, 0.94). Sixty-one patients (21.0%) had a history of cholecystectomy. Among them, the 95th percentile of BD diameters at hepatic
artery level was 7.9 mm (<50 years) and 12.3 mm (50 years). Among those without cholecystectomy, BD diameter was 6.2 mm (<50
years) and 7.7 mm (50 years). Cholecystectomy was associated with significantly larger BD diameters in both age groups (P < .001). Older
age was associated with larger BD diameters (P .004). Sex had no impact on BD diameter (P .842).
Conclusion: Patients after cholecystectomy may present with an enlarged BD unrelated to cholestasis. The BD diameter increases with age.
Clinicians should rely on cholecystectomy status, age, and laboratory results to determine needs of further investigation.

Resume


Objet: Evaluation retrospective de lincidence de la cholecystectomie, de l^age et du sexe sur le diametre du canal choledoque.
Materiel et methodes: De facon retrospective, nous avons revise les rapports de laboratoire et de tomodensitometrie abdominale a coupes
multiples avec contraste de 290 patients consecutifs (119 hommes, ^age moyen de 55,9 ans) qui se sont presentes sans cholestase au service
durgence de notre etablissement entre juin 2009 et ao^ut 2010. Le diametre du choledoque a ete mesure a trois endroits par deux observateurs
independants, deux fois a un mois dintervalle. La reproductibilite et la concordance ont ete evaluees au moyen du coefficient de correlation
intraclasse et danalyses de Bland-Altman. Des modeles lineaires mixtes ont ete utilises pour analyser les effets de la cholecystectomie, de
l^age et du sexe sur le diametre du choledoque.
Resultats: La reproductibilite et la concordance interevaluateur du diametre du choledoque etaient excellentes au niveau de lartere
hepatique droite (coefficient de correlation intercalaire de 0,94). Parmi les patients, 61 (21 %) presentaient des antecedents de chol-
ecystectomie. Le 95e centile du diametre du canal choledoque au niveau de lartere hepatique etait de 7,9 mm (moins de 50 ans) et de
12,3 mm (50 ans ou plus) chez ces patients. Chez les patients qui navaient pas subi de cholecystectomie, le diametre du choledoque etait de
6.2 mm (moins de 50 ans) et de 7,7 mm (50 ans ou plus). Des diametres nettement superieurs pour les deux groupes d^age (P < 0,001) etaient
associes a cette intervention. Les patients plus ^ages presentaient des diametres plus grands (P 0,004). Le sexe navait aucune incidence sur
le diametre du canal choledoque (P 0,842).

* Address for correspondence: Jessica Murphy-Lavallee, MD, FRCPC, E-mail address: jessica.murphy-lavallee.chum@ssss.gouv.qc.ca (J.
Department of Medical Imaging, University of Montreal and CRCHUM, Murphy-Lavallee).
H^
opital Saint-Luc, 1058 rue Saint-Denis, Montreal, Quebec H2X 3J4,
Canada.

0846-5371/$ - see front matter 2013 Canadian Association of Radiologists. All rights reserved.
http://dx.doi.org/10.1016/j.carj.2012.09.004
2 D. Landry et al. / Canadian Association of Radiologists Journal xx (2013) 1e6

Conclusion: Le choledoque des patients qui ont subi une cholecystectomie peut ^etre plus large sans quil ny ait de lien avec une cholestase.
Le diametre augmente toutefois avec l^age. Les cliniciens devraient se fier a letat de la cholecystectomie, a l^age et aux resultats de lab-
oratoire pour determiner si une investigation plus poussee est necessaire.
2013 Canadian Association of Radiologists. All rights reserved.

Key Words: Bile duct; Cholecystectomy; Cholestasis; Dilatation

It is a widely accepted concept that the bile duct (BD) of both total blood bilirubin level (reference range, 7-23 mmol/
increases in diameter after cholecystectomy. However, there is L) and blood levels of alkaline phosphatase (reference range,
little consensus in the available literature on this subject. The 36-110 IU), obtained within 24 hours of the contrast-enhanced
opinion dates back to the late 19th century, when Oddi [1] MDCT. Patients were not included if they had proven liver or
postulated that the choledochus dilates after removal of the pancreatic malignancy or disease. Patients chronically taking
gallbladder to serve as a reservoir for bile [2]. This phenom- opioid medication and those who had received morphine
enon was explained by the hypothesis that one function of the before the computed tomography (CT) were also excluded. A
gallbladder is to act as a tension bulb to maintain stable bile total of 354 patients were initially recruited, of whom, 29 had
pressure when the sphincter of Oddi is closed [3]. Hence, once liver cancer, 6 had pancreatic cancer, 5 had a biliary stent, 10
removed, the pressure gradients would be applied directly to had cholecystitis, 4 had liver transplantations, 2 had benefited
the BD, which would dilate in response. Subsequent research from a Whipple surgery, and 8 had received morphine before
on animals and postmortem studies on humans seemed to imaging. Thus, these 64 patients were excluded.
validate this hypothesis [2e5]. However, the advent of sono-
graphic technology and subsequent analyses of the biliary tree Scanning Technique
in the mid-20th century provided inconsistent and often
contradictory evidence [4,6e14]. Abdominal CT studies were performed on 64-row
Radiologists can be confronted with unanticipated dilated detector MDCT scanners (Philips Brillance 64 [Philips
extrahepatic BDs in patients in whom the necessity for further Healthcare, Celveland, OH]; Somatom Sensation 64
cholestatic investigation is unclear. Hence, knowing whether it [Siemens Healthcare, Forchheim, Germany]). The single
is expected that patients who had a cholecystectomy, who do portal venous-phase protocol consisted of images of the
not present with cholestasis, have more prominent extrahe- abdomen and pelvis acquired by using a 2.5-mm collimation
patic BDs than the general population would be of value and 70 seconds after intravenous injection of a bolus of 100 mL
help prevent unnecessary further, potentially invasive and iohexol contrast medium (Omnipaque 300; Bracco, Milan,
costly, investigation of the biliary system. Italy) with a power injector at a rate of 3.0 mL/s.
The purpose of this study was to retrospectively assess the
Image Evaluation
impact of cholecystectomy status, age, and sex on the BD
diameter by measuring the BD diameter in patients who
The diameters of the extrahepatic BD were measured at 3
underwent an abdominal multidetector computed tomog-
distinct locations: immediately superior to the pancreas
raphy (MDCT) for reasons unrelated to cholestasis.
(dpancreas), adjacent to the right hepatic artery (dartery), and
immediately below the first hepatic hilar bifurcation (dbifurc)
Materials and Methods (Figure 1). To minimize interobserver variations, all mea-
surements were taken only on axial images, perpendicular to
Our institutional review board approved this retrospective the cephalocaudal direction of the BD. The measurements
study and waived the need for informed consent. were performed independently by a radiology resident in his
fourth year of training (reader A [D.L.]) and a fellowship-
Study Population trained body-imaging radiologist with 6 years of experience
(reader B [J.M.L.]) by using our picture archiving and
We reviewed the laboratory results and contrast-enhanced communication system (AGFA Impax ES; AGFA Technical
MDCT images of 290 consecutive patients admitted to the Imaging Systems, Ridgefield Park, NJ). Both readers took the
emergency department of a tertiary care university-affiliated measurements twice, at a 1-month interval and were blinded to
hospital between June 2009 and August 2010. A systematic their previous reported values as well as the values taken by their
electronic chart review for each patient was conducted. colleague. This permitted us to evaluate inter- and intrareader
Patients were included if they were (a) 18 years old or older, reproducibility and agreement.
(b) had a contrast-enhanced abdomen MDCT, (c) presented
with symptoms unrelated to cholestasis (eg, appendicitis Statistical Analyses
workup, suspected diverticulitis, suspected occlusion or sub-
occlusion, epigastric discomfort, vague abdominal pain), (d) Quantitative variables were summarized as means (stan-
had proven absence of cholestasis by normal laboratory values dard deviations [SD]), and categorical variables were
Bile duct diameter and cholecystectomy / Canadian Association of Radiologists Journal xx (2013) 1e6 3

Figure 1. Transverse portal venous phase 64-row computed tomography image of a 75-year-old male patient who presented with right hydronephrosis caused
by a ureteral lithiasis. The bile duct diameter (arrows) was measured at the level of the pancreas (dpancreas) (A), at the crossing of the hepatic artery (dartery) (B),
and below the first hepatic hilar bifurcation (dbifurc) (C).

summarized as proportions and percentages. The sample size ICCs of inter- and intrareader reproducibility are summa-
of 290 patients was calculated to be able to detect a 1-mm rized in Tables 2 and 3, respectively.
difference in BD diameter with a power of .98 and a type I
error (alpha) of .01. Because previous studies reported an Inter-reader Agreement
average prevalence for cholecystectomy of 25% (with an SD
of 1.67% reported in 1 study) [15e19], a total of 290 patients Bland-Altman graphs were obtained for measurements at
was necessary, with 62 patients after cholecystectomy and each location (Figure 2) and revealed agreement only at the
228 controls (by using t test for unequal samples, non- level of the right hepatic artery. Indeed, there were only
matched pairs [20]). 93.4% and 91.4% of the differences contained within the
Inter- and intrareader reproducibilities were assessed limits of agreements at the suprapancreatic and hepatic
by intraclass correlation coefficients (ICC). Because the bifurcation levels, respectively. Further, when accepting
subjects and readers of our study were randomly chosen from a maximum difference of 2.0 mm between each readers
a bigger pool of individuals, a 2-way underlying analysis of measurements to be within boundaries of agreement, agree-
variance model was used [21]. An ICC value greater than ment was also obtained only at the level of the hepatic artery.
0.75 was interpreted as excellent reproducibility, values of Summarized in Table 4 are the averages of differences in
0.40-0.75 as fair to good reproducibility, and values of <0.40 measurements obtained by the 2 readers and the interval that
as poor reproducibility [22]. Agreement between the 2 contains 95% (2 SDs) of the differences in measurements.
readers regarding the BD diameters was assessed by Bland- The results obtained at the level of the intrahepatic bifurca-
Altman analysis to compute the limits of agreement [23,24]. tion yielded an average difference in measurements of
Significance was set at P < .05 for all tests. All statistical 1.1 mm, with a 95% confidence interval excluding zero.
analyses were performed by using statistical software
(R version 2.13.0 for Windows, Vienna, Austria; and pack- Effect of Cholecystectomy, Age, and Sex
ages irr v.0.83 and nlme 3.1-102 [25,26]). The effects of
cholecystectomy, age (dichotomized as <50 years of age and Because Bland-Altman analysis of the measurements
50 years of age), and sex on BD diameter were analysed between the 2 readers demonstrated that agreement was only
with linear mixed model analysis. This alllowed us to achieved at the level of the right hepatic artery, this level was
account for the repeated measurements by the 2 readers as selected to evaluate variations in BD diameters. There was
well as the effect of other potential covariates. a statistically significant increase in BD diameters in patients
with a history of cholecystectomy; on average, BD diameter
Results was 2.3 mm larger when compared with patients without

Study Population Table 1


Population demographics
A total of 290 patients (119 men; mean [SD] age, 55.9  Postcholecystectomy No cholecystectomy
14.5 years [range, 30-80 years]) comprised our results. Sixty- (n 61) (n 229)
one patients (21.0%) previously underwent cholecystectomy. Clinical
The demographics for each group are summarized in Table 1. Mean age (years), SD 64  12.5 54  14.3
Men, no. (%) 17 (28) 102 (45)
Laboratory
Inter- and Intrareader Reproducibility Total bilirubin level, 9.6  3.9 10.5  7.9
mmol/L
The inter- and intrareader reproducibility of BD diameter Alkaline phosphatase 77  16.1 68  21.7
measurements was excellent at the suprapancreatic and level, IU/L
hepatic artery levels, and good at the bifurcation level. The SD standard deviation.
4 D. Landry et al. / Canadian Association of Radiologists Journal xx (2013) 1e6

Table 2 clinician, and prevent unnecessary further, potentially invasive


Inter-reader reproducibility and costly, investigation of the biliary system.
Measurement level Suprapancreatic Hepatic artery Bifurcation The interest in demonstrating an impact of the diameter of
ICC 0.90 0.94 0.70 extrahepatic BDs in patients with a history of cholecystectomy
95% CI 0.87-0.92 0.92-0.95 0.07 to 0.87 has been present for many decades. In 1957, Anderson [6]
P value <.001 <.001 .034 published the results of a study conducted on 125 patients,
CI confidence interval; ICC intraclass correlation coefficients. with and without a history of cholecystectomy, who had an
intravenous cholecystography. Although technical difficulties
cholecystectomy (P < .001). A statistically significant
were encountered in some patients, he raised doubts on the
increase in BD diameters with increasing age was also found
long-held belief that the extrahepatic BD dilates after gall-
(P .004) (Figure 3). A history of cholecystectomy was
bladder removal. Subsequently, Mueller et al [9] conducted
associated with increased BD diameters, regardless of patient
one of the first US studies on the common BD diameter in 40
age (P < .001). Among patients with a history of cholecys-
patients before and after cholecystectomy for up to 20 months
tectomy, the 95th percentile of BD diameters at the hepatic
after surgery. Of these patients, only 1 patient presented with
artery level was 7.9 mm (<50 years) and 12.3 mm (50
persistent dilatation of the common BD. The patient was 85
years); among those without a history of cholecystectomy, it
years old, and the BD dilatation was attributed to physiologic
was 6.2 mm (<50 years) and 7.7 mm (50 years). Sex was
senile loss of muscular tone of the duct. The remaining
not found to be associated with statistically significant vari-
patients maintained or recovered normal-size BDs. Later on,
ations on BD diameter at any of the 3 levels investigated
many researchers reported similar findings when using US for
(P .842). The effect of covariates on BD diameters are
evaluation of the biliary tree.
summarized in Table 5.
Recently, Chawla et al [14] analysed common BD diam-
eter on chest computer tomodensitometry in patients who
Discussion presented for unrelated reasons and without cholestasis
(either clinically or via laboratory findings). They reported
It is widely accepted among radiologists that the extrahe- a series of 40 matched pairs and found that significant
patic BD dilates after cholecystectomy. However, the literature dilatation of the common BD was associated with prior
offers little consensus in this regard. We conducted our study to cholecystectomy. A review of the literature conducted in
investigate if cholecystectomy status, age, and sex had 1997 concluded that, although there is no consensus in the
measurable impacts on the diameter of the extrahepatic BD. scientific community, literary evidence suggests that BD
Most studies to date have investigated BD diameters in patients dilatation occurs in a majority of patients with a history of
planned to undergo cholecystectomy for cholecystitis cholecystectomy [12].
[7,8,10,11,13,27,28]. This approach suffers from selection In our study, a history of cholecystectomy was indeed
bias and cannot show if the effects on the BD diameter result associated with larger BD diameters in patients without
from cholecystectomy or the underlying obstruction of the BD. cholestasis. Measurements of the BD at 3 distinct locations by
Furthermore, in everyday practice, the question is not whether 2 readers on separate occasions provided our study with the
the BD has dilated after cholecystectomy; the most pertinent possibility to evaluate reproducibility as well as agreement
information is to know whether it is expected that patients who within each reader and between them. Analysis with ICCs
had a cholecystectomy who do not present with cholestasis showed that reproducibility of measurements obtained by each
have more prominent extrahepatic BDs than the general pop- reader was best at the level where the BD crosses the right
ulation. Indeed, the radiologist is often confronted with hepatic artery. Further investigation by using Bland-Altman
unanticipated extrahepatic BDs of generous calibre on graphs demonstrated that agreement was only reached at this
abdominal computed tomodensitometry or abdominal ultra- level. This observation is explained by the fact that the precise
sound (US) performed for reasons unrelated to cholestasis or location for measurement of the BD is achieved only at
biliary pathology in the absence of cholestasis (proven clini- a location that can be precisely identified by both readers.
cally and paraclinically). Knowing that a higher percentage of Because the BD crosses the path of the right hepatic artery at
patients who benefited from cholecystectomy will have almost 90 degrees, it yields a very unique point where the
prominent extrahepatic BDs without underlying biliary diameter can be obtained reliably. This is the classically rec-
pathology would reassure both the radiologist and the ommended level to measure the BD, both on US and CTs. Our

Table 3
Intrareader reproducibility
Reader A Reader B
Measurement level Suprapancreatic Hepatic artery Bifurcation Suprapancreatic Hepatic artery Bifurcation
ICC 0.97 1.00 0.92 0.94 0.98 0.83
95% CI 0.96-0.97 0.99-1.00 0.90-0.94 0.93-0.95 0.97-0.98 0.79-0.87
P value <.001 <.001 <.001 <.001 <.001 <.001
CI confidence interval; ICC intraclass correlation coefficient.
Bile duct diameter and cholecystectomy / Canadian Association of Radiologists Journal xx (2013) 1e6 5

Table 4
Mean of differences in measurements between readers
Measurement level Suprapancreatic Hepatic artery Bifurcation
Mean, mm 0.14 0.05 1.01
95% CI for the mean 0.01-0.28 0.15 to 0.06 0.90-1.13
difference, mm
Limits of agreement 2.3 to 2.6 1.9 to 1.8 1.2 to 3.2
CI confidence interval.

[6,9,12,14,29e33]. There was no effect of sex on the BD


diameter in our population, similar to previous studies [9,14].
Contrary to many previous studies, our study did not
attempt to determine if the extrahepatic BDs dilate in a given
patient after cholecystectomy. Such a study would be quite
difficult to conduct because patients who initially benefit from
imaging of the BDs in these instances could have some degree
of BD obstruction, hence the need for cholecystectomy. As
a result, the causality link between cholecystectomy and
dilated BDs is polluted by the possibility that BDs were
already dilated at presentation because of the initial pathology.
Indeed, in a few studies [6,8], some patients who were
recruited initially had BD diameters that fell within the normal
range and did not show an increase in calibre after cholecys-
tectomy. However, in other studies [9,10], the patients initially
presented with increased BD diameter. In everyday practice,
the radiologist does not need to know whether a patient will
eventually have dilated BDs after cholecystectomy. Rather, the
imaging specialist is often confronted with dilated extrahe-
patic BDs in a patient who already has benefited from chole-
cystectomy. As our study has shown, a greater proportion of
patients with a history of cholecystectomy will possess dilated
extrahepatic BDs with no cholestasis and should thus not be
investigated further regarding this finding.
There are several limitations to our study. First, the retro-
spective design of this study is prone to selection bias. However,
given that our data were based on consecutive patients, this
reflects the patient population at our institution. Second, we have
not included patients who presented with cholestasis, nor did we
include patients who had not benefited from laboratory workup
shortly before or after imaging to prove absence of cholestasis.

Figure 2. Bland-Altman plots, showing the mean difference between readers


A and B, and limits of agreement (95% confidence interval, dotted lines) for
the bile duct diameter at the (A) suprapancreatic, (B) hepatic artery, and (C)
intrahepatic bifurcation levels.

study reinforces the importance of measuring the BD at this


level to ensure reproducibility and consistency in measure-
ments obtained by different readers.
Measurements of the BD at the level of the right hepatic
artery showed that, at all ages, patients with a history of
cholecystectomy had statistically significant larger diame-
ters. Furthermore, regardless of cholecystectomy status, Figure 3. A scatter plot of bile duct diameters at the right hepatic artery
increasing age was associated with increased BD diameter. plotted by age; a 95th percentile curve fit is plotted for postcholecystectomy
These observations are consistent with many previous studies and noncholecystectomy status.
6 D. Landry et al. / Canadian Association of Radiologists Journal xx (2013) 1e6

Table 5
Average diameters at level of hepatic arterya
Cholecystectomy Yes No
All 7.1  2.4; (2.4, 11.8) mm P < .001 4.8  1.2; (2.4, 7.2) mm P < 0.001
Age <50 years 50 years
All 4.5  1.0; (2.5, 6.5) mm P .004 5.1  2.1; (1.0, 9.2) mm P .004
Cholecystectomy 6.1  0.9; (4.3, 7.9) mm P < .001 7.3  2.5; (2.4, 12.2) mm P < .001
No cholecystectomy 4.3  0.9; (2.5, 6.1) mm P < .001 4.8  1.4; (2.1, 7.5) mm P < .001
Sex Women Men
All 5.2  1.9; (1.5, 8.9) mm P .842 4.9  1.8; (1.4, 8.4) mm P .842
Cholecystectomy 7.1  2.4; (2.4, 11.8) mm P < .001 7.2  2.5; (2.3, 12.1) mm P < .001
No cholecystectomy 4.6  1.2; (2.2, 7.0) mm P < .001 4.6  2.7; (1.9, 7.3) mm P < .001
SD standard deviation.
a
Results are reported as: result  repeatability coefficient (1.96 SD); (95% limits of agreement interval).

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