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International Journal of Surgery 12 (2014) 886e892

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International Journal of Surgery


journal homepage: www.journal-surgery.net

Original research

Management of intrahepatic stones: The role of subcutaneous


hepaticojejunal access loop. A prospective cohort study
Mohamed I. Kassem, Magdy A. Sorour*, Abdel-Hamid A. Ghazal, Hany M. El-Haddad,
Mohamed T. El-Riwini, Hassan A. El-Bahrawy
Department of Surgery, Faculty of Medicine, University of Alexandria, Egypt

h i g h l i g h t s

 Recurrence of stones occurs frequently after surgical removal of intrahepatic stones.


 BLong-term access routes involving the subparietal hepaticojejunal access loop for stone retrieval have been developed.
 The closed subcutaneous access loop offers the advantage of permanent access for removal of intrahepatic stones.
 The subcutaneous access loop permitted easy access to intrahepatic ducts without the needs for cutaneous stomas.

a r t i c l e i n f o a b s t r a c t

Article history: Background: Patients with intrahepatic stones usually present with recurrent cholangitis, biliary sepsis
Received 25 April 2014 and intrahepatic abscesses, may develop liver atrophy and may progress to cholangiocarcinoma. Treat-
Received in revised form ment of intrahepatic stones is difficult and the disease progresses in most patients even after adequate
6 July 2014
treatment. Surgical removal of stones has been the standard management but residual stones and stone
Accepted 16 July 2014
Available online 28 July 2014
recurrence occur frequently whatever the technique. Because of the need for repeated biliary instru-
mentation, long-term access routes involving percutaneous transhepatic cholangioscopic lithotripsy
(PTCSL), hepaticocutaneousjejunostomy (HCJ) and subparietal hepaticojejunal access loop to permit
Keywords:
Intrahepatic stones
stone retrieval or stricture dilatation have been developed. Purpose: The aim of this work was to
Hepaticojejunostomy evaluate the outcome of subcutaneous hepaticojejunal access loop in the management of intrahepatic
Subcutaneous jejunal access loop stones. Patients and methods: Between January 2009 and January 2013, 42 patients with intrahepatic
stones underwent surgical treatment at the Gastrointestinal Surgery Unit, Main Alexandria University
Hospital. Demographic data, details of operative findings, follow up details, and treatment of recurrent
stones were analyzed. After approval of local ethics committee, all patients included in the study were
informed well about the procedure and an informed written consent was obtained from every patient
before carrying the procedure. Results: Forty-two patients (17 males and 25 females) with intrahepatic
stones underwent surgery with construction of a subcutaneous hepaticojejunal access loop. Stones were
confined to the left lobe in 25 patients, the right lobe in 3 patients and bilobar in 14 patients. Associated
extrahepatic stones were found in 33 patients. Twenty-two patients had associated intrahepatic duct
strictures. Five patients with atrophy of segments II and III underwent hepatic resection at the time of
access loop formation. The mean operation time was 4.9 h and mean blood loss was 440 mL. Mean
postoperative hospital stay was 10 days. Wound infection was the commonest complication, occurring in
5 (12%) patients. There were no specific complications attributable to the construction of the access loop.
The subcutaneous access loop was used to gain access to the biliary tree in 28 patients with residual or
recurrent stones. A total of 55 procedures (range 1e5) were attempted with successful access achieved in
all cases and successful stone clearance in 21 of the 28 patients, and all of them were symptom free for at
least 12 months after the last procedure. Partial stone clearance was achieved in the remaining seven
patients. These seven patients had different degrees of biliary strictures. Conclusion: The subcutaneous
access loop offers the advantage of permanent access for the successful management of retained or re-
formed intrahepatic stones with minimal morbidity since it permitted easy access to intrahepatic ducts

* Corresponding author.
E-mail address: magdysorour@hotmail.com (M.A. Sorour).

http://dx.doi.org/10.1016/j.ijsu.2014.07.264
1743-9191/© 2014 Surgical Associates Ltd. Published by Elsevier Ltd. All rights reserved.
M.I. Kassem et al. / International Journal of Surgery 12 (2014) 886e892 887

using the conventional forward-viewing endoscope or the choledochoscope, without the additional
morbidity of a biliary-cutaneous fistula or transhepatic access.
© 2014 Surgical Associates Ltd. Published by Elsevier Ltd. All rights reserved.

1. Introduction University Hospital. Demographic data, details of operative find-


ings, follow-up details, and treatment of recurrent stones were
Intrahepatic stones are defined as calculi located proximal to the analyzed. Patients with predominant intrahepatic calculi were
confluence of the right and left hepatic ducts, irrespective of the included; those with associated extensive extrahepatic bile duct
coexistence of gallstones in the common bile duct and/or gall- calculi or secondary biliary cirrhosis were excluded.
bladder [1e3]. This disease is prevalent in East and Southeast Asian
countries and infrequent in Western population. [1,4e8].
In most cases, intrahepatic stones consist of calcium bilirubinate 4. Methods
(brown pigment stones), but contain more cholesterol than those in
either the common bile duct or the gallbladder. Almost pure A post-intervention prospective cohort study was designed to
cholesterol stones are sporadically reported [9,10]. The aetiology of include all patients with intrahepatic stones who underwent sur-
intrahepatic stones is not exactly known, although recurrent bac- gery for stone retrieval with construction of a subcutaneous hep-
terial infection (mixed infections:- Escherichia coli, Klebsiella, aticojejunal access loop.
Streptococcus fecalis, Clostridia, and Bacteroides), parasitic infesta- After approval of the local ethics committees of both the General
tion (Clonorchis sinensis or Ascaris lumbricoides), ethnic background, Surgery Department and the Alexandria Faculty of Medicine, all
and stasis due to congenital abnormalities of the biliary tract have patients included in the study were well informed about the
been implicated in the pathogenesis [2,11,12]. Rarely, intrahepatic operative procedure and the possible complications and an
stones can form as a result of iatrogenic bile duct stricture, and informed written consent was obtained from each patient before
choledochal cysts [11]. Primary intrahepatic stones are associated surgery.
with strictures in up to 85 per cent of cases and the natural history All patients were subjected to complete history taking, thorough
is characterized by progression with recurrent attacks of biliary clinical examination, routine laboratory studies, liver enzymes,
sepsis [13]. Patients with intrahepatic stones usually present with serum bilirubin level, and CA19.9 measurements. Abdominal ul-
recurrent cholangitis, intrahepatic abscesses, and may develop liver trasonography, multi-slice CT (MSCT) abdomen, and MRI with
atrophy and secondary biliary cirrhosis [4,5]. The triad of symptoms magnetic resonance cholangiopancreatography (MRCP) were
e fever, jaundice, and right upper quadrant pain e is present in 60% routinely performed. All patients received prophylactic antibiotic
of cases [11]. The symptoms can be mild with minimal abdominal (3rd generation cephalosporin 1 g, intravenously) at the time of
tenderness and jaundice or severe with shock and mental confu- induction of anaesthesia and then every 4 h during the operation
sion. The disease may progress to epithelial dysplasia and chol- and twice daily thereafter for 5 days.
angiocarcinoma in 3%e8% of cases. [5,14]. A right subcostal incision with extension to the left, as appro-
Treatment of intrahepatic stones is complex and the disease priate, was used to provide exposure of the porta hepatis. The first
progresses in most patients even after adequate treatment [5,14]. step was cholecystectomy, unless the gallbladder had already been
Patients having stones and strictures confined to a liver segment/ removed, followed by bile duct exploration. Choledochotomy was
section/hemiliver with subsequent atrophy are best treated by sited close to the biliary confluence to allow easy extension to one
hepatic resection [15,16]. Surgical removal of stones has been the or both hepatic ducts, depending on the predominant location of
standard management but residual stones and stone recurrence stones for better clearance and wider anastomosis. Intrahepatic
occur frequently whatever the technique [11,17e20]. Because of the stones were removed using Desjardine's forceps, saline flushing,
need for repeated biliary instrumentation, long-term access routes and balloon extraction. Intraoperative flexible choledochoscopy
involving percutaneous transhepatic access tubes [21], or hep- (Karl Storz, Germany) with operating channels and end vision was
aticocutaneousjejunostomy (HCJ) to permit stone retrieval or used to identify and remove intrahepatic calculi using a
stricture dilatation have been developed [22e24]. These provide choledochoscope-guided biliary balloon catheter and metallic wire
good access to the biliary system but patients are left with the basket retriever. A mechanical basket lithotripter passed via the
unpleasant side effects of a biliary stoma [19,23]. Our experience working channel of a choledochoscope was used for fragmentation
with a subparietal hepaticojejunal access loop, without a stoma, in of big stones located beyond strictures. Occasionally stricture
the management of intrahepatic stones is reported. [18]. dilatation using an angioplasty balloon under fluoroscopic control
was used to remove all stones. Stone clearance was confirmed using
intraoperative cholangiogram. When liver atrophy was present
2. Aim of the work
hepatic resection was performed. A biliary-enteric anastomosis was
performed using a side-to-side anastomosis between the hepatic
The aim of this work was to evaluate the outcome of subcu-
duct confluence and a jejunal Roux-en-Y loop. If the left or right
taneous hepaticojejunal access loop in the management of intra-
duct was narrowed, the hepatic duct incision was extended beyond
hepatic stones.
the stricture to provide a wide anastomosis. A site 12-cm proximal
to the closed end of the jejunal loop was selected for anastomosis
3. Patients using a single layer of interrupted 3/0 polyglactin (Vicryl; Ethicon,
Johnson and Johnson) suture to the hepatic duct confluence. Two
Between January 2009 and January 2013, 42 patients with ligaclips were used to mark the anastomosis for later radiological
radiologically confirmed intrahepatic stones were admitted and identification. The length between the hepaticojejunostomy and
treated at the Gastrointestinal Surgery Unit, Main Alexandria the jejunojejunostomy was 50 cm. The closed proximal limb was
888 M.I. Kassem et al. / International Journal of Surgery 12 (2014) 886e892

passed through the anterior abdominal wall and was then fixed to flowed into the liver outlining the anastomosis and the intrahepatic
the wall in a subcutaneous position using 3/0 polyglactin sutures ducts. Antibiotic prophylaxis was given and biliary access was then
(Fig. 1). The limb between the hepaticojejunal anastomosis and the gained under direct vision. The skin over the access loop was
subcutaneous fixation should be short and straight. Ligaclips were incised to visualize the jejunal loop which was entered under vision
used to mark the jejunal loop by clipping the sutures holding the using a conventional esophagogastroscope (end view) or a chol-
access loop in place. An umbilical feeding tube was passed through edochoscope. The endoscope was passed through the subcutane-
the skin and into the access loop to permit postoperative ous access limb and negotiated towards the liver until the
cholangiography. hepaticojejunostomy was identified. After the anastomosis was
If obstructive jaundice, biliary pain or cholangitis subsequently entered, the hepatic duct was reached under fluoroscopic guidance.
developed, recurrent or residual stones were suspected. Abdominal A cholangiogram was then performed by the use of a three-way
ultrasonography followed by MRCP were then carried out. Once balloon catheter. Then a combination of Dormia basket and
residual or recurrent intrahepatic stones were identified, cholan- extraction balloons was used to extract calculi. In case of a duct
giography was carried out without sedation or local anaesthesia. stricture, a guidewire was inserted via the working channel of the
Contrast was first injected percutaneously into the subcutaneous scope and then through the strictured segment of the biliary tree. A
loop of jejunum (identified by the scar). After confirming that the balloon catheter was inserted over the guidewire and inflated to a
contrast was intraluminal by fluoroscopy, the patient was placed in maximum size (i.e. 5 mm) for 10 min to dilate the stricture. On
a Trendelenberg position and more contrast was injected, which completion, the ducts were flushed with saline. The skin and

Fig. 1. Side-to-side hepaticojejunostomy (HJ) between the hepatic duct confluence and a jejunal Roux-en-Y loop with construction of a subcutaneous access loop. Conventional
endoscope (end viewer) passed through the subcutaneous jejunal access loop for stone retrieval.
M.I. Kassem et al. / International Journal of Surgery 12 (2014) 886e892 889

jejunal loop were closed after the procedure. Patients were whom underwent hepatic resection (left lateral sectionectomy in 4
admitted overnight for observation and two further doses of anti- and left hepatectomy in 1) at the time of the access loop
biotics were administered following the procedure. construction.
Patients were reviewed 6 weeks after surgery, at 3-month in- A mild stricture happened when choledochoscopic access to the
tervals thereafter for the first year, and at 6-month intervals stones was impossible without dilatation. A severe stricture
thereafter, unless they became symptomatic again. Complete liver happened when a guide-wire could not pass through the stricture.
function tests and abdominal ultrasonography were done during A positive bile culture was obtained in 39 (93%) patients. The
the follow-up visits to detect residual stones. If there was a suspi- cultured organisms were E. coli in 15 patients (38%), Klebsiella in 11
cion of stone recurrence or evidence of cholangitis, the patient was (28%), and multiple organisms in 13 (33%) patients.
re-admitted for further evaluation and treatment. All patients were The mean operation time, including that for choledochoscopy,
followed up for a median of 30 (range 12e60) months. A minimum and cholangiography was 4.9 h and the mean blood loss was
of 12 months follow-up without evidence of residual or recurrent 440 mL. The mean postoperative hospital stay was 10 days. Minor
stones was considered satisfactory. Recurrent cholangitis was complications were encountered in 8 (19%) patients. Four patients
defined as occurrence of two separate episodes of clinical and presented with more than one complication. Wound infection was
biochemical features of cholangitis during the postoperative the commonest complication, occurring in 5 (12%) patients. Pul-
period. Patients with recurrent cholangitis were managed with monary complications occurred in 3 (7%) patients, and intra-
antibiotics, ursodeoxycholic acid and endoscopic stone extraction abdominal collections in 2 (4.8%) patients. Two (4.8%) patients
through the access loop. had biliary leak after left lateral sectionectomy. All responded to
Data were presented with numbers, percentage, arithmetic conservative treatment with full recovery. There were no specific
mean (X) and standard deviation (SD) and were analyzed using the complications attributable to the construction of the access loop.
SPSS (version 16) statistical software. P values less than 0.05 were None of the patients developed postoperative cholangitis prior to
considered to be statistically significant. stone recurrence and none presented with strictures at the site of
the bilioenteric anastomosis.
Recurrent cholangitis occurred in 22 (52%) patients. Recurrence
5. Results
of cholangitis occurred at a mean period of 10 months after the
initial surgical procedure, was always associated with recurrent
Forty-two patients with intrahepatic stones underwent surgery
stones, and required 2 hospital admissions per patient. The pres-
with construction of a subcutaneous hepaticojejunal access loop.
ence of intrahepatic strictures was associated with recurrent
Ten patients had previously undergone a total of 12 biliary tract
cholangitis.
operations prior to the definitive procedure. These included open
Fourteen patients (33%) had no residual or recurrent stones after
cholecystectomy in seven patients; laparoscopic cholecystectomy
the initial surgical procedure and did not require the access loop,
in three; common bile duct exploration and T-tube drainage in one;
the ‘no need group’. Retained or re-formed stones were found in 28
and common bile duct exploration and choledochoduodenostomy
(67%) patients. The subcutaneous access loop was used to gain
in the remaining patient. The patients' demographic data and
access to the biliary tree in all these patients. A total of 55 pro-
preoperative parameters are shown in Table 1.
cedures (range 1e5) were attempted with successful access ach-
Stones were mostly found in the left hemiliver. In patients with
ieved in all cases and successful stone clearance in 21 of the 28
right hemiliver involvement, stones were seen predominantly in
patients, and all of them were symptom free for at least 12 months
liver segments VI and VII. Associated extrahepatic stones were
after the last procedure, the ‘successful use group’. There was no
found in 33 patients. Twenty-two patients had associated intra-
significant complication of these procedures. Partial stone clear-
hepatic duct strictures. Atrophy of segments II and III was identified
ance was achieved in the remaining seven patients, the ‘failed use
before operation by computed tomography in five patients, all of
group’. These seven patients had different degrees of biliary stric-
tures. The flowchart in Fig. 2 summarizes the outcomes of stone
Table 1 retrieval through the subcutaneous access loop. Severe bile-duct
Patients' demographic data and preoperative parameters. stricture was the major cause for the failure to remove stones.
Characteristics Patients (n ¼ 42) Table 2 shows the parameters associated with the final outcomes of
the procedure.
Age 41 ± 8.4 (32e64)
Male:female 17:25
Of the 42 patients treated, 20 patients had no bile duct stricture,
Serum bilirubin (mg/dL) 5.5 ± 3.7 (1.1e17.3) 18 had a mild stricture, and 4 had a severe stricture (Table 3). In the
Serum ALT 79 ± 47 (32e237) no stricture group, the stone of one patient was large and impacted
Serum AST 87 ± 62 (23e326) and could not be removed completely. Of the 18 patients in the
Serum alkaline phosphatase 276 ± 172 (137e1047)
mild-stricture group, after endoscopic dilatation, stones could be
Presenting features
Abdominal pain 39 (93%) removed from 16 patients (89%) and were partially removed in the
Recurrent fever 34 (81%) remaining two patients. In the severe-stricture patients, the guide-
Obstructive jaundice 29 (69%) wire could not be passed through some strictures and the stones in
Cholangitis 25 (60%) all the 4 patients (100%) were not removed completely. These 4
Hepatomegaly 5 (12%)
Morphological features
patients underwent hepatic resection at the time of the access loop
Bilobar disease 14 (33%) construction.
Unilobar disease 28 (67%)
Left lobe 25 (60%) 6. Discussion
Right lobe 3 (7%)
Extrahepatic and intrahepatic calculi 33 (79%)
Intrahepatic calculi alone 9 (21%) Intrahepatic stones are frequently associated with intrahepatic
Associated atrophy of liver 5 (12%) strictures which may cause bile stasis, cholangitis and recurrent
Associated intrahepatic stricture 22 (52%) stone formation [25]. The principal approaches to intrahepatic
Mild stricture 18 (43%) stones are surgical exploration of bile duct and intrahepatic ducts
Severe stricture 4 (10%)
for stone removal with biliary drainage or hepatico-jejunostomy
890 M.I. Kassem et al. / International Journal of Surgery 12 (2014) 886e892

Patients with intrahepatic stones


(n = 42)

Hepaticojejunostomy with subcutaneous access loop

Residual or recurrent stones 'No need' group

(n = 28) Patients who did not need the access loop


(67%) No residual or recurrent stones
symptom free for a minimum
of 12 months
(n = 14)
(33%)

Stone retrieval via the subcutaneous access loop


(1 – 5 procedures)

'Successful use' group 'Failed use' group

Patients who did benefit from the access loop Patients who failed to benefit from the access loop
Successful clearance Partial clearance
(n = 21) (n = 7)
(50%) (17%)

Symptom free for at least


one year after the last procedure No stricture Mild stricture Severe stricture
big stone (n = 2) (n = 4)
(n = 1)

Hepatic resection

Fig. 2. Flowchart summarizes the outcome of subcutaneous hepaticojejunal access loop in the management of intrahepatic stones.

(with or without access loop construction), hepatic resection [26], [4,5,17,39,40]. This technique provides good access to the biliary
and percutaneous transhepatic cholangioscopic lithotripsy (PTCSL) tree [41]. However, the necessity of a stoma is unsatisfactory
[27,28]. The success rates with these procedures range from 72% to because of the unpleasant side-effects of mucus and bile leakage
92%. [29e31]. with associated cutaneous irritation and excoriation [17,21].
The incidence of retained stones after operation is about 55 per Routine early closure of the stoma has been recommended to avoid
cent and a number of strategies have been developed to enable these side-effects after removal of retained stones following sur-
removal of both retained and recurrent intrahepatic stones gery [42]. Stoma closure is associated with significant complica-
[5,15,25,32,33]. After removal of as many of the intrahepatic stones as tions of wound infection, fistula formation and parastomal hernia
possible, reconstruction of the biliary tree by chol- [43]. Furthermore, many patients required reopening of the
edochoduodenostomy has not proved to be a reliable method for stoma for removal of recurrent stones after only 2 years of follow-
management of subsequent intrahepatic stones [34,35]. Although up. [43].
direct endoscopic access is still possible, the presence of strictures, An alternative access to the biliary tree for intervention is the
peripheral stone impaction and ductal angulation make endoscopic percutaneous transhepatic cholangioscopic lithotripsy (PTCSL)
extraction difficult [36,37]. Cunha et al. [38] reported a biliary access approach. It is being increasingly used with the advent of the four-
technique for the long-term endoscopic management of intrahepatic angled choledochoscope [14]. The transhepatic route requires the
stones that involved a side-to-side duodenojejunostomy between development of a working tract which necessitates sequential
the isolated Roux-en-Y jejunal limb 20 cm distal to the biliary anas- dilatation over a period of up to 3 weeks, following which chol-
tomosis and the lateral duodenal wall 15 cm from the pylorus. To edochoscopy can be performed for stone removal or stricture
access the anastomosis, the endoscope must be negotiated through dilatation [44]. The procedure is not without complications, with
this duodenojejunostomy and then travels upward for about 20 cm. severe pain and bleeding resulting in treatment failure in many
The Roux-en-Y hepaticocutaneousjejunostomy (HCJ) has been cases [45]. Stone clearance rates of 80 per cent have been achieved
used to permit endoscopic access for removal of intrahepatic stones with repeated procedures [46,47]. The transhepatic catheter has
M.I. Kassem et al. / International Journal of Surgery 12 (2014) 886e892 891

Table 2 strictures as compared to no stones in those without stricture.


Parameters associated with final outcomes of the procedure. Various techniques have been used for postoperative access of
Parameter ‘No need’ ‘Successful use ‘Failed use biliary system in the treatment of recurrent stone with cholangitis
group (n ¼ 14) ’ group (n ¼ 21) ’ group (n ¼ 7) [43,48,52e54]. Postoperative choledochoscopic removal of stones
Common bile duct 12 16 5 through a T-tube tract was once popular; however Cheung et al.
calculi [52] reported poor overall success rate (50%) and technical diffi-
Bilobar disease 5 6 3 culties like inaccessibility of the ducts, failed manipulation due to
Unilobar disease 9 15 4
strictures, losing the tract during dilatation, and difficulties in
Associated intrahepatic e 16 6
stricture extracting large stones.
Postoperative cholangitis e 15 7 The closed subcutaneous access loop offers the advantage of a
Atrophy of liver e 1 4 permanent and re-usable access for stone removal with minimal
Hepatic resection e e 4
morbidity since it permitted easy access to intrahepatic ducts using
a conventional forward-viewing endoscope or a choledochoscope,
without the need for transhepatic tubes or cutaneous stomas.
been a major source of complaint and access is only temporary as Factors associated with ‘failed use’ “i.e. severe stricture” should
the fistula closes after removal of the catheter. [7,17]. be added to the exclusion criteria in patient selection. However,
In the present study, hepatic resection with subcutaneous expert opinion is of paramount importance in selecting patients for
hepaticojejunal access loop was performed only for patients with this procedure. Moreover, those who did not need the access loop
hemihepatic disease associated with atrophy. Twenty-eight (67%) ‘i.e. no need group’ and were symptom free for at least 12 months
patients had hemihepatic disease and 5 of these patients under- after stone retrieval and construction of the access loop may benefit
went hepatic resection. The present study has no experience with from the loop later in their life should they develop recurrent
hepatic resection for bilateral liver disease. Our policy for such stones.
patients was to perform surgical exploration and dilatation of
strictures followed by stone clearance and construction of a sub- Ethical approval
cutaneous hepaticojejunal access loop for biliary interventions in
the future should patients develop recurrent stones or cholangitis. Ethical approval was given by Ethical Committee of Alexandria
The subparietal access loop can be used for stone retrieval under Faculty of Medicine.
local anaesthesia [48]. The afferent loop can be identified fluoro-
scopically by determining the position of the ‘ligaclip runway Funding
lights’. The loop can be entered percutaneously between the
‘runway’ clips using a 21-gauge fine-bore needle with intermittent No sources of funding as all cases were done in the Main Uni-
contrast injections and a guidewire. A converting dilator allowed versity Hospital with no added costs.
percutaneous introduction of larger guidewire catheters directed
by fluoroscopy into the jejunal lumen where a combination of
Author contribution
Dormia baskets, angioplasty balloons and snare wires can be used
to fragment and extract calculi. Krige and Beningfield [49]
All authors share the study design, collection and analysis of
described a new double-entry access loop (DEAL) technique as a
data, performing operations and writing the paper.
modification of the subparietal single-entry access loop to enhance
percutaneous radiological entry and facilitate intrahepatic biliary
Conflicts of interest
intervention.
The subcutaneous access loop used in this study is a good
There are no specific conflicts of interest.
alternative to the subparietal access loop that allowed reliable ac-
cess to the biliary tree in all cases. The median number of pro-
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