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ORIGINAL ARTICLE: Clinical Endoscopy

Low symptomatic premature stent occlusion of multiple plastic stentsfor benign biliary strictures: comparing standard and prolonged stentchange intervals

Christopher Lawrence, MD, Joseph Romagnuolo, MD, FRCPC, MSc(Epid), K. Mark Payne, MD,Robert H. Hawes, MD, Peter B. Cotton, MD, FRCP, FRCS

Charleston, South Carolina, USA

Background: Benign biliary strictures are typically managed endoscopically whereby an increasing size ornumber of plastic stents is placed at ERCP. Stents are often changed every 3 to 4 months based on the knownmedian patency of a single biliary stent, but patency data for multiple biliary stents are lacking.

Objective: To assess the incidence of occlusion-free survival of multiple plastic biliary stents and the rate ofpremature occlusion if left in longer than 6 months.

Design: Retrospective.

Setting: Tertiary-care medical center (Charleston, SC).

Patients: Consecutive patients who received multiple plastic stents for benign nonhilar biliary strictures from1994 to 2008 were identified.

Interventions: Exchange of multiple plastic biliary stents within 6 months (group 1) or 6 months or longer(group 2) after placement.

Main Outcome Measurements: Symptomatic stent occlusion.

Results: Seventy-nine patients with nonhilar extrahepatic benign biliary stricture underwent 125 ERCPs withmultiple plastic biliary stents. Stents were scheduled for removal/exchange within 6 months in 52 patients (86ERCPs) compared with after 6 months in 22 patients (26 ERCPs). The median interval between multiple stentplacement and removal/exchange was 90 days for group 1 and 242 days for group 2. Premature stent occlusionoccurred in 4 of 52 (7.7%) patients in group 1 versus 1 of 22 (4.5%) in group 2, with significantly longerocclusion-free survival in group 2 (log-rank P � .0001).

Limitations: Retrospective study at a single tertiary referral center.

Conclusion: Multiple plastic biliary stents for benign nonhilar strictures were associated with a low rate ofpremature symptomatic stent occlusion at more than 6 months and a longer occlusion-free survival. (GastrointestEndosc 2010;72:558-63.)

Copyright © 2010 by the American Society for Gastrointestinal Endoscopy0016-5107/$36.00doi:10.1016/j.gie.2010.05.029

Received December 15, 2009. Accepted May 24, 2010.

Current affiliations: Medical University of South Carolina, Charleston,South Carolina, USA.

Reprint requests: Christopher Lawrence, MD, Medical University of SouthCarolina, 25 Courtenay Drive, ART 7100A, Charleston, SC 29425.

If you would like to chat with an author of this article, you may contact Dr.

bbreviation: BBS, Benign biliary stricture.

ISCLOSURE: The following authors disclosed financial relationshipselevant to this publication: Dr. Romagnuolo: consultant for Olympus;peaker honoraria from Cook. Dr. Hawes: services agreement with Olym-us; consultant for Boston Scientific; speaker honoraria from Cook. Dr.otton: consultant for and device royalties and support from Cook;upport from Boston Scientific; support from, consultant for, charityoard member of Olympus; consultant for and scientific advisory boardember of Barosense; consultant for and equity interest in Apollo En-osurgery. The other authors disclosed no financial relationships rele-

ant to this publication. Lawrence at lawrench@musc.edu.

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enign strictures of the extrahepatic biliary tree most com-only result from iatrogenic injury or chronic pancreatitis.n initial attempt at endoscopic therapy is generally pre-

erred with surgical reconstruction reserved for treatmentailures. Short-term relief of cholestatic symptoms and nor-alization of obstructive hepatic biochemistries after en-oscopic stenting is consistently demonstrated. Long-termuccess of endoscopic treatment is defined by patency ofhe biliary tree without the need for stents and depends onactors such as etiology and location of the stricture.

The superiority of managing extrahepatic benign biliarytrictures (BBSs) with increasing number and/or size of bili-ry stents across a biliary stricture has been demonstrated.1-7

ased on these data, a typical endotherapy protocol for BBSsnvolves ERCP every 3 months over approximately a 12-onth period. At ERCP, the biliary stent(s) are removed,

he stricture is evaluated, and progressively more and/orarger stents are replaced until the stricture resolves, athich point all stents are removed and liver tests areonitored for signs of recurrence. Stent change at

-month intervals has been recommended based on anxpected median stent patency of 77 to 126 days for aingle plastic stent.8-13

Although the patency of a single plastic biliary stent haseen rigorously evaluated, knowledge regarding the pa-ency of multiple plastic biliary stents is lacking. Despite aegimented stent follow-up protocol at our institution,hereby patients return every 3 months for stent ex-

hange, deviations from this protocol have naturally oc-urred. We report our experience in such patients, com-aring the outcomes of those occasions where multipleiliary stents have remained in place without intendedanipulation for a minimum of 6 months with those un-ergoing protocol-directed stent exchanges.

ETHODS

atientsConsecutive patients who underwent ERCP with place-

ent of multiple biliary plastic stents between June 1994nd June 2008 were identified by using the Medical Uni-ersity of South Carolina endoscopy database (GI-Trac;kron Systems Development, Charleston, SC). Patientseeting the following criteria were included for analysis:ultiple biliary stent insertion, generally including at leastne 10F plastic stent, nonhilar BBS. Patients were thenivided into 2 groups. Group 1 consisted of patients ad-ering to our usual stent protocol and returned soonerhan 6 months after placement of multiple biliary plastictents. Group 2 consisted of those patients who returnedor stent exchange 6 months or longer after multiple biliarytent placement.

nterventionsBiliary stents were placed endoscopically with or with-

ut a biliary sphincterotomy by using standard techniques.

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Balloon or bougie dilation of the stricture was performedat the discretion of the endoscopist. Multiple 10F Cotton-Leung biliary stents (Cook Medical Inc, Bloomington, Ind)were generally placed with the Fusion OASIS stent system(Cook Medical Inc) after its introduction; all patients re-ceived at least one 10F stent. Seven-French Cotton-Leungstents were inserted with a standard pushing catheter. Thestent length was selected to allow the shortest lengthpossible while simultaneously ensuring the internal stentflange rested upstream from the stricture. The distal endsof the stents were deployed within the duodenal lumen.

At the time of stent exchange, all biliary stents weregenerally removed. Choledocholithiasis was addressed byusing extraction balloons and/or baskets after stent re-moval. Stricture resolution was determined by assessingany or all of the following: the absence of waisting with anappropriately sized biliary dilation balloon, the ability topass an appropriately sized extraction balloon through thestricture, and drainage of contrast injected upstream of thestricture.

Periprocedural antibiotics were routinely administeredto patients with a liver transplant or primary sclerosingcholangitis. Otherwise, prophylaxis against cholangitiswas used at the discretion of the endoscopist and wasreserved for patients with incomplete drainage accordingto the American Society for Gastrointestinal Endoscopyguidelines.14 Stent follow-up was coordinated by a dedi-cated pancreaticobiliary nurse. Stent service for BBSs wasarranged approximately every 3 months at our institution.It is highly unusual for these stents to be exchanged at anoutside institution in our practice. However, the patients inthis analysis returned for stent service a minimum of 6months after multiple biliary stent placement; this delayfrom the standard stent service protocol occurred bothintentionally (ie, at the request of the endoscopist) andunintentionally (ie, patient lost to follow-up). No specificcriteria (eg, specific stent size or number, etiology of stric-ture) were required of those patients whose stent intervalwas intentionally extended.

Data collection and follow-upMedical records and elements of the endoscopic data-

base and ERCP reports were reviewed. The patients were

Take-home Message

● The median patency period of a single plastic biliary stentis approximately 3 months. Physical blockage of a plasticstent does not necessarily equate to symptomatic biliaryobstruction. Symptomatic stent occlusion occursinfrequently when multiple plastic biliary stents areplaced across non-hilar, benign biliary strictures, evenwhen left unmolested for longer than 6 months.

then followed up by using data extracted from return clinic

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nd/or ERCP visits as well as telephone contact with theatient and referring physicians. Premature stent occlusionas defined as worsened cholestatic liver test results of

ignificant severity to warrant stent exchange before thelanned stent exchange or symptoms of cholangitis. The

nterpretation of these signs and symptoms was made inhe context of other clinical data and preferably with thenput of the referring physician.

ata analysisDifferences in baseline factors were compared with a �2

r Fisher exact test for proportions and a Mann-Whitneyest for continuous variables (Stata version 7.0; StataCorp,ollege Station, Texas). For event rates, 95% binomialonfidence intervals were calculated, and the rates wereompared with a Fisher exact test between group 1 androup 2. Follow-up durations and times to occlusion wereiven as medians and ranges. Occlusion-free survival forach group was assessed with life-table analysis (censoredt time of last follow-up or at time of prophylactic stenthange), and the log-rank test was used to test for aifference. For patients who had multiple stenting epi-odes in their group, the survival analysis was performedy using data from the first entry of a given patient withinheir group because multiple stenting patency measure-ents in the same patient would not be, strictly speaking,

ndependent observations. Last, multivariate analysis (eg,ox model) was considered but because of the low eventate described in the following, this was not thought to beppropriate. We did perform a stratified analysis accordingo chronic pancreatitis because there appeared to be somembalance in this potential confounder between the 2roups.

ESULTS

Seventy-nine patients with nonhilar extrahepatic BBS

TABLE 1. Comparison of baseline characteristics of standard stmonths after placement (group 2)

Group 1: stent change at <6(n � 52)

Age (median, range) 56, 24-75

Sex, F:M 25:27

Indication, no. (%)

OLT 35 (67.3)

Postoperative injury 9 (17.3)

Chronic pancreatitis* 5 (9.6)

Other 3 (5.8)

OLT, Orthotopic liver transplantation; other, portal biliopathy (n � 1), primary*P � .05.

nderwent 125 ERCPs in which multiple plastic biliary

60 GASTROINTESTINAL ENDOSCOPY Volume 72, No. 3 : 2010

stents were placed; of these, follow-up was available for74 patients. Stents were planned to be removed and/orexchanged prophylactically within 6 months after place-ment in 52 patients (86 ERCPs), labeled as group 1. Stentswere planned to be removed and/or exchanged 6 monthsor longer after placement in 22 patients (26 ERCPs), la-beled as group 2.

Limited data (demographics and indication) for the his-torical control group were available (Table 1). Groups 1and 2 showed a similar age and sex distribution. The mostcommon indication in both groups was BBS complicatingliver transplantation. Chronic pancreatitis was representedsignificantly more often as an etiology of BBS in group 2(31.8% vs 9.6%; P � .03).

Group 2 (stent changes beyond 6 months)Patients from group 2 underwent a median of 1 ERCP

(range 0-10 ERCPs) with a biliary stent before maximalbiliary stent placement. The median number of days fromfirst ERCP with biliary stent to maximal stent placementwas 115 days (range 0-1000 days); maximal stent place-ment occurred at the second ERCP in 13 of 26 (50%) cases.The maximum aggregate stent size was a median 30F(range 17F-50F). Biliary sphincterotomy was effected in 16of 22 (72.7%) patients at or before the time that multiplestents were inserted. Stricture dilation was performed dur-ing 8 of 26 (30.8%) stent episodes.

Stents remained in situ without further intervention fora median of 242 days (range 180-630 days) once thestricture was unable to accommodate additional stents andthe endoscopist requested follow-up 6 months or longer(Table 2). The stent change was intentionally extended bythe ERCP physician to beyond 6 months in all patients but1. In the latter instance, the patient failed to adhere to thesuggested follow-up interval and returned after 6 months.Stones or sludge was noted on 11 of 23 (47.8%) occasions

hange group (group 1) with those having stent change >6

Group 2: stent change at >6 mo(n � 22) P value

51, 35-77 .45

7:15 .31

11 (50) .19

3 (13.6) 1.0

7 (31.8) .03

1 (4.5) 1.0

sing cholangitis (n � 2), postsphincterotomy stenosis (n � 1).

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No premature occlusions occurred in the first eligibletenting episode for patients in group 2 after a median of07.5 days. Counting all stenting episodes in this group,remature occlusion occurred at some point in 1 of 22atients (4.5% per patient [95% CI, 0.1%-22.8%], 1 of 26 or.8% per case). This patient presented with cholangitis 345ays after placement of four 10F stents to treat a postop-rative bile duct injury; she had previously tolerated mul-iple biliary stents routinely exchanged 254 and 264 daysfter placement. The patient was managed as an outpa-ient with stent removal (as the stricture had resolved) andral antibiotics. Three patients have not had clinical man-festations of biliary obstruction 210, 330, and 630 daysfter stenting (verified by telephone follow-up). Early ad-erse events were limited to a single episode of pyrexia 24ours after exchange of biliary stents 278 days old.

The strictures resolved in 18 of 20 (90%) patients; in theremaining patients, stricture resolution has not yet been

ssessed. The durability of the stricture resolution has noteen assessed. Two (10%) patients’ strictures persisted, inhe setting of chronic pancreatitis, and they received ad-itional stents.

omparison with group 1 (control group withtent changes within 6 months)

Group 1 subjects (who undertook stent change accord-ng to the usual protocol guidelines, with prophylactictent changes within 3 to 6 months) had a median 90-dayrange 30-165 days) interval between multiple stent place-ent and extraction.When we used the first stenting period for each patient

n each group, occlusion-free survival (Fig. 1) for group 1as significantly shorter than for group 2 (log-rank P �

0001). Symptomatic stent occlusion developed in 4 of 527.7% per patient, 4/86 or 4.6% per stenting episode)roup 1 patients at 32, 91, 103, and 165 days after place-ent of multiple biliary stents, all associated with the first

tenting episodes. Despite the shorter at-risk time periodor group 1, the premature occlusion rates between the 2roups was not significantly different at 3.1% (95% CI,8.1% to 14.5%; P � .62). The difference in stent survivalas still seen when stratified by etiology of chronic pan-

reatitis (P � .0003 for those with chronic pancreatitis, and� .0001 for those without). There was no significant

ifference in occlusion-free survival (log-rank P � .10) oftents in chronic pancreatitis patients in the entire cohort

TABLE 2. Stenting time period (to exchange or premature occlu

Stent change at <6 m

Stent period (median days, range) 90, 30-165

Premature occlusion, no. (%) 4 (7.7)

ersus that of those in patients without chronic pancreatitis

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(Fig. 2), making it unlikely that there was significant con-founding by this slightly imbalanced factor (and making itunlikely that the observed difference between the 2groups was because of this imbalance).

DISCUSSION

Biliary stents provide effective relief of the symptomsthat result from benign and malignant biliary strictures.Unfortunately, the benefits of stenting are temporary be-cause occlusion of the biliary stent occurs in the majorityof patients.9,12,13,15,16 Scheduled biliary stent changes aretypically performed every 3 months to avoid the unin-tended consequences of stent occlusion, which can be

) and crude premature occlusion rates

52) Stent at >6 mo (n � 22) P value

242, 180-630 �.0001

1 (4.5) .62

Figure 1. A, Occlusion-free survival in the standard stent change group(group 1). B, Occlusion-free survival in those returning for stent change6 months or longer after multiple biliary stent placement (group 2).Vertical bars represent 95% confidence intervals. Log-rank P � .0001.

sion

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accompanied by cholangitis.17 However, only a single

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iliary stent was placed in the majority of trials evaluatingtent patency. Although the patency of multiple biliarytents out to 3 months can be surmised from efforts totudy BBSs1,2,4-7,18 which appears high, the patency ofultiple stents beyond 3 months has not been reported.The current investigation demonstrates the feasibility of

xtending the interval between stent changes beyond thetandard 3-month period in patients who receive multipleiliary stents for benign strictures. Twenty-two patients inhis study had their stent change interval extended beyondmonths (median 8 months). One (3.8% of stent episodes)atient experienced symptomatic stent occlusion 345 daysfter stents were placed. The incidence of stent occlusionas certainly no higher (P � .86) than the 4.6% of stentpisodes found in our reference population undergoingcheduled change of multiple biliary stents sooner than 6onths, while avoiding 1 to 2 ERCPs per patient and the

elated costs.Inferences regarding patency of multiple biliary stents

an be made from a number of investigations in whichultiple stents were used to treat BBSs.1,2,4,5,7,18 Although

hese investigations did not focus primarily on stent pa-ency rates, a low risk of symptomatic stent occlusion was

igure 2. A, Occlusion-free survival in patients without chronic pancre-titis. B, Occlusion-free survival in patients with chronic pancreatitis.ertical bars represent 95% confidence intervals. Log-rank P � .10.

onsistently demonstrated. However, each adhered to a

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strict protocol of stent changes at intervals of 2 weeks18 to3 months. The report of the Rome group most closelyapproximates our methodology because their median in-terval between stent exchanges was 5 months, with amaximum interval of 10 months; they encountered a pre-mature occlusion rate of 18%.1 By comparison, the medianstent in situ interval in our study was considerably longerat 8 months, and 7 of 26 (26.9%) stent episodes extendedbeyond 10 months.

Stent occlusion invariably results from sludge consistingof bacteria and bacterial byproducts.17,19,20 However,physical blockage of the stent does not necessarily equatewith symptomatic occlusion (jaundice, cholangitis) of thebiliary system.21 Such a disconnect between stent patencyand clinical obstruction is well described with the use ofpancreatic duct stents and has led to the concept of a“wicking” function of stents that continues after blockageof the stent lumen.22-26 Wicking of fluid is likely even moreeffective with multiple stents because multiple stents con-sistently create a potential space for fluid to track, espe-cially as they repetitively shift in relation to each other.Additionally, the overall effective diameter is increasedwith multiple stents, sometimes approaching that of self-expandable metal stents.

The incidence of complications is frequently underes-timated in a retrospective analysis such as ours. A controlpopulation (group 2) was simultaneously evaluated forcomplications to address this potential weakness lest thepatients experiencing early stent blockage self-select outof the treatment group before reaching the necessary6-month threshold; data regarding aggregate stent size forgroup 2 were not available, creating a potential source ofbias. Future studies are necessary to determine whetherthe prolonged patency of multiple stents is attributable toaggregate size or multiplicity irrespective of size. Never-theless, the incidence of stent blockage in our patientswho adhered to the conventional stent change protocolapproximates that of other similar retrospective studies. Incontrast to our results in group 2, Bergman et al27 reportedstent-related complications in 70% of patients who did notadhere to stent change every 3 months. Our choice of anantibiotic with better biliary penetration and our practiceof aspirating contaminated bile above the stricture in anamount exceeding contrast injected are 2 possible expla-nations for such a disparity.

Antibiotic use in our 2 groups was not evaluated retro-spectively. Because of our strict adherence to an antibioticprophylaxis protocol, deviation from standard practicewould likely distribute evenly across groups. Althoughsuch deviation would affect immediate post-ERCP cholan-gitis, the available data would suggest that antibiotics havea negligible effect on stent patency.28

The retrospective nature of this study has other inherentlimitations. The lack of randomization does not excludethe possibility that bias was introduced. We did not estab-

lish any a priori conditions for inclusion in the prolonged

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tent group, and our technique of placing the maximalumber of stents allowed by the duct diameter did notiffer between the groups. Similarly, stricture dilation andiliary sphincterotomy were not standardized betweenroups and could have favored the extended stent group.uch issues can only be definitively answered with aandomized, controlled trial.

The safety and effectiveness of the standard biliary stenthange protocol to treat BBSs have been proven but areostly and involve a multitude of procedures. The burdenf repeated ERCPs is not insignificant; the median numberf ERCPs required to complete therapy has varied from 2o 8.1,2,4,5,29,30 Covered self-expanding metal stents canessen the need for frequent stent exchanges but are ex-ensive, eventually occlude, and may not always beetrievable.31-34

The optimal management of BBSs would achieve theesired long-term result by using the minimum number ofnterventions while simultaneously minimizing complica-ions. The outcome of current endoscopic techniques toreat biliary strictures is quite favorable and is generallyafe. The results of our retrospective study would suggesthat further improvements can be made in minimizing aatient’s exposure to repetitive endoscopic procedures yetaintain an excellent safety profile in terms of minimal

nterval cholangitis. Replication of these findings in a pro-pective study is desirable.

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