Cardiovasc lntervent Rad~ol (1992t 15:360-366

CardioVascular andInterventional Radiology .~ Springer-Verlag New York Inc. 1992

Metallic Stents in Benign Biliary Strictures: Three-Year Follow-Up Francesca Maccioni, Michele Rossi, Filippo Maria Salvatori, Paolo Ricci, Mario Bezzi, and Plinio Rossi 4a Cattedra dl Radiologia, Unlversit'h "'La Sapienza", Rome, Italy

Abstract. Eighteen patients with recurrent benign biliary strictures (BBS) were selected for metallic stents placement because they failed to respond to percutaneous balloon dilatation. None were candidates for surgical corrections. We used "Z'" single or double stents in 17 cases and a Wallstent in 1 case. After more than 3 years of follow-up (average period 37 months, range 30-41 months), I0 patients (55.5%) were a s y m p t o m a t i c without signs of bile stasis; 5 patients (27.7%) had recurrence of symptoms and were eventually retreated; and 3 patients (16.6%) died, 2 of obstructive jaundice and liver failure and 1 of metastatic gastric cancer. Recurrence was due to stent occlusion by tissue ingrowth in 3 cases, stent migration in 1 case, and an inflammatory lesion of the papilla of Vater in another case, with patency of the metallic stent. The overall patency rate, at 3-year follow-up was 68.7%. In our series, the main factor determinig long-term patency of metallic stents has been reactive tissue ingrowth. Nevertheless, long-term results obtained with metallic stents in recurrent benign biliary strictures should be considered satisfactory. In selected patients, metallic stents may represent the only long-term treatment available for maintaining bile flow.

Key words: Benign biliary strictures--Metallic s t e n t s - - M u c o s a l hyperplasia

In the last 4 years, balloon-expandable and self-expanding metallic stents (MS) have been successfully employed in arteries and veins to relieve obstruction and to prevent reocclusion from elastic recoil after angioplasty. The positive results obtained in vascular lesions [ i-4] have led m a n y authors to investigate Address reprint requests to" Plinio Rossi. M.D., 4a Cattedra di

Radiologia, Universita "'ka Sapienza,'" 00199 Rome, Italy

the use of metallic stents in the biliary tree to treat benign or malignant strictures [5-14]. In benign strictures, long-term stent patency is the most important factor to be considered, as patients have a long life e x p e c t a n c y . Once positioned, metallic stents cannot be r e m o v e d and surgical repair is generally not feasible. Mucosal hyperplasia and inflammatory reactive changes of the ductal wall m a y represent a possible cause of late stent obstruction in patients with benign biliary stenoses, as suggested in early experimental studies on animal models [6, 7]. We report here a 3-year follow-up of biliary metallic stents placed in 18 patients with recurrent benign biliary strictures (BBS), including the technical problems encountered, follow-up procedures, and possible causes of stent obstruction.

Materials and Methods During our clinical trial, from October 1988 to September 1989, 18 pahents with bemgn blliary strictures were treated with selfexpanding metathc stents. The group included 10 men and 8 women, ranging m age from 22 to 76 years (average age 60 years). The patients were selected from a group of 90 with benign bihary strictures treated percutaneously in our institution in the last 7 years, as described in previous papers [9. 10]. All t8 patients had a postsurgical stricture: 12 localized at the level of a biliary-enteric anastomosis, 5 in the common bile duct following cholecystectomy, and 1 at the level of a spontaneous hepato-duodenal fistula fotlowmg iatrogenic closure of the common bile duct (CBD). Five of the 18 patients had multiple intrahepatic narrowings from secondary cholangitis and 1 had been previously operated on for gastric cancer 10 years earlier. The patients were selected according to the followingcriteria: I) strictures not responding to repeated balloon dilatation (3-13 dilations/pt, average 4 dilatations/pt): 2) strictures not responding to prolongedcatheter drainage (4-38 months, average 13 months/ pt); and 3) patients no longer candidates for surgical repair because surgery was no longer technically possible or patients refused surgery (1o5 previous surgical interventions/pt). Twenty-nine self-expanding metallic stents were placed; 12 single and 10 double "Z" stents (Cook, Bloomington, IN, USA);

F Macciom et al.: Metallic Stents m Benign Blhary Strictures Table 1. Three-year ~ follow-up after self-expanding metallic endoprosthesis for benign biliary stricture Results

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Patency

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Asymptomatic Recurrence Died Total

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a 30-41 months, average 37 months 1, Overall patency rate (11 ~t6): 68.7% (two cases of late stent migration excludedl

6 single prototype stent~ lAnglomed, Karlsrue, Germany): and 1 Watlstent IMedinvent, Lausanne, Switzerland). The first 6 stents used had been made by Angiomed for experimental use only and were later discontinued. All other stents employed are now commercially available. The technical features of the stents and the techmque of insertion have been described in previous papers

[9]. After stent placement, the patmnts were momtored with periodic laboratory tests (bilirubin levels, liver enzymes), In asymptomatic patients we also took plain abdominal films to confirm the position of the metallic stent, did periodic liver ultrasound examinations to evaluate the size of intrahepatic bile ducts, and did computed tomography (CT) scans at the level of the stent ctopograms in two projections, different gantry angle, 2 mm slice, 2 mm interslice) to evaluate the endoluminal density, lnvasive procedures such as percutaneous transhepatic cholangiography (PTC) and biopsy were performed only in those patients wtth recurrent symptoms.

Results

Initial success after stent placement, with resolution of jaundice or pain. was achieved in 17 of the 18 patients; in 1 patient, the drainage catheter was left in place because of intrahepatic strictures. Early technical difficulties consisted of stent displacement or migration. In 2 cases, three stents (two single and one double "Z" stent) were dislodged into the duodenum during deployment and were later replaced with double stents after endoscopic removal. In 1 patient with a web-like stenosis of the CBD, three single stents were initially adequately placed but soon after slid above or below the lesion; a fourth double stent was subsequently placed. In 2 patients with a single stent at the level of a biliary-enteric anastomosis, the stents were no longer in place at 5-month follow-up, as confirmed by the abdominal films; 1 patient had recurrence of symptoms, and the other remains asymptomatic. At 3-year follow-up (30-41 months, average 37 months), 10 patients (55.5%) remained asymptomatic, 5 had recurrence of symptoms (27.7%), and 3 had died (16.6%) (Table 1). All 10 asymptomatic patients achieved complete remission of jaundice and cholangitis with normal bilirubin levels within 3 months after stent place-

361

ment. In 8/10 patients, laboratory findings and liver enzymes returned to normal levels within 6 months; in 2 patients, the alkaline phosphatase levels remained elevated for almost 1 year before decreasing to slightly above normal levels, reflecting chronic parenchymal damage. In 1 patient who still remains asymptomatic, the stent migrated into the bowel within 6 months after placement. CT examinations performed after approximately I year showed, in 6/8 patients, the presence of a soft tissue density inside the stent, associated with air or fluid density. The soft tissue density extended to different levels, and was generally more evident at the stricture in the middle of the stent. Some of these patients had subsequent CT scans at 2 and 3 years, which showed exactly the same soft tissue density within the stent compared to the first examination (Fig. 1). None of these patient had any episode of jaundice or cholangitis; neither underwent PTC or biopsy. In the group with recurrences, 3 patients returned for stent obstruction 4, 13, and 22 months after stent placement. Another patient had restenosis after stent migration and 1 had recurrent jaundice due to an inflammatory lesion of the papilla. The patient with a Wallstent at the site of a biliary-enteric anastomosis had recurrence of symptoms 4 months later. Removal of the hyperplastic tissue with a Simpson atherectomy catheter was attempted without success. Since then the patient has had an internal/external catheter placed through the stent to allow bile drainage. Another patient with two stents at the level of a bilioenteric anastomosis and at the site of the right hepatic duct, returned for recurrence of jaundice and cholangitis 22 months after stent placement (Fig. 2 A, B). A PTC showed almost complete stents obstruction by tissue ingrowth and intrahepatic lithiasis (Fig. 2C). The stones were so numerous and large enough to require percutaneous cholangioscopy and stone fragmentation with an electrohydraulic lithotriptor, and the stents were dilated with a balloon catheter. During this procedure, multiple biopsies were performed through the stent (Fig. 2D). The histological reports confirmed the presence of abundant granulation tissue with papillary hyperplastic simple columnar epithelium (Fig. 2E). The patient is asymptomatic 7 months after the removal of the drainage catheter. Another patient had recurrence of symptoms 13 months after stent positioning. A PTC showed the presence of tissue ingrowth occluding the stent. The stent was crossed, dilated, and drained with a catheter for 13 months. Thereafter, the catheter was removed and the patient was well for 6 months but later had some episodes of cholangitis.

362

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Fig, 1, A Seventy-one-year-old female patient with postcholecystectomy stricture of the common bite duct (CBD~, as shown by an ERCP. B Five months after balloon ddations and catheter stenting, a PTC demonstrated persistent stenosis. C A double "'Zstent'" was placed at the level o f the stricture, w~th optimal flow of contrast medium and re,~toration of adequate caliber of the CBD. D One year later. CT showed a parenchymat density par-

tially filling the stent, probably due to muco,~al hyperplasia. The study, performed at different levels, revealed different degrees of tissue ingrowth w~th.n stent ~Reprinted from [15] with permission). E Two years later. CT examination showed a soft tissue density inside the stent, of the same degree at the ,same level as after 1 year. The patient had no signs of jaundice. She still remains asymptomatic with normal bilirubin and enzyme levels.

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Fig. 2. A F~fly-etght-year-old female patient with a stenotic b[liary-enterlc anastomos~s performed to repair a p o s t c h o l e c y s t e c t o m y s m c t u r e . After multiple balloon d)latlons and 4 m o n t h s of catheter stentmg, the cholangiogram showed s t e n o s e s involving the a n a s t o m o s t s , the CBD, and the right hepatic duct (arrow). B T w o m o n t h s later, a double "'Z-stent'" was inserted across the a n a s t o m o s i s and a single one at the origin of the right hepatic duct. C Recurrence of s y m p t o m s began 22 m o n t h s after stent p l a c e m e n t A repeated PTC showed filling detects w~thin the duct due to stones, and w~thm the stent due to a tissue ingrowth, as confirmed at cholangioscopy, D T h e stones were removed with the aid of an electrohydraulic [ithotriptor, and multiple biopsies were performed within the stent. E T h e histological report revealed the presence of granulation t~ssue and hyperplastic c o l u m n a r epithelium. T h e stents were dilated and the patient was s u b s e q u e n t l y discharged (Figs. 2A-D reprinted from [15] with permission).

364 The patient with stent migration was treated again with balloon dilation but without a new metallic stent. Finally, another patient underwent a PTC for recurrence of symptoms 38 months after stent placement. The cholangiogram showed a lesion obstructing the CBD at the level of the papilla, below the stent, while the stent was free from filling defects. Subsequently, during an ERCP, a biopsy was performed at the level of the papilla: at the same level, 3 years earlier, a biopsy had revealed the presence of an adenocarcinoma; on this occasion, only an inflammatory lesion was found. Three patients died during the first 12 months after stent placement. In 1 patient with Hodgkin's disease, stent placement and expansion at the level of the main stricture was satisfactory, but the symptoms were not completely relieved because of multipie intrahepatic strictures from sclerosing cholangitis. The patient eventually died 9 months later of progression of his disease. Another patient with secondary sclerosing cholangitis and liver cirrhosis died 6 months later of liver failure, with recurrent jaundice and clinical signs of cholangitis. The third patient died of peritoneal spread from a gastric carcinoma removed 10 years earlier, with no signs of bile stasis. If we consider the overall patency rate of the stents positioned, excluding the 2 cases of stent dislodgement, 11/16 stents (68.7%) have maintained adequate patency after placement (Table I).

Discussion Three years ago, when we placed the first metallic stent in a patient with recurrent benign biliary stricture, there was no information available on clinical long-term patency. Partial obstruction of stents, due to mucosal hyperplasia, however, had already been described in animal models [6, 7]. Therefore, we limited our experience to a group of patients with recurrent BBS who had no therapeutic alternatives, because they were not responding to percutaneous treatment and were no longer candidates for surgical correction. Most of these patients had several previous unsuccessful surgical interventions and refused further surgery. In addition, in most cases, surgical correction of the stricture was considered extremely difficult technically and had a low chance of success. After metallic stent placement, we planned careful follow-up of these patients in order to obtain as much information as possible. Our experience now reaches over 40 months. Stent displacement is a possible early or late complication and generally occurs in the early phase

F. Maccioniet al.: MetallicStents in Benign Bdiary Strictures of operator experience, when one tries to correct stent position or dilate it after deployment. Proper stent design, such as double "Z" stent, usually prevents these complications [9, 15, 16]. The main cause for recurrence (3/4 cases) in our series was late stent occlusion by tissue ingrowth. In these patients, biopsy specimens obtained through cholangioscopes or by brushing confirmed the presence of hyperplastic epithelium and/or granulation tissue within the stent. Histological information available from those specimens were necessarily fragmentary and not comparable to those present in autopsy specimens. Nevertheless, they confirm the possibility of stent occlusion by benign tissue ingrowth. The presence of this phenomenon was also suggested in asymptomatic patients by CT findings. In most of the asymptomatic patients, CT examination showed a soft tissue density inside the stent, of various degrees at different levels, without significant changes at subsequent follow-up, suggesting the presence of reactive, hyperplastic tissue. We believe that in those patients, tissue ingrowth reaches a certain level and then stabilizes, without completely occluding the stent and thus allowing a physiological bile flow. This could be explained by the large final caliber reached by the stent, which is almost six 9times wider than the CBD. However, we cannot completely exclude the possible presence of bile sludge. Moreover, we also observed a case of Strecker stent occlusion 6 months after placement in a patient with malignant stricture of the CBD by metastatic lymph node compression; to our surprise, a brush biopsy revealed the presence of hyperplastic epithelium (Fig. 3). All patients with complete stent occlusion had a preexisting condition of diffuse cholangitis, with multiple intrahepatic strictures, which may explain the presence of abundant granulation tissue. Despite initial encouraging observations [9], in most patients with sclerosing cholangitis we obtained poor midand long-term results, with obstruction of the endoprostheses and subsequent need of biliary drainage. Reviewing our experience, we presently consider secondary sclerosing cholangitis a partial contraindication to the use of metallic stents, especially if they are used to correct intrahepatic ductal stenoses which generally can be successfully managed with balloon dilatation and catheter stenting only [16]. In conclusion, if patients are carefully selected, we do not think that the possibility of late tissue ingrowth contraindicates the use of metallic stents in benign lesions. We believe that a 68.7% 3-year patency rate in a group of patients without therapeu-

F. Macciom et al : Metallic Stems in Bemgn Bitiary Smctures

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366 tic a l t e r n a t i v e s s h o u l d be c o n s i d e r e d a s a t i s f a c t o r y result. M o r e o v e r , m o s t o f the p a t i e n t s with recurr e n c e c o u l d be r e - t r e a t e d , a l t h o u g h l o n g - t e r m results still h a v e to be e v a l u a t e d . O n the basis o f o u r e x p e r i e n c e with o v e r 130 p a t i e n t s t r e a t e d f o r b e n i g n biliary strictures f r o m 1983 to 1991, w e are c o n v i n c e d that r e p e a t e d b a l l o o n dil at at i o n s a n d c a t h e t e r s t e n t i n g r e p r e s e n t s the t r e a t m e n t o f c h o i c e f o r B B S w h e n surgical c o r r e c tion is no l o n g e r r e c o m m e n d e d [9, I0, 15]. T h e r e f or e, the o n l y i n d i c a t i o n f o r the use o f metallic stents is failure to r e s p o n d to p e r c u t a n e o u s t r e a t m e n t and. in this g r o u p o f p a t i e n t s , m e t a l l i c stents m a y represent the last r e s o r t to m a i n t a i n p a t e n c y o f the biliary tree w i t h o u t a p e r m a n e n t d r a i n a g e c a t h e t e r .

F. Maccloni et al.. Metallic Stents m Benign Bihary Strictures

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