Metallic stents in biliary disease MARY E. RODDIE ANDREAS ADAM
The main indication for the use of biliary endoprostheses is as an alternative to surgical bilioenteric bypass in the palliation of malignant bile duct obstruction, although they are occasionally used in the treatment of benign biliary strictures. Although some interventional radiologists believe that endoprostheses should be reserved for patients whose life expectancy is relatively short, in order to avoid the problem of stent occlusion (Ferrucci, 1985), we believe that endoprostheses should be inserted in virtually all patients with malignant obstructive jaundice in whom such insertion is technically feasible. Our preference for endoprostheses over internal/ external drainage catheters is based on a number of factors, including the fact that external catheters are associated with complications such as occasional leakage of bile around the catheter, and infection and pain at the skin entry site. However, our main objection to long-term external catheters is the permanent and unkind reminder to patients of their underlying malignancy and shortened life expectancy. The main objection to the use of indwelling stents has been the fact that they are likely to become occluded in patients with a relatively long life expectancy. This argument, however, is no longer valid as endoscopic and percutaneous stent changes have become routine procedures. Stents can be introduced transhepatically or endoscopically, and the choice of technique will be strongly influenced by the availability of local expertise. However, in most patients with unresectable, low-lying lesions such as pancreatic carcinoma, an endoscopic approach is preferable. In contrast, the proximal, high-level obstruction (especially when it results in isolation of multiple intrahepatic ductal systems) is best approached percutaneously by the interventional radiologist. PLASTIC
STENTS
Since the first description of percutaneous placement of a biliary endoprosthesis (Ahlstrom et al, 1986), attempts have been made to define the optimal configuration of biliary stents. Ideally, they should be easy to insert, have a low occlusion rate and produce minimal complications both during placement and once they have been released into the biliary system. Until BaiNi&eS Clinical GastroenterologyVol. 6, No. 2, June 1992 ISBN o-7020-1623-3
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recently, all endoprostheses have been made of plastic (Teflon, polyethylene, polyurethane, silicone or Percuflex), and various diameters and shapes have been used in an attempt to reduce the two most common causes of stent failure, namely stent occlusion and migration. These complications have been seen in approximately 6-23% and 3-6% of cases, respectively, in two large series (Mueller et al, 1985; Lammer and Neumayer, 1986). Occlusion Although stent occlusion may occur because of tumour overgrowth, the most common cause is bile encrustation; in patients who live longer than 6-18 months after placement of a plastic stent, occlusion will occur in approximately 20-30% (Teplick, 1991). However, nearly all blocked plastic endoprostheses can be changed either endoscopically or percutaneously (Jackson et al, 1990) and most patients, given the choice, prefer to have an additional procedure to replace the occluded stent rather than be left with a long-term external drainage catheter. Formation of encrustations depends on the mechanical and chemical surface characteristics of the stent material and on the surrounding bacterial population. Examination of occluded endoprostheses suggests that the initiating event is bacterial adherence to the stent surface, which is rapidly followed by deposition of a glycoprotein. Increasing numbers of bacteria result in deconjugation of bilirubin and deposition of calcium bilirubinate which eventually blocks the stent. Studies in vitro (Lammer et al, 1986) have shown that polyurethane and Percuflex stents have the lowest encrustation rates. However, owing to their flexibility, the walls of these stents have to be thicker, reducing the inner diameter; this is undesirable because there is an inverse relationship between the diameter of the lumen of biliary stents and the incidence of occlusion (Rey et al, 1985). Larger stents, on the other hand, require a large transhepatic track for their introduction with subsequent increased trauma to the liver and a larger risk of serious complications such as the formation of pseudoaneurysms, arteriobiliary or portobiliary fistulae, and intrahepatic and perihepatic bilomas. It is generally accepted that the optimum size for a transhepatically placed plastic stent is 12 French gauge. The maximum size of an endoscopically placed stent is governed by the size of the endoscope itself. Larger sphincterotomies are needed for the placement of bigger endoscopic stents with a resultant increase in the risk of bleeding, perforation and pancreatitis. Migration In an effort to combat the problems of stent migration, various designs have been introduced including spirals (Yeung et al, 1988), stents with collapsible mushrooms (Teplick et al, 1983) or subcutaneous plastic buttons attached to the endoprosthesis (Coons and Carey, 1983). The rate of migration of straight stents can be reduced by increasing stent length, but this has the disadvantage of leaving the lower end of the stent protruding into the duodenum, which (as well as leading to clogging of the lower portion by
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vegetable fibres) leads to contamination with bacteria from duodenal contents, which in turn predisposes to bile encrustation (Groen et al, 1987; Leung et al, 1988). However, this risk should be balanced by the possibility of endoscopic replacement. Such replacement is often fairly simple, even though the original stent may have been placed percutaneously. METALLIC
STENTS
In recent years various metallic stents developed for use in the vascular system have been tried in the biliary tree (Alvarado et al, 1989; Coons, 1989; Dick et al, 1989). The main advantage of metallic stents is that they can be introduced in a contracted state through a very small calibre track and achieve a large internal lumen following expansion. The former should theoretically reduce the incidence of complications associated with a large liver track or sphincterotomy, while the latter, coupled with the reduced surface area of metallic stents, should reduce the incidence of blockage due to bile encrustation. In their expanded state, metallic stents are partially embedded in the duct wall and this virtually eliminates the problem of migration. In addition, some metallic stent designs incorporate sharp ends or barbs which increase the security of maintaining stent position; this means that, in contrast with plastic stents, most metallic stents currently available cannot be removed. Commercially available metallic stents fall into two main categories: balloon-expandable and self-expandable. Balloon-expandable
stents
Balloon-expandable metallic stents (e.g. the Palmaz stent and Strecker stent) consist of a continuous, woven stainless steel wire mesh which is inserted over an angioplasty balloon through a lo-FG sheath and expanded when in an optimum position across the biliary stricture. Stents of 8-10 mm in diameter are available for use in the biliary tree. The cross-points of the mesh are soldered so the stent has the capacity to retain the diameter attained by the maximal balloon inflation. However, the rigidity inherent in this design makes it difficult to advance the stent around acute angles in the biliary system and may result in the stent being displaced from its position over the balloon (Palmaz et al, 1985). However, sufficient dilation of the track can usually overcome this problem. The lack of longitudinal flexibility limits its use to straight segments of duct-for angled segments, a series of short stents is required and the technical difficulty in achieving adequate overlap may result in tumour ingrowth through the gaps. Balloonexpandable metallic stents have therefore not been widely used in the biliary tree. Self-expandable stents The two main designs of self-expandable metallic stents are the Gianturco zigzag stent (Cook Inc., Bloomington, Ind, USA) and the Wallstent (Medinvent SA, Lausanne, Switzerland).
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The Gianturco stent is constructed of 0.45mm stainless steel wire with six zigzag bends soldered together to form a cylinder 1 S-3 cm in length and is introduced through a lo-FG sheath (Figure 1). Single stents are fitted near the midpoint with small barbs which engage in the stricture and prevent migration. Longer stents are made by connecting two to four stents by a wire strut. This not only increases flexibility but maintains the expansile force, since lengthening of an individual stent decreases its efficiency. Multiple stents are not barbed because the individual stents stabilize each other and prevent migration. The Rosch modification of the Gianturco stent, which is the type usually employed in the biliary tree, has a nylon suture running through eyelets at each end to control the diameter of the cylinder (Figure 2). Extrahepatic ducts require lo-mm diameter stents, while for intrahepatic biliary radicles, 8-mm stents are used. Most stents are used in tandem with a
Figure 1. Gianturco stents (unmodified). (a) On the left is a single stent fitted near the midpoint with small barbs. On the right is a longer stent consisting of three stents connected by a wire strut. (b) Gianturco stent loaded into a 12-FG sheath prior to implantation.
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Figure 2. R6sch modification of the Gianturco stent. A single stent is seen on the left and a double stent on the right.
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Figure 3. Wallstent: (a) when released, the Wallstent is extremely flexible in its longitudinal axis; (b) it can be mounted on a 7-FG catheter for introduction into the biliary tree.
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Figure 4. Irresectable hilar cholangiocarcinoma causing second-order duct involvement on the left and right. The right lobe was atrophic and it was therefore decided to stent the left lobe only. As segments II and III are no longer communicating because of tumour extension, each has to be stented separately. (a) Segment II has been cannulated and a tubogram demonstrates the hilar stricture. (b) Following cannulation of segment III, two Wallstents have been released side by side to drain the lateral segments of the left lobe. (c) A check tubogram before removal of the safety catheters demonstrates good decompression of the left-side bile ducts.
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retaining suture woven through the eyelets of each stent. Gianturco stents are excellent when dealing with benign biliary strictures (see below) but are unsuitable for malignant lesions because ingrowth of tumour results in their rapid occlusion in many cases (Coons, 1989; Irving et al, 1989). The Wallstent biliary endoprosthesis is identical in design to vascular and urethral Wallstents. It is made of stainless steel wire that has been woven into a tubular mesh (Figure 3). Since the cross-points are not soldered the wires are free to move over each other and the stent is therefore pliable, self-expanding and extremely flexible in its longitudinal axis. Its diameter can be substantially reduced by moderate elongation, which allows it to be mounted on a 7-FG catheter for introduction into the biliary system. This means that, unlike all other biliary stents, the Wallstent can often be inserted transhepatically in a one-stage procedure at the same time as percutaneous biliary drainage is performed, even in a patient with a complex hilar stricture such as the one illustrated in Figure 4. This has the advantage of shortening the patient’s stay in hospital, reducing the risk of bacterial contamination and minimizing patient discomfort. The mounted stent is constrained on the delivery catheter by a doubled-over membrane. To release the stent, the outer membrane is slowly withdrawn which allows the stent to return to its original diameter. Two radiopaque markers on the delivery catheter allow the proximal and distal ends of the stent to be identified at the time of release, hence enabling exact placement. The principles of placement of Wallstent endoprostheses are similar to those of plastic stent insertion but there are certain important differences of detail. Before stent placement the stricture is predilated with a lo-mm angioplasty balloon. An endoprosthesis of appropriate length is then chosen. For strictures at the hilum of the liver or the middle of the common bile duct, the authors prefer to use a long endoprosthesis which will have its proximal end peripherally in an intrahepatic duct and its lower end l-2cm above the ampulla of Vater. In cases of lower common bile duct lesions the stent must project through the ampulla into the duodenum. The policy of using long stents does not lead to obstruction of side branches draining into or converging with the duct containing the endoprosthesis within the liver. Such branches continue to drain through the side wall of the Wallstent even months after the initial placement of the endoprosthesis. The use of long stents delays occlusion caused by overgrowth of tumour above or below the stent. In patients with pancreatic carcinoma occluding the lower common bile duct, a long stent projecting above the hilum of the liver will help to prevent hilar duct obstruction due to enlarged lymph nodes containing metastases. Following selection of a stent of appropriate length, the introducing catheter is advanced until the distal metallic marker which corresponds with the lower end of the stent is immediately above the ampulla of Vater (except in patients with lower common bile duct lesions in whom the stent projects into the duodenum). The plastic membrane is then withdrawn until approximately half the endoprosthesis is expanded. The position of the upper end of the stent is then adjusted by withdrawing the endoprosthesis to an appropriate point within a peripheral hepatic duct. The stent is then released by complete withdrawal of the plastic membrane. The lo-mm
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Figure 5. Wallstents used for palliation of irresectable hilar cholangiocarcinoma. (a) A tubogram performed via a right-side biliary drainage catheter demonstrates obstruction of the left and right ducts by a hilar tumour. (b) The left-side ducts are also drained and two Wallstents are placed across the hilar stricture, one from the left and one from the right. (c) A final tubogram demonstrates decompression of all the intrahepatic ducts. This patient remained asymptomatic 8 months later.
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angioplasty balloon catheter may then be used to expand the stent at the point where it crosses the malignant stricture until it achieves its maximum internal diameter of 1 cm, but this manoeuvre is not essential as the stent exerts a continuous radial force and will expand spontaneously over the following few days. It may even be detrimental to postdilate in some cases, as passage of the balloon through the stent may dislodge it and change its position. Following release of the endoprosthesis, a 6-FG temporary external drainage catheter is advanced through the stent over the guide wire and is left in place overnight for check cholangiography to be carried out the following day, after which the catheter is removed. It is wise to preload an 8-FG plastic sheath over the introducing catheter of the Wallstent. The sheath is kept over the part of the catheter which is outside the body, and is not usually employed at all during insertion of the stent; however, if the endoprosthesis is pulled proximally during the procedure, but has not been completely released, the sheath makes it possible to reposition it by advancing the sheath over the Wallstent, thus closing it. The endoprosthesis, enclosed within the sheath, is advanced to the desired position; the sheath is then withdrawn and the stent is released. If it is desired to drain both sides of the liver in the case of a malignant hilar lesion, this can be done by deploying two Wallstents side by side, either through the same transhepatic track (in a T configuration) or through two different tracks, one on the left and one on the right (Figure 5). During the latter it is best to release the two stents simultaneously (using two operators) to avoid displacement of the first stent during the release of the second. Alternatively, two long 9-FG sheaths can be placed in the ducts and the endoprostheses partially released within the sheaths until most of each stent has expanded but has not been detached from the introducing catheter. The sheaths are then withdrawn before the endoprostheses are released completely. The side-by-side configuration has the advantage of allowing a more proximal placement of the upper ends of the endoprostheses within intrahepatic ducts, thus delaying occlusion by tumour overgrowth. In addition, the procedure of stent overlap for the purpose of unblocking a stent occluded by overgrowth of tumour is technically more straightforward when a side-by-side arrangement is used. This is achieved by inserting a catheter into the biliary tree through a puncture made as peripherally as possible, passing a guide wire through the occluded stent and using an introducing catheter to overlap a second stent with the first one, making sure that the end of the new stent projects well clear of the tumour. This manoeuvre restores patency of the biliary system and can be used on more than one occasion if recurrent occlusion occurs (Figure 6). In cases of advanced hilar malignancy extending into the liver, it may be necessary not only to unblock the Wallstent using the method described above, but also to drain the contralateral lobe if this has not already been stented. This requires the advancement of a guide wire through the mesh of the original stent . This is most easily achieved using a glidewire (Terumo Inc). A low-profile angioplasty catheter is then advanced over the wire and the balloon used to split the struts of the endoprosthesis, creating a hole in the side of the stent. A second endoprosthesis can then be placed through this hole to establish drainage of the originally undrained lobe.
M. E. RODDIE AND A. ADAM
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(b)
Figure 6. Stent overlap performed because of recurrent tumour overgrowth. (a) Plain film of three overlapping Wallstents (arrows) in a patient with a hilar cholangiocarcinoma who presented with tumour overgrowth of the proximal end of the stent on two occasions. As tumour grew into the liver, the stents were placed further into the intrahepatic ducts. (b) A tubogram performed prior to removal of the safety catheter after the third Wallstent had been placed.
Clinical results As metallic stents have only recently become available, few studies have been published and follow-up is still relatively short. However, it seems clear that Wallstents are best suited for malignant strictures while Gianturco stents are ideal for use in the management of difficult benign biliary strictures after surgery and balloon dilation have failed (Figure 7). Wallstents and malignant biliary strictures The results from five centres are summarized in Table 1 (Klein and Lammer, 1989; Neuhaus et al, 1989; Gillams et al, 1990; Gordon et al, 1990; Adam et al, 1991). The 30-day mortality rate is approximately 5%, which is significantly lower than the reported 15-24% rate after insertion of plastic stents (Coons and Carey, 1983; Mueller et al, 1985; Lammer and Neumayer, 1986). Stent migration has not been observed but stent occlusion has been seen in 5-45% of patients. Although stent occlusion due to bile encrustation has been observed (Gillams et al, 1990), blockage has more frequently been caused by tumour growth. In a few cases tumour ingrowth has occurred through the mesh of the stent, but more often, tumour overgrowth above or below the stent has been the cause of the blockage. Tumour overgrowth was encountered more frequently when short Wallstents were used and appreciation of the problem has led to the routine use of longer (10 cm) Wallstents
Figure 7. Gianturco stent used in a recurrent stricture at a bilioenteric anastomosis. The patient has hypertrophy of the left lobe of the liver following longstanding obstruction and subsequent atrophy of the right lobe. (a) A left-sided percutaneous transhepatic cholangiogram shows a tight anastomotic stricture (arrow). The dilated intrahepatic ducts contain numerous calculi. Repeated balloon dilation failed to dilate the stricture. (b) Following puncture of a subparietal access loop, a barbed Gianturco stent is placed across the anastomotic stricture using a retrograde approach. The stent has hardly opened. (c) One week after insertion the stent has partly opened. (d) One month after insertion the stent has almost fully opened. This degree of stricture dilatation could not have been achieved by balloon dilation alone, and has occurred because of the constant outward radial force exerted by the stent over a prolonged period of time.
Table
Reference Neuhaus et al, 1989 Gordon et al, 1990 Klein and Lammer, 1989 Gillams et al, 1990 Adam et al, 1991 Total
1.
Wallstents in malignant biliary strictures.
No. of patients I 31 34 40 41 153
Follow-up (months) 2.8 4.0 4.5 8.5 16.0 I
Obstruction (“ro) 0 37 5 45 I 19
Dislocation (%I 0 0 0 0 0 0
30-day mortality 0 6 3 7 I 5
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in an attempt to delay stent occlusion. In the authors’ own experience of 58 consecutive patients managed with Wallstents during a 28-month period, no tumour ingrowth or bile encrustation was seen, but 5 patients (8.5%) with Wallstent occlusion due to tumour overgrowth were treated successfully by the insertion of another stent overlapping the first (Jackson et al, in press). Gianturco stents in benign biliary strictures Benign biliary strictures represent a distinct therapeutic problem due to the high frequency of recurrence after treatment. Primary surgical repair, when performed by an experienced surgeon, has a success rate of 78-88% (Way et al, 1981; Pitt et al, 1982). Recurrences develop in 15-25% of cases but the success rate of surgical repair decreases as the number of attempts increases. Percutaneous balloon dilation has become a viable alternative to surgery in benign biliary strictures and has a reported success rate of 76-88% in iatrogenic non-anastomotic strictures and 67-73% in anastomotic strictures (Mueller et al, 1986; Moore et al, 1987; Williams et al, 1987). However, there is also a significant recurrence rate after balloon dilation, thought to be due to chronic inflammation and the presence of an elastic component in the scar tissue. In these patients plastic endoprostheses cannot be used for long-term drainage because of their tendency to occlude after 5-8 months. Long-term internal/external drainage tubes can be used but may be unacceptable to patients, many of whom are relatively young. Self-expanding stainless steel stents represent a solution because they exert continuous outward radial pressure to the bile duct and prevent elastic recoil of the diseased wall and possible repeat stricture formation. Results of three early trials using Gianturco stents in benign biliary strictures are summarized in Table 2 (Coons, 1989; Irving et al, 1989; Rossi et al, 1990). Although several Table
Reference Coons, 1989 Rossi et al, 1990 Irving et al, 1989 Total
2.
Gianturco stents in benign biliary strictures.
No. of patients
Follow-up (months)
15 17 11 43
6 (Al) 7
Obstruction (%) 13 12 7 11
Dislocation (B) 0 12 7 6
30-day mortality 0 0 0 0
stents have been misplaced at the time of stent insertion, only one delayed stent migration has been reported (Irving et al, 1989). This was a single, non-barbed Gianturco stent placed across a short anastomotic stricture which migrated into the jejunal loop after 5 months. This problem can be avoided by the use of barbed stents or by the use of a double stent with the midportion placed at the narrowest point of the stricture. Gianturco stent occlusion has been reported in 7-13% of cases; this is thought to be due to mucosal hyperplasia or fibrotic overgrowth in most cases, although a few cases have been due to stricture recurrence between the junction of two stents. No serious complications have been seen and the 30-day mortality
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has been zero. This compares favourably with the 7.7% mortality rate attributed to surgery (Pitt et al, 1981). The long-term patency rate and the effects of metallic stents on the bile duct wall have not yet been documented. Although the initial results appear promising, metallic biliary stents should only be used in the treatment of benign biliary strictures in selected cases where repeated balloon dilation has failed, until the questions concerning long-term outcome are resolved. SUMMARY
The development of self-expanding metallic endoprostheses which can be implanted easily, with minimal trauma, has revolutionized the non-surgical treatment of both benign and malignant biliary strictures. The Wallstent (Medinvent SA, Lausanne, Switzerland), a pliable, tubular stainless steel mesh, is the metallic stent of choice for treatment of malignant strictures and can be implanted in a single session resulting in a shortened hospital stay for patients undergoing palliation of irresectable biliary tumours. Although follow-up is currently rather limited, it appears that the occlusion rate of Wallstents will be lower than that of plastic endoprostheses and no cases of stent migration have been reported. The Gianturco zigzag stent (Cook Inc., Bloomington, Ind, USA) should not be used in malignant strictures because of rapid occlusion due to tumour ingrowth through the struts. However, it exerts a strong, continuous, outward radial force and is ideally suited for use in the small, but difficult to manage, group of patients with benign biliary strictures which recur despite surgery and repeated balloon dilations.
REFERENCES Adam A, Chetty N, Roddie M, Yeung E & Benjamin IS (1991) Self-expandable stainless steel endoprosthesis for treatment of malignant bile duct obstruction. American Journal of Roentgenology
156: 321-32.5.
Ahlstrom H, Lorelius LE & Jacobson G (1986) Inoperable biliary obstruction treated with percutaneously placed endoprosthesis. Act; Chi&gica Scandinavica 152: 301-303. Alvarado R, Palmaz JC. Garcia OJ. Tio FO & Rees CR (1989) Evaluation of nolvmer-coated balloon expandable stents in bile ducts. Radiology i70: 9k978. ’ ’ Coons HG (1989) Self-expanding stainless steel biliary stents. Radiology 170: 979-983. Coons HG & Carey PH (1983) Large-bore, long bihary endoprostheses (biliary stents) for improved drainage. Radiology 148: 89-94. Dicks R, Gillams A, Dooley JS & Hobbs KEF (1989) Stainless steel mesh stents for biliary strictures. Journal of Interventional Radiology 4: 95-98. Ferrucci JT (1985) Biliary endoprosthesis. In Ferrucci JT, Wittenberg J, Mueller PR & Simeone JF (eds) Interventional Radiolonv -, of_ the Abdomen, DD L . 267-281. Philadelnhia: 1 WB Saunders. Gillams A, Dick R, Dooley JS, Wallsten H & El-Din A (1990) Self-expandable stainless steel braided endoprostheses for biliary strictures. Radiology 174: 137-140. Gordon RL, Dick’BW. LaBerge JM, Doherty MM & Ring EJ (1990) Clinical comparison of percutaneous use of metallic expandable Wallstents and conventional plastic endoprostheses in malignant biliary obstruction. Radiology 177(P): 137.
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Groen AK, Out T, Huibregtse J, Delzenne B, Hoek FJ & Tygat GNJ (1987) Characterization of the contents of occluded biliary endoprostheses. Endoscopy 19: 57-59. Irving JD, Adam A, Dick R, Dondelinger RF, Lunderquist A & Roche A (1989) Gianturco expandable metallic biliary stents: results of a European clinical trial. Radiology 172: 321-326.
Jackson JE, Roddie ME, Yeung EYC, Benjamin IS & Adam A (1990) Biliary endoprosthesis dysfunction in patients with malignant hilar turnours: successful treatment by percutaneous replacement of the stent. American Journal of Roentgenology 155: 391-395. Jackson JE, Roddie ME, Chetty N, Benjamin IS & Adam A Management of occluded metallic self-expandable bihary endoprostheses. American Journal of Roentgenology (in press). Klein GE & Lammer J (1989) Primary implantation of expandable Wallstent endoprostheses for relief of obstructive jaundice. Radiology 173(P): 378. Lammer J & Neymayer K (1986) Biliary drainage endoprosthesis; experience with 201 placements. Radiology 159: 625-629. Lammer J, Stoeffler G, Petek WW & Hofler H (1986) In vitro long-term perfusion of different materials for biliary endoprostheses. Investigative Radiology 21: 329-331. Leung JWL, Ling TKW, Kung JLS & Valance-Owen J (1988) The role of bacteria in the blockage of bihary stents. Gastrointestinal Radiology 34: 19-22. Moore AV Jr, Illescas FF, Mills SR et al (1987) Percutaneous dilatation of benign strictures. Radiology
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Mueller PR, Ferrucci JT, Teplick SK et al (1985) Biliary stent endoprosthesis: analysis of complications in 113 patients. Radiology 156: 637-639. Mueller PR, vansonnenberg E, Ferrucci JT Jr et al (1986) Bihary stricture dilatation: multicentre review of clinical management in 73 patients. Radiology 160: 17-22. Neuhaus H, Hagenmuller F & Classen M (1989) Self-expanding bihary stents: preliminary clinical experience. Endoscopy 21: 225-228. Palmaz JC, Sibbitt RR, Reuter SR, Tio FO & Rice WJ (1985) Expandable intraluminal graft: a preliminary study. Radiology 156: 73-77. Pitt HA, Cameron JL, Postier RG & Gadacz TR (1981) Factors affecting mortality in biliary tract surgery. American Journal of Surgery 141: 66-70. Pitt HA, Miyamoto T, Parapatis SK, Tompkins RK & Longmire WP (1982) Factors influencing outcome in patients with postoperative bihary strictures. American Journal of Surgery 144: 14-21. Rey JF, Maupetit P & Graff M (1985) Experimental study of biliary endoprosthesis efficiency. Endoscopy 17: 145-148. Rossi P, Bezzi M, Salvatori FM, Maccioni F & Porcaro ML (1990) Recurrent benign biliary strictures: management with self-expanding metallic stents. Radiology 175: 661-665. Teplick SK (1991) Percutaneous transhepatic insertion of bihary endoprostheses. In Kadir S (ed.) Current Practice of Interventional Radiology, pp 557-562. Philadelphia: Decker. Teplick SK, Haskin PH, Goldstein RC et al (1983) A new biliary endoprosthesis. American Journal
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Way LW, Bernhoft America
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RA & Thomas MJ (1981) Biliary stricture. Surgical
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Williams HT Jr, Bender CE & May GR (1987) Benign postoperative biliary strictures: dilatation with fluoroscopic guidance. Radiology 163: 62%634. Yeung ECY, Adam A, Gibson RN, Benjamin IS & Allison DJ (1988) Spiral shaped biliary endoprosthesis: initial study. Radiology 168: 365-369.
The main indication for the use of biliary endoprostheses is as an alternative to surgical bilioenteric bypass in the palliation of malignant bile duct obstruction, although they are occasionally used in the treatment of benign biliary strictures. Although some interventional radiologists believe that endoprostheses should be reserved for patients whose life expectancy is relatively short, in order to avoid the problem of stent occlusion (Ferrucci, 1985), we believe that endoprostheses should be inserted in virtually all patients with malignant obstructive jaundice in whom such insertion is technically feasible. Our preference for endoprostheses over internal/ external drainage catheters is based on a number of factors, including the fact that external catheters are associated with complications such as occasional leakage of bile around the catheter, and infection and pain at the skin entry site. However, our main objection to long-term external catheters is the permanent and unkind reminder to patients of their underlying malignancy and shortened life expectancy. The main objection to the use of indwelling stents has been the fact that they are likely to become occluded in patients with a relatively long life expectancy. This argument, however, is no longer valid as endoscopic and percutaneous stent changes have become routine procedures. Stents can be introduced transhepatically or endoscopically, and the choice of technique will be strongly influenced by the availability of local expertise. However, in most patients with unresectable, low-lying lesions such as pancreatic carcinoma, an endoscopic approach is preferable. In contrast, the proximal, high-level obstruction (especially when it results in isolation of multiple intrahepatic ductal systems) is best approached percutaneously by the interventional radiologist. PLASTIC
STENTS
Since the first description of percutaneous placement of a biliary endoprosthesis (Ahlstrom et al, 1986), attempts have been made to define the optimal configuration of biliary stents. Ideally, they should be easy to insert, have a low occlusion rate and produce minimal complications both during placement and once they have been released into the biliary system. Until BaiNi&eS Clinical GastroenterologyVol. 6, No. 2, June 1992 ISBN o-7020-1623-3
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recently, all endoprostheses have been made of plastic (Teflon, polyethylene, polyurethane, silicone or Percuflex), and various diameters and shapes have been used in an attempt to reduce the two most common causes of stent failure, namely stent occlusion and migration. These complications have been seen in approximately 6-23% and 3-6% of cases, respectively, in two large series (Mueller et al, 1985; Lammer and Neumayer, 1986). Occlusion Although stent occlusion may occur because of tumour overgrowth, the most common cause is bile encrustation; in patients who live longer than 6-18 months after placement of a plastic stent, occlusion will occur in approximately 20-30% (Teplick, 1991). However, nearly all blocked plastic endoprostheses can be changed either endoscopically or percutaneously (Jackson et al, 1990) and most patients, given the choice, prefer to have an additional procedure to replace the occluded stent rather than be left with a long-term external drainage catheter. Formation of encrustations depends on the mechanical and chemical surface characteristics of the stent material and on the surrounding bacterial population. Examination of occluded endoprostheses suggests that the initiating event is bacterial adherence to the stent surface, which is rapidly followed by deposition of a glycoprotein. Increasing numbers of bacteria result in deconjugation of bilirubin and deposition of calcium bilirubinate which eventually blocks the stent. Studies in vitro (Lammer et al, 1986) have shown that polyurethane and Percuflex stents have the lowest encrustation rates. However, owing to their flexibility, the walls of these stents have to be thicker, reducing the inner diameter; this is undesirable because there is an inverse relationship between the diameter of the lumen of biliary stents and the incidence of occlusion (Rey et al, 1985). Larger stents, on the other hand, require a large transhepatic track for their introduction with subsequent increased trauma to the liver and a larger risk of serious complications such as the formation of pseudoaneurysms, arteriobiliary or portobiliary fistulae, and intrahepatic and perihepatic bilomas. It is generally accepted that the optimum size for a transhepatically placed plastic stent is 12 French gauge. The maximum size of an endoscopically placed stent is governed by the size of the endoscope itself. Larger sphincterotomies are needed for the placement of bigger endoscopic stents with a resultant increase in the risk of bleeding, perforation and pancreatitis. Migration In an effort to combat the problems of stent migration, various designs have been introduced including spirals (Yeung et al, 1988), stents with collapsible mushrooms (Teplick et al, 1983) or subcutaneous plastic buttons attached to the endoprosthesis (Coons and Carey, 1983). The rate of migration of straight stents can be reduced by increasing stent length, but this has the disadvantage of leaving the lower end of the stent protruding into the duodenum, which (as well as leading to clogging of the lower portion by
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vegetable fibres) leads to contamination with bacteria from duodenal contents, which in turn predisposes to bile encrustation (Groen et al, 1987; Leung et al, 1988). However, this risk should be balanced by the possibility of endoscopic replacement. Such replacement is often fairly simple, even though the original stent may have been placed percutaneously. METALLIC
STENTS
In recent years various metallic stents developed for use in the vascular system have been tried in the biliary tree (Alvarado et al, 1989; Coons, 1989; Dick et al, 1989). The main advantage of metallic stents is that they can be introduced in a contracted state through a very small calibre track and achieve a large internal lumen following expansion. The former should theoretically reduce the incidence of complications associated with a large liver track or sphincterotomy, while the latter, coupled with the reduced surface area of metallic stents, should reduce the incidence of blockage due to bile encrustation. In their expanded state, metallic stents are partially embedded in the duct wall and this virtually eliminates the problem of migration. In addition, some metallic stent designs incorporate sharp ends or barbs which increase the security of maintaining stent position; this means that, in contrast with plastic stents, most metallic stents currently available cannot be removed. Commercially available metallic stents fall into two main categories: balloon-expandable and self-expandable. Balloon-expandable
stents
Balloon-expandable metallic stents (e.g. the Palmaz stent and Strecker stent) consist of a continuous, woven stainless steel wire mesh which is inserted over an angioplasty balloon through a lo-FG sheath and expanded when in an optimum position across the biliary stricture. Stents of 8-10 mm in diameter are available for use in the biliary tree. The cross-points of the mesh are soldered so the stent has the capacity to retain the diameter attained by the maximal balloon inflation. However, the rigidity inherent in this design makes it difficult to advance the stent around acute angles in the biliary system and may result in the stent being displaced from its position over the balloon (Palmaz et al, 1985). However, sufficient dilation of the track can usually overcome this problem. The lack of longitudinal flexibility limits its use to straight segments of duct-for angled segments, a series of short stents is required and the technical difficulty in achieving adequate overlap may result in tumour ingrowth through the gaps. Balloonexpandable metallic stents have therefore not been widely used in the biliary tree. Self-expandable stents The two main designs of self-expandable metallic stents are the Gianturco zigzag stent (Cook Inc., Bloomington, Ind, USA) and the Wallstent (Medinvent SA, Lausanne, Switzerland).
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The Gianturco stent is constructed of 0.45mm stainless steel wire with six zigzag bends soldered together to form a cylinder 1 S-3 cm in length and is introduced through a lo-FG sheath (Figure 1). Single stents are fitted near the midpoint with small barbs which engage in the stricture and prevent migration. Longer stents are made by connecting two to four stents by a wire strut. This not only increases flexibility but maintains the expansile force, since lengthening of an individual stent decreases its efficiency. Multiple stents are not barbed because the individual stents stabilize each other and prevent migration. The Rosch modification of the Gianturco stent, which is the type usually employed in the biliary tree, has a nylon suture running through eyelets at each end to control the diameter of the cylinder (Figure 2). Extrahepatic ducts require lo-mm diameter stents, while for intrahepatic biliary radicles, 8-mm stents are used. Most stents are used in tandem with a
Figure 1. Gianturco stents (unmodified). (a) On the left is a single stent fitted near the midpoint with small barbs. On the right is a longer stent consisting of three stents connected by a wire strut. (b) Gianturco stent loaded into a 12-FG sheath prior to implantation.
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Figure 2. R6sch modification of the Gianturco stent. A single stent is seen on the left and a double stent on the right.
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Figure 3. Wallstent: (a) when released, the Wallstent is extremely flexible in its longitudinal axis; (b) it can be mounted on a 7-FG catheter for introduction into the biliary tree.
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Figure 4. Irresectable hilar cholangiocarcinoma causing second-order duct involvement on the left and right. The right lobe was atrophic and it was therefore decided to stent the left lobe only. As segments II and III are no longer communicating because of tumour extension, each has to be stented separately. (a) Segment II has been cannulated and a tubogram demonstrates the hilar stricture. (b) Following cannulation of segment III, two Wallstents have been released side by side to drain the lateral segments of the left lobe. (c) A check tubogram before removal of the safety catheters demonstrates good decompression of the left-side bile ducts.
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retaining suture woven through the eyelets of each stent. Gianturco stents are excellent when dealing with benign biliary strictures (see below) but are unsuitable for malignant lesions because ingrowth of tumour results in their rapid occlusion in many cases (Coons, 1989; Irving et al, 1989). The Wallstent biliary endoprosthesis is identical in design to vascular and urethral Wallstents. It is made of stainless steel wire that has been woven into a tubular mesh (Figure 3). Since the cross-points are not soldered the wires are free to move over each other and the stent is therefore pliable, self-expanding and extremely flexible in its longitudinal axis. Its diameter can be substantially reduced by moderate elongation, which allows it to be mounted on a 7-FG catheter for introduction into the biliary system. This means that, unlike all other biliary stents, the Wallstent can often be inserted transhepatically in a one-stage procedure at the same time as percutaneous biliary drainage is performed, even in a patient with a complex hilar stricture such as the one illustrated in Figure 4. This has the advantage of shortening the patient’s stay in hospital, reducing the risk of bacterial contamination and minimizing patient discomfort. The mounted stent is constrained on the delivery catheter by a doubled-over membrane. To release the stent, the outer membrane is slowly withdrawn which allows the stent to return to its original diameter. Two radiopaque markers on the delivery catheter allow the proximal and distal ends of the stent to be identified at the time of release, hence enabling exact placement. The principles of placement of Wallstent endoprostheses are similar to those of plastic stent insertion but there are certain important differences of detail. Before stent placement the stricture is predilated with a lo-mm angioplasty balloon. An endoprosthesis of appropriate length is then chosen. For strictures at the hilum of the liver or the middle of the common bile duct, the authors prefer to use a long endoprosthesis which will have its proximal end peripherally in an intrahepatic duct and its lower end l-2cm above the ampulla of Vater. In cases of lower common bile duct lesions the stent must project through the ampulla into the duodenum. The policy of using long stents does not lead to obstruction of side branches draining into or converging with the duct containing the endoprosthesis within the liver. Such branches continue to drain through the side wall of the Wallstent even months after the initial placement of the endoprosthesis. The use of long stents delays occlusion caused by overgrowth of tumour above or below the stent. In patients with pancreatic carcinoma occluding the lower common bile duct, a long stent projecting above the hilum of the liver will help to prevent hilar duct obstruction due to enlarged lymph nodes containing metastases. Following selection of a stent of appropriate length, the introducing catheter is advanced until the distal metallic marker which corresponds with the lower end of the stent is immediately above the ampulla of Vater (except in patients with lower common bile duct lesions in whom the stent projects into the duodenum). The plastic membrane is then withdrawn until approximately half the endoprosthesis is expanded. The position of the upper end of the stent is then adjusted by withdrawing the endoprosthesis to an appropriate point within a peripheral hepatic duct. The stent is then released by complete withdrawal of the plastic membrane. The lo-mm
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Figure 5. Wallstents used for palliation of irresectable hilar cholangiocarcinoma. (a) A tubogram performed via a right-side biliary drainage catheter demonstrates obstruction of the left and right ducts by a hilar tumour. (b) The left-side ducts are also drained and two Wallstents are placed across the hilar stricture, one from the left and one from the right. (c) A final tubogram demonstrates decompression of all the intrahepatic ducts. This patient remained asymptomatic 8 months later.
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angioplasty balloon catheter may then be used to expand the stent at the point where it crosses the malignant stricture until it achieves its maximum internal diameter of 1 cm, but this manoeuvre is not essential as the stent exerts a continuous radial force and will expand spontaneously over the following few days. It may even be detrimental to postdilate in some cases, as passage of the balloon through the stent may dislodge it and change its position. Following release of the endoprosthesis, a 6-FG temporary external drainage catheter is advanced through the stent over the guide wire and is left in place overnight for check cholangiography to be carried out the following day, after which the catheter is removed. It is wise to preload an 8-FG plastic sheath over the introducing catheter of the Wallstent. The sheath is kept over the part of the catheter which is outside the body, and is not usually employed at all during insertion of the stent; however, if the endoprosthesis is pulled proximally during the procedure, but has not been completely released, the sheath makes it possible to reposition it by advancing the sheath over the Wallstent, thus closing it. The endoprosthesis, enclosed within the sheath, is advanced to the desired position; the sheath is then withdrawn and the stent is released. If it is desired to drain both sides of the liver in the case of a malignant hilar lesion, this can be done by deploying two Wallstents side by side, either through the same transhepatic track (in a T configuration) or through two different tracks, one on the left and one on the right (Figure 5). During the latter it is best to release the two stents simultaneously (using two operators) to avoid displacement of the first stent during the release of the second. Alternatively, two long 9-FG sheaths can be placed in the ducts and the endoprostheses partially released within the sheaths until most of each stent has expanded but has not been detached from the introducing catheter. The sheaths are then withdrawn before the endoprostheses are released completely. The side-by-side configuration has the advantage of allowing a more proximal placement of the upper ends of the endoprostheses within intrahepatic ducts, thus delaying occlusion by tumour overgrowth. In addition, the procedure of stent overlap for the purpose of unblocking a stent occluded by overgrowth of tumour is technically more straightforward when a side-by-side arrangement is used. This is achieved by inserting a catheter into the biliary tree through a puncture made as peripherally as possible, passing a guide wire through the occluded stent and using an introducing catheter to overlap a second stent with the first one, making sure that the end of the new stent projects well clear of the tumour. This manoeuvre restores patency of the biliary system and can be used on more than one occasion if recurrent occlusion occurs (Figure 6). In cases of advanced hilar malignancy extending into the liver, it may be necessary not only to unblock the Wallstent using the method described above, but also to drain the contralateral lobe if this has not already been stented. This requires the advancement of a guide wire through the mesh of the original stent . This is most easily achieved using a glidewire (Terumo Inc). A low-profile angioplasty catheter is then advanced over the wire and the balloon used to split the struts of the endoprosthesis, creating a hole in the side of the stent. A second endoprosthesis can then be placed through this hole to establish drainage of the originally undrained lobe.
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(b)
Figure 6. Stent overlap performed because of recurrent tumour overgrowth. (a) Plain film of three overlapping Wallstents (arrows) in a patient with a hilar cholangiocarcinoma who presented with tumour overgrowth of the proximal end of the stent on two occasions. As tumour grew into the liver, the stents were placed further into the intrahepatic ducts. (b) A tubogram performed prior to removal of the safety catheter after the third Wallstent had been placed.
Clinical results As metallic stents have only recently become available, few studies have been published and follow-up is still relatively short. However, it seems clear that Wallstents are best suited for malignant strictures while Gianturco stents are ideal for use in the management of difficult benign biliary strictures after surgery and balloon dilation have failed (Figure 7). Wallstents and malignant biliary strictures The results from five centres are summarized in Table 1 (Klein and Lammer, 1989; Neuhaus et al, 1989; Gillams et al, 1990; Gordon et al, 1990; Adam et al, 1991). The 30-day mortality rate is approximately 5%, which is significantly lower than the reported 15-24% rate after insertion of plastic stents (Coons and Carey, 1983; Mueller et al, 1985; Lammer and Neumayer, 1986). Stent migration has not been observed but stent occlusion has been seen in 5-45% of patients. Although stent occlusion due to bile encrustation has been observed (Gillams et al, 1990), blockage has more frequently been caused by tumour growth. In a few cases tumour ingrowth has occurred through the mesh of the stent, but more often, tumour overgrowth above or below the stent has been the cause of the blockage. Tumour overgrowth was encountered more frequently when short Wallstents were used and appreciation of the problem has led to the routine use of longer (10 cm) Wallstents
Figure 7. Gianturco stent used in a recurrent stricture at a bilioenteric anastomosis. The patient has hypertrophy of the left lobe of the liver following longstanding obstruction and subsequent atrophy of the right lobe. (a) A left-sided percutaneous transhepatic cholangiogram shows a tight anastomotic stricture (arrow). The dilated intrahepatic ducts contain numerous calculi. Repeated balloon dilation failed to dilate the stricture. (b) Following puncture of a subparietal access loop, a barbed Gianturco stent is placed across the anastomotic stricture using a retrograde approach. The stent has hardly opened. (c) One week after insertion the stent has partly opened. (d) One month after insertion the stent has almost fully opened. This degree of stricture dilatation could not have been achieved by balloon dilation alone, and has occurred because of the constant outward radial force exerted by the stent over a prolonged period of time.
Table
Reference Neuhaus et al, 1989 Gordon et al, 1990 Klein and Lammer, 1989 Gillams et al, 1990 Adam et al, 1991 Total
1.
Wallstents in malignant biliary strictures.
No. of patients I 31 34 40 41 153
Follow-up (months) 2.8 4.0 4.5 8.5 16.0 I
Obstruction (“ro) 0 37 5 45 I 19
Dislocation (%I 0 0 0 0 0 0
30-day mortality 0 6 3 7 I 5
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in an attempt to delay stent occlusion. In the authors’ own experience of 58 consecutive patients managed with Wallstents during a 28-month period, no tumour ingrowth or bile encrustation was seen, but 5 patients (8.5%) with Wallstent occlusion due to tumour overgrowth were treated successfully by the insertion of another stent overlapping the first (Jackson et al, in press). Gianturco stents in benign biliary strictures Benign biliary strictures represent a distinct therapeutic problem due to the high frequency of recurrence after treatment. Primary surgical repair, when performed by an experienced surgeon, has a success rate of 78-88% (Way et al, 1981; Pitt et al, 1982). Recurrences develop in 15-25% of cases but the success rate of surgical repair decreases as the number of attempts increases. Percutaneous balloon dilation has become a viable alternative to surgery in benign biliary strictures and has a reported success rate of 76-88% in iatrogenic non-anastomotic strictures and 67-73% in anastomotic strictures (Mueller et al, 1986; Moore et al, 1987; Williams et al, 1987). However, there is also a significant recurrence rate after balloon dilation, thought to be due to chronic inflammation and the presence of an elastic component in the scar tissue. In these patients plastic endoprostheses cannot be used for long-term drainage because of their tendency to occlude after 5-8 months. Long-term internal/external drainage tubes can be used but may be unacceptable to patients, many of whom are relatively young. Self-expanding stainless steel stents represent a solution because they exert continuous outward radial pressure to the bile duct and prevent elastic recoil of the diseased wall and possible repeat stricture formation. Results of three early trials using Gianturco stents in benign biliary strictures are summarized in Table 2 (Coons, 1989; Irving et al, 1989; Rossi et al, 1990). Although several Table
Reference Coons, 1989 Rossi et al, 1990 Irving et al, 1989 Total
2.
Gianturco stents in benign biliary strictures.
No. of patients
Follow-up (months)
15 17 11 43
6 (Al) 7
Obstruction (%) 13 12 7 11
Dislocation (B) 0 12 7 6
30-day mortality 0 0 0 0
stents have been misplaced at the time of stent insertion, only one delayed stent migration has been reported (Irving et al, 1989). This was a single, non-barbed Gianturco stent placed across a short anastomotic stricture which migrated into the jejunal loop after 5 months. This problem can be avoided by the use of barbed stents or by the use of a double stent with the midportion placed at the narrowest point of the stricture. Gianturco stent occlusion has been reported in 7-13% of cases; this is thought to be due to mucosal hyperplasia or fibrotic overgrowth in most cases, although a few cases have been due to stricture recurrence between the junction of two stents. No serious complications have been seen and the 30-day mortality
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has been zero. This compares favourably with the 7.7% mortality rate attributed to surgery (Pitt et al, 1981). The long-term patency rate and the effects of metallic stents on the bile duct wall have not yet been documented. Although the initial results appear promising, metallic biliary stents should only be used in the treatment of benign biliary strictures in selected cases where repeated balloon dilation has failed, until the questions concerning long-term outcome are resolved. SUMMARY
The development of self-expanding metallic endoprostheses which can be implanted easily, with minimal trauma, has revolutionized the non-surgical treatment of both benign and malignant biliary strictures. The Wallstent (Medinvent SA, Lausanne, Switzerland), a pliable, tubular stainless steel mesh, is the metallic stent of choice for treatment of malignant strictures and can be implanted in a single session resulting in a shortened hospital stay for patients undergoing palliation of irresectable biliary tumours. Although follow-up is currently rather limited, it appears that the occlusion rate of Wallstents will be lower than that of plastic endoprostheses and no cases of stent migration have been reported. The Gianturco zigzag stent (Cook Inc., Bloomington, Ind, USA) should not be used in malignant strictures because of rapid occlusion due to tumour ingrowth through the struts. However, it exerts a strong, continuous, outward radial force and is ideally suited for use in the small, but difficult to manage, group of patients with benign biliary strictures which recur despite surgery and repeated balloon dilations.
REFERENCES Adam A, Chetty N, Roddie M, Yeung E & Benjamin IS (1991) Self-expandable stainless steel endoprosthesis for treatment of malignant bile duct obstruction. American Journal of Roentgenology
156: 321-32.5.
Ahlstrom H, Lorelius LE & Jacobson G (1986) Inoperable biliary obstruction treated with percutaneously placed endoprosthesis. Act; Chi&gica Scandinavica 152: 301-303. Alvarado R, Palmaz JC. Garcia OJ. Tio FO & Rees CR (1989) Evaluation of nolvmer-coated balloon expandable stents in bile ducts. Radiology i70: 9k978. ’ ’ Coons HG (1989) Self-expanding stainless steel biliary stents. Radiology 170: 979-983. Coons HG & Carey PH (1983) Large-bore, long bihary endoprostheses (biliary stents) for improved drainage. Radiology 148: 89-94. Dicks R, Gillams A, Dooley JS & Hobbs KEF (1989) Stainless steel mesh stents for biliary strictures. Journal of Interventional Radiology 4: 95-98. Ferrucci JT (1985) Biliary endoprosthesis. In Ferrucci JT, Wittenberg J, Mueller PR & Simeone JF (eds) Interventional Radiolonv -, of_ the Abdomen, DD L . 267-281. Philadelnhia: 1 WB Saunders. Gillams A, Dick R, Dooley JS, Wallsten H & El-Din A (1990) Self-expandable stainless steel braided endoprostheses for biliary strictures. Radiology 174: 137-140. Gordon RL, Dick’BW. LaBerge JM, Doherty MM & Ring EJ (1990) Clinical comparison of percutaneous use of metallic expandable Wallstents and conventional plastic endoprostheses in malignant biliary obstruction. Radiology 177(P): 137.
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Groen AK, Out T, Huibregtse J, Delzenne B, Hoek FJ & Tygat GNJ (1987) Characterization of the contents of occluded biliary endoprostheses. Endoscopy 19: 57-59. Irving JD, Adam A, Dick R, Dondelinger RF, Lunderquist A & Roche A (1989) Gianturco expandable metallic biliary stents: results of a European clinical trial. Radiology 172: 321-326.
Jackson JE, Roddie ME, Yeung EYC, Benjamin IS & Adam A (1990) Biliary endoprosthesis dysfunction in patients with malignant hilar turnours: successful treatment by percutaneous replacement of the stent. American Journal of Roentgenology 155: 391-395. Jackson JE, Roddie ME, Chetty N, Benjamin IS & Adam A Management of occluded metallic self-expandable bihary endoprostheses. American Journal of Roentgenology (in press). Klein GE & Lammer J (1989) Primary implantation of expandable Wallstent endoprostheses for relief of obstructive jaundice. Radiology 173(P): 378. Lammer J & Neymayer K (1986) Biliary drainage endoprosthesis; experience with 201 placements. Radiology 159: 625-629. Lammer J, Stoeffler G, Petek WW & Hofler H (1986) In vitro long-term perfusion of different materials for biliary endoprostheses. Investigative Radiology 21: 329-331. Leung JWL, Ling TKW, Kung JLS & Valance-Owen J (1988) The role of bacteria in the blockage of bihary stents. Gastrointestinal Radiology 34: 19-22. Moore AV Jr, Illescas FF, Mills SR et al (1987) Percutaneous dilatation of benign strictures. Radiology
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Mueller PR, Ferrucci JT, Teplick SK et al (1985) Biliary stent endoprosthesis: analysis of complications in 113 patients. Radiology 156: 637-639. Mueller PR, vansonnenberg E, Ferrucci JT Jr et al (1986) Bihary stricture dilatation: multicentre review of clinical management in 73 patients. Radiology 160: 17-22. Neuhaus H, Hagenmuller F & Classen M (1989) Self-expanding bihary stents: preliminary clinical experience. Endoscopy 21: 225-228. Palmaz JC, Sibbitt RR, Reuter SR, Tio FO & Rice WJ (1985) Expandable intraluminal graft: a preliminary study. Radiology 156: 73-77. Pitt HA, Cameron JL, Postier RG & Gadacz TR (1981) Factors affecting mortality in biliary tract surgery. American Journal of Surgery 141: 66-70. Pitt HA, Miyamoto T, Parapatis SK, Tompkins RK & Longmire WP (1982) Factors influencing outcome in patients with postoperative bihary strictures. American Journal of Surgery 144: 14-21. Rey JF, Maupetit P & Graff M (1985) Experimental study of biliary endoprosthesis efficiency. Endoscopy 17: 145-148. Rossi P, Bezzi M, Salvatori FM, Maccioni F & Porcaro ML (1990) Recurrent benign biliary strictures: management with self-expanding metallic stents. Radiology 175: 661-665. Teplick SK (1991) Percutaneous transhepatic insertion of bihary endoprostheses. In Kadir S (ed.) Current Practice of Interventional Radiology, pp 557-562. Philadelphia: Decker. Teplick SK, Haskin PH, Goldstein RC et al (1983) A new biliary endoprosthesis. American Journal
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Williams HT Jr, Bender CE & May GR (1987) Benign postoperative biliary strictures: dilatation with fluoroscopic guidance. Radiology 163: 62%634. Yeung ECY, Adam A, Gibson RN, Benjamin IS & Allison DJ (1988) Spiral shaped biliary endoprosthesis: initial study. Radiology 168: 365-369.
