Afferent Loop Syndrome: Treatment by Means of the Placement of Dual Stents

Vascular and Interventional Radiology Original Research Han et al. Use of Dual Stents for Treatment of Afferent Loop Syndrome Vascular and Interventional Radiology Original Research Kichang Han 1 Ho-Young Song 1 Jin Hyoung Kim 1 Jung-Hoon Park 1 Deok Ho Nam 2 Min-Hee Ryu 3 Jeong Hwan Yook 4 Han K, Song HY, Kim JH, et al. Keywords: afferent loop syndrome, percutaneous transhepatic biliary drainage, self-expandable metallic stent DOI:10.2214/AJR.12.8575 Received January 16, 2012; accepted after revision March 5, 2012. 1 Department of Radiology and Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine, 388-1, Poongnap 2-dong, Songpa-gu, Seoul 138-736, Republic of Korea. Address correspondence to H. Y. Song (hysong@amc.seoul.kr). 2 Department of Radiology, Kyung Hee University Hospital at Gangdong, School of Medicine, Kyung Hee University, Seoul, Republic of Korea. 3 Department of Internal Medicine, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea. 4 Department of General Surgery, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea. WEB This is a Web exclusive article. AJR 2012; 199:W761 W766 0361 803X/12/1996 W761 American Roentgen Ray Society Afferent Loop Syndrome: Treatment by Means of the Placement of Dual Stents OBJECTIVE. The purpose of this article is to assess the technical feasibility and clinical effectiveness of the placement of partially covered self-expandable dual stents in patients with afferent loop syndrome. MATERIALS AND METHODS. Data from 13 consecutive patients who had undergone partially covered dual stent placement for afferent loop syndrome after various types of surgery were retrospectively analyzed. Nine patients underwent stent placement via the percutaneous transhepatic biliary drainage tract, and four patients underwent placement via the peroral route. A total of 16 stents were used in this study (i.e., 15 dual stents and one fully covered esophageal stent). RESULTS. The route of stent insertion was determined on the basis of each patient s general condition, the site of obstruction, anatomic variations, and associated symptoms. Stent placement was technically successful in all patients. After stent placement, 12 of 13 patients experienced normalization of their abnormal biliary laboratory findings and decompression of the dilated bowel loop, whereas the remaining patient showed no change. This patient had to undergo the additional treatment of surgical jejunojejunostomy. No procedure-related complications occurred in any patients enrolled in this study. CONCLUSION. Placement of partially covered dual stents appears to be a promising technique that may offer successful palliation for patients who develop afferent loop syndrome after various types of surgery. A fferent loop syndrome is an uncommon complication following surgical procedures such as Billroth II gastrojejunostomy, and it occurs in approximately 0.3% of all cases [1]. It results from obstruction of the afferent loop at any site and is caused by a variety of postoperative complications, such as, adhesion, and kinking [2]. To manage afferent loop syndrome, surgical bypass procedures are considered to be the best way to resolve this condition. However, palliative surgical revisions were successfully performed in 75% of patients with afferent loop syndrome because of their poor general condition, peritoneal adhesion, or disseminated tumor [3, 4]. Alternatively, less-invasive nonsurgical procedures, such as percutaneous transhepatic biliary drainage (PTBD) and percutaneous enterostomy, have been used as a palliative option for poor surgical candidates [3 6]. Although percutaneous drainage provides excellent symptom relief, maintaining an internal tube can pose a risk for problems, such as patient inconvenience and infection [4]. Under these circumstances, the placement of bare or fully covered self-expandable metallic stents via various routes has been attempted, rather than the use of tube drainage [7 9]. However, some complications, such as tumor ingrowth and stent migration, have been reported in conventional self-expandable metallic stents. With the introduction of partially covered dual stents, such complications have dramatically decreased [10]. Recently, Gwon [11] reported successful outcomes after percutaneous transhepatic placement of partially covered dual stents in two patients with afferent loop syndrome. Because of the small sample size of the two patients in that report, further studies were needed to analyze the preferred method of stent insertion, as well as the clinical effectiveness of dual stents used to treat afferent loop syndrome. The purpose of this article is to assess the technical feasibility, clinical effectiveness, and optimal route of dual stent placement for afferent loop syndrome. AJR:199, December 2012 W761

Han et al. TABLE 1: Patient Characteristics Obstruction Patient No. Sex Age (y) Disease Surgery Interval a Site Cause Length (cm) 1 Female 27 Pancreatic head 2 Male 51 Advanced 3 Female 47 Advanced 4 Male 36 Distal CBD 5 Male 55 Advanced 6 Female 60 Distal CBD 7 Female 73 Distal CBD 8 Male 72 Advanced 9 Female 69 Pancreatic head 10 Male 52 Advanced 11 Male 66 Advanced 12 Female 71 Pancreatic head 13 Female 62 Advanced Materials and Methods Patients Before the procedure, informed consent for stent placement was obtained from each patient, and our institutional review board approved this retrospective study. The medical records of the patients enrolled in this study were thoroughly reviewed. Between April 2006 and June 2011, 13 Whipple 58 mo Mid Direct invasion by 50 mo Mid Direct invasion by 6 41 mo Proximal Extranodal invasion 3 PPPD 7 mo Mid Direct invasion by 7 13 mo Mid Extranodal invasion 7 PPPD 13 mo Proximal Direct invasion by 6 PPPD 7 mo Mid Direct invasion by 3 Distal gastrectomy with 7 mo Mid Extranodal invasion 4 Whipple 8 mo Mid Direct invasion by 5 Billroth II 53 mo Distal Direct invasion by 4 Billroth II 31 y Distal Extranodal invasion 2 Whipple 39 mo Distal Adhesion 6 Note CBD = common bile duct, PPPD = pylorus-preserving pancreatoduodenectomy. a Refers to the period between the initial surgery and the development of afferent loop syndrome. Fig. 1 Illustration of three types of obstruction: proximal, mid, and distal obstructions. 32 mo Distal Direct invasion by consecutive patients in whom afferent loop syndrome presented as cholangitis or pancreatitis were referred to the Division of Interventional Radiology. There were six men and seven women in the study (age range, 27 73 years; mean age, 57 years). On liver function tests, the serum levels of total bilirubin, direct bilirubin, and alkaline phosphatase were elevated in all patients. The underlying diseases and surgical procedures performed in these patients are shown in Table 1. The underlying diseases included advanced in seven patients, pancreatic head in three patients, and distal common bile duct in three patients. The obstructions were caused by direct invasion of the recurred tumor in eight patients, by extranodal invasion in four patients, and by postoperative adhesion in one patient. The obstructions were classified according to the location of the narrowed bowel segment: proximal, mid, or distal portion (Fig. 1). When the obstruction involved or occurred near the stump of the blind bowel loop, it was defined as proximal obstruction. Distal obstruction referred to obstruction in or near the surgical anastomotic sites, such as gastrojejunostomy in Billroth II and. Mid portion obstruction was defined as a lesion located between the proximal and distal portions of the afferent bowel loop. The cause of the obstruction, length of the narrowed segments, and location of the obstruction are shown in Table 1. The sites of obstructions included the proximal portion of the afferent bowel 5 5 W762 AJR:199, December 2012

Use of Dual Stents for Treatment of Afferent Loop Syndrome Fig. 2 Dual stent used in this study. Dual stent consists of two stents: outer partially covered stent (top) and inner bare-metal stent (bottom). Outer partially covered stent has three parts: proximal bare-metal stent, nylon mesh, and distal bare nitinol stent. loop in two patients, the mid portion in eight patients, and distal portion in four patients. B A Fig. 3 71-year-old woman with pancreatic who underwent peroral stent placement via Whipple operation. A, CT shows dilatation of afferent bowel loop (arrows) due to extranodal metastasis. B, Coil catheter was passed through afferent loop. C, Dual graft stent (arrows) was inserted into obstructed area. Stent and Placement Technique Two types of expandable stents were used in this study: one covered endoscopic stent (diameter, 20 mm; Hercules pyloric, S&G Biotech) and 16 partially covered dual stents (diameter, 18 mm; Hercules SP pyloric, S&G Biotech). In principle, partially covered dual stents were placed into all of the obstructed afferent loops. However, in one patient, because the delivery system for the dual stents was not able to be advanced into the stricture, a covered endoscopic stent was placed. On the basis of the route of stent placement, patients enrolled in this study were divided into two C groups: the percutaneous group and the peroral group. If there was an overt intrahepatic duct dilatation and the obstruction was located at the proximal or mid portion of the afferent loop, PTBD was first performed, after which stent placement along the PTBD tract was performed. When there was mild intrahepatic duct dilatation or the obstruction was located in the distal portion of the afferent bowel loop, the stent was introduced into the obstructed area via a peroral route. In one patient with the distal obstruction, peroral stent placement was attempted, but the bowel segment between the stomach and the obstruction was so tortuous that the guidewire could not be passed through the stricture. This patient underwent percutaneous stent placement using a PTBD tract. In some patients with a distal obstruction, the lesion involved not only the afferent loop but the efferent loop, thus causing dysphagia. In such cases, stents for the efferent loops were also placed via a peroral route. In peroral stent placement, partially covered dual stents were used in all cases. The dual stent (Hercules SP pyloric, S&G Biotech) used consisted of two parts: an outer partially covered stent and an inner bare nitinol stent (Fig. 2). The length and diameter of the stents used differed in each patient. The pharynx was topically anesthetized using an aerosol spray before the procedure, but drugs for sedation were not used. A 0.035-inch hydrophilic exchange guidewire (Radiofocus, Terumo) was inserted across the stricture. A coil catheter was then passed over the guidewire to the distal part end of the stricture. The exchange guidewire was replaced with a superstiff 260-cm-long guidewire, and the coil catheter was removed with the guidewire left in the stricture of the afferent bowel loop. The dual stent was inserted using the stent delivery system. The stent introducer set consisted of a polytetrafluoroethylene (Teflon) sheath 3.8 mm (11.4 French) in outer diameter and 120 cm long, a pusher coil catheter (outer diameter of 2.9 mm, inner diameter of 1.9 mm, and a guiding tip; Dawson-Mueller drainage catheter, Song-Lim gastric catheter, S&G Biotech). The stent delivery system for the outer stent was passed over the stiff guidewire through the stricture. The outer stent was deployed by withdrawing the sheath while the catheter pusher was held in place. Next, the inner stent was placed coaxially into the outer stent. All the patients underwent a barium study 1 3 days after stent placement to verify the position and patency of the stent (Fig. 3). In percutaneous stent placement, patients underwent PTBD using an 8.5-French multisidehole biliary drainage catheter. A catheter was placed beyond the ampulla of Vater. IV antibiotic treatment was initiated before PTBD and was continued for 5 days. When the patient s symptoms disappeared, enterography was performed to determine the location of the obstruction. Because the stricture in AJR:199, December 2012 W763

Han et al. the proximal or mid portion of the afferent bowel loop was readily accessible via a transhepatic access, this route was used for stent insertion. After removal of the drainage catheter over a 0.035-inch angled hydrophilic stiff guidewire (Radiofocus, Terumo), a 5-French cobra catheter (Torcon NB Advantage Catheter, Cook Medical) and the guidewire were advanced into the afferent bowel loop and manipulated across the stricture. The PTBD tract was first dilated using a 10-French dilator and then a 12-French dilator. Dilation of the stricture was performed using a balloon catheter before stent placement. The dual stents (Hercules SP pyloric, S&G Biotech) were then placed in the same fashion using peroral placement. The multisidehole drainage catheter was replaced at the end of the procedure. If the abnormal laboratory findings gradually decreased with the drainage tube clamped, a tubogram was done, and if it showed a well-positioned patent stent, the drainage catheter was removed (Fig. 4). Definition and Analysis of Data Data collected included the route of stent insertion, types of stents used, location of obstruction, need for repeat intervention, and complications. Technical success was defined as successful insertion of the stent into the area of interest via a peroral or percutaneous route. Clinical success was defined as a gradual decrease in the abnormal laboratory findings and decompression of the dilated bowel loop as seen on abdominal CT within 1 week after the stent insertion. Follow-Up After stent placement, follow-up for each patient was done with monthly radiography and physical examination in the outpatient clinic. Patients were advised to visit the hospital if symptoms developed during this time. When follow-up was not available, patients or their families were contacted by telephone on a monthly basis until their death. A C Fig. 4 69-year-old woman with pancreatic who underwent percutaneous stent placement via Whipple operation. A, CT shows dilation of afferent bowel loop (arrows) due to. B, Barium study performed before procedure shows long afferent bowel loop (arrows). C, Tubogram using iodinated contrast material via percutaneous transhepatic biliary drainage shows well-expanded and -positioned stent (arrows). Results Procedural and Functional Results Stent placement under fluoroscopic guidance was technically successful in all 13 patients. The 13 patients received 15 partially covered dual stents and one endoscopic stent. Thirteen stents were placed in the afferent loop stricture, and three stents were placed in the efferent loop stricture. There were nine percutaneous stent placements and four peroral stent placements. With peroral stent placement, all of the patients had distal obstructions. Eight patients with proximal or mid obstruction and one patient with distal obstruction underwent stent placement via the PTBD tract. In percutaneous stent placement, the PTBD was able to be removed 1 8 days after stent insertion (mean, 5.7 days). The patients clinical outcomes are summarized in Table 2. Clinical success was achieved in 12 of 13 patients (91.6%). Twelve patients responded to the procedure with nor- B W764 AJR:199, December 2012

Use of Dual Stents for Treatment of Afferent Loop Syndrome TABLE 2: Clinical Outcomes Patient No. No. of Stents Type of Stent malization of their serum bilirubin levels and improvement in symptoms, such as fever and abdominal pain. However, in one patient, the obstruction was very tight and showed acute angulation. The stent was successfully placed into the stricture, but it remained poorly expanded even after multiple sessions of balloon dilatation using a 16-mm balloon. The afferent bowel loop failed to decompress, and the serum bilirubin levels were not normalized. This patient had to undergo additional treatment, consisting of surgical jejunojejunostomy. Three patients underwent stent insertion for their obstructed efferent bowel loops because of s. In two patients, dual stents were simultaneously inserted in both the afferent and efferent loops. In the remaining one patient who had stent insertion via a PTBD tract because of an obstructed afferent loop, a stent for the efferent loop was later placed perorally. According to the Song classification [10], after the procedure, all of these patients showed improvement of at least one level in their dietary intake capacity. Complications and Repeat Intervention No procedure-related complications occurred in any of our patients. There were no delayed complications, such as stent migration or obstruction. Follow-Up Eleven of 13 patients died 41 756 days (mean, 221 days) after stent placement as a result of the progression of their disease or from Stent Length (cm) Route Symptom Improvement Complication 1 1 Dual 8 PTBD Yes None 2 1 Dual 8 PTBD Yes None 3 2 Dual 4 PTBD Yes None 4 1 Dual 10 PTBD Yes None 5 1 Dual 10 PTBD Yes None 6 1 Dual 8 PTBD Yes None 7 1 Dual 6 PTBD Yes None 8 1 Dual 6 PTBD Yes None 9 1 Covered a 9 PTBD Yes None 10 2 Dual 4 Peroral Yes None 11 2 Dual 4 Peroral Yes None 12 1 Dual 8 Peroral No None 13 1 Dual 8 PTBD Yes None Note PTBD = percutaneous transhepatic biliary drainage. a Covered endoscopic stent (Hercules SP pyloric, S&G Biotech; diameter, 20 mm). pneumonia. The remaining two patients are still alive 174 209 days after stent placement (mean, 191 days). In the 12 clinically successful patients, the primary stents remained patent during their survival time (range, 41 507 days; mean, 144 days; median, 143 days). Discussion Afferent loop syndrome is a condition associated with various surgical procedures that create a resulting afferent bowel loop. Although surgical conversions have been the treatment of choice, percutaneous tube drainage or stent placement has been performed as a palliative treatment for patients who cannot tolerate surgery [6 8]. In recent years, partially covered dual stents have been used for benign or malignant gastroduodenal obstructions and showed better outcomes than those seen in previous studies done with bare or fully covered self-expandable metallic stents [12 16]. This suggests the possibility that dual stents are an alternative stent type for use with afferent loop syndrome. In our study, placement of partially covered dual stents was quite successful in providing palliation for patients with afferent loop syndrome. However, there was a clinical failure in one patient. In this patient, the stent was successfully inserted but failed to expand fully because of the tight and acutely angulated lesion. As a result, the stent did not provide sufficient drainage to decompress the distended bowel loop. This suggests that when the lesion is tight and acutely angulated, stent insertion might not be the best treatment option for the patient. In one patient, because the afferent bowel loop before the stricture was very long and tortuous, we were not able to advance the stent introducer set (outer diameter, 11.4 French) for the dual stent. As an alternative, we decided to use an endoscopic stent, because the outer diameter of its introducer set was only 10 French. We thought that it would provide better access to the lesion because it was more flexible than that for the dual stent. Although the stent was for endoscopic placement, we successfully inserted the stent for the stricture via PTBD under fluoroscopic guidance. It was the smaller diameter of the stent introducer set that made it possible to place the stent into the stricture. Accordingly, if the afferent bowel loop before the lesion is too long and tortuous, other stent types with a smaller stent delivery system should then be considered. There are two different routes of stent insertion for treating afferent loop syndrome: the percutaneous and peroral routes. The percutaneous approach using PTBD or enterostomy tubes provides better access to the lesion in the proximal or mid portion of the afferent bowel loop. In contrast, peroral stent insertion is a better option for a distal obstruction involving surgical anastomotic sites, because the distance between the mouth and the lesion is short enough to be able to successfully advance a guidewire. However, depending on the surgery performed and the surgeon s preferences, the resulting anatomic changes varied from one to another. Accordingly, other than the site of obstruction, there are some other factors to consider when choosing either percutaneous or peroral stent placement. Regardless of the site of obstruction, if the patient has severe cholangitis or biliary sepsis due to a dilated afferent loop and CT shows overt intrahepatic duct dilatation, it is obvious that percutaneous drainage must be done first. Subsequent stent placement along the tube should then be done. In addition, when the bowel segment between the stomach and the lesion is too far or is tortuous, peroral stent placement can be difficult and a percutaneous approach should be considered. In a patient with massive ascites, PTBD is contraindicated and a peroral approach should be considered. There is also a special situation in which the obstruction is in the distal portion and the lesion may cause not only afferent loop syndrome but also dysphagia by narrowing both bowel loops. Under these circumstances, peroral placement of two stents, one in the afferent loop and one in the efferent loop, offers AJR:199, December 2012 W765

Han et al. a good treatment option. In three of our study patients, stents were successfully inserted and relieved afferent loop dilatation and dysphagia. Since Caldicott et al. [8] successfully placed a stent for afferent loop obstruction via the transhepatic route, there have been similar attempts primarily using covered stents. This is because covered stents usually prevent tumor ingrowth more successfully than bare stents do [12 14]. When it comes to fully covered metallic stents, stent migration is not rare, and overall migration rates of 21 26% have been reported [13, 14]. To manage the issue of migration, a dual expandable nitinol stent was used in a study, and the migration rates decreased to 2% [10]. Recently, Gwon [11] reported two cases of successful percutaneous placement of covered self-expandable nitinol stents for the treatment of afferent loop without any complications. In the current study, because no stent migration occurred, there was a clinical success rate of 91.6%. This promising result suggests the possibility of the use of partially covered dual stents as the optimal stent type for treating afferent loop syndrome. In conclusion, the placement of covered self-expandable dual stents appears to be a treatment modality that may offer successful palliation for patients with afferent loop syndrome after various types of surgery. The route of stent insertion must be determined according to the best interest of the patient. For this reason, the patient s general condition, the site of obstruction, postoperative anatomic variations, and associated symptoms must be taken into consideration before each procedure. References 1. Jordan GL. Surgical management of postgastrectomy problems. Arch Surg 1971; 102:251 259 2. Fisher JE, Fegelman E. Johannigman J. Surgical complications. In: Schwartz SI, Shires GT, Spencer FC, Daly JM, Fisher JE, Galloway AC, eds. Principles of surgery, 7th ed. New York, NY: McGraw-Hill, 1999:441 483 3. Moriura S, Nakahara R, Ichikawa T, et al. Jaundice due to afferent loop obstruction following Roux-en-Y reconstruction. Gastroenterol Surg 1996; 19:1895 1899 4. Moriura S, Takayama Y, Nagata J, et al. Percutaneous bowel drainage for jaundice due to afferent loop obstruction following pancreatoduodenectomy: report of a case. Surg Today 1999; 29:1098 1101 5. Lee LI, Teplik SK, Haskin PH, Sammon JK, Wolferth C, Amron G. Refractory afferent loop problems: percutaneous transhepatic management of two cases. Radiology 1987; 165:49 50 6. Yao NS, Wu CW, Tiu CM, Liu JM, Whang-Peng J, Chen LT. Percutaneous transhepatic duodenal drainage as an alternative approach in afferent loop syndrome with secondary obstructive jaundice in recurrent. Cardiovasc Intervent Radiol 1998; 21:350 353 7. Kim YH, Han JK, Lee KH, Kim TK, Kim KW, Choi BI. Palliative percutaneous tube enterostomy in afferent loop syndrome presenting as jaundice: clinical effectiveness. J Vasc Interv Radiol 2002; 13:845 849 8. Caldicott DG, Ziprin P, Morgan R. Transhepatic insertion of a metallic stent for the relief of malignant afferent loop obstruction. Cardiovasc Intervent Radiol 2000; 23:138 140 9. Yoshida H, Mamada Y, Taniai N, et al. Percutaneous transhepatic insertion of metal stents with a double-pigtail catheter in afferent loop obstruction following distal gastrectomy. Hepatogastroenterology 2005; 52:680 682 10. Song HY, Shin JH, Yoon CJ, et al. A dual expandable nitinol stent: experience in 102 patients with malignant gastroduodenal strictures. J Vasc Interv Radiol 2004; 15:1443 1449 11. Gwon DI. Percutaneous transhepatic placement of covered, self-expandable nitinol stent for the relief of afferent loop syndrome: report of two cases. J Vasc Interv Radiol 2007; 18:157 163 12. Song HY, Lee DH, Seo TS, et al. Retrievable covered nitinol stents: experiences in 108 patients with malignant esophageal strictures. J Vasc Interv Radiol 2002; 13:285 293 13. Jung GS, Song HY, Kang SG, et al. Malignant gastroduodenal obstructions: treatment by means of a covered expandable metallic stent-initial experience. Radiology 2000; 216:758 763 14. Park KB, Do YS, Kang WK, et al. Malignant obstruction of gastric outlet and duodenum: palliation with flexible covered metallic stents. Radiology 2001; 219:679 683 15. Song HY, Kim TH, Choi E, et al. Metallic stent placement in patients with recurrent after gastrojejunostomy. J Vasc Interv Radiol 2007; 18:1538 1546 16. Jung GS, Song HY, Seo TS, et al. Malignant gastric outlet obstructions: treatment by means of coaxial placement of uncovered and covered expandable nitinol stents. J Vasc Interv Radiol 2002; 13:275 283 W766 AJR:199, December 2012