Tumor Overgrowth After Expandable Metallic Stent Placement: Experience in 583 Patients With Malignant Gastroduodenal Obstruction

Vascular and Interventional Radiology Original Research Jang et al. Stent Placement for Malignant Gastroduodenal Obstruction Vascular and Interventional Radiology Original Research Jong Keon Jang 1 Ho-Young Song Jin Hyoung Kim Min Song Jung-Hoon Park Eun Young Kim Jang JK, Song HY, Kim JH, Song M, Park JH, Kim EY Keywords: expandable metallic stent, malignant gastroduodenal obstruction, tumor overgrowth DOI:10.2214/AJR.10.5861 Received September 28, 2010; accepted after revision November 28, 2010. 1 All authors: 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). WEB This is a Web exclusive article. AJR 2011; 196:W831 W836 0361 803X/11/1966 W831 American Roentgen Ray Society Tumor Overgrowth After Expandable Metallic Stent Placement: Experience in 583 Patients With Malignant Gastroduodenal Obstruction OBJECTIVE. The objective of our study was to assess the incidence, predictive factors, and treatment of tumor overgrowth after placement of expandable metallic dual stents in patients with malignant gastroduodenal obstruction. MATERIALS AND METHODS. Expandable metallic dual stents were inserted under fluoroscopic guidance in 583 patients with symptomatic malignant gastroduodenal obstruction. We retrospectively reviewed prospectively collected patient records to determine the incidence and treatment of tumor overgrowth after stent placement and used multivariate analysis to determine factors predicting tumor overgrowth. RESULTS. Tumor overgrowth occurred after stent placement in 22 of 583 patients (3.8%) (range, 41 634 days; mean, 179.0 days). Duodenal lesions (odds ratio [OR], 4.505; p = 0.002), longer survival time (OR, 1.003; p = 0.001), and length of obstruction (OR, 0.783; p = 0.035) were independent predictors of tumor overgrowth. Twenty of the 22 patients were successfully treated by placement of a second dual stent, whereas the other two patients refused placement of a second stent or other further treatment. Overall, 19 of 20 patients (95%) showed improvement in symptoms after second stent placement. Duodenal perforation occurred in one of the 20 patients 125 days after placement of a second stent and was treated surgically. CONCLUSION. Tumor overgrowth seems to be an uncommon complication of expandable metallic dual stent placement in patients with malignant gastroduodenal obstruction. Tumor overgrowth is associated with duodenal lesions, longer survival time, and shorter stricture length. Tumor overgrowth can be successfully managed by coaxial insertion of a second dual-expandable metallic stent into the obstructed first stent. M alignant gastroduodenal obstructions can occur in up to 20% of patients with primary gastric, duodenal, and pancreatic cancers [1]. Presenting symptoms include nausea, vomiting, abdominal distention, pain, and poor oral intake, which can lead to dehydration, malnutrition, and poor quality of life. Placement of bare or covered self-expanding stents has been established as a noninvasive palliative method of treating patients with unresectable cancers causing gastric or duodenal obstruction [2 10]. Stent insertion is associated with higher clinical success rates, shorter durations of hospital stay, and lower rates of morbidity and mortality than palliative surgery [11, 12]. However, stent use has several drawbacks including recurrent obstruction as a result of progressive tumor ingrowth in patients implanted with bare metal stents [3, 6] and stent migration in patients implanted with covered stents [8, 9]. To overcome these problems, a dual-expandable nitinol stent has been devised [13]. The dual stent has been reported to have several advantages over conventional stents including lower rates of migration, greater resistance to tumor ingrowth, and ease of placement [2, 8 10]. Nevertheless, recurrent symptoms such as nausea and vomiting as a result of tumor overgrowth and resultant stent collapse were observed in 10.8% of patients after stent placement [14]. Tumor overgrowth has been reported to occur in 17.2% of patients who receive bare metal stents and 6.9% of those who receive covered stents [15, 16]. To our knowledge, however, no study to date has evaluated the incidence of and predictive factors for tumor overgrowth after placement of dual stents in patients with malignant gastroduodenal obstruction. Furthermore, little is known about the treatment of these patients and their clinical outcomes. We therefore evaluated the incidence of, predictive factors for, and interventional AJR:196, June 2011 W831

Jang et al. management of tumor overgrowth in 583 patients with symptomatic malignant gastroduodenal obstruction who were treated with dual stent placement. Materials and Methods Patients From February 2001 to February 2010, 583 consecutive patients with malignant gastroduodenal obstructions were treated by implantation of dual stents under fluoroscopic guidance. The characteristics of this patient population are shown in Table 1. Because of advanced or metastatic disease or medical comorbidity, none of the 583 patients were considered a candidate for surgery; however, all had obstructive symptoms such as nausea, vomiting, bloating, or abdominal pain. These patients were histologically diagnosed by endoscopic biopsy, percutaneous needle aspiration biopsy, or forceps biopsy during percutaneous transhepatic or endonasal biliary drainage. We retrospectively reviewed the prospectively collected records on the incidence of tumor overgrowth after stent placement. Informed consent was obtained from each patient, and the study was approved by our institutional review board. Stent Placement and Follow-Up The stents used in this study were expandable nitinol dual stents (Hercules SP Pyloric, S&G Biotech) (Fig. 1) consisting of an outer, partially covered stent and an inner, bare nitinol stent. The inner stent is 10 mm shorter than the outer stent and serves to expand the nylon mesh portion of the outer stent and to increase the radial force of the dual stent. More details about the dual stent and stent placement techniques are provided elsewhere [8, 12, 13, 17]. All patients underwent a barium study 1 3 days after stent placement to confirm the position and patency of the stent. Patients were advised to resume oral intake of liquids within 24 hours and to advance to a low-residue diet as tolerated. The status of oral food intake was monitored at 1-month intervals on an outpatient basis. A barium study was performed 1 month after stent placement to detect delayed complications such as stent migration or obstruction. Additional follow-up barium studies or endoscopy examinations were performed only in patients with recurrent symptoms. When a clinical examination was not practical and the patient remained alive, the patient or member of his or her family was contacted by telephone to obtain information about obstructive symptoms and food intake capacity. Patients who had recurrent symptoms caused by tumor overgrowth were treated by placement of a second dual stent (Fig. 2). Techniques to insert a second dual stent coaxially into the obstructed first stent with overlap at both ends are described elsewhere [18]. Tumor overgrowth was classified into three types according to location (Fig. 3), and placement of the second stent was classified into five patterns on the basis of the location of the second stent (Fig. 4). In pattern I, a second stent was placed from the upper end of the proximal tumor overgrowth to the proximal part of the first dual stent. In pattern II, a second stent was placed from the upper end of the proximal tumor overgrowth to the distal end of the dual stent. In pattern III, a second stent was placed from the distal part of the first dual stent to the lower end of the distal tumor overgrowth. In pattern IV, a second stent was placed from the proximal part of the first dual stent to the lower end of the distal tumor overgrowth. In pattern V, a second stent was placed from the upper end of the proximal tumor overgrowth to the lower end of the distal tumor overgrowth. Definition and Analysis of Data Tumor overgrowth was defined as narrowing of the gastroduodenum above or below the nylon mesh of the outer stent as a result of tumor growth, as shown by endoscopic and radiologic findings. The patient s ability to swallow was expressed as a dysphagia score similar to that used in patients with malignant dysphagia [17]: A score of 0 denoted the ability to eat a normal diet; 1, the ability to eat solid food; 2, the ability to eat soft food; 3, the ability to swallow liquids only; 4, no oral intake without vomiting; and 5, no oral intake with vomiting. An improvement in dysphagia was defined as a change in the dysphagia score by one or more grades 1 week after stent placement. Univariate analysis was performed to compare variables between patients with and those without tumor overgrowth. The Student t test was used to compare continuous variables and Fisher exact test was used to compare categoric variables. Fig. 1 Photograph shows outer partially covered stent (top), inner bare nitinol stent (middle), and assembled dual-expandable nitinol stent (bottom) (Hercules SP Pyloric, S&G Biotech). TABLE 1: Characteristics of 583 Patients in Study Population Characteristic Value Age (y) Mean ± SD 61.3 ± 12.8 Range 15 87 Sex, no. (%) of patients Men 390 (66.9) Women 193 (33.1) Site of obstruction, no. (%) of patients Peripyloric region 301 (51.6) Nonperipyloric region, duodenum 209 (35.9) alone Anastomosis (Billroth I, Billroth II) 63 (10.8) Jejunum 10 (17) Source of malignancy, no. (%) of patients Primary Gastric cancer 331 (56.8) Duodenal cancer 18 (3.1) Secondary Pancreatic cancer 99 (17.0) Cholangiocarcinoma 53 (9.1) Gallbladder cancer 33 (5.7) Metastasis 30 (5.1) Anastomosis 19 (3.3) A multivariate logistic regression model with forward stepwise selection was used to determine independent predictive factors associated with tumor overgrowth. Only variables with a p value of < 0.2 during univariate analysis (Student t test or Fisher exact test) were included in the multivariate logistic regression model. This lenient p value was chosen to avoid rejection of a variable that could W832 AJR:196, June 2011

Stent Placement for Malignant Gastroduodenal Obstruction Fig. 2 Radiographs obtained during placement of dual stent in 49-year-old man with gastric cancer involving gastric outlet. A, Barium radiograph obtained immediately after stent placement shows good downstream passage of contrast medium. B, Passage of injected contrast medium through multipurpose coil catheter shows tumor overgrowth (arrows) from distal part of dual stent to second portion of duodenum 349 days after placement of dual stent. C, Barium radiograph obtained immediately after placement of second dual stent using pattern III method shows good passage of contrast medium at region of tumor overgrowth (arrows). potentially contribute to the prediction of outcome in multivariable analysis. A two-sided p value of < 0.05 was considered statistically significant. All statistical analyses were performed using a statistics software package (SPSS version 12.0, SPSS). After interventional management for tumor overgrowth had been performed, clinical outcomes were evaluated retrospectively. Results Incidence of Tumor Overgrowth The mean follow-up period after placement of the first stent was 268.3 days (range, 87 802 days), during which time tumor overgrowth occurred in 22 of 583 patients (3.8%) within 41 634 days (mean, 179.0 days) after placement of the first stent. Of the 22 patients, 19 were men and three were women ranging in age from 27 to 80 years (mean, 56.6 ± 11.1 [SD] years). Nine of the patients had type 1 obstructions, 10 had type 2, and three had type 3. The obstructions were located in the duodenal region (n = 15), the gastric outlet (n = 5), and the site of anastomosis (n = 2). The median survival time of the 22 patients was 235.5 days (Table 2). A Factors Predictive of Tumor Overgrowth The following variables were found to have a p value of < 0.2 during univariate analysis and were included in the multiple logistic regression model: age, sex, site of obstruction, length of obstruction, and survival time. Multivariate analysis confirmed that duodenal region (p = 0.002), longer survival time (p = 0.001), and shorter length of obstruction (p = 0.035) were independent predictors of tumor overgrowth (Table 3). The p value of the Hosmer-Lemeshow goodness-of-fit test was 0.713. Reintervention and Functional Results Twenty of the 22 patients with tumor overgrowth were treated by means of coaxial placement of a second dual stent into the first stent with overlap at both ends; the other two patients refused further treatment and received total parenteral nutrition until death. All 20 patients required only one stent to traverse the site of obstruction. Of the 20 patients, four were treated by the pattern I method; two, by pattern II; seven, by pattern III; four, by pattern IV; and three, by pattern V. B C AJR:196, June 2011 W833

Jang et al. Fig. 3 Schematic drawing shows types of obstructions caused by tumor overgrowth. Type 1 shows luminal narrowing of dual stent around proximal end. Type 2 shows luminal narrowing of dual stent around distal end. Type 3 shows luminal narrowing at both proximal and distal stent ends. Dysphagia scores before and after the placement of a second stent are summarized in Table 4. Sixteen of the 20 patients (80%) who received second stents were able to subsequently eat soft foods and 10 were able to eat solid foods (50%). The median dysphagia scores before and after the procedures were 4 and 1.5, respectively. Overall, 19 of 20 patients (95%) showed an improvement of more than one grade in their level of dietary intake. One patient with a dysphagia score of 3 before placement of a second stent showed no improvement in score, but follow-up barium endoscopy showed a patent stent lumen. The patient felt more comfortable ingesting liquids than soft or solid food. Complications and Follow-Up After Placement of a Second Stent One patient with pancreatic cancer had a duodenal perforation 125 days after placement of a second stent using the pattern IV method. The site of perforation was at the normal duodenum proximal to the tumor bed. The cause of perforation was pressure necrosis from the ends of the bare parts of the stents. The patient was successfully treated by surgery (i.e., closure of the perforation site after removal of the bare parts of the stents followed by a palliative gastrojejunostomy) and antibiotics. To remove the bare parts of the stents during surgery, the stents placed proximal to the tumor bed were cut with scissors. The patient died of diffuse metastasis of pancreatic cancer 392 days after surgery. Two of the 20 patients who received second stents experienced recurrence of symptoms because of food impaction 17 and 93 days, respectively, after second stent placement. Both patients were managed endoscopically. The median survival time for all patients and for patients with tumor overgrowth were 92.0 and 235.5 days, respectively. Discussion We found that the rate of tumor overgrowth after dual stent placement was 3.8% (22/583) and that tumor overgrowth tended to occur Fig. 4 Schematic drawing shows five patterns of overlap that depend on location of both ends of first and second stents. In pattern II, distal end of second stent overlaps with first stent; in pattern IV, proximal end of second stent overlaps with first stent. late after dual stent placement (mean, 179.0 days; range, 41 634 days). Factors independently predictive of tumor overgrowth were duodenal region (p = 0.002), longer survival time (p = 0.001), and length of stricture (p = 0.035). In 20 of the 22 patients, tumor overgrowth was managed by placement of a second dual stent coaxially into the obstructed initial stent with good results. The overall rates of recurrent obstruction caused by tumor overgrowth in patients re- TABLE 2: Characteristics of Patients With and of Those Without Tumor Overgrowth Characteristic No Tumor Overgrowth Tumor Overgrowth p No. of patients 561 22 Age (y) 0.175 Mean ± SD 61.4 ± 12.8 57.6 ± 11.1 Sex, no. (%) of patients 0.063 Male 372 (66.3) 19 (86.4) Female 189 (33.7) 3 (13.6) Site of obstruction, no. (%) of patients 0.007 Duodenal region 216 (38.5) 15 (68.2) Nonduodenal region 345 (61.5) 7 (31.8) Source of malignancy, no. (%) of patients 0.660 Primary 337 (60.1) 12 (54.5) Nonprimary 224 (39.9) 10 (45.5) Length of obstruction 0.038 Mean ± SD 6.7 ± 3.2 5.3 ± 1.9 Survival time 0.000 Mean ± SD 148.9 ± 168.5 319.7 ± 205.1 W834 AJR:196, June 2011

Stent Placement for Malignant Gastroduodenal Obstruction TABLE 3: Results of Multivariate Logistic Regression Analysis for Evaluation of Factors Predictive of Tumor Overgrowth ceiving bare metal stents has been reported to range from 3% to 46% in studies with more than two but fewer than 36 patients [4, 15, 19]. Although these overall recurrence rates do not differ significantly from those observed in patients receiving dual stents, recurrent obstructive symptoms occurred relatively sooner after implantation of bare metal stents, with mean times ranging from 24 to 133 days [4, 15, 19]. In contrast, we found that the mean symptom-free period after dual stent implantation was 179.0 days. Tumor overgrowth after implantation of covered stents has been observed in five of 68 patients (7.4%) and in four of 24 patients (16.7%) [20, 21]; these incidences are higher than we observed with dual stents. In those previous studies, the mean times to stent reobstruction were 161.2 and 271.3 days, respectively [20, 21]. Degradation of the membranes of covered stents is related to the duration of TABLE 4: Comparison of Dysphagia Scores Before and After the Placement of a Second Stent Dysphagia Score Variable No. (%) of Patients Odds Ratio 95% CI p Sex 0.040 Male 378 (66.9) 0.264 0.074 0.938 Female 187 (33.1) 1.000 Site of obstruction 0.002 Duodenal region 340 (60.2) 4.505 1.727 11.752 Nonduodenal region 225 (39.8) 1.000 Length of obstruction 565 (100) 0.783 0.624 0.983 0.035 Survival time 565 (100) 1.003 1.001 1.005 0.001 Note There were 18 surviving patients at the time this article was written. Before Stent Placement After Stent Placement 0 0 2 1 0 8 2 2 6 3 5 4 4 6 0 5 7 0 Median score 4 1.5 Mean score 3.9 1.6 Note All data except median and mean scores are number of patients. A score of 0 denoted the ability to eat a normal diet; 1, the ability to eat solid food; 2, the ability to eat soft food; 3, the ability to swallow liquids only; 4, no oral intake without vomiting; and 5, no oral intake with vomiting. stent placement [22]. Membranes made of polyurethane and silicone rubber are susceptible to chemical degradation after exposure to acidic gastric fluid, bile salts, and certain hydrolytic enzymes in pancreatic secretion [23, 24], suggesting that degradation of the stent membrane caused tumor ingrowth or overgrowth. However, the nylon mesh used in dual stents is a biocompatible and strongly chemical-resistant material [13]. We are not aware of any reports of membrane degradation or disruption in clinical studies of dual stents. Thus, our findings indicate that dual stents have advantages over conventional stents because of their longer symptom-free periods and their greater resistance to tumor growth. There are several explanations for the factors we found to predict tumor overgrowth after dual stent placement. First, tumor overgrowth after gastroduodenal stent placement was significantly more common at the duodenum than at other locations. This greater incidence at the duodenum may be because of the smaller diameter of the duodenum compared with the stomach or because of the greater aggressiveness of the underlying cancers that obstruct the duodenum, such as pancreatic cancer and cholangiocarcinoma, compared with gastric cancer that causes gastric obstruction. The median survival time of patients with gastroduodenal obstructions caused by pancreaticobiliary malignancies was found to be 60 days (range, 30 90 days) [25 27], whereas the median survival times in patients with obstructions caused by gastric cancer was reported to be 110 150 days [28 30]. We also found that patients with a shorter length of obstruction had longer survival times. Because the length of the obstruction was proportional to progression of the tumor, a longer length of obstruction represented a significant risk of tumor progression and a relatively short survival time. Treatment of reobstructive symptoms by placement of several types of second stents allows patients to resume oral intake until death or the end of follow-up without recurrence of obstructive symptoms [4, 5, 17, 18]. Of the 20 patients who underwent placement of a second stent, 19 (95%) showed an improvement of more than one grade in the dysphagia score (19 of 20), and none experienced new reobstructive symptoms until death or the end of follow-up. Gastroduodenal perforation is a life-threatening complication. A systematic review of 32 published articles on metallic stenting under fluoroscopic or endoscopic guidance, which included a total of 606 patients with malignant gastroduodenal obstruction, found that perforation occurred in 0.7% of patients who underwent placement of self-expanding metal stents for gastroduodenal malignancies [31]. The gastroduodenal perforation rate was found to be extremely low, 0.00 0.48%, in patients receiving dual stents [13, 14, 20], which is similar to the rate we observed (0.17%). In the patient with the perforation, the second stent had been implanted using the pattern IV method. The perforation was caused by pressure necrosis at the normal duodenum proximal to the tumor bed. Placement of dual-expandable colorectal stents for the treatment of malignant colorectal obstruction was found to result in perforation rates of 6.03 11.03% [32, 33], which is much higher than those observed after placement of stents for gastroduodenal obstruction. Dual colorectal stents usually have thicker wires (0.229 mm) than gastroduodenal stents (0.2 mm) because of the need for a greater hoop strength, a parameter that describes the ability of a stent to withstand external forces. Following the same principle, implantation of a second stent providing greater hoop strength was used to manage tumor overgrowth. Using the pattern IV method, two bare parts of the dual stents were placed at the same level. Because the two 0.2-mm nitinol wires overlapped, the hoop strength may have been increased. In contrast, stents with greater hoop strength may result in decreased flexibility, thereby increasing the risk of perforation. Tumor overgrowth is one of several complications that causes recurrent obstructive symptoms after dual stent placement. Stents eluting anticancer drugs have been reported to reduce tumor cell proliferation and prevent tumor overgrowth, both in animals and in humans in clinical trials [34, 35]. Thus, use of these stents may reduce tumor burden. Further investigations are necessary to determine the optimal drug and concentration AJR:196, June 2011 W835

Jang et al. that can prevent or reduce tumor overgrowth without damaging adjacent normal tissue. The principal limitation of this study is its nonrandomized and retrospective design, which inherently decreases the statistical power of the study. In contrast, the large patient population is a strength of this study. In conclusion, we have shown that tumor overgrowth is an uncommon complication after the placement of dual-expandable metallic stents in patients with malignant gastroduodenal obstruction. Factors predictive of tumor overgrowth include the presence of the stent in the duodenal region, longer survival time, and shorter length of obstruction. Obstruction of the stent can be managed by coaxial placement of a second dual stent into the initial stent. References 1. van Heek NT, van Geenen RC, Busch OR, Gouma DJ. Palliative treatment in peri- pancreatic carcinoma: stenting or surgical therapy? Acta Gastroenterol Belg 2002; 65:171 175 2. 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