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ORIGINAL ARTICLE
Year : 2021  |  Volume : 17  |  Issue : 5  |  Page : 1261-1268

A novel irradiation stent versus conventional irradiation stent for malignant dysphagia: A prospective randomized controlled trial


1 Nanjing Medical University; Department of Radiology, Center of Interventional Radiology and Vascular Surgery, Medical School, Zhongda Hospital, Southeast University, Nanjing, China
2 Department of Radiology, Center of Interventional Radiology and Vascular Surgery, Medical School, Zhongda Hospital, Southeast University, Nanjing, China
3 Department of Oncology, The Third Affiliated Hospital of Soochow University, Changzhou, China

Date of Submission01-Feb-2021
Date of Acceptance07-Oct-2021
Date of Web Publication27-Nov-2021

Correspondence Address:
Jin-He Guo
Nanjing Medical University, Nanjing; Department of Radiology, Center of Interventional Radiology and Vascular Surgery, Zhongda Hospital, Southeast University, 87 Dingjiaqiao Road, Nanjing 210009
China
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jcrt.jcrt_185_21

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 > Abstract 


Aim: To evaluate whether a novel irradiation stent (NIS) could decrease the rate of recurrent dysphagia, compared to the conventional irradiation stent (CIS) in patients with malignant dysphagia.
Materials and Methods: We performed an open-label randomized controlled trial of participants with malignant dysphagia. A total of 94 participants were parallelly allocated into the NIS group or the NIS group between April 2019 and April 2020. The primary endpoint was the rate of recurrent dysphagia. The secondary endpoints included technical success, clinical success, overall survival, and adverse events.
Results: The technical success rate and the clinical success rate was 100.0% (47/47) in both groups. The median follow-up period was 189 days (range 14–422 days). Recurrent dysphagia was observed in 12.8% (6/47) of patients in the NIS group and 31.9% (15/47) in the CIS group (P = 0.026). Tissue/tumor growth occurred in 4 patients (8.5%) after NIS placement and 12 (25.5%) after CIS placement (P = 0.028). Stent migration occurred in 2 patients (4.3%) after NIS placement and 3 (6.4%) after CIS placement (P = 0.646). No food obstruction was found in both groups. The median overall survival was 177 days (95% confidence interval [CI] 139–214) in the NIS group and 168 days (95% CI 153–183) in the CIS group (P = 0.932). The incidence of severe adverse events was comparable between the two groups (21.3% vs. 17.0%, P = 0.600).
Conclusions: In patients with malignant dysphagia, compared with CIS, NIS could decrease the rate of tissue/tumor growth without increase the rate of stent migration and therefore decrease the rate of recurrent dysphagia.

Keywords: Irradiation stent, malignant dysphagia, randomized controlled trial


How to cite this article:
Zhu GY, Lu J, Wang C, Guo JH. A novel irradiation stent versus conventional irradiation stent for malignant dysphagia: A prospective randomized controlled trial. J Can Res Ther 2021;17:1261-8

How to cite this URL:
Zhu GY, Lu J, Wang C, Guo JH. A novel irradiation stent versus conventional irradiation stent for malignant dysphagia: A prospective randomized controlled trial. J Can Res Ther [serial online] 2021 [cited 2022 May 27];17:1261-8. Available from: https://www.cancerjournal.net/text.asp?2021/17/5/1261/331307




 > Introduction Top


Worldwide, esophageal cancer is the eighth most common malignant tumor and the sixth leading cause of cancer-related deaths.[1] The prognosis of esophageal cancer is poor, and the 5-year survival rate is <20%.[2],[3] In the past 3 decades, modest improvements have been achieved in the treatment of patients with esophageal cancer.[4] At present, the treatment methods of esophageal cancer mainly include surgical resection and chemoradiotherapy. Surgical resection is the preferred method for early-stage esophageal cancer. However, most patients are diagnosed at an advanced stage and lose the opportunity of surgery due to the insidious onset of esophageal cancer. Concurrent chemoradiotherapy can offer the satisfactory outcomes in these patients. For most patients (70%–90%), dysphagia is the main symptom.[5],[6] Placement of a self-expandable metallic stent (SEMS) has become the most commonly used palliative treatment.[7] It can rapidly restore luminal patency, maintain nutritional replenishment, and improve the quality of life (QoL).[8] However, the long-term efficacy after SEMS placement remains poor due to tumor ingrowth or overgrowth.[9]

Brachytherapy has been widely accepted as a valid alternative to SEMS placement in patients with malignant dysphagia.[9],[10] An irradiation stent, on which the radioactive iodine-125 (125I) seeds were strapped to the outer surface, has been designed to delay postoperative tumor growth.[11] Single-center and multicenter randomized controlled trials (RCTs) have demonstrated that placement of the irradiation stent can improve patency and prolong overall survival in patients with advanced esophageal cancer.[12],[13] However, the irradiation stent placement did not reduce recurrent dysphagia. The rate of recurrent dysphagia was reported to range from 28% to 37% in patients who received irradiation stent placement, which was mainly caused by tissue/tumor growth or stent migration.[12],[13]

To decrease the rate of recurrent dysphagia, a novel irradiation stent (NIS) has been designed. The primary aim of this study is to evaluate whether the NIS could decrease the rate of recurrent dysphagia, compared to the conventional irradiation stent (CIS) in patients with malignant dysphagia. In addition, technical success, clinical success, overall survival, and adverse events were also compared between the two groups.


 > Materials and Methods Top


Study design and participants

This monocentric RCT was approved by the institutional review board, and written informed consent was obtained from all patients before enrollment. The inclusion criteria were: (i) histologically confirmed malignant stricture located in the esophagus or gastric cardia; (ii) progressive dysphagia with the Ogilvie dysphagia score of 3 or 4 (0, no dysphagia; 1, normal diet avoiding certain foods; 2, semi-solid diet; 3, fluids only; and 4, complete dysphagia);[14] (iii) unresectable tumors due to extensive lesions, metastases, or poor medical condition; (iv) patients with clear consciousness, cooperation; (v) Eastern Cooperative Oncology Group (ECOG) performance status score of 0–3. Exclusion criteria were: (i) The superior border of the lesion extending beyond the level of the seventh cervical vertebrae; (ii) previous treatment with stent placement or surgical resection for the same condition; (iii) ulcerative esophageal cancer; (iv) esophageal fistula; and (v) severe hepatic inadequacy or renal inadequacy.

Randomization and masking

Recruited patients were randomly allocated, with a 1:1 ratio, into the NIS group or the CIS group. The randomization sequence was computer-generated using a block randomization method with a block size of 4. The coded treatment assignments were stored in opaque envelopes to maintain allocation concealment. With the radiologists being the only exception, all patients and investigators were masked to group assignment.

Features of irradiation stents

The NIS (Micro-tech, Nanjing, China) and the CIS (Micro-tech) were braided from nitinol alloy wires. Both stents were covered with a silicon membrane to resist tumor/tissue ingrowth. The CIS is a partially covered SEMS, with a fully covered stent body and bared flanges on either end. While the NIS is a fully covered SEMS, of which stent flares are barrel-shaped with a lasso at the proximal end to facilitate stent removal. The NIS is composed of several separated segments. Each segment is connected with nylon lines. The NIS is also a double-layered stent. The outer uncovered nitinol wires were overlapped in both end portions of the covered stent. This design could facilitate the stent to anchor to the esophageal wall [Figure 1].
Figure 1: Feature of the novel irradiation stent. The novel irradiation stent (Micro-tech, Nanjing, China) was braided from nitinol alloy wires and fully covered with a silicon membrane. Stent flares are barrel-shaped with a lasso at the proximal end to facilitate stent removal. The novel irradiation stent is composed of several separated segments, and each segment is connected with long nylon lines. The novel irradiation stent is also a double-layered stent. The outer uncovered nitinol wires were overlapped in both end portions of the covered stent

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Sheaths (4.8 mm long and 0.8 mm wide) carrying 125I radioactive seeds (CIAE-6711; Chinese Atomic Energy Science Institution, Beijing, China) are attached to the outer surface of the stent body. The 125I seed has a half-life of 59.4 days, with the half penetration distance of 20 mm. The principal photon emissions are 27.4–31.5 keV X-ray and 35.5 keV γ-ray. The seeds were loaded into the sheaths immediately before the procedure. The dose and distribution of 125I seed were calculated based on a treatment planning system (TPS, University of Beijing Aeronautics and Astronautics, Beijing, China). The stents are available in 60, 80, 100, 120, and 140 mm in length, with diameters of 16/22, 18/24, or 20/26 mm (body/flare) after full expansion.

Procedure

Stent placement was performed under a C-arm angiographic unit (Innova 3100; GE Healthcare, Waukesha, WI, USA) by experienced interventional radiologists. The pharynx and larynx were routinely anesthetized before stent placement. A 5-F catheter was inserted transorally across the stricture, and then iodinated contrast medium was injected via the catheter to detect the shape of the stricture. A 0.035-inch super-stiff guidewire was exchanged through the catheter. A stent delivery catheter was then passed over the guidewire to deploy the stent on the target lesion. The length of the stent should be at least 2 cm longer at each end of the stricture.

All patients were remained in the radioprotective wards after the procedure until discharge. Management related to the safety of the irradiation stents was based on the criteria recommended by the International Commission on Radiological Protection.

After stent placement, patients accepted a liquid diet for 1 day, then the diet was advanced gradually to a solid diet. The position of the stent and the seeds were confirmed fluoroscopically after 7 days.

Follow-up

Patients were evaluated 7 days after stent placement, every month for first 6 months, and every 3 months thereafter until the patient's death or last follow-up. For patients still being alive at the end of the study (October 30, 2020), the minimum duration of follow-up was 6 months. Clinical signs and imaging examinations (esophagography or computed tomography scan) were evaluated. When recurrent dysphagia recurred, an endoscopic examination was performed to confirm.

Endpoints

The primary endpoint was the rate of recurrent dysphagia. Recurrent dysphagia was defined as the recurrence of obstructive symptoms caused by tissue/tumor growth or stent migration, with a dysphagia score of >2 after initial successful treatment of dysphagia. Dysphagia was investigated with the Ogilvie score as mentioned above. Stent patency was defined as the time from stenting to the first episode of recurrent dysphagia.

The secondary endpoints included technical success, clinical success, overall survival, and adverse events. Technical success was defined as placement of the stent in the target position and good passage of contrast medium through the stent. Clinical success was defined as relief of dysphagia with a decrease of at least one point in the Ogilvie score within 7 days after stent placement. Overall survival was defined as the time from stenting to death. Adverse events were assessed according to the Common Terminology Criteria for Adverse Events version 5.0 (CTCAE v5.0).

Statistical analysis

Previous studies demonstrated the cumulative recurrent restenosis rate of the CIS was approximately 28%–37% in patients with malignant dysphagia.[12],[13] We calculated the sample size needed to detect a >15% difference between the CIS and the NIS. Hence, we estimated the cumulative recurrent restenosis rate to be 33% in the CIS group versus 15% in the NIS group. We projected an enrollment period of 12 months, an entire trial period of 18 months, a two-sided targeted significance level of 0.05, a statistical power of 80%, and an attrition rate of 10%, resulting in a minimum sample size of 47 per group. Sample size estimation was conducted using the PASS11 software (NCSS, LLC., Kaysville, Utah, USA).

Analyses were done in an intention-to-treat group, including all patients enrolled in the study and received randomization. Data were presented using mean and standard deviations for normally distributed continuous variables, median and interquartile range for nonnormally distributed continuous variables, and numbers and percentages for categorical variables. Continuous variables were analyzed with the independent sample t-test or the Mann–Whitney U-test, and categorical variables were analyzed with the Pearson Chi-square test or Fisher's exact test. Dysphagia scores before and after stent placement were analyzed with the Wilcoxon signed-rank test. Stent patency was analyzed by both Cox regression on the cause-specific hazard ratio (CSHR) and Fine-Gray regression on sub-distributional hazard ratio (SHR) to show the direct and indirect effects of stent types on recurrent dysphagia. In the Cox regression model, patients without recurrent dysphagia were censored at the date of the last follow-up or the date of death. In the Fine-Gray regression model, living patients without recurrent dysphagia were censored at the date of the last follow-up, and death was regarded as a competing event. Overall survival was estimated according to the Kaplan-Meier method, and living patients were censored at the date of the last follow-up. Predictive factors for survival were evaluated by the Cox regression model, and factors with a P < 0.10 in the univariate analysis were entered into the multivariate analysis. Two-sided tests were performed and a P < 0.05 was considered statistically significant. All analyses were performed using STATA 14 (Stata Corp LP, College Station, Texas, USA).


 > Results Top


Patient characteristics

A total of 94 patients from 122 candidates were enrolled between April 2019 and April 2020. After randomization, 47 patients were assigned to the NIS group, and the other 47 patients were assigned to the CIS group [Figure 2]. Baseline characteristics of the enrolled patients are well balanced in [Table 1].
Figure 2: Trial CONSORT diagram

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Table 1: Baseline characteristics

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Primary endpoint

Recurrent dysphagia was observed in 12.8% (6/47) of patients in the NIS group and 31.9% (15/47) in the CIS group (P = 0.026). Tissue/tumor growth occurred in 4 patients (8.5%) after NIS placement, and 12 (25.5%) after CIS placement (P = 0.028). Stent migration occurred in 2 patients (4.3%) after NIS placement and 3 (6.4%) after CIS placement (P = 0.646). No food obstruction was found in both groups. Cox regression analysis showed that the NIS group had superior outcomes to the CIS group in terms of stent patency (CSHR 0.356; 95% CI 0.138–0.918; P = 0.033), which was in line with the result displayed by the Fine-Gray regression analysis (SHR 0.359; 95% CI 0.139–0.926; P = 0.034) [Figure 3]. Besides, stent type was the only factor for stent patency [Table 2].
Figure 3: Cox regression analysis and Fine-Gray regression analysis of stent patency. Cox regression analysis showed that the novel irradiation stent group had superior outcomes to conventional irradiation stent group in terms of stent patency (cause-specific hazard ratio 0.356; 95% confidence interval 0.138–0.918; P = 0.033), which was in line with the result displayed by the Fine-Gray regression analysis (sub-distributional hazard ratio 0.359; 95% confidence interval 0.139–0.926; P = 0.034)

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Table 2: Stenosis analysis

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The managements for tissue/tumor growth included additional SEMS placement (2 in the NIS group vs. 6 in the CIS group), additional irradiation stent placement (2 in the NIS group vs. 5 in the CIS group), and nasointestinal tube insertion (1 in the CIS group). All the migrated stents were successfully removed. After stent removal, 3 patients received second irradiation stent placement (1 in the NIS group and 2 in the CIS group), and 2 patients (1 in each group) refused re-intervention because of tumor shrinkage and symptom relief. For these patients with stent migration, no radioactive seed loss, acute gastritis, ulceration, or perforation was found.

Secondary endpoints

The technical success rate was 100.0% (47/47) in both groups. No radioactive seed-related technical failures were encountered. The clinical success rate was also 100.0% in both groups. Within 7 days after stent placement, the mean dysphagia scores decreased from 3.23 ± 0.43 to 1.15 ± 0.62 in the NIS group and from 3.34 ± 0.48 to 1.13 ± 0.71 in the CIS group (each P < 0.001). Relief of dysphagia was comparable between the two groups (P = 0.340).

During a median follow-up period of 189 days (range 14–422 days), 5 (5.3%) patients were alive at the end of the study, 7 (7.4%) patients lost to follow-up, and 35 (87.2%) patients died. The causes of death included severe infection (n = 7, 7.4%), upper gastrointestinal hemorrhage (n = 4, 4.3%), and cachexia or multiple organ failure (n = 83, 88.3%). The median overall survival was 177 days (95% CI 139–214) in the NIS group and 168 days (95% CI 153–183) in the CIS group (P = 0.932). Stent type did not influence the overall survival of patients (P = 0.932). A dysphagia score before treatment, ECOG score, TNM classification, and previous treatment were independent risk factors for overall survival in the multivariate regression analysis [Table 3].
Table 3: Adverse events

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Stent-related adverse events, including chest pain, hemorrhage, aspiration pneumonia, nausea/vomiting, and fistula formation were monitored. The incidence of each adverse event was similar between the NIS and CIS groups in both early and late phases. A total of 23 events of Grade ≥3 were recorded in 18 (19.1%) patients: 10 were in the NIS group and 8 in the CIS group. The incidence was comparable between the two groups (21.3% vs. 17.0%, P = 0.600). Nearly two-thirds of patients experienced retrosternal discomfort or pain after stent placement, while most of them had spontaneous pain relief within 3 days. For patients with severe or persistent chest pain, the symptoms were relieved by narcotic analgesics. Except 4 patients (2 in each group) died due to acute upper gastrointestinal hemorrhage, patients with esophageal hemorrhage recovered spontaneously or through medication. Although nausea and vomiting are relatively common, the patients' symptoms are mild.


 > Discussion Top


The present prospective study demonstrated that this NIS could successfully decrease the rate of recurrent dysphagia compared with the CIS in patients with malignant dysphagia. Besides, no differences in secondary outcomes were found between the two groups, including technical success, clinical success, overall survival, and adverse events.

Historically, the long-term efficacy after stent placement in advanced esophageal cancer has been restricted by postoperative recurrent dysphagia. Brachytherapy has been proposed as an alternative option to stent placement. Although the CIS has delivered satisfactory results in prolonging overall survival in those patients.[12],[13] The high rate of recurrent dysphagia after irradiation stent placement has been regarded as a dilemma in clinical practice. In this study, the rate of recurrent dysphagia in the CIS group was 31.9%, which was comparable to the previous result (33.3%). While the rate of recurrent dysphagia in the NIS group significantly decreased to 12.8%. Moreover, the rate of recurrent dysphagia in the NIS group seems better than those reported in previous studies (21.8%–28.6%).[12],[13] These results fulfilled the initial aim of the design of such a new irradiation stent.

Tissue/tumor growth were the most common reasons for recurrent dysphagia in the whole cohort. Meanwhile, the rate of tissue/tumor growth in the NIS group (8.5%) was significantly lower than that in the CIS group (25.5%). We speculate that this result benefited from the reduction of the uncovered surface area, which theoretically could alleviate the mechanical stimulation to surrounding tissue. Besides, the design of segmented stent applied in the NIS was able to provide lower axial force, which could make the stent compliable to the esophageal anatomy and relieve the hyperblastosis.[15]

The design of segmented and fully covered stent of NIS has been a concern whether it could increase the incidence of stent migration. Some fully covered SEMS, such as the Wallflex stent has a migration rate of 12.5%.[16] In this study, the incidence of stent migration was similarly low in two groups. This maybe contribute to the dumbbell-shaped flanges, the attached seed sheaths, which act as anti-migration struts. As for the NIS, the design of segmented stent is helpful to keep both stent and seed sheaths in an adequate position in the esophageal tract, and the overlapped nitinol mesh in both ends of the stent is beneficial to anchor the stent to the esophageal wall. Both the Cox regression analysis and the Fine-Gray regression analysis showed that the NIS group had better outcomes than the CIS group in terms of stent patency.

The patients in the NIS group did not obtain the benefit in survival compared to those in the CIS group. Both groups shared comparable median overall survival to previous multicentric RCT.[13] Moreover, stent type did not rank as an independent risk factor for overall survival. In the regression analysis, the dysphagia score before treatment, ECOG score, TNM classification, and previous treatment were independent risk factors for overall survival.

Analysis of pooled data from the recent meta-analysis showed that severe adverse events occur in about 20%–22.6% of cases after placement with partially-covered and fully-covered SEMS.[9],[17] In our study, the incidence of adverse events was comparable between the NIS group and the CIS group (21.3% vs. 17.0%). The predominant adverse event after stent placement was retrosternal discomfort or pain, while most of them spontaneously recovered without any treatment. Noteworthily, a total of 4 patients (4.3%) died due to acute upper gastrointestinal hemorrhage, which seemed higher than that reported of 2%.[9] Radiation therapy has been regarded as a risk factor in the safety consideration during the irradiation stent placement. In our cohort, nearly one fifth patients received previous or post external radiotherapy. Fortunately, radiation-related adverse events were not observed.

The study has several limitations. First, this study was conducted at a single center with a relatively small sample. Further multicenter, large-sample RCT was needed. Second, improvement of QoL was one of the major goals of stent placement while the QoL was not recorded in this study. Third, all stents were placed under the fluoroscopic guidance. The feasibility and efficacy of endoscopic placement warrants further investigation.


 > Conclusions Top


In patients with malignant dysphagia, compared with CIS, NIS could decrease the rate of tissue/tumor growth without increase the rate of stent migration, and therefore decrease the rate of recurrent dysphagia.

Financial support and sponsorship

This study was Jiangsu Provincial Special Program of Social Development (SBK20190350, BE2019750) and National Natural Science Foundation of China (81971716, 82001935).

Conflicts of interest

There are no conflicts of interest.



 
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Zhu HD, Guo JH, Mao AW, Lv WF, Ji JS, Wang WH, et al. Conventional stents versus stents loaded with (125) iodine seeds for the treatment of unresectable oesophageal cancer: A multicentre, randomised phase 3 trial. Lancet Oncol 2014;15:612-9.  Back to cited text no. 13
    
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Ogilvie AL, Dronfield MW, Ferguson R, Atkinson M. Palliative intubation of oesophagogastric neoplasms at fibreoptic endoscopy. Gut 1982;23:1060-7.  Back to cited text no. 14
    
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Fuccio L, Mandolesi D, Farioli A, Hassan C, Frazzoni L, Guido A, et al. Brachytherapy for the palliation of dysphagia owing to esophageal cancer: A systematic review and meta-analysis of prospective studies. Radiother Oncol 2017;122:332-9.  Back to cited text no. 17
    


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