J Neurogastroenterol Motil 2023; 29(3): 306-313  https://doi.org/10.5056/jnm21240
Randomized Controlled Trial of Anti-reflux Mucosectomy Versus Radiofrequency Energy Delivery for Proton Pump Inhibitor-refractory Gastroesophageal Reflux Disease
Yan Wang, Meihui Lv, Lin Lin,* and Liuqin Jiang*
Department of Gastroenterology, The First Affiliated Hospital of Nanjing Medical University, Nanjing, China
Correspondence to: *Liuqin Jiang, MD
Department of Gastroenterology, The First Affiliated Hospital of Nanjing Medical University, 300 Guangzhou Road, Nanjing, Jiangsu 210029, China
Tel: +86-025-68303472, Fax: +86-13951017379, E-mail: jiangliuqin@163.com
Lin Lin, MD, PhD
Department of Gastroenterology, The First Affiliated Hospital of Nanjing Medical University, 300 Guangzhou Road, Nanjing, Jiangsu 210029, China
Tel: +86-025-68303472, Fax: +86-13951709069, E-mail: lin9100@aliyun.com

Liuqin Jiang and Lin Lin are equally responsible for this study.
Yan Wang and Meihui Lv equally contributed to this study.
Received: December 14, 2021; Accepted: April 25, 2022; Published online: June 19, 2023
© The Korean Society of Neurogastroenterology and Motility. All rights reserved.

cc This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Abstract
Background/Aims
The efficacy and safety of anti-reflux mucosectomy (ARMS) or radiofrequency energy delivery in the treatment of gastroesophageal reflux disease (GERD) have been reported, but the difference between the 2 remains unclear.
Methods
This was a single center, randomized, comparative clinical study. Patients with symptoms of heartburn and/or regurgitation despite proton pump inhibitor treatment were randomly assigned to either ARMS group (n = 20) or radiofrequency group (n = 20). Primary outcome was the standardized GERD questionnaire (GERDQ) at 2 years after the procedures. Secondary outcomes were the proportions of patients with complete proton pump inhibitor (PPI) cessation and patients satisfied with the treatment.
Results
A total of 18 patients randomized to ARMS and 16 to radiofrequency were analyzed in this study. The operation success rate of the 2 groups was 100%. In both ARMS and radiofrequency groups, GERDQ scores at 2 years after the procedures were significantly lower than that before operation (P = 0.044 and P = 0.046). At 2 years postoperatively, the scores of GERDQ did not differ between the 2 groups (P = 0.755). There was no significant difference in the rate of discontinuation of PPIs and patient satisfaction in the ARMS and radiofrequency groups (P = 0.642 and P = 0.934).
Conclusions
The clinical efficacy of ARMS and radiofrequency for the PPI-refractory GERD is equivalent. ARMS, the efficacy of which could be maintained for at least 2 years, is promising endoscopic management for the treatment of refractory GERD.
Keywords: Gastroesophageal reflux; Humans; Proton pump inhibitors
Introduction

Gastroesophageal reflux disease (GERD) is a widely prevalent disorder characterized by the symptoms of heartburn and/or regurgitation.1 It could cause long-term complications and compromise the quality of life. While proton pump inhibitors (PPIs) are widely prescribed for the treatment of GERD, long-term use of PPIs is associated with an increased risk of infection and gastric cancer.2 Furthermore, a considerable proportion of GERD patients frequently experienced symptoms despite PPI treatment.3 Patients with PPI-refractory gastroesophageal reflux disease (RGERD) are defined as those whose symptoms are not responsive to a standard dose of at least 8-week PPI treatment.4 Fundoplication is currently the preferred surgical treatment for RGERD.5,6 However, the surgical trauma and postoperative complications limit its application. The development of minimally invasive endoscopic procedures including anti-reflux mucosectomy (ARMS) and radiofrequency (RF) energy delivery provide novel ideas in the treatment of RGERD.7

Stretta RF energy delivery is a new technique which was approved for GERD treatment in 2000.8 RF can result in scar and fibrosis formation above and below the esophagogastric junction (EGJ) to increase lower esophageal sphincter (LES) pressure. Additionally, RF may help to inhibit the gastric distension-induced transient lower esophageal sphincter relaxations to achieve its therapeutic effect.9 ARMS is an emerging endoscopic technique which was first reported by Inoue et al10 in 2014. The therapeutic mechanism underlying ARMS is to make partial or complete removal of mucosal tissue of EGJ or cardia to promote scar formation and contraction, increase LES pressure, and to prevent gastroesophageal reflux. Previous studies have reported that ARMS may be an effective endoscopic operation to reduce the PPI dose in patients with GERD.11 The efficacy and safety of ARMS and RF in the treatment of GERD have been reported in early studies, but the difference in treatment outcomes between these two has yet to be reported. Our study is aimed to compare the clinical efficacy and safety between ARMS and RF energy delivery in PPI-refractory GERD.

Materials and Methods

Patients Selection and Study Design

This study is a single-center, randomized, controlled study. Forty patients whose symptoms are not responsive to a standard dose of at least 8-week PPI treatment participated in this study from March 2019 to August 2019. The refractory symptoms are defined as less than 50% improvement of GERD questionnaire (GERDQ) score after 8-week PPI treatment (omeprazole 20 mg, once a day, or rabeprazole 10 mg, twice a day).12 The inclusion criteria for patients enrolled in this study were as follows: diagnosed as RGERD; were 18 to 70 years old; provided written consent for the participation of this study. Patients with one or more of the following criteria were excluded: had a history of peptic stricture or ulcer; upper gastrointestinal tract surgery or tumor; severe esophageal motility disorders; Los Angeles classification grade C or D; hiatus hernia > 2 cm; were pregnant or breastfeeding or plan to become pregnant during the research; any contraindication related to ARMS or RF. This study protocol was reviewed and approved by the Ethics Committee of our hospital (2018-SR-271).

Clinical characteristics including the gender, body mass index, and course of GERD were recorded in detail before the procedures. The GERD symptoms were evaluated by GERDQ. Patients were divided into either ARMS or RF group randomly by drawing lots. All eligible patients underwent upper gastrointestinal endoscopy and 24-hour impedance-pH monitoring before the procedures. Follow-up was conducted at 2 years after the operation, and the GERDQ score of each patient was calculated. Registry information is Chinese Clinical Trial Registry (ChiCTR1900022246).

Anti-reflux Mucosectomy Procedure

Patients were placed in the supine position and ARMS was performed under general anesthesia. The endoscope (GIF-Q260J; Olympus, Tokyo, Japan) was equipped with a cap on the front end. The endoscopic mucosal resection (EMR) method was used to perform ARMS. Two-thirds of the circumference of gastric cardia mucosa along the lesser curvature, 1 cm above the z-line and 2 cm under the z-line, in the retroflexed position was marked, preserving mucosa along the greater curve approximately twice the diameter of the endoscope. After injecting the submucosa along the markings with a mixture of 0.9% sodium chloride solution, indigo carmine, and epinephrine, the mucosal surface was raised. The mucosectomy was repeatedly carried out until the complete excision of marked area was achieved. After the submucosa was inspected for hemostasis and deeper tissue injury, the endoscope was removed. All the procedures were performed by an experienced practitioner. Routine fasting was performed for 24 hours after operation, soft diet and normal diet were given within 2 and 3 days, respectively.

Stretta Radiofrequency Energy Delivery Procedure

Upper gastrointestinal endoscopy was performed and the location of EGJ was confirmed. A guide wire was introduced through the endoscope and the endoscope was then removed. The RF catheter (Medi Equip Medical Technology, Harbin, China), made up with a balloon-basket with 4 treatment elements, was inserted along the guide wire. After the balloon was inflated, the electrode needles were deployed, and RF energy was delivered for 1 minute. The needles were then withdrawn, and the balloon was deflated, followed by the catheter rotated 45° for the next RF delivery. This process is repeated at the z-line and 1.5 cm, 1.0 cm, 0.5 cm above, and below the z-line (7 levels, 56 lesions). The needle was rotated by 30° each time at the gastric cardia and 0.5 cm above it (2 levels, 24 lesions).13 After the mucosa was inspected for fresh bleeding, the endoscope was removed. All the RF procedures were performed by a single experienced practitioner. Patients were asked to take acid suppression medication for 4 weeks after the procedure.

Twenty-four-hour Multichannel Intraluminal Impedance and pH Monitoring

All participants underwent off-PPI impedance-pH monitoring for 24 hours using an ambulatory monitoring system (Medtronic, Heerlen, The Netherlands). Before the tests, patients needed to stop taking prokinetic drugs or PPIs at least 2 weeks. Patients were asked to record the symptoms, meals, and timing of the supine posture during the 24 hours of measurement. Reflux episodes, prolonged acid reflux episodes, acid exposure time, and DeMeester score were recorded.

Outcome Evaluation

Perioperative outcomes including operative complications and the presence or absence of serious adverse events were recorded. Primary outcome was the GERDQ at 2 years after the procedures. GERDQ is a standardized diagnostic scale based on the Reflux Disease Questionnaire.14 Patients completed the following 6 questions before and 2 years after operation: heartburn, regurgitation, nausea, epigastric pain, sleep disturbance because of heartburn or regurgitation, and over-the-counter medication use. A score ≥ 9 is a predictor of the proven GERD.15 Secondary outcomes were proportions of patients with complete PPI cessation and patients satisfied with the treatment.

Statistical Methods

Sample size was determined based on a two-sided α of 0.05, a β of 0.02, and 20% loss to follow-up and it showed that 20 patients should be enrolled in each group. Continuous parameters were expressed as mean and standard deviation or median (interquartile range) and were compared using Mann-Whitney U test, or paired or unpaired Student’s t test, as appropriate. Categorical variables were analyzed using the chi-squared test or Fisher’s exact test. Statistical significance was set at P < 0.05.

Results

Baseline Data and Impedance-pH Parameters

Figure 1 shows the patient selection process. Of 40 patients for randomization, 2 and 3 participants withdrew before undergoing the procedures, respectively. One patient who underwent RF lost to follow-up. A total of 34 patients (18 underwent ARMS, 16 underwent RF) were analyzed in this study. Demographic data and baseline disease characteristics did not differ between both treatment arms (Table 1) (all P > 0.05). There were no significant differences between the 2 groups regarding the occurrence of hiatal hernia, Barrett’s esophagus, and Los Angeles classification grade A or B esophagitis (all P > 0.05). The DeMeester score, reflux episodes and total percent of time with pH < 4 were similar between the groups (all P > 0.05).

Table 1 . Baseline Data and Impedance-pH Parameters of Patients

Baseline dataARMS (n = 18)RF (n = 16)P-value
Age (yr)59.39 ± 14.0554.31 ± 13.050.285
Female patients8 (44.44)5 (31.25)0.429
BMI (kg/m2)23.97 ± 2.9722.22 ± 2.480.072
Duration of symptoms (yr)5.5 (2.8, 12.5)4.0 (2.0, 9.5)0.405
Current alcohol use2 (11.11)7 (43.75)0.052
Current smoking4 (22.22)4 (25.00)0.999
Hiatal hernia6 (33.33)3 (18.75)0.448
LA grade A or B18 (100.00)14 (87.50)0.214
Barrett’s esophagus0 (0.00)1 (6.25)0.471
Gastric atrophy2 (11.11)0 (0.00)0.487
GERDQ score13.44 ± 2.1512.75 ± 1.980.337
Results of MII-pH monitoring
DeMeester Score31.7 (22.0, 66.7)27.0 (19.7, 44.4)0.369
Reflux episodes88.0 (77.5, 186.8)125.0 (68.0, 160.0)0.981
Total % of time with pH < 48.6 (6.4, 18.3)6.3 (3.7, 12.7)0.182
Episodes of prolonged acid reflux5.0 (2.8, 12.8)2.0 (0.0, 9.5)0.091

ARMS, anti-reflux mucosectomy; RF, radiofrequency energy delivery; BMI, body mass index; LA, Los Angeles classification; GERDQ, gastroesophageal reflux disease questionnaire; MII-pH, multichannel intraluminal impedance pH.

Data are expressed as mean ± SD, n (%), or median (interquartile range).



Figure 1. Flowchart indicating trail design. ARMS, anti-reflux mucosectomy; RF, radiofrequency energy delivery.

Patient Perioperative Outcomes

The operation success rate of the 2 groups was 100%. As shown in Table 2, the proportion of patients who reported abdominal pain or bloating did not differ between the 2 groups (both P > 0.05). In both groups, there were no serious adverse events, no need for dilation or surgery, and no 30-day mortality. No patient experienced postoperative bleeding or esophageal stricture.

Table 2 . Patient Perioperative Outcomes in Both Groups

Patient outcomesARMS
(n = 18)
RF
(n = 16)
P-value
Reported abdominal pain9 (50.00)5 (31.25)0.315
Reported bloating2 (11.11)1 (6.25)0.999
Serious adverse events0 (0.00)0 (0.00)-
Need for dilation0 (0.00)0 (0.00)-
30 day mortality0 (0.00)0 (0.00)-

ARMS, anti-reflux mucosectomy; RF, radiofrequency energy delivery.

Data are expressed as n (%).



Results at 2-year Endpoint

At 2 years after procedures (Fig. 2), the GERDQ score significantly improved from 13.44 ± 2.15 to 10.00 ± 6.00 in patients who underwent ARMS (P = 0.027), while from 12.75 ± 1.98 to 9.81 ± 4.71 in RF group (P = 0.044). There was no significant difference in postoperative GERDQ score between the 2 groups (P = 0.921).

Figure 2. Gastroesophageal reflux disease questionnaire (GERDQ) score before and 2 years after either anti-reflux mucosectomy (ARMS) or radiofrequency (RF) energy delivery. The horizontal bar in the box indicates the median, the box represents the interquartile range, and the line outside the box represents 10th and 90th percentile values.

Two years postoperatively (Fig. 3), the majority of patients in both ARMS and RF groups were able to completely discontinue the PPI therapy, the difference was not statistically significant (61.11% vs 68.75%, P = 0.642). Most patients in both groups were satisfied with the current treatment effect (61.11% vs 62.50%, P = 0.934). The proportion of patients who have ever experienced dysphagia after the procedures was higher in ARMS group than in RF group (P = 0.046). However, all the symptoms of postoperative dysphagia subsided toward normality over time and did not persist at 2 years postoperatively. The endoscopic findings and details before and after the procedures are shown in Figure 4.

Figure 3. Results at the 2-year endpoint. (A) Percentage of patients with complete proton pump inhibitor (PPI) cessation in anti-reflux mucosectomy (ARMS) or radiofrequency (RF) energy delivery group. (B) Percentage of patients satisfied with treatment of ARMS or RF. (C) Percentage of patients who experienced postoperative dysphagia.

Figure 4. Endoscopic views of 2 patients. (A-C) Endoscopic views of one patient in the anti-reflux mucosectomy (ARMS) group. (A) Before ARMS. A retroflexed view of the endoscopy demonstrated cardiac relaxation. (B) Immediately after ARMS. Two-thirds of circumferential piecemeal mucosectomy was performed. The scope was removed after complete hemostasis. (C) Appearance at 2 years after ARMS. Endoscopy in retroflexion showed a robust esophagogastric junction (EGJ). The cardia mucosa is tightly wrapped around the endoscopy, and the wound healed well. (D-F) Endoscopic views of another patient in the radiofrequency energy delivery (RF) group. (D) Before RF. Several bands of mucosal hyperemia were observed at the lower esophagus above the z-line. (E) Immediately after RF. Small cautery burns induced by radiofrequency energy were seen at the EGJ. (F) Two years after RF. The esophagus was unobstructed and had normal color, the esophageal mucosa was smooth, and the z-line was clear.
Discussion

This trial provided the first prospective, randomized, controlled comparison between ARMS and RF therapy in a population of patients with PPI-refractory GERD. We demonstrated no difference between ARMS and RF in controlling GERD symptoms after a follow-up period of 2 years. At 2 years postoperatively, except for significantly higher incidence of postoperative dysphagia in patients allocated to ARMS, no differences were observed between ARMS and RF in terms of any other study variables, including the proportions of patients with complete PPI cessation and patient satisfaction.

The effectiveness of ARMS and RF in the treatment of RGERD has been reported in the previous studies. ARMS could improve subjective symptoms, acid exposure time, DeMeester score as well as flap valve grade and EGJ distensibility.16 RF was also proved to be effective in relieving reflux esophagitis symptoms and reducing GERD health-related quality of life score, acid exposure time, and DeMeester score in Chinese patients with GERD.17 One of what are common between these 2 endoscopic procedures is that both leave no artificial devices or prostheses in situ. Arts et al18 demonstrated that the RF procedure was associated with decrease of the EGJ compliance, which further indicates that the therapeutic mechanism between ARMS and RF is partly similar. Laparoscopic fundoplication is currently the gold standard surgical treatment for GERD patients who are refractory to medical management. Literature data proved that the ARMS and laparoscopic Nissen fundoplication had comparable quality of life outcomes, while ARMS had better intraoperative outcomes.19 Compared to Toupet fundoplication, RF was superior in improving the LES pressure and DeMeester score.20 However, the side-by-side comparison of treatment outcomes between ARMS and RF groups is rare. In this trial, ARMS and RF were equally effective in improving the GERD symptoms after a 2-year follow-up. Accordingly, ARMS and RF represent effective and durable anti-reflux procedures that can be offered to RGERD patients who are not willing to undergo invasive surgical procedure.

The postoperative PPI cessation and satisfaction with outcomes in the ARMS cohort were comparable to that in RF group. In ARMS group, 61.11% of patients were off PPIs completely at 2 years postoperatively, which is consistent with previous studies with reported postoperative PPI cessation rate ranging from 50.00% to 69.40%.11,21,22 The PPI elimination rate of 68.75% in RF group is also similar to early studies which showed rates of 62.00-87.00%.23 The proportion of patients who were satisfied with ARMS outcomes has not been reported. The patient satisfaction rate after RF (62.50%) is slightly lower than that in previous study conducted in Chinese population, which showed rate of 92.60% and 96.30% at 6 months and 12 months after RF.17 The reason may be that patients included in our study were all PPI-refractory GERD patients.

Dysphagia caused by excessive stenosis of the EGJ after ARMS remains a concern. In this study, we found that the proportion of patients who reported transient postoperative dysphagia was higher in ARMS group than that in RF group. Previous studies showed that 8.00% to 16.00% patients experienced dysphagia requiring endoscopic balloon dilation after ARMS.11,22 The rate of dysphagia after ARMS has not been reported. The result of RF-related dysphagia is consistent with previous studies, with rates of postoperative dysphagia ranging from 0.00% to 8.30%.24-26 RF may hold the advantage of fewer dysphagia complaints. However, scarring around the resection area is physiologic process, and postoperative dysphagia is an anticipated event and has subsided toward normality over time after ARMS. Consequently, transient dysphagia after ARMS in this trial may not be a clinically significant issue. Methods to reduce postoperative dysphagia involve preserving the esophageal squamous mucosa and preventing the scar from contracting.

In this study, one limitation is the lack of sham operation group as a control group, which made us unable to determine the effect of ARMS or RF compared to untreated group. Next, postoperative endoscopy and impedance-pH data, which would provide the objective evidence of reflux control, was not included. Because only a small number of patients with recurrent symptoms were willing to have further endoscopy and impedance-pH testing, postoperative data may be insufficient and biased. Last is the relatively small number of participants from a single medical center in this trial. Further multiple-center studies with large sample size are needed to investigate potential risk factors for postoperative side effect and poor clinical outcomes in patients undergoing ARMS.

In conclusion, the clinical efficacy of ARMS is comparable to that of RF in treating PPI-refractory GERD. Although RF may be superior to ARMS with regard to postoperative dysphagia, complaints of dysphagia in both groups subsided toward normality over time. The treatment effect of both endoscopic procedures can be maintained for at least two years. In patients with persistent GERD symptoms after initial standard dosing of PPI, ARMS can also be considered as a clinically viable endoscopic minimally invasive management.

Financial support

None.

Conflicts of interest

None.

Author contributions

Yang Wang, Meihui Lv, Lin Lin, and Liuqin Jiang contributed in writing, editing, and proofreading of the article; Lin Lin and Liuqin Jiang conceptualized and designed the structure of the article and supervised the writing; and Lin Lin and Liuqin are guarantors of the article.

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