ABSTRACT
BACKGROUND:
The addition of endoscopic ablative therapy plus proton pump inhibitors or fundoplication is postulated for the treatment of patients with long-segment Barrett´s esophagus (LSBE); however, it does not avoid acid and bile reflux in these patients. Fundoplication with distal gastrectomy and Roux-en-Y gastrojejunostomy is proposed as an acid suppression-duodenal diversion procedure demonstrating excellent results at long-term follow-up. There are no reports on therapeutic strategy with this combination.
AIMS:
To determine the early and long-term results observed in LSBE patients with or without low-grade dysplasia who underwent the acid suppression-duodenal diversion procedure combined with endoscopic therapy.
METHODS:
Prospective study including patients with endoscopic LSBE using the Prague classification for circumferential and maximal lengths and confirmed by histological study. Patients were submitted to argon plasma coagulation (21) or radiofrequency ablation (31). After receiving treatment, they were monitored at early and late follow-up (5–12 years) with endoscopic and histologic evaluation.
RESULTS:
Few complications (ulcers or strictures) were observed after the procedure. Re-treatment was required in both groups of patients. The reduction in length of metaplastic epithelium was significantly better after radiofrequency ablation compared to argon plasma coagulation (10.95 vs 21.15 mms for circumferential length; and 30.96 vs 44.41 mms for maximal length). Intestinal metaplasia disappeared in a high percentage of patients, and histological long-term results were quite similar in both groups.
CONCLUSIONS:
Endoscopic procedures combined with fundoplication plus acid suppression with duodenal diversion technique to eliminate metaplastic epithelium of distal esophagus could be considered a good alternative option for LSBE treatment.
HEADINGS:
Barrett Esophagus; Endoscopy; Radiofrequency Ablation; Argon Plasma Coagulation; Fundoplication; Gastrectomy
RESUMO
RACIONAL:
A adição de terapia ablativa endoscópica associado a inibidores da bomba de prótons ou fundoplicatura tem sido postulada para o tratamento de pacientes com esôfago de Barrett de segmento longo (EBSL), no entanto, essa conduta não evita o refluxo ácido/biliar nesses pacientes. A fundoplicatura com gastrectomia distal e gastrojejunostomia em Y de Roux (FGD-Y) foi proposta como procedimento de supressão de ácido, demonstrando excelentes resultados no seguimento a longo prazo. Não há relatos na literature com a combinação dessa estratégia terapêutica.
OBJETIVOS:
Determinar os resultados precoces e a longo prazo observados em pacientes com EBSL com ou sem dysplasia de baixo grau, submetidos a FGD-Y, combinado com terapia endoscópica.
MÉTODOS:
Estudo prospectivo incluindo pacientes com EBSL, empregando a classificação de Praga, sendo o comprimento circunferencial (C) e máximo (M) e confirmado por estudo histológico. Os pacientes foram submetidos à coagulação com plasma de argônio (CPA, 21 pacientes) ou ablação por radiofrequência (ARF, 31 pacientes). Após o tratamento, eles foram seguidos precoce e tardiamente (5–12 anos), mediante avaliação endoscópica e histológica.
RESULTADOS:
Foram observadas poucas complicações após o procedimento (úlcera ou estenose). Re-tratamento foi necessário em ambos os grupos de pacientes. A redução do comprimento do epitélio metaplásico foi significativamente melhor após ARF em comparação com CPA (10,95 versus 21,15 mm para C e 30,96 versus 44,41 mm para M). A metaplasia intestinal desapareceu em elevada porcentagem de pacientes, e os resultados histológicos a longo prazo foram bastante semelhantes em ambos os grupos.
CONCLUSÕES:
Procedimentos endoscópicos combinados com fundoplicatura e gastrectomia distal e gastrojejunostomia em Y de Roux, para eliminar o epitélio metaplásico do esôfago distal podem ser considerados uma boa opção alternativa para o tratamento da EBSL.
DESCRITORES:
Esôfago de Barrett; Endoscopia; Ablação por Radiofrequência; Coagulação com Plasma de Argônio; Fundoplicatura; Gastrectomia
INTRODUCTION
Chronic gastroesophageal reflux disease (GERD) is associated with the metaplastic transformation of normal squamous epithelium to premalignant specialized intestinal metaplasia (IM), frequently within the long segment of Barrett´s esophagus (LSBE), which may progress to low-grade dysplasia (LGD), high-grade dysplasia (HGD), or even esophageal adenocarcinoma (EAC). The results of treatment with proton pump inhibitors (PPIs) or surgery with fundoplication alone are intensively discussed among gastroenterologists and surgeons1111 Ciovica R, Riedl O, Neumayer C, Lechner W, Schwab GP, Gadenstätter M. The use of medication after laparoscopic antireflux surgery. Surg Endosc. 2009;23(9):1938-46. https://doi.org/10.1007/s00464-008-0271-8.
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. Medical treatment fails to control bile reflux, and the reflux of acid and bile after an ineffective antireflux barrier plays a fundamental role in the genesis and progression of IM and dysplasia44 Anaparthy R, Sharma P. Progression of Barrett oesophagus: role of endoscopic and histological predictors. Nat Rev Gastroenterol Hepatol. 2014;11(9):525-34. https://doi.org/10.1038/nrgastro.2014.69.
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,1919 Desai TK, Krishnan K, Samala N, Singh J, Cluley J, Perla S, et al. The incidence of oesophageal adenocarcinoma in non-dysplastic Barrett's oesophagus: a meta-analysis. Gut. 2012;61(7):970-6. https://doi.org/10.1136/gutjnl-2011-300730.
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,2929 Kahn A, Al-Qaisi M, Kommineni VT, Callaway JK, Boroff ES, Burdick GE, et al. Longitudinal outcomes of radiofrequency ablation versus surveillance endoscopy for Barrett's esophagus with low-grade dysplasia. Dis Esophagus. 2018;31(4). https://doi.org/10.1093/dote/dox120.
https://doi.org/10.1093/dote/dox120...
. Endoscopic techniques for the eradication of IM and dysplasia are proposed, including endoscopic submucosal dissection (ESD), endoscopic radiofrequency ablation (RFA), argon plasma coagulation (APC), photodynamic therapy, and cryotherapy1818 De Palma GD. Management strategies of Barrett's esophagus. World J Gastroenterol. 2012;18(43):6216-25. https://doi.org/10.3748/wjg.v18.i43.6216.
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,2626 Haidry RJ, Dunn JM, Butt MA, Burnell MG, Gupta A, Green S, et al. Radiofrequency ablation and endoscopic mucosal resection for dysplastic Barrett's esophagus and early esophageal adenocarcinoma: outcomes of the UK National Halo RFA Registry. Gastroenterology. 2013;145(1):87-95. https://doi.org/10.1053/j.gastro.2013.03.045.
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,2828 Hubbard N, Velanovich V. Endoscopic endoluminal radiofrequency ablation of Barrett's esophagus in patients with fundoplications. Surg Endosc. 2007;21(4):625-8. https://doi.org/10.1007/s00464-007-9199-7.
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,4141 Orman ES, Li N, Shaheen NJ. Efficacy and durability of radiofrequency ablation for Barrett's Esophagus: systematic review and meta-analysis. Clin Gastroenterol Hepatol. 2013;11(10):1245-55. https://doi.org/10.1016/j.cgh.2013.03.039.
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,4444 Phoa KN, van Vilsteren FG, Weusten BLAM, Bisschops R, Schoon EJ, Ragunath K, et al. Radiofrequency ablation vs endoscopic surveillance for patients with Barrett esophagus and low-grade dysplasia: a randomized clinical trial. JAMA. 2014;311(12):1209-17. https://doi.org/10.1001/jama.2014.2511.
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,4545 Reed CC, Shaheen NJ. Management of Barrett esophagus following radiofrequency ablation. Gastroenterol Hepatol (N Y). 2019;15(7):377-86. PMID: 31391808.. Among the ablative modalities, RFA is the most employed3434 Krajciova J, Vackova Z, Spicak J, Martinek J. Radiofrequency ablation for Barrett's esophagus-related neoplasia. Minerva Chir. 2018;73(4):366-77. https://doi.org/10.23736/S0026-4733.18.07783-0.
https://doi.org/10.23736/S0026-4733.18.0...
.
A large volume of published data consistently documented high rates of complete eradication of IM and dysplasia, reduced risk of EAC, and low rates of complications, thus establishing RFA as the preferred modality44 Anaparthy R, Sharma P. Progression of Barrett oesophagus: role of endoscopic and histological predictors. Nat Rev Gastroenterol Hepatol. 2014;11(9):525-34. https://doi.org/10.1038/nrgastro.2014.69.
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,4949 Subramanian CR, Triadafilopoulos G. Endoscopic treatments for dysplastic Barrett's esophagus: resection, ablation, what else? World J Surg. 2015;39(3):597-605. https://doi.org/10.1007/s00268-014-2636-6.
https://doi.org/10.1007/s00268-014-2636-...
. While this procedure can eradicate either IM or LGD, recurrence can be observed over time once acid and bile reflux are not permanently eliminated with medical treatment.
The combination of fundoplication with endoscopic therapy is postulated as a valid option, showing good initial and long-term results2727 Han S, Low DE. Laparoscopic antireflux surgery: are old questions answered? Should it be used conjoined with endoscopic therapy for Barrett's esophagus? Arq Bras Cir Dig. 2022;35:e1664. https://doi.org/10.1590/0102-672020210002e1664.
https://doi.org/10.1590/0102-67202021000...
. However, laparoscopic fundoplication in LSBE patients fails to create an effective and permanent antireflux barrier, in almost 30% of cases66 Braghetto I, Csendes A, Burdiles P, Korn O. Antireflux surgery, highly selective vagotomy and duodenal switch procedure: post-operative evaluation in patients with complicated and non-complicated Barrett's esophagus. Dis Esophagus. 2000;13(1):12-7. https://doi.org/10.1046/j.1442-2050.2000.00066.x.
https://doi.org/10.1046/j.1442-2050.2000...
,1414 Csendes A, Bragheto I, Burdiles P, Smok G, Henriquez A, Parada F. Regression of intestinal metaplasia to cardiac or fundic mucosa in patients with Barrett's esophagus submitted to vagotomy, partial gastrectomy and duodenal diversion. A prospective study of 78 patients with more than 5 years of follow up. Surgery. 2006;139(1):46-53. https://doi.org/10.1016/j.surg.2005.05.022.
https://doi.org/10.1016/j.surg.2005.05.0...
. Fundoplication combined with highly selective vagotomy is associated with high rate of recurrence of Barrett's esophagus (BE) and its complications1717 Csendes A, Orellana O, Figueroa M, Lanzarini E. Long-term (18 Years) results of patients with long-segment Barrett esophagus submitted to acid suppression-duodenal diversion operation: better than nissen fundoplication? Ann Surg. 2023;277(2):252-8. https://doi.org/10.1097/SLA.0000000000004760.
https://doi.org/10.1097/SLA.000000000000...
.
Therefore, we performed the fundoplication with distal gastrectomy and Roux-en-Y gastrojejunostomy in LSBE patients to avoid acid and bile reflux, called acid suppression, and obtain an early and safe eradication with diversion procedure, known as acid suppression-duodenal diversion (AS-DD). With this procedure, regression of IM to cardiac mucosa was observed in 38% and LGD to IM in 80% of cases, at very long follow-up1414 Csendes A, Bragheto I, Burdiles P, Smok G, Henriquez A, Parada F. Regression of intestinal metaplasia to cardiac or fundic mucosa in patients with Barrett's esophagus submitted to vagotomy, partial gastrectomy and duodenal diversion. A prospective study of 78 patients with more than 5 years of follow up. Surgery. 2006;139(1):46-53. https://doi.org/10.1016/j.surg.2005.05.022.
https://doi.org/10.1016/j.surg.2005.05.0...
,1717 Csendes A, Orellana O, Figueroa M, Lanzarini E. Long-term (18 Years) results of patients with long-segment Barrett esophagus submitted to acid suppression-duodenal diversion operation: better than nissen fundoplication? Ann Surg. 2023;277(2):252-8. https://doi.org/10.1097/SLA.0000000000004760.
https://doi.org/10.1097/SLA.000000000000...
,3535 Lenglinger J, Riegler M. Radiofrequency ablation if Barrett's esophagus persists after fundoplication? Surg Endosc. 2010;24(9):2363-4. https://doi.org/10.1007/s00464-010-0938-9.
https://doi.org/10.1007/s00464-010-0938-...
. Despite these excellent results, we propose to add ablation in patients with LSBE C5M5 (Prague classification33 Anand O, Wani S, Sharma P. When and how to grade Barrett's columnar metaplasia: the Prague system. Best Pract Res Clin Gastroenterol. 2008;22(4):661-9. https://doi.org/10.1016/j.bpg.2008.02.001.
https://doi.org/10.1016/j.bpg.2008.02.00...
) or more to obtain early and permanent elimination of IM or LGD, considering the risk of progression at an incidence rate, for any dysplasia, of 1.4 cases/100 person-years and HGD/EAC of 0.9/100 person-years3131 Kelty CJ, Falk GL. Anti-reflux surgery does not remove cancer risk in Barrett's esophagus. Surg Endosc. 2011;25(12):3948; author reply 3949-50. https://doi.org/10.1007/s00464-011-1748-4.
https://doi.org/10.1007/s00464-011-1748-...
,3939 Ma M, Shroff S, Feldman M, DeMarshall M, Price C, Tierney A, et al. Risk of malignant progression in Barrett's esophagus indefinite for dysplasia. Dis Esophagus. 2017;30(3):1-5. https://doi.org/10.1093/dote/dow025.
https://doi.org/10.1093/dote/dow025...
. Therefore, in this way, we can prevent disease progression.
Up to date there are no reports with the combination of this procedure with endoscopic therapy.
The objective of this study was to determine the early and long-term results observed in LSBE patients (with or without LGD) who underwent AS-DD procedure combined with endoscopic therapy.
METHODS
Patients
This is a prospective study including patients with LSBE confirmed by endoscopic and histological study that demonstrated the presence of IM and/or LGD (inclusion criteria). In order to have a very clean universe of participants, exclusion criteria considered patients with short-segment BE (<3 cm), hiatal hernia >4 cm, previous esophago-gastric surgery, obesity with BMI>32, adenocarcinoma of the esophagus, and those HGD submitted to ESD. The admitted group consisted of 52 patients, 28 men with a mean age of 55.9 years (range 41–71) and 24 women with a mean age of 54.1 years (range 35–71). All of them had repeated endoscopic and histologic diagnoses of LSBE C5M5 or more for at least three years before their inclusion in this study. They underwent two endoscopic procedures in two different periods depending on the endoscopic therapy availability. A group of 21 patients received APC between March 2010 and December 2012, and another group of 31 patients underwent RFA from March 2012 to December 2019. Table 1 shows the demographic characteristics of the patients and BE extension of each group. They underwent endoscopic procedure between three and six months after AS-DD technique.
Demographic characteristics of patients submitted to argon plasma coagulation or radiofrequency ablation for the treatment of Barrett's esophagus.
The present study was performed in line with the Helsinki Declaration principles. Approval was granted by the Ethics Committee of our hospital and written consent was applied to patients before the indication of the surgical procedure. All patients gave their written informed consent to be included in this study.
Surgical technique
Nissen fundoplication plus selective vagotomy, distal gastrectomy with Roux-en-Y gastrojejunostomy with an alimentary limb of at least 80 cm was performed according to a previously described AS-DD plus fundoplication technique55 Andrew B, Alley JB, Aguilar CE, Fanelli RD. Barrett's esophagus before and after Roux-en-Y gastric bypass for severe obesity. Surg Endosc. 2018;32(2):930-36. https://doi.org/10.1007/s00464-017-5768-6.
https://doi.org/10.1007/s00464-017-5768-...
,1414 Csendes A, Bragheto I, Burdiles P, Smok G, Henriquez A, Parada F. Regression of intestinal metaplasia to cardiac or fundic mucosa in patients with Barrett's esophagus submitted to vagotomy, partial gastrectomy and duodenal diversion. A prospective study of 78 patients with more than 5 years of follow up. Surgery. 2006;139(1):46-53. https://doi.org/10.1016/j.surg.2005.05.022.
https://doi.org/10.1016/j.surg.2005.05.0...
,3535 Lenglinger J, Riegler M. Radiofrequency ablation if Barrett's esophagus persists after fundoplication? Surg Endosc. 2010;24(9):2363-4. https://doi.org/10.1007/s00464-010-0938-9.
https://doi.org/10.1007/s00464-010-0938-...
.
Postoperatively, upper endoscopy was performed to determine the onset and characteristics of the Barrett's epithelium according to the Prague classification33 Anand O, Wani S, Sharma P. When and how to grade Barrett's columnar metaplasia: the Prague system. Best Pract Res Clin Gastroenterol. 2008;22(4):661-9. https://doi.org/10.1016/j.bpg.2008.02.001.
https://doi.org/10.1016/j.bpg.2008.02.00...
. Measurements were performed to determine the circumferential and maximal lengths of the metaplastic epithelium, from the gastroesophageal junction towards the proximal.
Histologic analysis
According to the current guidelines77 Braghetto I, Csendes A, Figueroa M, Lasnibat JP, Vasquez J, Torres R, et al. Cirugía de supresión ácida y derivación duodenal laparoscópica vs abierta en esófago de Barrett extenso: resultados y complicaciones a corto y largo plazo. Rev Chil Cir. 2017;69(6):452-8. https://doi.org/10.1016/j.rchic.2017.05.007
https://doi.org/10.1016/j.rchic.2017.05....
,99 Braghetto I, Korn O, Valladares H, Debandi A, Díaz JC, Brunet L. Laparoscopic surgical treatment for patients with short- and long-segment Barrett's esophagus: which technique in which patient? Int Surg. 2011;96(2):95-103. https://doi.org/10.9738/cc29.1.
https://doi.org/10.9738/cc29.1...
,1414 Csendes A, Bragheto I, Burdiles P, Smok G, Henriquez A, Parada F. Regression of intestinal metaplasia to cardiac or fundic mucosa in patients with Barrett's esophagus submitted to vagotomy, partial gastrectomy and duodenal diversion. A prospective study of 78 patients with more than 5 years of follow up. Surgery. 2006;139(1):46-53. https://doi.org/10.1016/j.surg.2005.05.022.
https://doi.org/10.1016/j.surg.2005.05.0...
,1515 Csendes A, Braghetto I, Burdiles P, Korn O. Roux-en-Y long limb diversion as the first option for patients who have Barrett's esophagus. Chest Surg Clin N Am. 2002;12(1):157-84. https://doi.org/10.1016/s1052-3359(03)00072-3.
https://doi.org/10.1016/s1052-3359(03)00...
,1616 Csendes A, Burdiles P, Braghetto I, Korn O, Díaz JC, Rojas J. Early and late results of the acid suppression and duodenal diversion operation in patients with Barrett's esophagus: analysis of 210 cases. World J Surg. 2002;26(5):566-76. https://doi.org/10.1007/s00268-001-0269-z.
https://doi.org/10.1007/s00268-001-0269-...
, circumferential and staggered biopsies 4-quadrant with 1 cm each were removed from the proximal border of the Barrett´s epithelium until close to the gastric esophagogastric junction (EGJ)4747 Shaheen NJ, Falk GW, Iyer PG, Gerson LB; American College of Gastroenterology. ACG clinical guideline: diagnosis and management of Barrett's esophagus. Am J Gastroenterol. 2016;111(1):30-50; quiz 51. https://doi.org/10.1038/ajg.2015.322.
https://doi.org/10.1038/ajg.2015.322...
. The number of biopsies for each patient ranged from 18 to 56 depending on the follow-up period. Cardiac mucosa was described as the presence of mucus-secreting columnar cells (carditis). Specialized columnar epithelium was characterized by the presence of IM with well-defined goblet cells. LGD was defined as the presence of nuclear atypia involving the mucosal surface, nuclear stratification in the crypt base, and preserved architecture. HGD corresponded to the presence of marked nuclear atypia, distorted crypt architecture, and nuclear stratification extending to luminal surface.
Equipment and procedure
For the APC, it was used an electrosurgical unit with Argon module EMED™ ES 350-100-008 (EC manufacturer, Ryzowa, Poland) with a reusable flexible probe, GIT, 2.3 mm diameter, 2,2 m length. The argon beam was applied to produce the electrical coagulation and complete removal of metaplastic surface endoscopically visualized (Figure 1).
As for RFA, gastrointestinal ablation system Barrx™ RFA energy generator (Medtronic Corporation, BARRX Medical, Sunnyvale, California) was used. After determining the length and characteristics of the ablation area, a sizing balloon catheter was initially introduced to determine the diameter of the ablation catheter to be used. For the treatment of wide surfaces of Barrett's epithelium, the circumferential flex ablation (360º express) balloon catheter (3 cm length, 31 mm diameter) was initially introduced, administering a brief burst of <1s of thermal energy applied circularly to the esophageal wall. In the last patients, we used the self-sizing balloon catheter.
The BarrxTM system with TTS-1100 (15.7 mm length, 7.5 mm width) for focal ablation was used to treat smaller areas of metaplastic tissue. Different catheters were employed depending on the areas to be ablated (Figure 2).
Endoscopic visualization before and after radiofrequency ablation for long segment Barrett´s esophagus in patients submitted to fundoplication and Roux-en-Y distal gastrectomy.
Parameters evaluation
Complications: frequency of early post-procedure complications.
Endoscopic images: comparison of Barrett´s epithelium length before and after the procedure.
Histology: eradication, residual presence, reappearance, or progression of IM/LGD.
Definitions
Eradication: complete disappearance of goblet cells or LGD.
Residual island: presence of isolated islands of goblet cells or LGD after the procedure.
Reappearance: presence of anomalies is confirmed again after complete eradication of MI or LGD in the first or second control.
Progression: progression from IM to LGD or from LGD to HGD is confirmed
Follow-up: patients were monitored by endoscopic and histologic analysis initially at the 6th month after the procedure. Biopsies were taken from both the residual columnar and squamous epithelium areas. Later, patients were evaluated annually with endoscopic and histological examination according to the same protocol. In APC group, the mean follow-up was 9.2 standard deviation ±1.9 years (range from 8 to 12 years) and in RFA group the mean follow-up was 7.6±2.1 years (range from 5 to 11 years). Depending on the endoscopic and histologic findings, patients were submitted to retreatment, mainly with APC, due to the presence of residual metaplastic islands or residual IM in Barrett's tongues. (Figure 3)
RESULTS
The circumferential and maximal extensions of EGJ in the APC group were 30.47±8.05 mm and 54.76±9.81 mm, respectively. In patients undergoing RFA, the length of circumferential limit was 47.30±9.6 (p=0.07), and 71.33±18.1 mm for the maximal length (p=0.27) (Table 1).
After the initial endoscopic treatment, only one session of treatment with RFA was necessary to eliminate columnar epithelium in 26 of the 31 subjects (p=0.002), while seven patients (33.3%) needed two or three retreatment sessions after APC. In the RFA group, five patients had complementary retreatment: four were submitted to APC and one to ESD due to LGD (Table 2; Figure 3).
Number of sessions required for complete initial eradication of endoscopic image of Barrett´s esophagus after argon plasma coagulation compared to radiofrequency ablation treatment.
The complications observed after both procedures are shown in Table 3. Strictures were successfully treated with dilatation with Savary's bougie. Table 4 shows the circumferential and maximal lengths of the metaplastic mucosa before and after each procedure. The decrease in circumferential length was 10.95mm in the group subjected to APC (p=0.09, p>0.05) and 21.15 mm in the group subjected to RFA. (p=0.0001, p<0.05). Regarding the decrease in maximal height after APC, it was 30.96 mm (p=0.0001, p<0.05) and 44.41 mm post RFA. (p=0.0001, p<0.05) (Figure 4). Table 5 shows the results of the histological study after endoscopic therapy. During the follow-up in the APC group, regression to carditis was observed in 14 patients, while 6 out of 20 patients presented residual island of IM or buried metaplastic cells that were subsequently subjected to retreatment with new sessions of APC.
Complications observed after endoscopic argon plasma coagulation and radiofrequency ablation procedure in patients with Barrett´s esophagus.
Extension of columnar epithelium area after the endoscopic treatment according Prague Classification33 Anand O, Wani S, Sharma P. When and how to grade Barrett's columnar metaplasia: the Prague system. Best Pract Res Clin Gastroenterol. 2008;22(4):661-9. https://doi.org/10.1016/j.bpg.2008.02.001.
https://doi.org/10.1016/j.bpg.2008.02.00... before and after argon plasma coagulation and radiofrequency ablation (final results).
Circumferential and maximal length of Barrett´s epithelium before and after argon plasma coagulation and radiofrequency ablation in patients with Barrett´s esophagus submitted to fundoplication and Roux-en-Y distal gastrectomy.
Histologic results after treatment with argon plasma coagulation or radiofrequency ablation in patients with intestinal metaplasia alone or with dysplasia: results observed during follow-up.
Complete eradication in one patient with IM and LGD was observed, but another patient also submitted to APC, presented reappearance of IM during follow-up. In the RFA group, regression to carditis with mucin-secreting cells was confirmed in 17 of 25 patients, but three patients showed residual IM (p=0.02, p<0.05), treated with complementary APC. In four out of six patients with IM with LGD, the complete eradication was achieved. In another patient, the appearance of LGD was observed at one-year follow-up and was submitted to ESD, while another patient presented reappearance of IM alone, being submitted to a new session of APC. The observed results demonstrated the efficacy of RFA in the treatment of these histological lesions.
Late complications from laparoscopic AS-DD operation before the endoscopic procedure were minimal. One patient with severe dysphagia, who required endoscopic dilation due to fundoplication stenosis, had no satisfactory outcome, so it was converted to Toupet partial fundoplication surgery, with no mortality. Another patient developed a hiatal hernia with “candy-cane syndrome” eight years later, and was submitted to revision surgery.
DISCUSSION
BE is usually the result of severe chronic reflux disease. Reducing or eliminating esophageal epithelium's exposure to acid and bile is essential to achieve long-term regression of BE1313 Copetti H, Copetti L, Copetti L, Felin GD, Felin GD, Felin CD, et al. Risk of preneoplastic lesions in mucosal projections of different sizes of the columnar epithelium in the lower esophagus. Arq Bras Cir Dig. 2022;35:e1674. https://doi.org/10.1590/0102-672020220002e1674.
https://doi.org/10.1590/0102-67202022000...
. However, it is questionable whether the use of proton pump inhibitors or antireflux operations are more effective to accomplish this goal1010 Bright T, Watson DI, Tam W, Game PA, Astill D, Ackroyd R, et al. Randomized trial of argon plasma coagulation versus endoscopic surveillance for barrett esophagus after antireflux surgery: late results. Ann Surg. 2007;246(6):1016-20. https://doi.org/10.1097/SLA.0b013e318133fa85.
https://doi.org/10.1097/SLA.0b013e318133...
,3131 Kelty CJ, Falk GL. Anti-reflux surgery does not remove cancer risk in Barrett's esophagus. Surg Endosc. 2011;25(12):3948; author reply 3949-50. https://doi.org/10.1007/s00464-011-1748-4.
https://doi.org/10.1007/s00464-011-1748-...
.
Medical treatment of GERD proves ineffective at controlling LSBE1919 Desai TK, Krishnan K, Samala N, Singh J, Cluley J, Perla S, et al. The incidence of oesophageal adenocarcinoma in non-dysplastic Barrett's oesophagus: a meta-analysis. Gut. 2012;61(7):970-6. https://doi.org/10.1136/gutjnl-2011-300730.
https://doi.org/10.1136/gutjnl-2011-3007...
,3434 Krajciova J, Vackova Z, Spicak J, Martinek J. Radiofrequency ablation for Barrett's esophagus-related neoplasia. Minerva Chir. 2018;73(4):366-77. https://doi.org/10.23736/S0026-4733.18.07783-0.
https://doi.org/10.23736/S0026-4733.18.0...
. Fundoplication can reduce both acid and bile reflux to normal levels, but patients with LSBE present more severe anatomical and pathophysiological alterations3333 Korn O, Csendes A, Burdiles P, Lanzarini E, Henríquez A. Anatomic damage of the lower esophageal sphincter after subtotal gastrectomy. Arq Bras Cir Dig. 2022;34(4):e1633. https://doi.org/10.1590/0102-672020210002e1633.
https://doi.org/10.1590/0102-67202021000...
.
Surgery in these cases cannot achieve an effective anti-reflux barrier. Post-surgical failure is observed three times more frequently than in non-Barrett's patients. (5–12% vs 12–39%)2424 Gutschow CA, Schröder W, Bludau M, Vallböhmer D, Prenzel KL, Bollschweiler E, et al. Value of distal gastrectomy as a remedial operation for failed fundoplication. Zentralbl Chir. 2011;136(3):249-55. https://doi.org/10.1055/s-0030-1247386.
https://doi.org/10.1055/s-0030-1247386...
,2525 Gutschow CA, Schröder W, Prenzel K, Bollschweiler E, Romagnoli R, Collard JM, et al. Impact of antireflux surgery on Barrett's esophagus. Langenbecks Arch Surg. 2002;387(3-4):138-45. https://doi.org/10.1007/s00423-002-0303-0.
https://doi.org/10.1007/s00423-002-0303-...
,5050 Williams VA, Watson TJ, Gellersen O, Feuerlein S, Molena D, Sillin LF, et al. Gastrectomy as a remedial operation for failed fundoplication. J Gastrointest Surg. 2007;11(1):29-35. https://doi.org/10.1007/s11605-006-0048-0.
https://doi.org/10.1007/s11605-006-0048-...
,5151 Wilshire CL, Louie BE, Shultz D, Jutric Z, Farivar AS, Aye RW. Clinical outcomes of reoperation for failed antireflux operations. Ann Thorac Surg. 2016;101(4):1290-6. https://doi.org/10.1016/j.athoracsur.2015.10.027.
https://doi.org/10.1016/j.athoracsur.201...
. Therefore, the possibility of achieving regression of Barrett's metaplasia after fundoplication alone is rare and Barrett's progression to LGD and HGD as well as EAC following surgery is observed repeatedly44 Anaparthy R, Sharma P. Progression of Barrett oesophagus: role of endoscopic and histological predictors. Nat Rev Gastroenterol Hepatol. 2014;11(9):525-34. https://doi.org/10.1038/nrgastro.2014.69.
https://doi.org/10.1038/nrgastro.2014.69...
,2121 Formentini A, Schwarz A, Straeter J, Stanescu A, Henne-Bruns D. Treatment of Barrett's esophagus with argon plasma coagulation and antireflux surgery. A retrospective analysis. Hepatogastroenterology. 2007;54(79):1991-6. PMID: 18251146..
Due to the persistence of IM, efforts are focused on eliminating metaplastic mucosa and preventing disease progression, by combining endoscopic therapy with either medical or surgical treatment of GERD2727 Han S, Low DE. Laparoscopic antireflux surgery: are old questions answered? Should it be used conjoined with endoscopic therapy for Barrett's esophagus? Arq Bras Cir Dig. 2022;35:e1664. https://doi.org/10.1590/0102-672020210002e1664.
https://doi.org/10.1590/0102-67202021000...
. To achieve this objective, an effective treatment is required to eliminate acid and bile reflux. Some authors state repeated ablation sessions to obtain eradication, but these results are observed in non-operated patients, maintained only with medical treatment. Hence, some authors suggest performing antireflux surgery combined with eradication therapy in these patients2121 Formentini A, Schwarz A, Straeter J, Stanescu A, Henne-Bruns D. Treatment of Barrett's esophagus with argon plasma coagulation and antireflux surgery. A retrospective analysis. Hepatogastroenterology. 2007;54(79):1991-6. PMID: 18251146.,2222 Franchimont D, Van Laethem JL, Devière J. Argon plasma coagulation in Barrett's esophagus. Gastrointest Endosc Clin N Am. 2003;13(3):457-66. https://doi.org/10.1016/s1052-5157(03)00040-0.
https://doi.org/10.1016/s1052-5157(03)00...
.
The combination of fundoplication plus an endoscopic APC or RFA procedure is published as a promising treatment for patients with BE and LGD at a follow-up of 6–8 years2020 Santos RS, Bizekis C, Ebright M, DeSimone M, Daly BD, Fernando HC. Radiofrequency ablation for Barrett's esophagus and low-grade dysplasia in combination with an antireflux procedure: a new paradigm. J Thorac Cardiovasc Surg. 2010;139(3):713-6. https://doi.org/10.1016/j.jtcvs.2009.10.032.
https://doi.org/10.1016/j.jtcvs.2009.10....
,4040 O’Connell K, Velanovich V. Effects of Nissen fundoplication on endoscopic endoluminal radiofrequency ablation of Barrett's esophagus. Surg Endosc. 2011;25(3):830-4. https://doi.org/10.1007/s00464-010-1270-0.
https://doi.org/10.1007/s00464-010-1270-...
. Some data suggest that individuals with prior fundoplication are more likely to have a durable response to eradication, although such an assertion remains inconclusive4040 O’Connell K, Velanovich V. Effects of Nissen fundoplication on endoscopic endoluminal radiofrequency ablation of Barrett's esophagus. Surg Endosc. 2011;25(3):830-4. https://doi.org/10.1007/s00464-010-1270-0.
https://doi.org/10.1007/s00464-010-1270-...
.
RFA, performed either before or after surgery, is safe and effective for reducing or eliminating IM and dysplasia. The timing of the two procedures is debatable. For example, although fundoplication before ablation can straighten the esophagus and heal esophagitis, fundoplication itself can interfere with effective RFA by obscuring the EGJ landmarks or making access to the distal segments of the IM more difficult.
Performing surgery after ablation can also be more difficult due to transmural inflammatory changes, or complete ablation can never be possible because of an anatomical distortion of the esophagus (angulation, dilatation, and shortening)66 Braghetto I, Csendes A, Burdiles P, Korn O. Antireflux surgery, highly selective vagotomy and duodenal switch procedure: post-operative evaluation in patients with complicated and non-complicated Barrett's esophagus. Dis Esophagus. 2000;13(1):12-7. https://doi.org/10.1046/j.1442-2050.2000.00066.x.
https://doi.org/10.1046/j.1442-2050.2000...
. However, we performed the procedure with minimal difficulty. The results with RFA six months after surgery seem to be better than those observed with APC, with fewer complications and increased efficacy in eradicating IM and dysplasia, regardless of the number of sessions required. Eradication of the metaplastic epithelium is achieved in 59–62% of cases, with a percentage of buried cells between 19–52% after APC. The success in eradicating IM after RFA is 78–95%2020 Santos RS, Bizekis C, Ebright M, DeSimone M, Daly BD, Fernando HC. Radiofrequency ablation for Barrett's esophagus and low-grade dysplasia in combination with an antireflux procedure: a new paradigm. J Thorac Cardiovasc Surg. 2010;139(3):713-6. https://doi.org/10.1016/j.jtcvs.2009.10.032.
https://doi.org/10.1016/j.jtcvs.2009.10....
,4242 Pagani M, Granelli P, Chella B, Antoniazzi L, Bonavina L, Peracchia A. Barrett's esophagus: combined treatment using argon plasma coagulation and laparoscopic antireflux surgery. Dis Esophagus. 2003;16(4):279-83. https://doi.org/10.1111/j.1442-2050.2003.00347.x.
https://doi.org/10.1111/j.1442-2050.2003...
. The most recent reports published these data up to 8–10 years of follow-up.
Our results on the modification of circumferential and maximal length of the metaplastic epithelium corroborate other studies which reporte a decrease in the BE length in −2.7 cm (range from −6 to −4 cm). Others observe a decrease in mean BE length from 6.2 to 1.2 cm after treatment (p=0.001). The higher number of RFA treatment (p<0.05) is associated with higher endoscopic and histologic success (p<0.05). All patients receiving three or more treatments have complete resolution of Barrett's metaplasia2121 Formentini A, Schwarz A, Straeter J, Stanescu A, Henne-Bruns D. Treatment of Barrett's esophagus with argon plasma coagulation and antireflux surgery. A retrospective analysis. Hepatogastroenterology. 2007;54(79):1991-6. PMID: 18251146.,3737 Lord RVN. Antireflux surgery for Barrett's oesophagus. ANZ J Surg. 2003;73(4):234-6. https://doi.org/10.1046/j.1445-1433.2003.02569.x.
https://doi.org/10.1046/j.1445-1433.2003...
,4646 Rees JR, Lao-Sirieix P, Wong A, Fitzgerald RC. Treatment for Barrett's oesophagus. Cochrane Database Syst Rev. 2010;2010(1):CD004060. https://doi.org/10.1002/14651858.CD004060.pub2.
https://doi.org/10.1002/14651858.CD00406...
.
A review of 18 studies, including 3,802 patients reported the efficacy of the treatment and six studies including 540 patients reported the durability. Complete eradication of MI was achieved in 78–92% (95%CI 70–86) of cases, complete eradication of dysplasia was achieved in 92% (95%CI 87–95), and progression to cancer was observed in 0.2–1.5% during treatment and 0.7% after eradication (95%CI 3–7)11 Ackroyd R, Tam W, Schoeman M, Devitt PG, Watson DI. Prospective randomized controlled trial of argon plasma coagulation ablation vs. endoscopic surveillance of patients with Barrett's esophagus after antireflux surgery. Gastrointest Endosc. 2004;59(1):1-7. https://doi.org/10.1016/s0016-5107(03)02528-8.
https://doi.org/10.1016/s0016-5107(03)02...
,22 Amadi C, Gatenby P. Barrett's oesophagus: current controversies. World J Gastroenterol. 2017;23(28):5051-67. https://doi.org/10.3748/wjg.v23.i28.5051.
https://doi.org/10.3748/wjg.v23.i28.5051...
.
Based on a recent meta-analysis, there is a significant reduction in the risk of progression to HGD or EAC among patients with BE-LGD treated with RFA compared to those undergoing endoscopic surveillance. Endoscopic eradication with RFA should be the preferred approach for BE-LGD44 Anaparthy R, Sharma P. Progression of Barrett oesophagus: role of endoscopic and histological predictors. Nat Rev Gastroenterol Hepatol. 2014;11(9):525-34. https://doi.org/10.1038/nrgastro.2014.69.
https://doi.org/10.1038/nrgastro.2014.69...
,3232 Klair JS, Zafar Y, Nagra N, Murali AR, Jayaraj M, Singh D, et al. Outcomes of radiofrequency ablation versus endoscopic surveillance for Barrett's esophagus with low-grade dysplasia: a systematic review and meta-analysis. Dig Dis. 2021;39(6):561-8. https://doi.org/10.1159/000514786.
https://doi.org/10.1159/000514786...
,3636 Lim YC, Fitzgerald RC. Diagnosis and treatment of Barrett's oesophagus. Br Med Bull. 2013;107:117-32. https://doi.org/10.1093/bmb/ldt025.
https://doi.org/10.1093/bmb/ldt025...
. However, the recurrence after initial complete eradication ranges from 21.5 to 33% of patients, but it does not assure that the acid and bile reflux is eliminated over time with medical treatment or fundoplication alone, which is obtained when AS-DD is performed. This could be considered the main advantage of our idea.
Adverse events are observed in about 20% (mainly pain) of cases and complications in less than 10%, the most frequent being esophageal stenosis in around 5–12%. Esophageal perforation is rare. Post-procedure mortality is not reported2323 Goers TA, Leão P, Cassera MA, Dunst CM, Swanström LL. Concomitant endoscopic radiofrequency ablation and laparoscopic reflux operative results in more effective and efficient treatment of Barrett esophagus. J Am Coll Surg. 2011;213(4):486-92. https://doi.org/10.1016/j.jamcollsurg.2011.06.419.
https://doi.org/10.1016/j.jamcollsurg.20...
. The results observed in the present study comparing APC and RFA are in accordance with other publications22 Amadi C, Gatenby P. Barrett's oesophagus: current controversies. World J Gastroenterol. 2017;23(28):5051-67. https://doi.org/10.3748/wjg.v23.i28.5051.
https://doi.org/10.3748/wjg.v23.i28.5051...
,3030 Kauttu T, Räsänen J, Krogerus L, Sihvo E, Puolakkainen P, Salo JA. Long-term results of ablation with antireflux surgery for Barrett's esophagus: a clinical and molecular biologic study. Surg Endosc. 2012;26(7):1892-7. https://doi.org/10.1007/s00464-011-2121-3.
https://doi.org/10.1007/s00464-011-2121-...
,3434 Krajciova J, Vackova Z, Spicak J, Martinek J. Radiofrequency ablation for Barrett's esophagus-related neoplasia. Minerva Chir. 2018;73(4):366-77. https://doi.org/10.23736/S0026-4733.18.07783-0.
https://doi.org/10.23736/S0026-4733.18.0...
,4343 Parikh K, Khaitan L. Radiofrequency ablation coupled with Roux-en-Y gastric bypass: a treatment option for morbidly obese patients with Barrett's esophagus. J Surg Case Rep. 2016;2016(3):rjw007. https://doi.org/10.1093/jscr/rjw007.
https://doi.org/10.1093/jscr/rjw007...
.
The role of surgery is to provide an absolute barrier to acid and bile contents. But, in patients with LSBE, fundoplication alone can fail to control acid and bile reflux11 Ackroyd R, Tam W, Schoeman M, Devitt PG, Watson DI. Prospective randomized controlled trial of argon plasma coagulation ablation vs. endoscopic surveillance of patients with Barrett's esophagus after antireflux surgery. Gastrointest Endosc. 2004;59(1):1-7. https://doi.org/10.1016/s0016-5107(03)02528-8.
https://doi.org/10.1016/s0016-5107(03)02...
,88 Braghetto I, Korn O, Figueroa-Giralt M, Valenzuela C, Burgos AM, Mandiola C, et al. Laparoscopic redo fundoplication alone, redo nissen fundoplication, or toupet fundoplication combined with roux-en-y distal gastrectomy for treatment of failed nissen fundoplication. Arq Bras Cir Dig. 2022;35:e1678. https://doi.org/10.1590/0102-672020220002e1678.
https://doi.org/10.1590/0102-67202022000...
,4848 Signorini F, Viscido G, Bocco MCA, Obeide L, Moser F. Impact of gastric bypass on erosive esophagitis and Barret's esophagus. Obes Surg. 2020;30(4):1194-9. https://doi.org/10.1007/s11695-019-04333-1.
https://doi.org/10.1007/s11695-019-04333...
. Therefore, we must perform AS-DD to avoid both types of refluxes (acid and bile), to obtain optimal results in terms of eradication and no progression of histological alterations in the long term. This technique has been performed by our group in LSBE patients for many years. In recent decades, it is recognized as a good alternative, especially in obese patients, reporting IM regression in more than 90% and dysplasia regression in 60% of cases, without progression to dysplasia or adenocarcinoma. The proposed technique for eradicating IM with or without LGD could offer even greater success88 Braghetto I, Korn O, Figueroa-Giralt M, Valenzuela C, Burgos AM, Mandiola C, et al. Laparoscopic redo fundoplication alone, redo nissen fundoplication, or toupet fundoplication combined with roux-en-y distal gastrectomy for treatment of failed nissen fundoplication. Arq Bras Cir Dig. 2022;35:e1678. https://doi.org/10.1590/0102-672020220002e1678.
https://doi.org/10.1590/0102-67202022000...
,1212 Cobey F, Oelschlager B. Complete regression of Barrett's esophagus after Roux-en-Y gastric bypass. Obes Surg. 2005;15(5):710-2. https://doi.org/10.1381/0960892053923932.
https://doi.org/10.1381/0960892053923932...
,1515 Csendes A, Braghetto I, Burdiles P, Korn O. Roux-en-Y long limb diversion as the first option for patients who have Barrett's esophagus. Chest Surg Clin N Am. 2002;12(1):157-84. https://doi.org/10.1016/s1052-3359(03)00072-3.
https://doi.org/10.1016/s1052-3359(03)00...
,3838 Luckett T, Allamneni C, Cowley K, Eick J, Gullick A, Peter S. Length of Barrett's segment predicts failure of eradication in radiofrequency ablation for Barrett's esophagus: a retrospective cohort study. BMC Gastroenterol. 2018;18(1):67. https://doi.org/10.1186/s12876-018-0799-6.
https://doi.org/10.1186/s12876-018-0799-...
. However, there is only one case previously reported4343 Parikh K, Khaitan L. Radiofrequency ablation coupled with Roux-en-Y gastric bypass: a treatment option for morbidly obese patients with Barrett's esophagus. J Surg Case Rep. 2016;2016(3):rjw007. https://doi.org/10.1093/jscr/rjw007.
https://doi.org/10.1093/jscr/rjw007...
, and so, that is the reason this option requires validation with further studies.
The limitations of this study are:
-
It is not a randomized study;
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There is a low number of patients;
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No manometric and 24-hr pH meter evaluations were performed; and
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The follow-up is medium-term.
The strength of this study is that it provides results in a prospective cohort of patients with serial endoscopic and histologic evaluations.
CONCLUSIONS
The elimination of metaplastic or dysplastic epithelium and the permanent reduction of acid and bile reflux are crucial to preventing BE progression. RFA combined with the AS-DD technique is feasible and can effectively treat BE lesions, avoiding progression to EAC, and probably could be the most suitable option without substantial morbidity and operative mortality.
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Central MessageChronic gastroesophageal reflux disease is associated with the metaplastic transformation of normal squamous epithelium to premalignant specialized intestinal metaplasia, frequently within the long segment of Barrett´s esophagus, which may progress to low- or high-grade dysplasia, or even esophageal adenocarcinoma. Endoscopic techniques for the eradication of intestinal metaplasia and dysplasia are proposed, including endoscopic submucosal dissection, endoscopic radiofrequency ablation, argon plasma coagulation, photodynamic therapy, and cryotherapy. The combination of fundoplication with endoscopic therapy is postulated as a valid option, showing good initial and long-term results.
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PerspectivesThe elimination of metaplastic or dysplastic epithelium and the permanent reduction of both acid and bile reflux are crucial to prevent the progression of Barrett's esophagus. Radiofrequency ablation combined with acid suppression-duodenal diversion technique is feasible and can effectively treat Barrett's esophagus lesions, avoiding progression to esophageal dysplasia or adenocarcinoma and probably could be the best option without great morbidity and operative mortality.
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Financial source: None
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Editorial Support: National Council for Scientific and Technological Development (CNPq).
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20Santos RS, Bizekis C, Ebright M, DeSimone M, Daly BD, Fernando HC. Radiofrequency ablation for Barrett's esophagus and low-grade dysplasia in combination with an antireflux procedure: a new paradigm. J Thorac Cardiovasc Surg. 2010;139(3):713-6. https://doi.org/10.1016/j.jtcvs.2009.10.032
» https://doi.org/10.1016/j.jtcvs.2009.10.032 -
21Formentini A, Schwarz A, Straeter J, Stanescu A, Henne-Bruns D. Treatment of Barrett's esophagus with argon plasma coagulation and antireflux surgery. A retrospective analysis. Hepatogastroenterology. 2007;54(79):1991-6. PMID: 18251146.
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22Franchimont D, Van Laethem JL, Devière J. Argon plasma coagulation in Barrett's esophagus. Gastrointest Endosc Clin N Am. 2003;13(3):457-66. https://doi.org/10.1016/s1052-5157(03)00040-0
» https://doi.org/10.1016/s1052-5157(03)00040-0 -
23Goers TA, Leão P, Cassera MA, Dunst CM, Swanström LL. Concomitant endoscopic radiofrequency ablation and laparoscopic reflux operative results in more effective and efficient treatment of Barrett esophagus. J Am Coll Surg. 2011;213(4):486-92. https://doi.org/10.1016/j.jamcollsurg.2011.06.419
» https://doi.org/10.1016/j.jamcollsurg.2011.06.419 -
24Gutschow CA, Schröder W, Bludau M, Vallböhmer D, Prenzel KL, Bollschweiler E, et al. Value of distal gastrectomy as a remedial operation for failed fundoplication. Zentralbl Chir. 2011;136(3):249-55. https://doi.org/10.1055/s-0030-1247386
» https://doi.org/10.1055/s-0030-1247386 -
25Gutschow CA, Schröder W, Prenzel K, Bollschweiler E, Romagnoli R, Collard JM, et al. Impact of antireflux surgery on Barrett's esophagus. Langenbecks Arch Surg. 2002;387(3-4):138-45. https://doi.org/10.1007/s00423-002-0303-0
» https://doi.org/10.1007/s00423-002-0303-0 -
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Publication Dates
-
Publication in this collection
18 Sept 2023 -
Date of issue
2023
History
-
Received
10 June 2023 -
Accepted
13 July 2023