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LAPAROSCOPIC ANTIREFLUX SURGERY: ARE OLD QUESTIONS ANSWERED? SHOULD IT BE USED CONJOINED WITH ENDOSCOPIC THERAPY FOR BARRETT’S ESOPHAGUS?

CIRURGIA LAPAROSCÓPICA ANTI-REFLUXO: AS ANTIGAS PERGUNTAS SÃO RESPONDIDAS? DEVE SER USADO JUNTO À TERAPIA ENDOSCÓPICA PARA O ESÔFAGO DE BARRETT?

HEADINGS:
Gastroesophageal Reflux; Fundoplication; Laparoscopy; Barrett’s Esophagus

DESCRITORES:
Refluxo Gastroesofágico; Fundoplicatura; Laparoscopia; Esôfago de Barrett

Relationship of Barrett’s esophagus, gastroesophageal reflux disease, and esophageal adenocarcinoma

Barrett’s esophagus (BE) represents the morphological premalignant manifestation of gastroesophageal reflux disease (GERD), which develops as a consequence of the dysfunction and failure of the antireflux mechanism3838. Que J, Garman KS, Souza RF, Spechler SJ. Pathogenesis and Cells of Origin of Barrett’s Esophagus. Gastroenterology. 2019;157(2):349-364.e1. doi: 10.1053/j.gastro.2019.03.072.
https://doi.org/10.1053/j.gastro.2019.03...
. BE involves the formation of intestinal metaplasia (IM) from the squamous epithelium of the esophagus, which is a reparative response to reflux-induced damage3737. Peters Y, Al-Kaabi A, Shaheen NJ, Chak A, Blum A, Souza RF, Di Pietro M, Iyer PG, Pech O, Fitzgerald RC, Siersema PD. Barrett oesophagus. Nat Rev Dis Primers. 2019;5(1):35. doi: 10.1038/s41572-019-0086-z.
https://doi.org/10.1038/s41572-019-0086-...
. Although the prevalence in Western countries is about 1-2% in the general population and about 10% in population who report acid reflux symptoms, the accurate prevalence of BE in the general population is difficult to determine as the majority of individuals with BE are not diagnosed4040. Rex DK, Cummings OW, Shaw M, Cumings MD, Wong RK, Vasudeva RS, Dunne D, Rahmani EY, Helper DJ. Screening for Barrett’s esophagus in colonoscopy patients with and without heartburn. Gastroenterology. 2003;125(6):1670-7. doi: 10.1053/j.gastro.2003.09.030.
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,4242. Ronkainen J, Aro P, Storskrubb T, Johansson SE, Lind T, Bolling-Sternevald E, Vieth M, Stolte M, Talley NJ, Agréus L. Prevalence of Barrett’s esophagus in the general population: an endoscopic study. Gastroenterology. 2005;129(6):1825-31. doi: 10.1053/j.gastro.2005.08.053.
https://doi.org/10.1053/j.gastro.2005.08...
. Epidemiological and histopathological evidence indicate that many cases of esophageal adenocarcinoma (EAC) arise in individuals with BE by the progression of IM (nondysplastic Barrett’s esophagus [NDBE]) and indefinite for dysplasia (IND) to dysplasia (including low-grade dysplasia [LGD] and high-grade dysplasia [HGD]) and finally to neoplasia4646. Schlemper RJ, Riddell RH, Kato Y, Borchard F, Cooper HS, Dawsey SM, Dixon MF, Fenoglio-Preiser CM, Fléjou JF, Geboes K, et al. The Vienna classification of gastrointestinal epithelial neoplasia. Gut. 2000;47(2):251-5. doi: 10.1136/gut.47.2.251.
https://doi.org/10.1136/gut.47.2.251...
. To date, dysplasia remains the best available marker of cancer risk in patients with BE.

Since BE is considered a complication of chronic GERD, it is perhaps not surprising that risk factors for gastric reflux are also strongly associated with BE3030. Lagergren J, Ye W, Lagergren P, Lu Y. The risk of esophageal adenocarcinoma after antireflux surgery. Gastroenterology. 2010;138(4):1297-301. doi: 10.1053/j.gastro.2010.01.004.
https://doi.org/10.1053/j.gastro.2010.01...
,5454. Taylor JB, Rubenstein JH. Meta-analyses of the effect of symptoms of gastroesophageal reflux on the risk of Barrett’s esophagus. Am J Gastroenterol. 2010;105(8):1729, 1730-7; quiz 1738. doi: 10.1038/ajg.2010.194.
https://doi.org/10.1038/ajg.2010.194...
. Reflux-induced injury has been linked to cellular and molecular changes in the esophagus1212. Dunbar KB, Agoston AT, Odze RD, Huo X, Pham TH, Cipher DJ, Castell DO, Genta RM, Souza RF, Spechler SJ. Association of Acute Gastroesophageal Reflux Disease With Esophageal Histologic Changes. JAMA. 2016;315(19):2104-12. doi: 10.1001/jama.2016.5657.
https://doi.org/10.1001/jama.2016.5657...
,3939. Reid BJ, Li X, Galipeau PC, Vaughan TL. Barrett’s oesophagus and oesophageal adenocarcinoma: time for a new synthesis. Nat Rev Cancer. 2010;10(2):87-101. doi: 10.1038/nrc2773.
https://doi.org/10.1038/nrc2773...
. Symptoms of heartburn and regurgitation are strongly associated with the presence of BE, and duration of GERD symptoms may also be a risk factor for BE77. Bennett C, Vakil N, Bergman J, Harrison R, Odze R, Vieth M, Sanders S, Gay L, Pech O, Longcroft-Wheaton G, et al. Consensus statements for management of Barrett’s dysplasia and early-stage esophageal adenocarcinoma, based on a Delphi process. Gastroenterology. 2012;143(2):336-46. doi: 10.1053/j.gastro.2012.04.032.
https://doi.org/10.1053/j.gastro.2012.04...
. Although GERD is a strong risk factor for both BE and EAC, 40-50% of patients with these disorders do not report chronic reflux symptoms, suggesting that silent reflux or other risk factors such as male sex5757. van Blankenstein M, Looman CW, Johnston BJ, Caygill CP. Age and sex distribution of the prevalence of Barrett’s esophagus found in a primary referral endoscopy center. Am J Gastroenterol. 2005;100(3):568-76. doi: 10.1111/j.1572-0241.2005.40187.x.
https://doi.org/10.1111/j.1572-0241.2005...
, age 50 or older4343. Rubenstein JH, Mattek N, Eisen G. Age- and sex-specific yield of Barrett’s esophagus by endoscopy indication. Gastrointest Endosc. 2010;71(1):21-7. doi: 10.1016/j.gie.2009.06.035.
https://doi.org/10.1016/j.gie.2009.06.03...
, white race5858. Wang A, Mattek NC, Holub JL, Lieberman DA, Eisen GM. Prevalence of complicated gastroesophageal reflux disease and Barrett’s esophagus among racial groups in a multi-center consortium. Dig Dis Sci. 2009;54(5):964-71. doi: 10.1007/s10620-009-0742-3.
https://doi.org/10.1007/s10620-009-0742-...
, central obesity2828. Kubo A, Cook MB, Shaheen NJ, Vaughan TL, Whiteman DC, Murray L, Corley DA. Sex-specific associations between body mass index, waist circumference and the risk of Barrett’s oesophagus: a pooled analysis from the international BEACON consortium. Gut. 2013;62(12):1684-91. doi: 10.1136/gutjnl-2012-303753.
https://doi.org/10.1136/gutjnl-2012-3037...
, and cigarette smoking99. Cook MB, Shaheen NJ, Anderson LA, Giffen C, Chow WH, Vaughan TL, Whiteman DC, Corley DA. Cigarette smoking increases risk of Barrett’s esophagus: an analysis of the Barrett’s and Esophageal Adenocarcinoma Consortium. Gastroenterology. 2012;142(4):744-53. doi: 10.1053/j.gastro.2011.12.049.
https://doi.org/10.1053/j.gastro.2011.12...
also likely play a role in the pathogenesis of BE and EAC.

Although BE is well-established precursor for EAC, the assumption that all patients who develop EAC go through the same reflux-induced response leading to adenocarcinoma was challenged by a retrospective analysis that found that only 46% of patients with EAC presented with endoscopic confirmation of BE and histopathological evidence of IM4545. Sawas T, Killcoyne S, Iyer PG, Wang KK, Smyrk TC, Kisiel JB, Qin Y, Ahlquist DA, Rustgi AK, Costa RJ, et al. Identification of Prognostic Phenotypes of Esophageal Adenocarcinoma in 2 Independent Cohorts. Gastroenterology. 2018;155(6):1720-1728.e4. doi: 10.1053/j.gastro.2018.08.036.
https://doi.org/10.1053/j.gastro.2018.08...
. Furthermore, comparison of patients with EAC who had confirmed BE at presentation to those without BE suggested the existence of two EAC phenotypes with different tumor behavior and response to therapy4545. Sawas T, Killcoyne S, Iyer PG, Wang KK, Smyrk TC, Kisiel JB, Qin Y, Ahlquist DA, Rustgi AK, Costa RJ, et al. Identification of Prognostic Phenotypes of Esophageal Adenocarcinoma in 2 Independent Cohorts. Gastroenterology. 2018;155(6):1720-1728.e4. doi: 10.1053/j.gastro.2018.08.036.
https://doi.org/10.1053/j.gastro.2018.08...
. These findings raise the question of whether EAC always develops through the IM-dysplasia-EAC sequence.

Current management of Barrett’s esophagus

Accepting that a controversy exists, the natural course of progression to dysplasia and cancer in BE in the majority of patients is thought to be stepwise from NDBE to LGD to HGD and cancer. The annual cancer risk depends on the degree of dysplasia, such as 0.33% if there is no dysplasia, 0.54% with LGD, and 7% with HGD4747. 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. doi: 10.1038/ajg.2015.322.
https://doi.org/10.1038/ajg.2015.322...
. Thus, the management is based on disease stages.

1. Nondysplastic Barrett’s esophagus

Proton-pump inhibitor (PPI) therapy is recommended to control reflux symptoms in patients with NDBE. The American College of Gastroenterology (ACG)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. doi: 10.1038/ajg.2015.322.
https://doi.org/10.1038/ajg.2015.322...
, American Gastroenterological Association (AGA)5252. Spechler SJ, Sharma P, Souza RF, Inadomi JM, Shaheen NJ; American Gastroenterological Association. American Gastroenterological Association technical review on the management of Barrett’s esophagus. Gastroenterology. 2011;140(3):e18-52; quiz e13. doi: 10.1053/j.gastro.2011.01.031.
https://doi.org/10.1053/j.gastro.2011.01...
, and American Society for Gastrointestinal Endoscopy (ASGE5. ASGE Technology Committee, Thosani N, Abu Dayyeh BK, Sharma P, Aslanian HR, Enestvedt BK, Komanduri S, Manfredi M, Navaneethan U, Maple JT, et al. ASGE Technology Committee systematic review and meta-analysis assessing the ASGE Preservation and Incorporation of Valuable Endoscopic Innovations thresholds for adopting real-time imaging-assisted endoscopic targeted biopsy during endoscopic surveillance of Barrett’s esophagus. Gastrointest Endosc. 2016;83(4):684-98.e7. doi: 10.1016/j.gie.2016.01.007.
https://doi.org/10.1016/j.gie.2016.01.00...
)4646. Schlemper RJ, Riddell RH, Kato Y, Borchard F, Cooper HS, Dawsey SM, Dixon MF, Fenoglio-Preiser CM, Fléjou JF, Geboes K, et al. The Vienna classification of gastrointestinal epithelial neoplasia. Gut. 2000;47(2):251-5. doi: 10.1136/gut.47.2.251.
https://doi.org/10.1136/gut.47.2.251...
all recommend that surveillance endoscopy with four-quadrant biopsies at 2-cm intervals every 3-5 years for NDBE. PPI therapy is associated with a 71% decrease in the risk of developing HGD and EAC in patients with BE5050. Singh S, Garg SK, Singh PP, Iyer PG, El-Serag HB. Acid-suppressive medications and risk of oesophageal adenocarcinoma in patients with Barrett’s oesophagus: a systematic review and meta-analysis. Gut. 2014;63(8):1229-37. doi: 10.1136/gutjnl-2013-305997.
https://doi.org/10.1136/gutjnl-2013-3059...
. Long-term therapy (>2-3 years) has a higher protective effect5050. Singh S, Garg SK, Singh PP, Iyer PG, El-Serag HB. Acid-suppressive medications and risk of oesophageal adenocarcinoma in patients with Barrett’s oesophagus: a systematic review and meta-analysis. Gut. 2014;63(8):1229-37. doi: 10.1136/gutjnl-2013-305997.
https://doi.org/10.1136/gutjnl-2013-3059...
. Chemoprevention to inhibit the progression to cancer in patients with BE is currently being assessed. Various medications such as aspirin, metformin, and statins have been studied. A randomized controlled trial indicated that the combination of high-dose esomeprazole plus aspirin had the strongest protective effect compared with low-dose esomeprazole without aspirin at a median follow-up of 8.9 years2525. Jankowski JAZ, de Caestecker J, Love SB, Reilly G, Watson P, Sanders S, Ang Y, Morris D, Bhandari P, Brooks C, et al. Esomeprazole and aspirin in Barrett’s oesophagus (AspECT): a randomised factorial trial. Lancet. 2018;392(10145):400-408. doi: 10.1016/S0140-6736(18)31388-6.
https://doi.org/10.1016/S0140-6736(18)31...
. However, the ACG guidelines do not currently recommend chemoprevention for all patients with BE, but suggest it should be considered in patients with BE who are appropriate candidates for aspirin use for cardioprotection4747. 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. doi: 10.1038/ajg.2015.322.
https://doi.org/10.1038/ajg.2015.322...
.

2. Indefinite for dysplasia

In BE IND, either the epithelial abnormalities are insufficient for a diagnosis of dysplasia, or the nature of the epithelial abnormalities is uncertain due to inflammation or technical difficulties with specimen processing. The risk of HGD or cancer within 1 year of the diagnosis of IND varies between 1.9% and 15%5555. Thota PN, Kistangari G, Esnakula AK, Gonzalo DH, Liu XL. Clinical significance and management of Barrett’s esophagus with epithelial changes indefinite for dysplasia. World J Gastrointest Pharmacol Ther. 2016;7(3):406-11. doi: 10.4292/wjgpt.v7.i3.406.
https://doi.org/10.4292/wjgpt.v7.i3.406...
. The recommendation from ACG4747. 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. doi: 10.1038/ajg.2015.322.
https://doi.org/10.1038/ajg.2015.322...
for management is to optimize acid suppressive therapy for 3-6 months and then to repeat esophagogastroduodenoscopy (EGD). If indefinite dysplasia is noted again, repeat endoscopy in 12 months is recommended5959. Westhoff B, Brotze S, Weston A, McElhinney C, Cherian R, Mayo MS, Smith HJ, Sharma P. The frequency of Barrett’s esophagus in high-risk patients with chronic GERD. Gastrointest Endosc. 2005;61(2):226-31. doi: 10.1016/s0016-5107(04)02589-1.
https://doi.org/10.1016/s0016-5107(04)02...
.

3. Low-grade dysplasia

Most patients with an initial diagnosis of LGD (73%) are downstaged to NDBE or to IND after review by expert gastrointestinal pathologists1010. Duits LC, Phoa KN, Curvers WL, Ten Kate FJ, Meijer GA, Seldenrijk CA, Offerhaus GJ, Visser M, Meijer SL, Krishnadath KK, et al. Barrett’s oesophagus patients with low-grade dysplasia can be accurately risk-stratified after histological review by an expert pathology panel. Gut. 2015;64(5):700-6. doi: 10.1136/gutjnl-2014-307278.
https://doi.org/10.1136/gutjnl-2014-3072...
. Patients with confirmed and persistent LGD are at higher risk of progression1111. Duits LC, van der Wel MJ, Cotton CC, Phoa KN, Ten Kate FJW, Seldenrijk CA, Offerhaus GJA, Visser M, Meijer SL, Mallant-Hent RC, et al. Patients With Barrett’s Esophagus and Confirmed Persistent Low-Grade Dysplasia Are at Increased Risk for Progression to Neoplasia. Gastroenterology. 2017;152(5):993-1001.e1. doi: 10.1053/j.gastro.2016.12.008.
https://doi.org/10.1053/j.gastro.2016.12...
. Once LGD is confirmed by a second gastrointestinal pathologist, the patient should be considered for endoscopic ablation. A landmark study demonstrated the benefit of radiofrequency ablation in achieving complete eradication of dysplasia (90.5% vs. 22.7% for a sham procedure) and complete eradication of IM (77.4% vs. 2.3% for a sham procedure)4949. Shaheen NJ, Sharma P, Overholt BF, Wolfsen HC, Sampliner RE, Wang KK, Galanko JA, Bronner MP, Goldblum JR, Bennett AE, et al. Radiofrequency ablation in Barrett’s esophagus with dysplasia. N Engl J Med. 2009;360(22):2277-88. doi: 10.1056/NEJMoa0808145.
https://doi.org/10.1056/NEJMoa0808145...
. Patients with confirmed LGD who do not undergo eradication therapy should have surveillance endoscopy every 6-12 months.

4. High-grade dysplasia

As with LGD, the diagnosis of HGD needs to be confirmed by a second pathologist with gastrointestinal expertise. In the past, the treatment was esophagectomy, but due to demonstrated lower morbidity and equivalent efficacy of radiofrequency ablation, the current treatment of choice is endoscopic mucosal resection (EMR) of raised lesions, followed by radiofrequency ablation of the entire affected segment2323. Hu Y, Puri V, Shami VM, Stukenborg GJ, Kozower BD. Comparative Effectiveness of Esophagectomy Versus Endoscopic Treatment for Esophageal High-grade Dysplasia. Ann Surg. 2016;263(4):719-26. doi: 10.1097/SLA.0000000000001387.
https://doi.org/10.1097/SLA.000000000000...
. Pathology is best assessed by EMR, especially in areas of nodularity and ulceration. A randomized controlled study of 42 patients with HGD was randomized between radiofrequency ablation and sham procedure. Complete eradication of dysplasia was achieved in 81% of ablation patients versus 19% with the sham procedure4949. Shaheen NJ, Sharma P, Overholt BF, Wolfsen HC, Sampliner RE, Wang KK, Galanko JA, Bronner MP, Goldblum JR, Bennett AE, et al. Radiofrequency ablation in Barrett’s esophagus with dysplasia. N Engl J Med. 2009;360(22):2277-88. doi: 10.1056/NEJMoa0808145.
https://doi.org/10.1056/NEJMoa0808145...
. Eradication of IM was achieved in 77% of ablation patients versus 2% of patients with the sham therapy4949. Shaheen NJ, Sharma P, Overholt BF, Wolfsen HC, Sampliner RE, Wang KK, Galanko JA, Bronner MP, Goldblum JR, Bennett AE, et al. Radiofrequency ablation in Barrett’s esophagus with dysplasia. N Engl J Med. 2009;360(22):2277-88. doi: 10.1056/NEJMoa0808145.
https://doi.org/10.1056/NEJMoa0808145...
. Results of 3-year follow-up from the same cohort showed complete eradication of dysplasia in 98% and of IM in 91%4848. Shaheen NJ, Overholt BF, Sampliner RE, Wolfsen HC, Wang KK, Fleischer DE, Sharma VK, Eisen GM, Fennerty MB, Hunter JG, et al. Durability of radiofrequency ablation in Barrett’s esophagus with dysplasia. Gastroenterology. 2011;141(2):460-8. doi: 10.1053/j.gastro.2011.04.061.
https://doi.org/10.1053/j.gastro.2011.04...
. Endoscopic eradication therapy is recommended for all patients with BE and HGD without the potential comorbidity and side effects associated with esophageal resection. Short segment Barrett’s (<3 cm) with HGD can also be assessed for complete ablation with EMR alone. Alternatively, surveillance every 3 months is an option if the patient does not wish to undergo eradication therapy4848. Shaheen NJ, Overholt BF, Sampliner RE, Wolfsen HC, Wang KK, Fleischer DE, Sharma VK, Eisen GM, Fennerty MB, Hunter JG, et al. Durability of radiofrequency ablation in Barrett’s esophagus with dysplasia. Gastroenterology. 2011;141(2):460-8. doi: 10.1053/j.gastro.2011.04.061.
https://doi.org/10.1053/j.gastro.2011.04...
.

What is the role of antireflux surgery in the treatment of Barrett’s esophagus?

Because dysplasia in BE carries an increased risk of progression to cancer, the current standard of care in these patients is EMR of visible lesions, followed by ablation of the flat mucosa, with the aim of achieving complete eradication of IM77. Bennett C, Vakil N, Bergman J, Harrison R, Odze R, Vieth M, Sanders S, Gay L, Pech O, Longcroft-Wheaton G, et al. Consensus statements for management of Barrett’s dysplasia and early-stage esophageal adenocarcinoma, based on a Delphi process. Gastroenterology. 2012;143(2):336-46. doi: 10.1053/j.gastro.2012.04.032.
https://doi.org/10.1053/j.gastro.2012.04...
,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. doi: 10.1038/ajg.2015.322.
https://doi.org/10.1038/ajg.2015.322...
. A key part of treatment during this time is maximal acid suppression with continuous PPI treatment1616. Fitzgerald RC, di Pietro M, Ragunath K, Ang Y, Kang JY, Watson P, Trudgill N, Patel P, Kaye PV, Sanders S, et al. British Society of Gastroenterology. British Society of Gastroenterology guidelines on the diagnosis and management of Barrett’s oesophagus. Gut. 2014;63(1):7-42. doi: 10.1136/gutjnl-2013-305372.
https://doi.org/10.1136/gutjnl-2013-3053...
.

PPIs are today the main component of medical treatment for GERD, because they are the most effective medications to decrease gastric acid production, leading to healing of esophagitis and relief of symptoms3131. Maret-Ouda J, Markar SR, Lagergren J. Gastroesophageal Reflux Disease: A Review. JAMA. 2020;324(24):2536-2547. doi: 10.1001/jama.2020.21360.
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. However, PPIs only change the pH of the refluxate, without modifying the occurrence and the number of reflux episodes5353. Tamhankar AP, Peters JH, Portale G, Hsieh CC, Hagen JA, Bremner CG, DeMeester TR. Omeprazole does not reduce gastroesophageal reflux: new insights using multichannel intraluminal impedance technology. J Gastrointest Surg. 2004;8(7):890-7; discussion 897-8. doi: 10.1016/j.gassur.2004.08.001.
https://doi.org/10.1016/j.gassur.2004.08...
. Therefore, symptoms tend to recur after discontinuation of PPIs, and some patients on PPIs have refractory symptoms due to ongoing reflux.

Successful elimination of reflux symptoms does not guarantee control of acid reflux. Often, BE patients do not experience heartburn due to the reduced sensitivity of the columnar mucosa to the acidic and bilious refluxate2121. Herbella FA, Tedesco P, Nipomnick I, Fisichella PM, Patti MG. Effect of partial and total laparoscopic fundoplication on esophageal body motility. Surg Endosc. 2007;21(2):285-8. doi: 10.1007/s00464-006-0108-2.
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. In addition, while PPI stops acid reflux, patients may still have regurgitation as a consequence of an incompetent lower esophageal sphincter (LES)3232. Mariotto R, Herbella FAM, Andrade VLÂ, Schlottmann F, Patti MG. Validation of a new water-perfused high-resolution manometry system. Arq Bras Cir Dig. 2021;33(4):e1557. doi: 10.1590/0102-672020200004e1557.
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and the quality of esophageal peristalsis3333. Mendes-Filho AM, Godoy ESN, Alhinho HCAW, Galvão-Neto MDP, Ramos AC, Ferraz ÁAB, Campos JM. Fundoplication conversion in roux-en-y gastric bypass for control of obesity and gastroesophageal reflux: systematic review. Arq Bras Cir Dig. 2017;30(4):279-282. doi: 10.1590/0102-6720201700040012.
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. Potentially most significantly, PPIs do not eliminate the reflux of bile, a major contributor to the pathogenesis of BE66. Ayazi S, Hagen JA, Chan LS, DeMeester SR, Lin MW, Ayazi A, Leers JM, Oezcelik A, Banki F, Lipham JC, et al. Obesity and gastroesophageal reflux: quantifying the association between body mass index, esophageal acid exposure, and lower esophageal sphincter status in a large series of patients with reflux symptoms. J Gastrointest Surg. 2009;13(8):1440-7. doi: 10.1007/s11605-009-0930-7.
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,1313. Elias PS, Castell DO. The Role of Acid Suppression in Barrett’s Esophagus. Am J Med. 2017;130(5):525-529. doi: 10.1016/j.amjmed.2016.12.032.
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,2626. Kauer WK, Peters JH, DeMeester TR, Ireland AP, Bremner CG, Hagen JA. Mixed reflux of gastric and duodenal juices is more harmful to the esophagus than gastric juice alone. The need for surgical therapy re-emphasized. Ann Surg. 1995;222(4):525-31; discussion 531-3. doi: 10.1097/00000658-199522240-00010.
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.

As many as 40% of patients with heartburn have either an incomplete or complete lack of response to once-daily PPIs2222. Hershcovici T, Fass R. Step-by-step management of refractory gastresophageal reflux disease. Dis Esophagus. 2013;26(1):27-36. doi: 10.1111/j.1442-2050.2011.01322.x.
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. The proportion of patients with persistent troublesome heartburn despite once-daily PPI use was 32% in randomized trials and 17% in nonrandomized trials; the proportion of patients with persistent regurgitation was 28% in randomized and nonrandomized trials1414. El-Serag H, Becher A, Jones R. Systematic review: persistent reflux symptoms on proton pump inhibitor therapy in primary care and community studies. Aliment Pharmacol Ther. 2010;32(6):720-37. doi: 10.1111/j.1365-2036.2010.04406.x.
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. In addition, increasing evidence has highlighted the risk of adverse events and side effects after long-term PPI treatment, including kidney disease and injury22. Al-Aly Z, Maddukuri G, Xie Y. Proton Pump Inhibitors and the Kidney: Implications of Current Evidence for Clinical Practice and When and How to Deprescribe. Am J Kidney Dis. 2020;75(4):497-507. doi: 10.1053/j.ajkd.2019.07.012.
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, Clostridium difficile infection1717. Freedberg DE, Kim LS, Yang YX. The Risks and Benefits of Long-term Use of Proton Pump Inhibitors: Expert Review and Best Practice Advice From the American Gastroenterological Association. Gastroenterology. 2017;152(4):706-715. doi: 10.1053/j.gastro.2017.01.031.
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, community-acquired pneumonia1515. Eusebi LH, Rabitti S, Artesiani ML, Gelli D, Montagnani M, Zagari RM, Bazzoli F. Proton pump inhibitors: Risks of long-term use. J Gastroenterol Hepatol. 2017;32(7):1295-1302. doi: 10.1111/jgh.13737.
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, fractures due to osteoporosis2424. Ito T, Jensen RT. Association of long-term proton pump inhibitor therapy with bone fractures and effects on absorption of calcium, vitamin B12, iron, and magnesium. Curr Gastroenterol Rep. 2010;12(6):448-57. doi: 10.1007/s11894-010-0141-0.
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, gastric cancer88. Cheung KS, Chan EW, Wong AYS, Chen L, Wong ICK, Leung WK. Long-term proton pump inhibitors and risk of gastric cancer development after treatment for Helicobacter pylori: a population-based study. Gut. 2018;67(1):28-35. doi: 10.1136/gutjnl-2017-314605.
https://doi.org/10.1136/gutjnl-2017-3146...
, and increased risk of COVID-1944. Almario CV, Chey WD, Spiegel BMR. Increased Risk of COVID-19 Among Users of Proton Pump Inhibitors. Am J Gastroenterol. 2020;115(10):1707-1715. doi: 10.14309/ajg.0000000000000798.
https://doi.org/10.14309/ajg.00000000000...
.

Antireflux surgery (ARS) aims to repair the antireflux barrier, which is defective in patients with BE3434. O’Riordan JM, Byrne PJ, Ravi N, Keeling PW, Reynolds JV. Long-term clinical and pathologic response of Barrett’s esophagus after antireflux surgery. Am J Surg. 2004;188(1):27-33. doi: 10.1016/j.amjsurg.2003.10.025.
https://doi.org/10.1016/j.amjsurg.2003.1...
. As a result, the function of the LES is improved, the gastroesophageal flap valve is restored, and acid or duodenal reflux into the esophagus is decreased compared to medical treatment alone4444. Salo JA, Salminen JT, Kiviluoto TA, Nemlander AT, Rämö OJ, Färkkilä MA, Kivilaakso EO, Mattila SP. Treatment of Barrett’s esophagus by endoscopic laser ablation and antireflux surgery. Ann Surg. 1998;227(1):40-4. doi: 10.1097/00000658-199801000-00006.
https://doi.org/10.1097/00000658-1998010...
. The most common indication for ARS is refractory symptoms or persistent esophagitis that is not responding to medical therapy11. Abbas AE, Deschamps C, Cassivi SD, Allen MS, Nichols FC 3rd, Miller DL, Pairolero PC. Barrett’s esophagus: the role of laparoscopic fundoplication. Ann Thorac Surg. 2004;77(2):393-6. doi: 10.1016/S0003-4975(03)01352-3.
https://doi.org/10.1016/S0003-4975(03)01...
. The most commonly performed surgical procedure for GERD is laparoscopic fundoplication, which enhances the esophagogastric junction ability to prevent reflux into the esophagus1919. Garg SK, Gurusamy KS. Laparoscopic fundoplication surgery versus medical management for gastro-oesophageal reflux disease (GORD) in adults. Cochrane Database Syst Rev. 2015;2015(11):CD003243. doi: 10.1002/14651858.CD003243.pub3.
https://doi.org/10.1002/14651858.CD00324...
. A 5-year follow-up of 372 patients included in an randomized control trial comparing the PPI esomeprazole with laparoscopic fundoplication found similar remission rates in the medication group (92%; 95%CI 89-96%) and surgery group (85%; 95%CI 81-90%), but worse symptoms of acid regurgitation in the medication group (13%) compared with the surgery group (2%)1818. Galmiche JP, Hatlebakk J, Attwood S, Ell C, Fiocca R, Eklund S, Långström G, Lind T, Lundell L; LOTUS Trial Collaborators. Laparoscopic antireflux surgery vs esomeprazole treatment for chronic GERD: the LOTUS randomized clinical trial. JAMA. 2011;305(19):1969-77. doi: 10.1001/jama.2011.626.
https://doi.org/10.1001/jama.2011.626...
. A few studies have compared the effect of ARS on BE with best medical therapy and indicated that the surgery intervention had significantly less dysplasia de novo3535. Parrilla P, Martínez de Haro LF, Ortiz A, Munitiz V, Molina J, Bermejo J, Canteras M. Long-term results of a randomized prospective study comparing medical and surgical treatment of Barrett’s esophagus. Ann Surg. 2003;237(3):291-8. doi: 10.1097/01.SLA.0000055269.77838.8E.
https://doi.org/10.1097/01.SLA.000005526...
and a greater probability of BE regression3333. Mendes-Filho AM, Godoy ESN, Alhinho HCAW, Galvão-Neto MDP, Ramos AC, Ferraz ÁAB, Campos JM. Fundoplication conversion in roux-en-y gastric bypass for control of obesity and gastroesophageal reflux: systematic review. Arq Bras Cir Dig. 2017;30(4):279-282. doi: 10.1590/0102-6720201700040012.
https://doi.org/10.1590/0102-67202017000...
. Laparoscopic fundoplication is safe and has been associated with a very low short-term mortality (0.1-0.2%). Complications and, more importantly, side effects of gas bloat and inability to belch and vomit can occur and should be a component of counseling and discussion with the patient preoperatively6161. Yadlapati R, Hungness ES, Pandolfino JE. Complications of Antireflux Surgery. Am J Gastroenterol. 2018;113(8):1137-1147. doi: 10.1038/s41395-018-0115-7.
https://doi.org/10.1038/s41395-018-0115-...
.

Other indications for ARS in patients with BE include younger patients who do not wish to commit themselves to lifelong PPI therapy. It is particularly important that these patients are counseled that the surgery is being considered to control their GERD and decrease their reliance on PPIs, not to eliminate the requirement for long-term endoscopic Barrett’s follow-up1919. Garg SK, Gurusamy KS. Laparoscopic fundoplication surgery versus medical management for gastro-oesophageal reflux disease (GORD) in adults. Cochrane Database Syst Rev. 2015;2015(11):CD003243. doi: 10.1002/14651858.CD003243.pub3.
https://doi.org/10.1002/14651858.CD00324...
.

The optimum timing of ARS in patients with Barrett’s has not been standardized. Some reports have suggested that performing ARS at the time of ablative therapy can decrease the number and improve the efficiency of endoscopic Barrett’s ablation2020. 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. doi: 10.1016/j.jamcollsurg.2011.06.419.
https://doi.org/10.1016/j.jamcollsurg.20...
. Failure of laparoscopic fundoplication can often be linked to applying incorrect indications of inadequate preoperative assessment3636. Patti MG, Allaix ME, Fisichella PM. Analysis of the Causes of Failed Antireflux Surgery and the Principles of Treatment: A Review. JAMA Surg. 2015;150(6):585-90. doi: 10.1001/jamasurg.2014.3859.
https://doi.org/10.1001/jamasurg.2014.38...
. As a result, accurate preoperative assessment including endoscopy, high-resolution manometry, and selective application of objective pH testing to define those who will benefit from the ARS, i.e., those with LES dysfunction and strong symptom correlation, is recommended. There are recognized advantages of having the procedures conducted in centers with high volume experience and with the capability of delivering the full spectrum of diagnostic workup, surgical treatment, and follow-up of GERD and BE4141. Riegler M, Kristo I, Nikolic M, Rieder E, Schoppmann SF. Update on the management of Barrett’s esophagus in Austria. Eur Surg. 2017;49(6):282-287. doi: 10.1007/s10353-017-0504-y.
https://doi.org/10.1007/s10353-017-0504-...
.

Controversies are still present regarding the progression of Barrett’s following ARS. One study based on a Swedish population showed that ARS failed to prevent the development of esophageal cancer when compared with the corresponding population2929. Lagergren J, Bergström R, Lindgren A, Nyrén O. Symptomatic gastroesophageal reflux as a risk factor for esophageal adenocarcinoma. N Engl J Med. 1999;340(11):825-31. doi: 10.1056/NEJM199903183401101.
https://doi.org/10.1056/NEJM199903183401...
. Other studies have suggested that successful ARS protects against progression to malignancy; however, this has not been confirmed in prospective trials or large cohort studies3030. Lagergren J, Ye W, Lagergren P, Lu Y. The risk of esophageal adenocarcinoma after antireflux surgery. Gastroenterology. 2010;138(4):1297-301. doi: 10.1053/j.gastro.2010.01.004.
https://doi.org/10.1053/j.gastro.2010.01...
,5656. Tran T, Spechler SJ, Richardson P, El-Serag HB. Fundoplication and the risk of esophageal cancer in gastroesophageal reflux disease: a Veterans Affairs cohort study. Am J Gastroenterol. 2005;100(5):1002-8. doi: 10.1111/j.1572-0241.2005.41007.x.
https://doi.org/10.1111/j.1572-0241.2005...
,6060. Wilson H, Mocanu V, Sun W, Dang J, Jogiat U, Kung J, Switzer N, Wong C, Karmali S. Fundoplication is superior to medical therapy for Barrett’s esophagus disease regression and progression: a systematic review and meta-analysis. Surg Endosc. 2021. doi: 10.1007/s00464-021-08543-6.
https://doi.org/10.1007/s00464-021-08543...
.

Increasingly, patients with LGD are undergoing successful endoscopic ablation2727. Klair JS, Zafar Y, Nagra N, Murali AR, Jayaraj M, Singh D, Rustagi T, Krishnamoorthi R. 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):561-568. doi: 10.1159/000514786.
https://doi.org/10.1159/000514786...
. Patients with LGD can be considered for ARS5151. Skrobić O, Simić A, Radovanović N, Ivanović N, Micev M, Peško P. Significance of Nissen fundoplication after endoscopic radiofrequency ablation of Barrett’s esophagus. Surg Endosc. 2016;30(9):3802-7. doi: 10.1007/s00464-015-4677-9.
https://doi.org/10.1007/s00464-015-4677-...
, and recent reports suggest that fundoplication is superior to medical therapy in avoiding Barrett’s progression and promoting Barrett’s regression6060. Wilson H, Mocanu V, Sun W, Dang J, Jogiat U, Kung J, Switzer N, Wong C, Karmali S. Fundoplication is superior to medical therapy for Barrett’s esophagus disease regression and progression: a systematic review and meta-analysis. Surg Endosc. 2021. doi: 10.1007/s00464-021-08543-6.
https://doi.org/10.1007/s00464-021-08543...
. There are currently very few data on whether successful ARS decreases the incidence of recurrence following successful ablation of either LGD or HGD.

Antireflux surgery can be considered in patients following successful ablation of HGD. However, many surgeons would advocate an extended period of stable postablation endoscopic follow-up before proceeding with ARS. Some practitioners recommend repeating objective pH testing following ARS in patients with NDBE as well as those with LGD or HGD postablation33. Allaix ME, Patti MG. Antireflux surgery for dysplastic Barrett. World J Surg. 2015;39(3):588-94. doi: 10.1007/s00268-014-2632-x.
https://doi.org/10.1007/s00268-014-2632-...
. Whether this testing should be done before medical therapy is discontinued has not been extensively studied33. Allaix ME, Patti MG. Antireflux surgery for dysplastic Barrett. World J Surg. 2015;39(3):588-94. doi: 10.1007/s00268-014-2632-x.
https://doi.org/10.1007/s00268-014-2632-...
.

CONCLUSION

The current recommended BE treatment is maximal acid suppression with PPIs and histamine-2 blockers, while in some cases, fundoplication is required to control reflux refractory to medical therapy. In our opinion, laparoscopic ARS can be an appropriate alternative and even a preferred option from medical therapy for highly selected candidates. Minimal morbidity and near zero mortality in high volume centers along with multiple studies demonstrating long-term success of antireflux operations support this approach. However, post-treatment surveillance continues to be a required component of long-term treatment because the risk of progression to dysplasia still exists. Nevertheless, a prospective randomized controlled trial is needed to confirm the therapeutic effect and long-term outcomes of laparoscopic ARS versus medical therapy plus or minus endoscopic ablation in patients with BE. In addition, future comparisons of maximal medical therapy versus other surgical techniques (LINX device) and endoscopic antireflux procedures such as TIF (Transoral Incisionless Fundoplication) and Stretta are also warranted.

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  • 1
    How to cite this article: Han S, Low DE. ABCD Arq Bras Cir Dig. 2022;35:e1664. https://doi.org/10.1590/0102-672020210002e1664
  • Financial support: none.

Publication Dates

  • Publication in this collection
    24 June 2022
  • Date of issue
    2022

History

  • Received
    25 Aug 2021
  • Accepted
    27 Oct 2021
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