Late Results of the Surgical Treatment of 125 Patients with Short-Segment Barrett Esophagus

ORIGINAL ARTICLE Late Results of the Surgical Treatment of 125 Patients With Short-Segment Barrett Esophagus

Attila Csendes, MD; Italo Braghetto, MD; Patricio Burdiles, MD; Gladys Smok, MD; Ana Henrı´quez, MTC; Ana Maria Burgos, MD

Hypothesis: The results of surgical treatment of pa- Main Outcome Measures: Late subjective and objec- tients with long-segment Barrett esophagus (BE) have been tive outcomes of the 3 different surgical procedures. extensively reported. However, few publications refer to the results of surgery 5 years after the fact among pa- Results: No operative mortality and only 2 postopera- tients with short-segment BE. This study aimed to de- tive complications (1.6%) occurred. The regression from termine the late results of 3 surgical procedures in pa- intestinal metaplasia to cardiac or oxyntocardiac mu- tients with short-segment BE by subjective and objective cosa occurred in 60.8% to 65.4% of the patients, at a mean measurements. time of 39 to 56 months after surgery. Visick grading showed Visick grade I or II in 86.3% to 100.0% of the Design: Prospective, nonrandomized study starting on patients. No progression to low- or high-grade dyspla- March 1, 1987, and ending on December 31, 2005. sia or adenocarcinoma occurred. Setting: A prospective, descriptive study of a group of Conclusions: On the basis of these results, laparo- patients. scopic Nissen fundoplication seems to be the surgical op- tion for patients with short-segment BE because it is less Patients: A total of 125 patients with short-segment BE underwent 3 operations in different periods: duodenal invasive, has fewer side effects, and produces good re- switch plus highly selective vagotomy and antireflux tech- sults in the long-term follow-up. nique in 31 patients, vagotomy plus partial gastrectomy and Roux-en-Y loop with antireflux surgery in 58 patients, and laparoscopic Nissen fundoplication in 36 patients. Arch Surg. 2009;144(10):921-927

ARRETT ESOPHAGUS (BE) IS A and long-segment BE (if this distance is condition in which the nor- more than 3 cm). mal squamous epithelium of The outcomes of the surgical treatment the distal esophagus is re- of patients with long-segment BE have been placed by an abnormal co- extensively published by many authors and lumnarB epithelium that undergoes 2 meta- summarized by some of us in several re- plastic changes. The first change is in the view articles.9-11 However, despite patients appearance of cardiac mucosa, and the sec- with short-segment BE being much more ond is in the presence of specialized in- common than patients with long-segment testinal metaplasia.1-7 This disease is the BE, the results of surgical treatment among final consequence of long-standing duo- patients with short-segment BE have been denogastroesophageal reflux, and its analyzed and published by only 6 groups of authors,12-17 to our knowledge. There- See Invited Critique fore, the purpose of the present prospec- at end of article tive study was to determine the late subjective and objective outcomes of 3 different importance lies in its association with a risk surgical procedures performed in different Author Affiliations: of a 30- to 125-fold development of ad- time periods as treatment of patients with Departments of Surgery short-segment BE: laparoscopic Nissen fun- (Drs Csendes, Braghetto, enocarcinoma. Currently, BE is divided into 2 groups8: short-segment BE (if the doplication,18 open antireflux surgery with Burdiles and Burgos, and 19 Ms Henrı´quez) and Pathology endoscopic distance between the gastro- duodenal switch, and open antireflux sur- (Dr Smok), Clinical Hospital, esophageal junction and the upper limit gery with distal gastrectomy plus Roux- University of Chile, Santiago. of the columnar mucosa is less than 3 cm) en-Y loop.20,21

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©2009 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 10/02/2021 METHODS tive peristaltic contraction. The presence of a mechanically incompetent sphincter was diagnosed if at least 1 of the following parameters was present: resting pressure equal to or less than 6 PATIENTS mm Hg, an abdominal length equal to or less than 10 mm, and a total length equal to or less than 20 mm. This test was per- This prospective, nonrandomized study started on March 1, formed before and 1 to 2 years after surgery. 1987, when a special surgical protocol was established for patients with BE, either with a short- or long-segment columnar ESOPHAGEAL 24-HOUR pH MONITORING epithelium, and ended on December 31, 2005.20 A total of 125 patients with short-segment BE were included; all the patients Esophageal 24-hour pH monitoring was performed after a 12- had BE secondary to chronic pathologic gastroesophageal re- hour fast by introducing the catheter (Digitrapper Synectics; flux. Exclusion criteria included cardiac intestinal metaplasia, Stockholm, Sweden) through the nose. The catheter was placed hiatal hernia without BE, scleroderma or achalasia with short- 5 cm proximal to the manometric upper limit of the LES (which segment BE, and low- or high-grade dysplasia (these patients is why manometric measurements are always performed be- were described in another publication19). Patients with esoph- fore pH is studied). The details of this procedure have been pub- ageal or cardial adenocarcinoma were also excluded. lished previously.8,19-21 Among the 6 different parameters that can be evaluated, the most practical is the total percentage of CLINICAL QUESTIONNAIRE time in which the intraesophageal pH remains below 4, which is usually less than 4% in 24 hours. A careful clinical assessment that assessed the presence of typi- cal gastroesophageal reflux symptoms was performed in all pa- ESOPHAGEAL 24-HOUR SPECTROPHOTOMETRIC tients before and several times after surgery. For the late clinical evaluation, a modified Visick gradation was used, as BILIRUBIN MONITORING previously described.10,18 Esophageal 24-hour spectrophotometric bilirubin monitoring was developed to determine the magnitude of duodenogastroesopha- ENDOSCOPIC EXAMINATION geal reflux by measuring the total intraluminal concentration of bilirubin at the distal esophagus.8,19,20 Special dietary advice was All endoscopic procedures were performed by 2 of the authors given to the patient concerning certain foods, the consumption (A.C. and I.B.) using an XQ-20 endoscope (Olympus Corpo- of which interferes with measurements. The final calculation is ration; Tokyo, Japan) and later a video endoscope manufac- based on the percentage of time that bilirubin is measured in the tured by the same company. Extensive details of the proce- esophagus with an absorbance greater than 0.2 (usually below 8,10,19,21 dures have been published previously. The presence of 2% during 24-hour monitoring session). isolated or confluent erosions was carefully recorded, as well as the presence of a hiatal hernia, which was defined as a sac- like structure between the diaphragmatic pinch-cock and the DEFINITION OF REGRESSION endoscopic gastroesophageal junction. This procedure was performed in all patients before and several times after surgery (ev- For the present study, regression of intestinal metaplasia was ery 1 or 2 years). considered to be the disappearance of intestinal metaplasia into cardiac or oxyntocardiac mucosa in 2 consecutive endoscopic and biopsy studies. HISTOLOGIC ANALYSIS

In all patients, 4 biopsy specimens were obtained immediately STATISTICAL ANALYSIS below the squamous-columnar junction and 2 samples 2 cm dis- tally. They were submerged in a 10% formalin solution and stained For statistical evaluation, the Mann-Whitney test, Fisher ex- ␹2 Ͻ with hematoxylin-eosin and Alcian blue at pH 2.5 to determine act test, and test were used, with P .05 considered to be the type of epithelium that lined the distal esophagus. Fundic mu- statistically significant. All values are expressed as means and cosa was identified by the presence of parietal and chief cells at standard deviations. the deep glandular layer. Cardiac mucosa was identified by the presence of mucous-secreting columnar cells. Oxyntocardiac mu- SURGICAL PROCEDURES cosa was defined by the presence of parietal cells and mucous- secreting columnar cells. Intestinal metaplasia was defined by the Three surgical techniques were used in these 125 patients with presence of well-defined goblet cells, confined by positive stain- short-segment BE in different periods: (1) acid suppression and ing with Alcian blue. The presence of Helicobacter pylori was in- duodenal diversion procedure20,21 performed by laparotomy, a vestigated in the gastroesophageal biopsy specimens and the an- truncal or selective vagotomy, an antireflux procedure, partial trum specimens. distal gastrectomy, and a Roux-en-Y gastrojejunal anastomo- sis with a loop 70 cm long (this technique was used between ESOPHAGEAL MANOMETRIC STUDIES 1987 and 1995); (2) laparotomic duodenal switch procedure, associated with highly selective vagotomy and an antireflux sur- gery19 (this operation was performed between 1992 and 1995); Esophageal manometric studies were performed after a 12- 18 hour fast with the patient in the supine position. The complete and (3) laparoscopic Nissen fundoplication (this procedure details have been extensively published in previous re- has been performed from 1996 to the present). ports.8,19-21 Three manometric characteristics were determined at the lower esophageal sphincter (LES): total length (in milli- ANTIREFLUX SURGERY meters), abdominal length (in millimeters), and resting pressure (in Hg of mercury), as well as the amplitude of the contrac- Two types of antireflux technique were used in these patients. tion of the distal esophageal waves (in millimeters of mercury). The first technique was Nissen fundoplication, either open or An amplitude of less than 30 mm Hg was considered an ineffec- laparoscopic, whose surgical steps were described in detail in

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©2009 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 10/02/2021 Table 1. Clinical and Endoscopic Features of 125 Patients With Short-Segment Barrett Esophagusa

Duodenal Switch Acid Suppression—Duodenal Diversion Laparoscopic Nissen Fundoplication Feature (n=31) (n=58) (n=36) Age, mean, y 52 53.7 51.9 Reflux symptoms, No. (%) 31 (100) 58 (100) 36 (100) Barrett esophagus length, mm 23.5 24.5 22.3 Erosive esophagitis, No. (%) 17 (55) 24 (41) 11 (31) Hiatal hernia, No. (%) 12 (39) 17 (29) 14 (39) Intestinal metaplasia, No. (%) 31 (100) 58 (100) 36 (100) No. of postoperative endoscopies per patient 4.2 3.1 3.0 Length of hospital stay, mean (SD), d 6.2 (1) 5.9 (1.2) 3.0 (0.5)

a P values are Ͼ.90 for duodenal switch vs acid suppression duodenal diversion, Ͻ.001 for duodenal switch vs laparoscopic Nissen fundoplication, and Ͻ.001 for laparoscopic Nissen fundoplication vs acid suppression duodenal diversion.

a previous publication.18,22 Basically, a 4-cm “floppy” wrap was developed gastric stasis after surgery, which required en- created, which sutured the anterior and posterior walls of the doscopic dilatation, with uneventful posterior evolution. gastric fundus after division of 3 to 4 short gastric vessels. A After vagotomy and partial gastrectomy, 1 patient devel- 360° wrap was constructed around the esophagogastric junc- oped a gastric fistula, which required subsequent operation in a “floppy” fashion; late complications, such as displace- tion and drainage, with an excellent postoperative course. ment or intussusceptions of the wrap, were prevented by the suturing of the proximal and distal stitches to the esophageal The only significant difference among these operations was wall. This procedure was designed to restore the normal mano- observed in the length of the hospital stay, which was sig- metric characteristics of the LES. The second technique was nificantly shorter for laparoscopic fundoplication com- posterior gastropexy with calibration of the cardia, or Hill- pared with the other 2 techniques. Larrain technique.22,23 Three to 4 short gastric vessels were al- Table 2 gives the manometric features before and af- ways divided. The posterior crus of the diaphragm was ap- ter the antireflux procedure in the 3 groups. Because this proximated with 2 nonabsorbable silk stitches. For posterior test only measures the effect of antireflux technique on gastropexy and calibration of the cardia, the procedure was per- the LES and the amplitude of distal esophageal waves, formed by the approximation of the anterior portion of the gas- the changes after surgery were similar. There was an in- troesophageal junction or cardia with its posterior equivalent from right to left in an “adjusted” or calibrated long wrap, using crease in LES pressure compared with preoperative val- 4 to 5 nonabsorbable interrupted stitches. The last stitch was ues, which was statistically significant in all groups. There evaluated by a tense ring created around a 30F bougie cath- was an increase in the abdominal length of the LES com- eter. Two stitches of this calibration were then sutured to the pared with preoperative values, which was highly statis- distal segment of the crus (posterior gastropexy). This proce- tically significant in all 3 groups. There was a statisti- dure is thought to work by helping the patient to regain the cally significant increase in the total length of the LES in normal tension of the sling fibers of the LES and to increase all groups. There was a statistically significant decrease the length of the abdominal portion of the sphincter by means in the presence of an incompetent LES. There was a simi- of posterior gastropexy. lar increase in the amplitude of the distal esophageal waves after surgery but without statistical significance. The com- RESULTS parison of each parameter in the 3 groups, eg, of values before and after surgery, showed no statistically signifi- The main clinical and endoscopic features of the 125 pa- cant difference. tients with short-segment BE are given in Table 1.No Table 3 gives the results of the functional studies be- significant differences were found among the 3 groups in fore and after surgery in each group. The 24-hour pH any parameter evaluated. Among the 31 patients who un- monitoring before surgery and the Bilitec studies before derwent the laparotomic duodenal switch procedure, the surgery showed similar results in all 3 groups (PϾ.5). antireflux technique was a posterior gastropexy with car- After the antireflux procedure, a significant reduction was dial calibration in 20 patients and a Nissen fundoplica- seen in acid reflux in all groups compared with preop- tion in 11. Among the 58 patients who underwent the acid erative values. However, this reduction was not uni- suppression and duodenal diversion procedure, poste- form: after duodenal switch, 80.7% of the patients had rior gastropexy with cardial calibration was performed in acid reflux with normal or below-normal values; an en- 31 patients and a Nissen fundoplication in 27 patients. tirely similar value (82.8%) of reduction of acid reflux Among patients who underwent the laparoscopic proce- was observed among patients with acid suppression who dure, Nissen fundoplication was performed in 33 pa- underwent the duodenal diversion procedure. How- tients and calibration of the cardia in 3 patients. There- ever, after Nissen fundoplication only 75.0% of the pa- fore, Nissen fundoplication was used in 71 patients and tients showed absence of abnormal acid reflux. The re- posterior gastropexy with calibration of the cardia in 54 sults of the 24-hour bile monitoring were evaluated before patients. No operative mortality was observed. The post- and after surgery mainly in the open procedures: they operative course was uneventful in all patients who un- showed an abolition of duodenoesophageal reflux of 83% derwent laparoscopic Nissen fundoplication. One pa- to 100% compared with preoperative values. This moni- tient who underwent the duodenal switch procedure toring was not performed after Nissen fundoplication.

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©2009 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 10/02/2021 Table 2. Manometric Features Before and After Surgery in Patients With Short-Segment Barrett Esophagusa

Acid Suppression— Laparoscopic Nissen Feature Duodenal Switch Duodenal Diversion Fundoplication Lower esophageal sphincter pressure, mm Hg Before surgery 9.2 (5.3) 6.6 (3.6) 7.4 (3.4) After surgery 12.2 (3.3) 12.7 (3.6) 13.8 (2.2) P value Ͻ.001 Ͻ.001 Ͻ.001 Abdominal length, mm Before surgery 5.5 (5.0) 3.1 (4.1) 2.9 (2.9) After surgery 14 (5.8) 11.1 (2.8) 11.9 (2.6) P value Ͻ.001 Ͻ.001 Ͻ.001 Total length, mm Before surgery 32.8 (8.7) 29.4 (7.8) 32.1 (6.6) After surgery 40.4 (9.2) 34.5 (5.8) 36.9 (5.9) P value Ͼ.03 Ͻ.003 Ͼ.09 Incompetent lower esophageal sphincter, % Before surgery 76 90 91 After surgery 15 6 0 P value Ͻ.001 Ͻ.001 Ͻ.001 Amplitude distal esophageal waves, mm Hg Before surgery 52.5 (30.4) 51.1 (28.2) 54.8 (28.6) After surgery 61.2 (24.9) 65.7 (24.3) 77.0 (43.7) P value Ͻ.20 Ͻ.10 Ͻ.11

a Values are expressed as mean (SD) unless otherwise indicated.

Table 3. Functional Studies Before and After Surgery in Patients With Short-Segment Barrett Esophagusa

Acid Suppression— Laparoscopic Nissen Duodenal Switch Duodenal Diversion Fundoplication Study (n=31) (n=58) (n=36) 24-h pH monitoring, % of time with pH Ͻ4in24h Before surgery 16.6 (16.5) 20.1 (16.5) 18.1 (16.3) After surgery 2.8 (2.5) 3.1 (7.3) 5.5 (7.8) P value Ͻ.001 Ͻ.001 Ͻ.001 24-h Bilitec studies, % of time with bilirubin absorbance Ͼ0.2 in 24 h Before surgery 21.5 (20.2) 24.6 (24.6) 6.8 (8.1) After surgery 1.5 (2.5) 0.4 (0.37) NA P value Ͻ.001 Ͻ.001 NA

Abbreviation: NA, not applicable. a Values are expressed as mean (SD).

Table 4 gives the histologic changes at the short- inhibitors again to remain asymptomatic. These grades segment columnar mucosa in its comparison of patients were registered in 86% of patients after duodenal switch, before and several times after surgery. In each group at in 94% of patients after acid suppression and the duo- least 3 endoscopic and biopsy procedures were per- denal diversion procedure, and in 100% of patients after formed after surgery. Some patients were lost to follow- laparoscopic fundoplication. Visick grades III and IV cor- up, and all evaluations were performed only after 12 responded to patients with persistence of esophagitis or months of the operation. Mean follow-up varied from 54 with dumping syndrome. None of the patients showed to 106 months. Persistence of intestinal metaplasia after progression to low- or high-grade dysplasia or adeno- at least 3 endoscopic and histologic analyses was ob- carcinoma. served in a similar proportion of patients in each group (35%-39%), a finding that was not statistically significant (PϾ.7). Regression to cardiac or oxyntocardiac mu- COMMENT cosa occurred in 61% to 65% of the patients comparing all groups, without statistical significance (PϾ.58). The The results of the present prospective, nonrandomized time to regression varied from 39 to 56 months after sur- study suggest that in patients with short-segment BE who gery, without statistical significance (PϾ.11). undergo surgical treatment, laparoscopic Nissen fundo- Table 5 gives the Visick gradation months after sur- plication is the procedure of choice compared with the gery. We considered Visick grades I and II to be good other 2 more aggressive surgical procedures. In these pa- postoperative results, although Visick grade II corre- tients with short-segment BE, regression from intestinal sponded to patients who had to start taking proton pump metaplasia to cardiac or oxyntocardiac mucosa oc-

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©2009 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 10/02/2021 Table 4. Histologic Changes at the Columnar Mucosa in Patients With Short-Segment Barrett Esophagus

Acid Suppression— Laparoscopic Nissen Duodenal Switch Duodenal Diversion Fundoplication Histologic Change (n=31) (n=58) (n=36) P Value Mean follow-up, mo 106 76.3 54.3 Persistence of intestinal metaplasia, No. (%) 8 (36) 18 (35) 9 (39) Ͻ.70 Regression to cardiac mucosa or oxyntocardiac mucosa, No. (%) 14 (64) 34 (65) 14 (61) Ͻ.80 Time to regression, mo 55.7 39.2 48.8 Ͻ.11

Table 5. Visick Grading Months After Surgery in Patients With Short-Segment Barrett Esophagus

Acid Suppression— Laparoscopic Nissen Duodenal Switch Duodenal Diversion Fundoplication (n=22) (n=52) (n=23) Follow-up, mo 106.0 76.3 54.3 No. (%) of patients Visick grade I 15 (68.2) 46 (88.4) 17 (73.9) Visick grade II 4 (18.2) 3 (5.8) 6 (26.1) Visick grades III-IV 3 (13.6) 3 (5.8) NA

Abbreviation: NA, not applicable.

curred in nearly 60% of the patients, at a mean time of copy was reported in most patients. There was a loss of 50 months after the procedure. In addition, no progres- intestinal metaplasia in 56% of the patients at a period sion to low- or high-grade dysplasia occurred. of 30 months after surgery. The fourth report15 de- For most surgeons dedicated to the care of patients scribed 9 patients with short-segment BE who under- with BE, the surgical treatment is focused on the rees- went Nissen-Rossetti fundoplication, with a 67% regres- tablishment of the competence of the LES. Careful re- sion from intestinal metaplasia to squamous epithelium view of all publications concerning this topic9 shows that at a mean follow-up of 45 months. This finding is in- final results are usually shown in a mixed fashion. To our triguing because the regression of intestinal metaplasia knowledge, only 6 publications have focused their re- is to cardiac or oxyntocardiac mucosa and rarely to com- sults exclusively on patients with short-segment BE plete disappearance of the columnar mucosa and its re- (Table 6). placement by squamous epithelium. The strength of this The first report12 followed up 22 patients with short- study is the performance of complete functional stud- segment BE for 5 years, including another 9 patients who ies, which found that 42% of patients with BE had an ab- underwent mucosal thermal ablation. There was a loss normal acid reflux test result late after surgery. This study of intestinal metaplasia to cardiac or cardiac-fundic mu- showed again what we have pointed out several times: cosa in 59% of the patients. No mention of the time to control of symptoms does not happen parallel to the abol- regression was given. The main problems with this re- ishment of acid reflux. The fifth report16 described 11 pa- port are that the investigators performed only 1 postop- tients who underwent laparoscopic Nissen fundoplica- erative endoscopy plus biopsy in most patients and no tion. The follow-up is short (28 months after surgery), functional studies are reported. From the whole group and no functional studies were reported. In 6 patients (66 patients), including both patients with short- (55%) regression to cardiac mucosa occurred. The sixth segment and long-segment BE, moderate to severe gas- publication17 followed up 59 patients with short- troesophageal reflux disease symptoms were present in segment BE who underwent laparoscopic Nissen fundo- 35%, antisecretory medications were used in 27%, and plication. The criterion of the authors for regression was an additional operation was performed in 7 patients (11%). a decrease or disappearance of the columnar lined distal The second report13 includes 33 patients with short- esophagus, but no mention is made of loss of intestinal segment BE who mainly underwent laparoscopic Nis- metaplasia. No functional studies were reported. sen fundoplication. At least 2 postoperative endosco- In our study, we started to perform an acid suppres- pies and biopsies were performed. Regression from sion and duodenal diversion procedure for patients with intestinal metaplasia to cardiac mucosa occurred in 33% BE20 in 1987 based on the fact that the harmful refluxate of the patients, after a follow-up of 50 months. No func- material in the esophagus is composed mainly of gastric tional studies were reported. The third report was prob- and duodenal juice. Later, we included another type of ably the most complete study; it included manometric duodenal diversion19 for patients with BE, which in- and 24-hour pH monitoring evaluations before and af- cluded, besides the Roux-en-Y loop as part of the duo- ter surgery. The problems with this study were mainly denal switch, an antireflux procedure plus highly selec- the short endoscopic follow-up period (30 months after tive vagotomy. In 1995, we gradually incorporated surgery) and the fact that only 1 postoperative endos- laparoscopic Nissen fundoplication as the only surgical

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Regression of Intestinal Time to No. of No. of Antireflux Follow-up, Metaplasia, Regression, Postoperative Source Patients Procedure mo No. (%) mo Endoscopies Bowers et al,12 2002 22 Laparoscopic Nissen fundoplication 60 13 (59) NA 1 Gurski et al,13 2003 33 Laparoscopic Nissen fundoplication 50 11 (33) 50 2 Oelschlager et al,14 2003 54 Laparoscopic Nissen fundoplication 30 30 (56) 30 1 O’Riordan et al,15 2004 9 Laparoscopic Nissen-Rossetti fundoplication and open 45 6 (67) 45 2 Zaninotto et al,16 2005 11 Laparoscopic Nissen fundoplication 28 6 (55) 28 2 Biertho et al,17 2007 59 Laparoscopic Nissen fundoplication 50 NA NA 2 Csendes et al,18 2005 22 Duodenal switch 106 14 (64) 54 4 52 Acid suppression–duodenal diversion 76 34 (65) 38 3 23 Laparoscopic Nissen fundoplication 54 14 (61) 48 3

Abbreviation: NA, not applicable.

technique for these patients18 because it is much less laparoscopic Nissen fundoplication is the procedure of aggressive than the other 2 techniques and we had choice because it is less invasive, has fewer side effects, conquered the learning curve for the laparoscopic antire- and produces good results in long-term follow-up, reflux procedure. Besides, in a prospective, randomized trial sults that are similar to those found with other more ag- that compared the results of laparoscopic Nissen fundo- gressive surgical techniques. plication with calibration of the cardia with posterior gastropexy, we demonstrated similar late results at 10 years Accepted for Publication: July 22, 2008. of follow-up,22 which is why we adopted Nissen fundopli- Correspondence: Attila Csendes, MD, Department of Sur- cation as the antireflux procedure of choice. The careful gery, Clinical Hospital, University of Chile, Santos Dumont follow-up of all 125 patients who underwent these 3 pro- 999, Santiago, Chile ([email protected]). cedures that assessed subjective and objective variables Author Contributions: Study concept and design: Csendes showed that the results are similar comparing the 3 tech- and Braghetto. Acquisition of data: Braghetto, Smok, and niques, measured with symptomatic evaluations (Visick Henrı´quez. Analysis and interpretation of data: Csendes, grading), functional studies (manometric tests, 24-hour pH Braghetto, Burdiles, and Burgos. Drafting of the manu- monitoring, and 24-hour bile monitoring), and histologic script: Henrı´quez and Burgos. Critical revision of the manu- evaluations expressing the percentage of loss of intestinal script for important intellectual content: Csendes, Bur- metaplasia to cardiac or oxyntocardiac mucosa. diles, and Smok. Statistical analysis: Burgos. Administrative, Finally, the less aggressive surgical approach has shown technical, and material support: Smok and Henrı´quez. Study that laparoscopic Nissen fundoplication is the treat- supervision: Burdiles. ment of choice when dealing with the surgical treat- Financial Disclosure: None reported. ment of patients with short-segment BE. Patients with low-grade dysplasia were not included in this study and REFERENCES have been described elsewhere.21 As described recently 24 for patients with long-segment BE, none of our pa- 1. Falk GW. Barrett’s esophagus. Gastroenterology. 2002;122(6):1569-1591. tients who underwent the duodenal diversion proce- 2. DeMeester SR, Peters JH, DeMeester TR. Barrett’s esophagus. Curr Probl Surg. dure has developed high-grade dysplasia or adenocarci- 2001;38:549-640. noma, even after 120 months of follow-up. Although the 3. Navaraman RM, Winster MC. Barrett’s esophagus. Postgrad Med J. 1998;74:655- follow-up after Nissen fundoplication is shorter (54 657. 4. Spechler SJ. Barrett’s esophagus. N Engl J Med. 2002;346(11):836-842. months), we have not seen any progression among these 5. Cameron AJ. Management of Barrett’s esophagus. Mayo Clin Proc. 1998;73(5): patients. We need a longer follow-up to determine the 457-461. real effect of this technique. We ask other authors to re- 6. Spechler SJ. Barrett’s esophagus. Semin Oncol. 1994;21(4):431-437. port their results with a much longer follow-up (no stud- 7. DeMeester TR. Surgical therapy for Barrett’s esophagus: prevention, protection 1 and excision. Dis Esophagus. 2002;15(2):109-116. ies have more than 5 years, and 2 studies have only 2 ⁄2 8. Csendes A, Smok G, Quiroz J, et al. Clinical, endoscopic and functional studies years of follow-up) and to perform at least 3 postopera- in 408 patients with Barrett’s esophagus, compared to 174 cases of intestinal tive endoscopies in each patient and incorporate func- metaplasia of the cardia. Am J Gastroenterol. 2002;97(3):554-560. tional studies in their evaluations to determine by sev- 9. Csendes A. Surgical treatment of Barrett’s esophagus: 1980-2003. World J Surg. eral objective parameters the real long-term effect of 2004;28(3):225-231. 10. Csendes A, Burdiles P, Braghetto I, et al. Dysplasia and adenocarcinoma after Nissen fundoplication. We do not believe that a fol- classic antireflux surgery in patients with Barrett’s esophagus: the need for long- low-up by telephone or written questionnaire is an ad- term subjective and objective follow-up. Ann Surg. 2002;299:178-185. equate way to determine the late results of a particular 11. Csendes A, Burdiles P, Braghetto I, Korn O. Adenocarcinoma appearing very late surgical procedure, especially when dealing with pa- after antireflux surgery for Barrett’s esophagus: long-term follow-up, review of the literature and addition of six patients. J Gastrointest Surg. 2004;8(4):434-441. tients with BE. 12. Bowers SP, Mattar SG, Smith CD, Waring JP, Hunter JG. Clinical and histologic In conclusion, after we compared 3 different opera- follow-up after antireflux surgery for Barrett’s esophagus. J Gastrointest Surg. tions for patients with short-segment BE, we found that 2002;6(4):532-539.

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©2009 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 10/02/2021 13. Gurski RR, Peters JH, Hagen JA, et al. Barrett’s esophagus can and does regress 20. Csendes A, Burdiles P, Braghetto I, Korn O, Dı´az JC, Rojas J. Early and late re- after antireflux surgery: a study of prevalence and predictive features. sults of the acid suppression and duodenal diversion operation in patients with J Am Coll Surg. 2003;196(5):706-713. Barrett’s esophagus: analysis of 210 cases. World J Surg. 2002;26(5):566- 14. Oelschlager BK, Barreca M, Chang L, Oleynikov D, Pellegrini CA. Clinical and patho- 576. logic response of Barrett’s esophagus to laparoscopic antireflux surgery. Ann 21. Csendes A, Smok G, Burdiles P, Braghetto I, Castro C, Korn O. Effect of duode- Surg. 2003;238(4):458-466. nal diversion on low-grade dysplasia in patients with Barrett’s esophagus: analy- 15. O’Riordan JM, Byrne PJ, Ravi N, Keeling PW, Reynolds JV. Long-term clinical sis of 37 patients. J Gastrointest Surg. 2002;6(4):645-652. and pathologic response of Barrett’s esophagus after antireflux surgery. Am J 22. Csendes A, Burdiles P, Korn O, Braghetto I, Huertas C, Rojas J. Late results of a Surg. 2004;188(1):27-33. randomized clinical trial comparing total fundoplication versus calibration of the 16. Zaninotto G, Cassaro M, Pennelli G, et al. Barrett’s epithelium after antireflux surgery. cardia with posterior gastropexy. Br J Surg. 2000;87(3):289-297. J Gastrointest Surg. 2005;9(9):1253-1261. 23. Csendes A. Highly selective vagotomy, posterior gastropexy and calibration of 17. Biertho L, Dallemagne B, Dewandre J-M, et al. Laparoscopic treatment of Bar- rett’s esophagus: long-term results. Surg Endosc. 2007;21(1):11-15. the cardia. In: Jamieson N, ed. Surgery of the Esophagus. Edinburgh, Scotland: 18. Csendes A, Burdiles P, Korn O. Laparoscopic Nissen fundoplication: the “right Churchill Livingstone; 1998:273-281. posterior” approach. J Gastrointest Surg. 2005;9(7):985-991. 24. Csendes A, Braghetto I, Burdiles P, Smok G, Henrı´quez A, Parada F. Regression 19. Csendes A, Braghetto I, Burdiles P, Dı´az JC, Maluenda F, Korn O. A new physi- of intestinal metaplasia to cardiac or fundic mucosa in patients with Barrett’s ological approach for the surgical treatment of patients with Barrett’s esopha- esophagus submitted to vagotomy, partial gastrectomy and duodenal diver- gus: technical considerations and results in 65 patients. Ann Surg. 1997;226 sion: a prospective study of 78 patients with more than 5 years of follow up. (2):123-133. Surgery. 2006;139(1):46-53.

INVITED CRITIQUE Questions Regarding Surgery to Correct Short-Segment BE

arrett esophagus develops as a consequence of 3. Does loss of intestinal metaplasia eliminate the risk long-standing reflux of gastric juice into the of esophageal adenocarcinoma? B esophagus, and it is likely that continued 4. What is different about the intestinal metaplasia reflux drives the progression of BE to dysplasia and in the patients who lost it after surgery, and are these the adenocarcinoma. Both acid and bile have been impli- patients in whom BE would never have progressed any- cated in the development of BE, and increasingly there way (in other words, is persistence of intestinal meta- is evidence that the relative proportions of each and plasia a marker for a subtype of intestinal metaplasia that the resultant pH of the refluxed gastric juice may be is more likely to progress)? important in this process. In many patients, BE, once 5. Does the degree of reduction of reflux correlate with it develops, never progresses. However, an important the likelihood of regression? and unresolved issue is whether medical or surgical 6. How often does regression happen with incom- intervention can alter the natural history of BE such plete control of reflux? that progression does not occur in those in whom BE 7. Is control of acid, bile, or both the most important otherwise would have progressed. Regression or loss factor in regression of intestinal metaplasia? of intestinal metaplasia certainly suggests an alteration It is hoped that the answers to these and other ques- in the natural history, and Csendes and colleagues tions will come from continued clinical and laboratory report in this issue of the Archives of Surgery that there studies on this fascinating condition. was loss of intestinal metaplasia in approximately 60% of patients with short-segment BE after surgical cor- Steven R. DeMeester, MD rection of reflux. However, a number of important issues remain unanswered: Correspondence: Dr DeMeester, Department of Cardio- 1. Is intestinal metaplasia, once lost, gone forever? thoracic Surgery, 1510 San Pablo St, Ste 514, Los Ange- 2. When, if ever, can surveillance endoscopy be ter- les, CA 90033 ([email protected]). minated in patients who lost their intestinal metaplasia? Financial Disclosure: None resported.

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