This study analyzed 101 patients who underwent esophagectomy and gastric pull-up surgery for advanced achalasia over a mean follow-up of 10.5 years. The incidence of esophagitis and Barrett's epithelium in the esophageal stump increased significantly over time, with 70% of patients exhibiting esophagitis and 57.5% exhibiting Barrett's epithelium at 10 or more years post-surgery. Five patients developed cancer in the esophageal stump, including three squamous cell carcinomas and two adenocarcinomas. The development of these mucosal alterations is likely due to exposure of the esophageal stump to duodenogastric reflux and increasing gastric acid secretion over time.

1. Annals of Surgical Oncology 15(10):2903–2909
DOI: 10.1245/s10434-008-0057-1
Barrett’s Esophagus (BE) and Carcinoma in the Esophageal
Stump (ES) After Esophagectomy with Gastric Pull-Up in
Achalasia Patients: A Study Based on 10 Years Follow-Up
Julio Rafael Mariano da Rocha, MD, Ulysses Ribeiro Jr., MD,
´
Rubens A. A. Sallum, MD, Sergio Szachnowicz, MD, and Ivan Cecconello, MD
Department of Gastroenterology, University of Sao Paulo Medical School, Rua Oscar Freire, 1546 Apto 171,
˜
05409-010 Sao Paulo, SP, Brazil
˜
Background: Subtotal esophagectomy and gastric pull-up with cervical anastomosis is the
main treatment for advanced achalasia. This surgical technique has been associated to
esophagitis and also Barrett’s epithelium following esophagectomy.
Aim: To analyze late clinical, endoscopic, and pathologic findings in the esophageal stump
(ES) mucosa after subtotal esophagectomy in patients treated for advanced chagasic achalasia.
Methods: 101 patients submitted to esophagectomy and cervical gastroplasty were fol-
lowed-up prospectively for a mean of 10.5 ± 8.8 years. All patients underwent clinical,
endoscopic and histopathological evaluation every 2 years. Gastric acid secretion was also
assessed.
Results: The incidence of esophagitis in the esophageal stump (45.9% at 1 year; 71.9% at
5 years, and 70.0% at 10 years follow-up); gastritis in the transposed stomach (20.4% at
1 year, 31.0% at 5 years, and 40.0% at 10 or more years follow-up), and the occurrence of
ectopic columnar metaplasia and Barrett’s Esophagus in the ES (none until 1 year; 10.9%
between 1 and 5 years; 29.5% between 5 and 10 years; and 57.5% at 10 or more years follow-
up), all rose over time. Gastric acid secretion returns to its preoperative values 4 years post-
operatively. Esophageal stump cancer was detected in the setting of chronic esophagitis in five
patients: three squamous cell carcinomas and two adenocarcinomas.
Conclusion: (1) Esophagitis and Barrett’s esophagus in the esophageal stump rose over
time. (2) These mucosal alterations and the development of squamous cell carcinoma and
adenocarcinoma are probably due to exposure to duodenogastric reflux, and progressively
higher acid output in the transposed stomach.
Key Words: Achalasia—Megaesophagus—Barrett’s esophagus—Cervical esophageal stump
cancer—Esophagectomy.
Surgical techniques targeting the esophagogastric sents the main treatment for the advanced stage of this
junction (i.e., Heller myotomy and partial fundopli- disease.1 It is a safe procedure with acceptable mor-
cation) result in poor outcome in the treatment of ad- bidity and mortality, and reasonable postoperative
vanced form of chagasic achalasia.1 Esophagectomy outcome for benign disease.1,2 However, complica-
and gastric pull-up with cervical anastomosis repre- tions of both refluxates (gastric and duodenal-pan-
creatic) in the esophageal stump have been observed
Published online July 10, 2008. during long-term follow-up.3 This condition has been
Address correspondence and reprint requests to: Julio Rafael associated with esophagitis and also Barrett’s epithe-
Mariano da Rocha, MD; E-mail: jrmarian@terra.com.br lium following esophagectomy,4 and may serve as a
Published by Springer Science+Business Media, LLC Ó 2008 The Society of model of mucosal alterations study in the esophageal
Surgical Oncology, Inc.
2903

2. 2904 J. R. M. da ROCHA ET AL.
mucosa. We have previously demonstrated and re- entire stomach was utilized for gastric transposition
ported the presence of Barrett’s epithelium in the until January 1999, and a thin gastric tube (3.5 cm
esophageal cervical stump in adult patients.4–6 width) after this time. The mean length of the cervical
The pathophysiology of Barrett’s esophagus is not esophageal stump was 5 cm. Pyloroplasty was per-
completely known, but it is hypothesized to result from formed in all patients.
chronic reflux of acid and bile, which harm the
esophageal mucosa with the development of columnar
Clinical and Radiological Assessment
metaplasia with potentially premalignant phenotype.
Barrett’s metaplasia is common in the general popu- Before and after surgical treatment all the patients
lation and the risk of progression to dysplasia and were assessed by clinical, radiological, and endoscopic
cancer is 6–8 per 1,000 per year in individuals with long examinations. Postoperatively, clinical and endoscopic
segment (length >3 cm), demonstrating the need to evaluation was performed at 1 year, 5 years, and 10 or
better understand this entity and the mechanisms that more years after the operation. The following clinical
leads to its establishment and progression.7 parameters were studied: dysphagia, regurgitation,
Barrett’s esophagus following esophagectomy may heartburn, diarrhea, dumping syndrome, fasting gastric
be of relevance since it is possible to estimate the residues and body mass index (BMI).
duration of the reflux, as well as the amount and type
of refluxates in the stump.
Imaging Control
Additionally, it is noteworthy that the risk of
esophageal squamous cell carcinoma development is X-ray study of upper gastrointestinal tract and
increased in chagasic achalasia. The incidence varies gastric emptying time was studied before and after
from 1% to 8.6% and it is 33 times more frequent surgical treatment.
than in the general population.8
Thus, the aim of this investigation was to analyze
Endoscopic Assessment
late clinical, endoscopic, and pathologic findings in the
esophageal remnant mucosa after esophagectomy and Upper gastrointestinal endoscopy and also multi-
gastric pull-up with cervical anastomosis in patients ple esophageal and gastric biopsies were performed in
treated for advanced chagasic achalasia. We could all patients every 2 years. The presence of esophagitis
delineate the effects of the continuum refluxate on the (Savary–Miller grades 1–4), metaplastic columnar
esophageal stump mucosa resulting in esophagitis, mucosa, and/or Barrett’s esophagus was recorded, as
development of Barrett’s epithelium and carcinoma. well as the length of any esophageal columnar mu-
cosa in the esophageal stump. The presence of gas-
tritis, or bile in the transposed stomach was also
PATIENTS AND METHODS described.
From January 1977 to December 2005, 101 pa-
Gastric Acid Secretion Studies
tients with advanced chagasic achalasia (severe dys-
phagia, dilation greater than 7 cm, sigmoid Gastric acid secretion studies were performed on
esophagus, esophageal atony, and complications of 28 patients (6 and 48 months postoperative). Secre-
previous surgical therapies) were submitted to sub- tion was assessed by acid secretion test (basal secre-
total esophagectomy and gastric pull-up with pylo- tion and pentagastrin-stimulated maximum acid
roplasty. Fifty patients were men (49.5%), and mean output [MAO]).
age was 45.6 ± 12.5 years (range 17–75 years). The
patients were followed up prospectively for a mean of
Pathologic Assessment
10.5 ± 8.8 years (range 2–40 years).
This study was approved by the Research and Collected biopsies were stained by hematoxylin
Ethics Committee of the University of Sao Paulo
˜ and eosin (H&E) and the pathological results were
Medical School. reviewed by experienced pathologists. Columnar
epithelium in the esophageal remnant was defined by
Surgical Procedure the presence of esophageal columnar epithelium with
or without specialized intestinal metaplasia. Esoph-
A transhiatal subtotal esophagectomy with gastric agitis was graded histologically according to the
pull-up to the cervical region was performed. The established criteria.9
Ann. Surg. Oncol. Vol. 15, No. 10, 2008

3. ESOPHAGEAL STUMP CARCINOMA AFTER ESOPHAGECTOMY 2905
FIG. 2. Stomach in mediastinal position with elongated shape and
good passage of the contrast to the duodenum.
FIG. 1. Barium study of the upper gastrointestinal tract, showing a TABLE 2. Endoscopic findings after esophagectomy and
sigmoid esophagus with stasis of the contrast. gastric pull-up in 101 advanced chagasic achalasia patients
1 Year 5 Years 5–10 >10 Years
TABLE 1. Symptoms after esophagectomy and gastric (%) (%) Years (%) (%)
pull-up in 101 advanced chagasic achalasia patients Normal 53.6 41.6 23.0 29.9
Esophagitis 45.9 71.9 — 70.0
1 Year (%) 5 Years (%) >10 Years (%) Gastritis 20.4 31.1 — 40.0
Columnar epithelium 0 10.9 29.5 57.5
Dysphagia 21.8 9.2 6.8
Regurgitation 54.5 64.6 77.3
Heartburn 41.6 56.9 65.9
Diarrhea 30.3 10.1 0
Dumping syndrome 10.1 1 0
Weight gain 79.6 86.3 87.1 1-5 Ys 5-10 Ys 10-15 Ys
100
90
80
70
Statistical Analysis
60
Nonparametric data were analyzed using chi- 50
40
squared and Fisher’s exact test for contingency
30
tables, and the Wilcoxon’s test and Mann–Whitney 20
U-test were used to compare pre- and postoperative 10
findings. For parametric data, an unpaired t-test was 0
used for comparison of differences between means in Mild Moderate Severe
the groups. Statistical significance was endorsed by a FIG. 3. Grade of gastritis in 101 advanced chagasic achalasia pa-
P-value of less than 0.05. tients.
Ann. Surg. Oncol. Vol. 15, No. 10, 2008

4. 2906 J. R. M. da ROCHA ET AL.
TABLE 3. Gastric acid secretion studies on 28 advanced chagasic achalasia patients who had undergone esophagectomy with
gastric pull-up
Gastric acid BS BS 6 months BS 4 years MAO MAO 6 months MAO 4 years
output preoperative postoperative postoperative P value* preoperative postoperative postoperative P value*
Mean 1.23 1.02 1.43 0.035 16.25 8.59 14.44 0.043
Median 1.2 0.84 1.23 15 7.08 13.25
Standard deviation 0.801 1.035 0.96 8.00 6.89 8.31
Minimum 0.3 0.4 0.7 1.48 0 4.36
Maximum 3.9 3.83 4.48 37.44 29.44 35.4
* Wilcoxon nonparametric test; BS, basal secretion; MAO, pentagastrin-stimulated maximum acid output.
18
RESULTS
16
14
The indication for esophagectomy in this study 12
population was advanced chagasic achalasia, as 10
exemplified by Fig. 1. 8
Late clinical symptoms after esophagectomy and 6
gastric pull-up are shown in Table 1. 4
Complete postoperative resolution of the dyspha- 2
0
gic syndrome was obtained in all 44 patients fol- Pre-operative Post-operative Post-operative
lowed-up for 10 or more years (from 10 to 40 years) 6 months 48 months
except in three patients (6.82%) who still complained BS MAO
of mild dysphagia. Significant postoperative body
weight increase was also noted, particularly in those FIG. 4. Gastric acid secretion returns to normal preoperative
patients who exhibited preoperative larger body values after 4 years of surgical treatment (BS = basal/MAO); 28
patients.
weight deficit.
Postoperative diarrhea occurred frequently up to
1 year (30.3%), but it was of mild degree from the
third month on. There was a rapid resolution of this conditions (Table 3). Acidity recovery can be seen in
symptom after 1 year of postoperative follow-up and Fig. 4.
it was attributed to vagotomy and pyloroplasty. H2 blockers and, more recently, proton pump
Based on postoperative imaging studies, the inhibitors were administered in all patients in order to
stomach assumed an elongated shape with longitu- prevent peptic ulcer formation at the esophageal
dinal mucosal folds in mediastinal position (Fig. 2). remnant or transposed gastric tube. Nevertheless, the
Late endoscopic findings are demonstrated in use of such medications did not avoid the occurrence
Table 2. The prevalence of esophagitis increased after of Barrett’s esophagus, however, there was a ten-
the first postoperative year from 45.92% to 71.88% dency to delay the appearance and the size of
after 5 years, and 70.0% after 10 or more years columnar epithelium. In cases of more severe biliar
postoperatively. Thus, there was a steady rate of reflux (12.9%), bile binding agents, including cole-
esophagitis after 5 postoperative years (Table 2). stiramine were utilized sporadically.
There was also a significant increase in the grade of Thirty-six patients had developed columnar meta-
esophagitis severity over time. plasia during follow-up (Fig. 5). Among those,
Diffuse gastritis in the transposed stomach oc- intestinal metaplasia in the esophageal remnant was
curred at increased rate after 5 years of follow-up evident in 23 patients during follow-up (Fig. 6). The
(Fig. 3). The presence of bile at the esophageal rem- relationship between the presence of columnar
nant in these patients was evidenced by endoscopic metaplasia and intestinal metaplasia can be observed
examinations. in Fig. 7. Columnar metaplasia was detected in the
The severity of clinical symptoms did not relate to esophageal remnant in 11/101 (10.9%) of the patients
the worsening of esophagitis over time. followed-up between 1 and 5 years after surgery; 18/
Gastric acid secretion studies revealed the acidity 61 (29.5%) of the patients between 5 and 10 years
capacity of the gastric epithelium to return to pre- after surgery, and 23/40 (57.5%) followed-up 10 or
operative conditions, both in basal and stimulated more years after the operation.
Ann. Surg. Oncol. Vol. 15, No. 10, 2008

5. ESOPHAGEAL STUMP CARCINOMA AFTER ESOPHAGECTOMY 2907
FIG. 5. Metaplastic columnar mucosa in the esophageal stump. Red salmon color mucosa may be seen.
30 28,5
26,2
25
21,6
20
15
10,1
10 26.2
5
0 0 1
0
< 12 18-60 60-120 > 120
months months months months
Columnar Metaplasia Intestinal metaplasia
FIG. 7. Relationship between the columnar epithelium and the
presence of intestinal metaplasia.
Considering the 61 patients followed-up for 5 or
more years, 46 cases (75.4%) presented esophagitis
and three of those developed squamous cells carci-
noma in the esophageal stump. One of these cases
was a patient with in situ squamous cell carcinoma
bordering Barrett’s epithelium, detected 15 years
after the operation. The others were diagnosed in
advanced stage (inoperable), 22 and 34 years after
operation. These latter two patients had been lost to
FIG. 6. Histological appearance of the Barrett’s epithelium with follow-up for 8 or more years and returned for
the presence of specialized cells (intestinal metaplasia) (9400). evaluation due to severe dysphagia caused by an
advanced carcinoma in the esophageal stump.
Barrett’s esophagus was always preceded by Two of the patients with intestinal metaplasia in
esophagitis and was first observed at 1 year and the esophageal remnant (2/23), had developed high-
6 months postoperatively. grade dysplasia, 13 and 19 years after the operation.
There was a highly significant association between The close follow-up of these two patients have per-
the development of Barrett’s epithelium and the time mitted the diagnosis of in situ adenocarcinoma, 1 and
interval post esophagectomy. On the other hand, 3 years after the initial dysplasia identification,
there was no statistically significant association be- respectively (Fig. 8). They were treated successfully
tween esophagitis and age, sex, and body mass index by endoscopic mucosal resection and are still being
(data not shown). followed up now.
Ann. Surg. Oncol. Vol. 15, No. 10, 2008

6. 2908 J. R. M. da ROCHA ET AL.
time. (2) Increasing incidence of diffuse gastritis of
the transposed stomach, starting at 5 years follow-up
and more, significantly associated with esophagitis in
the esophageal remnant. (3) Development of squa-
mous cell carcinoma in three cases in the esophageal
remnant. (4) Development of in situ adenocarcinoma
in the esophageal remnant in two cases, treated suc-
cessfully by endoscopic resection.
The pathogenesis concerning these mucosal alter-
ations, could be explained by the following factors:
(1) resection of gastroesophageal transition; (2)
recovery of gastric acid secretion 4 years after sur-
gery; (c) higher serum gastrin levels, and simulta-
neous biliopancreatic and acid-peptic reflux to the
transposed stomach and esophageal remnant.4–6,14–19
In patients that underwent esophagectomy mainly
for cancer, O’ Riordan et al.18 reported a 50% inci-
FIG. 8. In situ adenocarcinoma in the Barrett’s epithelium of the
esophageal stump (9400). dence of columnar metaplasia above the anastomosis
in 48 postesophagectomy patients, with a median
follow-up of 26 months (range 12–67 months). Spe-
DISCUSSION cialized intestinal metaplasia was detected in 54% of
those patients. The prevalence of columnar meta-
Esophagectomy and gastric pull-up with cervical plasia did not relate to the magnitude of acid or bile
anastomosis is currently the procedure of choice in reflux, to preoperative neoadjuvant therapies, or to
the management of advanced chagasic achalasia.1,2 the original tumor histology. However, the duration
Nonetheless, this type of reconstruction after esoph- of the reflux was the most significant parameter, with
ageal resection causes modifications in anatomy and increasing prevalence over time. The authors con-
physiology on the upper gastrointestinal tract.10–12 cluded that the duration of acid and bile reflux, ra-
Gastric and duodenal refluxate have been docu- ther than the volume of reflux, underlies the
mented in 60–80% of esophageal resected patients.12 development of metaplasia.
In 1991 and 1992 we reported the presence of Bar- In the present investigation, we did not find any
rett’s epithelium developed in the esophageal stump Barrett’s esophagus until 1 year and 6 months of
of chagasic achalasia patients.4–6 Resection or dis- follow-up; at 2 years of follow-up we could detect
ruption of natural antireflux mechanisms, esopha- only 1/101 patient (0.98%) with Barrett ‘s esophagus;
geal-gastric direct anastomosis, pyloroplasty, however the incidence of Barrett’s rose to 11.2% in
impairment of gastric motility, recovery of acid 5 years and 57.5% in 10 or more years of follow-up.
secretion from gastric conduit, and impaired motility The Barrett’s incidence may be lower in this investi-
of esophageal remnant all contribute to esophageal gation because chagasic achalasia patients have
stump mucosal damage.10–13 decreased preoperative gastric acid secretion.20
We sought in this study to evaluate the impact of It is well known that bile salts injure both the
long-term continuous refluxate in the esophageal gastric and the esophageal mucosa and their harmful
stump mucosa. effects are strengthened by the action of gastric
Barrett’s esophagus might occur in the esophageal secretion.3,11–13 The latter mechanism seems to be
remnant in the cases of chronic esophagitis of long- responsible for esophagitis in the esophageal rem-
standing duration.4–6,14–19 This hypothesis was con- nant, similar to what occurs in patients with reflux
firmed with the endoscopic diagnosis and histologic esophagitis and Barrett’s esophagus with the organ in
proof of the existence of Barrett’s esophagus in the the normal position.
remaining cervical esophagus. Barrett’s esophagus in the esophageal cervical
Long-term follow-up has revealed complications stump begins with columnar type epithelium, between
that, if adequately treated, do not influence the clin- 18 and 60 months and generally changes to intestinal
ical outcome, but lead to a number of concerns: (1) pattern between 5 and 10 years. The length of Bar-
Increasing incidence of esophagitis and Barrett’s rett’s esophagus varies between 1 and 4 cm and often
esophagus in the esophageal cervical stump over appears in a fingerlike form. Barrett’s esophagus is
Ann. Surg. Oncol. Vol. 15, No. 10, 2008

7. ESOPHAGEAL STUMP CARCINOMA AFTER ESOPHAGECTOMY 2909
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