Diseases of the Esophagus (2020)00,1–9

DOI: 10.1093/dote/doaa060

Original Article

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Comparison of Esophagectomy outcomes between a National Center, a National
Audit Collaborative, and an International database using the Esophageal
Complications Consensus Group (ECCG) standardized definitions

John V. Reynolds,1 Noel Donlon,1 Jessie A. Elliott,1 Claire Donohoe,1 Narayanasamy Ravi,1 Madhan Kumar
Kuppusamy,2 Donald E. Low2
1
National Esophageal and Gastric Cancer Center, St James’s Hospital and Trinity College, Dublin, Ireland, and
2
Virginia Mason Medical Center, Seattle, WA, USA

SUMMARY. The ECCG developed a standardized platform for reporting operative complications, with consensus
definitions. The Dutch Upper Gastrointestinal Cancer Audit (DUCA) published a national comparison against
these benchmarks. This study compares ECCG data from the Irish National Center (INC) with both published
benchmark studies. All patients undergoing multimodal therapy or surgery with curative intent from 2014 to 2018
inclusive were studied, with data recorded prospectively and entered onto a secure online database (Esodata.org).
219 patients (mean age 67; 77% male) underwent open resection, 66.6% via transthoracic en bloc resection. 30-
day and 90-day mortality were 0.0 and 0.9%,nrespectively. Anastomotic leak rate was 5.4%, pneumonia 18.2%,
respiratory failure 10%, ARDS 2.7%, atrial dysrhythmia 22.8%, recurrent nerve injury 3%, and delirium in 5%
of patients. Compared with both ECCG and DUCA, where MIE constituted 47 and 86% of surgical approaches,
respectively, overall complications were similar, as were severity of complications; however, anastomotic leak rate
was several-fold less, and mortality was significantly lower (P < 0.001). In this consecutive series and comparative
audit with benchmark averages from the ECCG and DUCA publications, a low mortality and anastomotic leak
rate were the key differential findings. Although not risk stratified, the severity of complications from this ‘open’
series is consistent with series containing large numbers of total or hybrid MIE, highlighting a need to adhere to
these strictly defined definitions in further prospective research and randomized studies.
KEY WORDS: esophageal cancers, esophagectomy, complications.

INTRODUCTION In the CROSS RCT, for instance, respiratory com-

Surgery for cancer of the esophagus and the esoph-
agogastric junction (EGJ) is an exemplar model of
complex major surgery, with relatively high risks
of major morbidity and mortality.1,2 Operative
mortality has decreased markedly in recent decades,
reflecting perhaps an increased concentration of
surgery in high-volume centers, and recent RCTs
suggest a mortality rate of less than 4% as a
modern benchmark.3,4 Notwithstanding reduced
mortality, and the advent of minimally invasive (MIE)
and robotic-assisted approaches, complication rates
appear to remain high, irrespective of approach, with
associated significant costs, resource requirement, a
protracted impact on health-related quality of life,
and possible link to adverse oncologic outcomes.5–8
plications were observed in 45% of patients, cardiac
arrhythmias in 19%, and anastomotic leaks in 26%.4
At this time, consequently, there is an increased
attention on specific complications, their cause,
prevention, and management.9
In this context, a barrier existed up to recently due
to the lack of a consistent lexicon to define compli-
cations, with specific complications often not defined
at all, or variable terms utilized.10 To enable research
in this area, and comparison with published studies,
and national and international comparative audit and
benchmarking, the Esophageal Complications Con-
sensus Group (ECCG) was established in 2011. Stan-
dardized definitions were initially agreed following a
Delphi survey and consensus among 21 high-volume

Address correspondence to: John V. Reynolds, Trinity Centre, St. James’s Hospital, Dublin 8, Ireland. Email: reynoljv@tcd.ie
Conflicts of interest: The authors declare no conflict of interest.
Funding: None declared.

© The Author(s) 2020. Published by Oxford University Press on behalf of International Society for Diseases of the Esophagus. All rights
reserved. For permissions, please e-mail: journals.permissions@oup.com 1
2 Diseases of the Esophagus
academic centers across 14 countries. The Esodata
(Esodata.org) collaboration evolved from such an ini-
tiative, creating an enormously powerful dataset of
contemporary international practice and outcomes.11
The ECCG definitions are already established nation-
ally within the Dutch Upper Gastrointestinal Can-
cer Audit (DUCA) and are being used in current
RCTs. 12,13
There are two major publications that utilize
the ECCG definitions. In the first, a benchmark
study from the original ECCG consortium, which
represents a 2-year study of 2,704 patients from 24
centers, 52.1% with open and 47.9% undergoing
MIE approaches, the reported rate of pneumonia
was 14.6%, atrial dysrhythmia 14.5%, and 11.4%
for anastomotic leaks, with a 30-day mortality of
2.4% and 4.5% for 90-day mortality.14 The second
report, from DUCA, included 1,617 patients from
22 hospitals, with 86% treated by MIE. Pneumonia
was reported in 21%, atrial dysrhythmia in 15%,
anastomotic leaks in 19%, and 30-day and 90-day
mortality was 1.7 and 2.4%, respectively.12 In Ireland,
centralization of esophageal cancer surgery was
established in 2014, with four designated centers,
including this National Center (INC) that uniquely
in Ireland has utilized ECCG-defined data from the
outset.
The primary objective was to evaluate the value of
the ECCG standardized definitions as an audit tool
through comparative analysis with both the ECCG
benchmark publication and the DUCA study. We
sought insight into key complications, in particular,
anastomotic leak rates and pneumonia, as well as
grading and severity of complications and assessment
of validity of specific ECCG complication definitions,
with implications from this open INC surgical series
for benchmark complication reporting in an increas-
ingly minimally invasive era.
METHODS
Patients undergoing esophageal resection at St.
James’s Hospital, Dublin, the designated Irish
National Esophageal and Gastric Center (INC)
between January 2014 and December 2018, were
prospectively studied. For locally advanced esophageal
and EGJ adenocarcinoma (AEG type I and II),
preoperative chemoradiation [cisplatin, fluorouracil
and 40-44Gy] or the CROSS protocol of carboplatin,
paclitaxel, and 41.4 Gy was used.4 Some patients
received etoposide, cisplatin or oxaliplatin, and
fluorouracil or capecitabine.15 Most surgery was
an open en bloc esophagectomy including a right
thoracotomy, with intrathoracic or cervical anas-
tomosis. A transhiatal esophagectomy (THE) was
considered for patients with cT1–2 N0 disease at the
EGJ where an en bloc resection and lower mediastinal
lymphadenectomy could be performed or for those
with multifocal in situ cancer. It was also considered
for higher risk operative cases, mainly due to respira-
tory morbidity and concern of tolerance of one lung
anesthesia, or age, in particular over 80. All cases had
a pyloroplasty. Patients with AEG type III tumors
were excluded unless they underwent a transthoracic
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resection due to extensive esophageal involvement.
Salvage cases were excluded. Data are prospectively
recorded in a database (Dendrite, London, UK),
which is maintained by a full-time data manager
who abstracts all relevant clinical, radiologic, and
pathologic data from electronic records and files and
attends weekly meetings of the multidisciplinary team
where all current surgical complications are recorded.
ECCG definitions have been used since 2014 in addi-
tion to our institution data sets and registered with
Esodata.org since January 2015. IRB approval was
obtained.
Patients are risk assessed with pulmonary function
testing, echocardiogram, and a preoperative assess-
ment by both a specialist anesthetist and a physio-
therapist. Patients with major respiratory or cardiac
disease, such as severe chronic obstructive pulmonary
disease (COPD), pulmonary fibrosis, cardiac failure,
cardiomyopathy, with impairment at rest or limited
exercise tolerance, are precluded from surgery, as are
patients with decompensated liver disease.
The standard protocol includes a thoracic epidu-
ral, and relative intraoperative fluid restriction, at
approximately 500 mL/hour. All intrathoracic and
cervical anastomoses are sutured using a standardized
approach with one layer of interrupted 3.0 PDS
(polydioxanone) sutures (Ethicon, Johnson & John-
son, Dublin). Patients are extubated immediately
after surgery and managed in ICU for a minimum
of 24 hours before transfer to a specialist surgical
ward. All patients are fed via jejunostomy from
day 1. Early mobilization from POD1 is overseen
and progressed on successive days. A water-soluble
contrast swallow is performed on POD4 in all patients
with a thoracic anastomosis. Where the anastomosis
is cervical, swallowing is assessed on POD4 by a
speech and language therapist, complimented by
video fluoroscopy if there is concern of aspiration.
Where a leak is suspected, a CT scan with oral
contrast is obtained and an endoscopic assessment
made in most cases. All other complications were
recorded as defined in the ECCG, as well as in the
Clavien–Dindo score of severity of complications.16
STATISTICAL ANALYSIS
Statistical analysis was performed using SPSS® (ver-
sion 18.0) software (SPSS, Chicago, IL, USA). The
INC series was compared separately with the ECCG
data which were collected between January 2015 and
 Use of ECCG definitions for comparative audit 3

Table 1 Patient demographics and operative data

INC ECCG P DUCA P

n = 219 n = 2,704 n = 1,617

Sex
Female 51 23.3% 607 22.4% 0.777 388 24% 0.818
Male 168 76.7% 2,096 77.5% 1,228 76%

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Unknown 0 0.0% 0 0.0& 1 0.1%
Age group, years
< 40 6 2.7% 66 2.4% 0.823 6 0.3% <0.0001
41–50 19 8.6% 217 8.0% 76 4.7%
51–60 63 28.8% 721 26.7% 316 19.6%
61–70 78 35.7% 1,100 40.7% 739 45.6%
71–80 47 21.5% 532 19.7% 451 28%
> 80 6 2.7% 67 2.5% 29 1.8%
BMI†
<18.5 3 1.3% 184 6.8% 0.0002 47 2.9% 0.003
18.5–25 66 30.2% 1,085 40.1% 657 40.6%
25–30 94 42.9% 908 33.6% 642 39.7%
>30 50 22.9% 526 19.5% 265 16.4%
Unrecorded 6 2.7% 0 0% 6 0.4%
ASA status score
1 15 6.8% 412 15.2% 0.321 255 15.8% <0.0001
2 127 58.0% 1,249 46.2% 1,012 62.6%
3 77 35.2% 992 36.7% 340 21.1%
4 0 0% 49 1.9% 7 0.4%
5 0 0% 1 0% 0 0%
Tumor location
OG Junction and distal 180 82.2% 2,281 84.4% 0.009 1,348 83% 0.321
Proximal half esophagus 39 17.8% 304 11.2% 241 15%
Fundus 0 0 18 1.1%
Surgical Approach
Open 219 100% 1,407 52.1% <0.0001 229 14% <0.0001
Minimally Invasive 0 0% 1,296 47.9% 1,388 85.8%
Open esophagectomy
Transhiatal 73 33.3% 283 20.1% <0.0001 109 47.6% 0.002
Transthoracic 146 66.6% 1,124 79.9% 120 52.4%
Resection Margins
R0 206 94.0% 2,414 93.4% 0.697 1,532 95.4% 0.219
R1 13 6.0% 157 6.1% 65 4.1%
R2 0 0% 14 0.5% 1 0.5%

†P-values reported for BMI <25 versus 25–30 versus >30; ASA 1–2 versus 3–5; OG junction, distal esophagus and fundus versus upper
esophagus; R0 versus R1–2

December 2016, and the DUCA series collected from
January 2016 to December 2017. A significance level
of 0.05 was used for all analyses, and all P values
reported are two tailed. Association of categorical
variables was assessed using χ 2 test or Fisher’s exact
test where appropriate.
RESULTS
Patient demographics and operative comparisons
In total, 219 patients underwent an esophageal
resection for cancer during this 5-year period, 76.7%
male, with a median (range) age of 67 (24–86), 53
(24.2%) were over 70; 77 patients (35.2%) were ASA 3,
19% had COPD, 16% had a cardiac history, and 9.6%
had diabetes mellitus. All patients had open surgery,
146 (66.6%) via en bloc transthoracic resection, 103
(70.5%) of these having a thoracic anastomosis.
A third of cases had THE. The R0 rate was 94%
(Table 1).
In comparison with ECCG, the age and
co-morbidity profile was similar, with 35% and 37%
being ASA 3 in INC and ECCG, respectively. Obesity
was evident in 22.9%, with 65.8% overweight or
obese, compared with 19.5 and 63%, respectively
(P = 0.0002). In the DUCA series, the ASA 3 and
obesity rates were significantly (P < 0.001) less, at
19.5 and 16.4%, respectively, and the median age
was significantly higher. In all studies, over 80% of
resections were for tumors in the distal half of the
esophagus or the esophagogastric junction. About,
27, 21, and 7% underwent upfront surgery in the INC,
ECCG, and DUCA series, respectively. In the ECCG
data, 46% underwent neoadjuvant chemoradiation
and 30% perioperative chemotherapy, compared with
88 and 5%, respectively, in DUCA, and 42 and 28%,
respectively, in the Irish cohort.
Complications
Comparing the INC, ECCG, and DUCA, 54, 59
and 65%, respectively, experienced a postoperative
4 Diseases of the Esophagus
Table 2 Incidence of ECCG complications
Complications† INC
n = 219
No 101 46%
Yes 118 54%
0 101 46.1%
1 49 22.4%
2 29 13.2%
3 16 7.3%
4 or more 24 11%
†Incidence of complication as per ECCG complication platform definitions
complication. In a direct comparison with ECCG
data (Table 2), 46.6 and 41% experienced no compli-
cation (P = 0.138) and 18.3 and 18.5% experienced
three or more complications, respectively (P = 0.431)
Using the ECCG definitions, Table 3 shows the
differences between groups. Gastrointestinal compli-
cations were significantly (P < 0.001) less in the INC
group, in particular, the leak rate from the anasto-
mosis, staple line or localized conduit necrosis, the
incidence was 5.4% (12/219) in the INC, 11.4% in
the ECCG series, and 19% in DUCA. In this series,
nine were in thoracic anastomoses, an 8% rate, with
two cases presenting on readmission after 30 days,
and three in cervical anastomoses, a 2.5% leak rate.
For INC, ECCG, and DUCA, respectively, conduit
failure was seen in 1.3, 1.3, and 1%, and chyle leak in
5.4, 4.7, and 8.6%. Delayed gastric emptying requiring
intervention was not observed in the INC compared
with 6.7% in the ECCG (P < 0.0001) and 1.7% in the
DUCA populations (P = 0.999).
The recorded pneumonia rate was similar, at 18.2%
in the INC, compared with 14.6% in ECCG and
21.1% in DUCA series. The ARDS/respiratory failure
rates were 2.7%/10% in INC, significantly (P = 0.041)
higher than 1.8%/7% for ECCG, and 1.5%/5.2% for
DUCA (P < 0.05). Pleural effusions were drained in
15, 9.9, and 7.7% of INC, ECCG, and DUCA cohorts,
respectively (P = 0.002). Atrial dysrhythmia was sig-
nificantly (P < 0.05) higher at 22.8% in the INC com-
pared with 14.5 and 13.9% for ECCG and DUCA,
respectively, as was sepsis (P < 0.05) at 5.9, 1.9, and
1.1%, respectively, and multisystem organ failure at 4,
1, and 0.1%, respectively. The 30-day readmission was
10, 11 and 15% in the INC, ECCG, and DUCA series,
respectively.
Complications with level of complexity defined as per
ECCG
The low rate of most specific complications precludes
statistical analysis due to insufficient numbers of
observations. For leak rates, occurring in 5.4% of
cases, 45% required no intervention, 45% requiring
drainage by interventional radiology, and just one
patient required surgery, with an overall reoperation
ECCG P
n = 2,704
1,108 41% 0.138
1,595 59%
1,108 41.0% 0.431
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689 25.5%
405 15.0%
238 8.8%
262 9.7%
rate of 0.4%, and conduit necrosis rate of 0.4%. This
contrasts with 3 and 0.9%, respectively, for the ECCG
report and 5.1 and 0.6%, respectively, in the DUCA
series (Table 4).
For chyle leak, in the INC, ECCG, and DUCA
series, a leak occurred in 5.5, 4.7, and 8.6%, respec-
tively, with type III, requiring interventional or sur-
gical therapy, 0.4, 1.1, and 1.3%, respectively. The
incidence of recurrent nerve injury in this series was
3.2%, with five patients (2.2%) undergoing a thyro-
plasty. This compared with 4 and 4.3% rate in the
ECCG and DUCA series, with 0.2 and 0.1% under-
going a surgical intervention.
Complication severity as per Clavien-Dindo
In the INC data, 53.9% patients suffered a complica-
tion, significantly less (P < 0.001) compared with 59%
for ECCG and 67% for DUCA, respectively. Clavien–
Dindo ≥III was 30.9%, and ≥ IIIb was 14.9%, com-
pared with 31.1 and 16.9% for ECCG, and 30, and
18% for DUCA (P = ns). In the INC series, there
was no 30-day mortality, and two patients (0.9%)
died between 30 and 90 days, this was significantly
(P < 0.05) different than ECCG 30-day mortality of
2.4% and 4.5% within 90 days. For DUCA, this was
1.7% for 30-day mortality and 2.4% for 90-day mor-
tality, with no significant difference. The 30-day read-
mission rate was 10, 10.2, and 15% in the INC, ECCG,
and DUCA series, respectively (P = ns) (Table 5).
DISCUSSION
The ECCG consensus represents major progress in
the standardized reporting of complications for the
complex operation of esophageal cancer resection,
with enormous potential value for national and
international benchmarking of data, clinical trials,
and clinical research. This focus on strict definitions
is particularly required at a time where minimally
invasive approaches, or hybrid techniques, and
robotic-assisted surgery, is evolving rapidly, and where
the evidence-base will largely focus on a reduction in
complication rate and recovery of quality of life. This
report from a well-structured academic high-volume
 Use of ECCG definitions for comparative audit 5

Table 3 Incidence of complications according to the ECCG definitions

Complication Groups INC ECCG P DUCA P

Gastrointestinal 25 11.4% 606 22.4% 0.001 392 24.2% <0.0001

Esophagogastric leak from anastomosis, 12 5.4% 307 11.4% 0.007 307 19% <0.0001
staple line or localized conduit necrosis
Conduit necrosis/failure 3 1.3% 34 1.3% 0.754 13 1% 0.426

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Ileus requiring intervention 1 0.4% 46 1.7% 0.257 12 1% 0.999
Small bowel obstruction 3 1.3% 12 0.4% 0.097 4 0.3% 0.041
Feeding J-tube complication 2 0.9% 27 1.0% 0.999 55 3.4% 0.058
Pyloromyotomy/pyloroplasty complication 1 0.4% 5 0.2% 0.374 6 0.4% 0.590
Clostridium difficile infection 1 0.4% 23 0.9% 0.999 2 0.1% 0.317
Pancreatitis 2 0.9% 8 0.3% 0.169 3 0.2% 0.111
GI bleeding requiring intervention or 0 0.0% 21 0.8% 0.399 1 0.06% 0.999
transfusion
Liver dysfunction 4 1.8% 6 0.2% 0.005 5 0.3% 0.015
Delayed gastric emptying requiring 0 0.0% 180 6.7% <0.0001 7 1.7% 0.999
intervention or delaying discharge or
requiring maintenance of NG drainage
>7 days post-op
Pulmonary 69 31.5% 752 27.8% 0.243 529 32.7% 0.358
Pneumonia 40 18.2% 396 14.6% 0.149 341 21.1% 0.334
Pleural effusion requiring additional 33 15.0% 267 9.9% 0.015 124 7.7% 0.0002
drainage procedure
Pneumothorax requiring intervention 2 0.9% 91 3.4% 0.044 68 4.2% 0.013
Atelectasis mucous plugging requiring 6 2.7% 85 3.1% 0.740 18 11.1% 0.047
bronchoscopy
Respiratory failure requiring reintubation 22 10% 189 7.0% 0.041 84 5.2% 0.002
Acute respiratory distress syndrome 6 2.7% 27 1.8% 0.033 24 1.5% 0.159
Acute aspiration 3 1.3% 27 1.0% 0.488 25 1.6% 0.999
Tracheobronchial injury 2 0.9% 11 0.4% 0.254 11 0.7% 0.662
Chest tube drainage for >10 days post-op 1 0.4% 13 0.5% 0.999 11 0.7% 0.999
Cardiac 51 23.3% 455 16.8% 0.020 276 17.1% 0.030
Cardiac arrest requiring CPR 2 0.9% 28 1.0% 0.999 9 0.6% 0.631
Myocardial infarction 1 0.4% 28 0.6% 0.720 5 0.3% 0.534
Atrial dysrhythmia requiring intervention 50 22.8% 393 14.5% 0.002 224 13.9% 0.0008
Ventricular dysrhythmia requiring 0 0.0% 15 0.9% 0.621 23 1.4% 0.100
intervention
Congestive heart failure requiring 1 0.4% 25 0.4% 0.717 17 1.1% 0.713
intervention
Pericarditis requiring intervention 1 0.4% 12 0.1% 0.999 3 0.2% 0.399
Thromboembolic 5 2.3% 141 5.2% 0.053 45 2.8% 0.826
DVT 2 0.9% 25 0.9% 0.999 4 0.2% 0.154
PE 2 0.9% 33 1.2% 0.999 35 2.2% 0.306
Stroke 1 0.4% 4 0.1% 0.323 1 0.06% 0.224
Peripheral thrombophlebitis 0 0.0% 79 2.9% 0.004 4 0.25% 0.999
Urologic 18 8.2% 224 8.3% 0.999 66 4.1% 0.009
Acute renal insufficiency 11 5.0% 39 1.4% 0.0009 11 0.7% <0.0001
Acute renal failure requiring dialysis 6 2.7% 24 0.9% 0.021 5 0.3% 0.0007
Urinary tract infection 1 0.4% 68 2.5% 0.060 20 1.2% 0.501
Urinary Retention requiring reinsertion of 0 0.0% 104 3.8% 0.0004 32 2% 0.026
urinary catheter; delaying discharge or
discharge with urinary catheter
Infection 28 12.8% 383 14.2% 0.615 120 7.4% 0.011
Wound infection requiring opening wound 9 4.1% 20 0.7% 0.0002 37 2.3% 0.108
or antibiotics
Central IV line infection requiring removal 6 2.7% 55 2.0% 0.458 10 0.6% 0.008
or antibiotics
Intrathoracic/intra-abdominal abscess 5 2.3% 65 2.4% 0.999 37 2.3% 0.999
Generalized sepsis as per CDC definition 12 5% 52 1.9% 0.002 17 1.1% <0.0001
Other infections requiring antibiotics 6 2.7% 227 8.4% 0.002 20 1.2% 0.116
Neurological/psychiatric complications 28 12.8% 254 9.4% 0.121 172 10.6% 0.355
Recurrent laryngeal nerve injury 7 3.1% 114 4.2% 0.597 70 4.3% 0.589
Acute delirium 11 5.0% 105 3.9% 0.370 97 6% 0.648
Delirium tremens 3 1.3% 16 0.6% 0.166 2 0.1% 0.014
Other neurologic injury 0 0.0% 33 1.2% 0.172 10 0.6% 0.619
Wound/diaphragm complications 3 1.4% 78 2.9% 0.280 30 1.9% 0.790
Thoracic wound dehiscence 0 0.0% 40 1.5% 0.070 16 1% 0.243
Acute abdominal wall dehiscence/hernia 2 0.9% 33 1.2% 0.999 7 0.4% 0.293
Acute diaphragmatic hernia 1 0.4% 8 0.3% 0.505 7 0.4% 0.999
Other complications 24 11.0% 185 6.8% 0.029 138 8.5% 0.252
Chyle leak 12 5.4% 128 4.7% 0.620 139 8.6% 0.148
Reoperation for reasons other than bleeding, 7 3.1% 39 1.4% 0.080 17 1.1% 0.018
anastomotic leak or conduit necrosis
Multisystem organ failure 9 4.1% 27 1.0% 0.001 2 0.1% <0.0001
Table 4 Complication definitions summary

INC ECCG DUCA

Anastomosis leak Grade

Definition: full thickness GI No leak 208 95.0% 2,403 88.9% 1,310 81%
defect involving esophagus, Type I: local defect requiring no change in therapy or 5 2.3% 90 3.3% 92 5.7%
anastomosis, staple line, or treated medically or with dietary modification
6 Diseases of the Esophagus

conduit irrespective of Type II: localized defect requiring interventional but not 6 2.7% 131 4.8% 131 8.1%
presentation or method of surgical therapy
identification Type III: localized defect requiring surgical therapy 1 0.4% 80 3.0% 83 5.1%
Conduit necrosis/failure Grade
Definition: postoperative No conduit necrosis 216 98.6% 2,672 98.8% 1,604 99.2%
identification of conduit Type I: conduit necrosis foal identified endoscopically 2 0.9% 2 0.1% 1 0.1%
necrosis (Treatment—additional monitoring or non-surgical therapy)
Type II: conduit necrosis focal identified endoscopically 0 0% 7 0.3% 3 0.2%
& not associated with free anastomotic or conduit leak
(Treatment—surgical therapy not involving esophageal diversion)
Type III: Conduit necrosis extensive 1 0.4% 23 0.9% 9 0.6%
(Treatment—treated with conduit resection with diversion)
Recurrent laryngeal nerve Grade
injury involvement
Definition: vocal cord No recurrent laryngeal nerve injury 212 96.8% 2,595 96.0% 1,547 95.7%
dysfunction postresection. Type I: transient injury requiring no therapy 1 0.4% 87 3.2% 61 3.8%
Confirmation & assessment Type II: injury requiring elective surgical procedure, for 1 0.4% 16 0.5% 5 0.3%
should be by direct example, thyroplasty or medialization procedure
examination Type IIIa: unilateral injury requiring acute surgical 5 2.2% 2 0.1% 0 0%
intervention (due to aspiration or respiratory issues), for
example, thyroplasty or medialization procedure
Type IIIb: bilateral Injury requiring acute surgical 0 0% 4 0.1% 1 0.1%
intervention (due to aspiration or respiratory issues); for
example; thyroplasty or medialization procedure
Chyle leak severity Grade
Definition: milky discharge No chyle leak 207 94.5% 2,578 95.3% 1,478 91.4%
upon initiation of enteric Type Ia: <1 L output, Treatment—enteric dietary 3 1.3% 67 2.5% 68 4.2%
feeds and/or pleural fluid modifications
analysis demonstrating Type Ib: >1 L output, Treatment—enteric dietary 0 0% 10 0.4% 3 0.2%
triglyceride level > 100 mg/dL modifications
and/or chylomicrons in Type IIa: <1 L output, Treatment—total parenteral 7 3.2% 11 0.4% 14 0.9%
pleural fluid nutrition
Type IIb: >1 L output, Treatment—total parenteral 1 0.4% 6 0.2% 8 0.5%
nutrition
Type IIIa: <1 L output, Treatment—interventional or 0 0% 12 0.4% 2 0.1%
surgical therapy
Type IIIb:>1 L output, Treatment—interventional or 1 0.4% 20 0.7% 19 1.2%
surgical therapy

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Table 5 Clavien–Dindo classification of surgical complications
Complication severity INC ECCG
No complication 101 46.1% 1,108
Grade I 10 4.5% 203
Grade II 42 19.1% 551
Grade IIIa 33 15.0% 384
Grade IIIb 5 2.2% 178
Grade IVa 16 7.3% 173
Grade IVb 10 4.5% 36
Grade V (30 day) 0 0% 65
Grade V (90 day) 2 0.9% 121
Grade ≥ IIIb 33 15 508
designated national center, with exclusively open sur-
gical approaches, represents a contemporary opportu-
nity to compare and contrast with the original ECCG
benchmark series of 2,704 patients from 24 hospitals
and 1,607 patients from 22 hospitals in the Nether-
lands within DUCA, and to also seek a broader
interpretation with respect to modern international
standards of care.
All series reflect modern practice from high-
volume centers, with low mortality, yet complications
still occur in over 50% of patients. The most dreaded
outcome in surgery is a postoperative death, followed
arguably by an anastomotic leak or gastric conduit
necrosis, which may represent a failure of technique.
Prior systematic reviews of the literature pre-1980,
from 1980–1988, and from 1990–2000 reported
mortality rates of 29, 13, and 6.7%, respectively.17–19
A modern benchmark may be 4% or less.4 In this
INC series, no 30-day mortality was observed and
two deaths occurred within 90 days (0.9%), one from
ARDS postmultimodal therapy and the other from
repeated mesenteric ischemia in a patient with atrial
fibrillation, and this compares favorably (P < 0.05)
with 90-day mortality of 4.5 and 2.4%, respectively,
for the ECCG and DUCA series. To our knowledge,
the publication in 2007 of 340 consecutive patients
by Low et al, with 0.3% mortality, represents the
lowest published mortality rate in a high-volume
series, and the focus on a standardized clinical
pathway in a specialist center was cited as a key
factor in achieving this outcome.20 It is the possible
similar factors of structure and process that apply
at this Center, and that an ability to rescue from
severe complications is more likely to be embedded
in high-volume institutions.21,22 In addition to the
management of complications, a low mortality rate
may reflect surgery on a more selected lower risk
cohort or reduced complications. A comparison
of demographics, including ASA, co-morbidities,
and obesity rates, suggests that case selection was
not a relevant factor. There were also no major
differences in the severity of complications, with
Clavien–Dindo ≥ IIIb and < 5 in 14% at this Center,
14.3% in the ECCG, and 16% in DUCA. Accordingly,
without knowing the exact causes of mortality in
Use of ECCG definitions for comparative audit 7
P DUCA P
41.0% <0.0001 605 37% <0.0001
7.5% 150 9%
20.4% 379 23%
14.2% 192 12%
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6.6% 128 8%
6.4% 110 7%
1.3% 11 1%
2.6% 0.014 27 1.7% 0.066
4.5% 0.008 38 2.4% 0.221
18.8% 0.205 287 17.7% 0.393
these other series, or the management of severe
complications, it is not possible to conclude that the
management of severe complications is a major factor
for low mortality; nonetheless, it may be a reasonable
inference.21,22
A key finding, possibly linked to the mortality rate,
is a low anastomotic leak rate of 5.4%, twofold less
than 11.4% in the ECCG, and almost fourfold less
than the 19% in the DUCA series (P < 0.001). In the
Seattle series with 0.3% mortality, an anastomotic
leak was reported in just 3.8% of patients.20 These
leak rates contrast with high reported anastomotic
leak rates in the CROSS RCT, at 26%.4 A more recent
study, also from the Netherlands, reported a 17% leak
rate for thoracic anastomoses, and 21.9% for cervical
anastomoses.23 Clearly, a wide spectrum of leak rates
is evident even in the leading international centers,
and the optimization of technique and outcome is
clearly an imperative to further improve outcome.24
The grading of leaks within ECCG is a major
advance, as type I and type II leaks can be managed
relatively simply; hence, an important feature of our
experience is that type III leaks, requiring surgical
therapy, and typically more serious, revealed the
greatest proportional differences, with 0.4% at the
INC, 3% within ECCG, and 5.1% in the DUCA
report. There are myriad technical approaches to an
anastomosis, as well as key factors including conduit
perfusion, anesthetic factors, and comorbidities,
as well as postoperative care and the impact of
other complications. Notwithstanding, this series
has shown that that a simple uniform standardized
sutured approach resulted in low leak rates.24,25 This
is apposite in an MIE era. Although we do not know
the differential leak rate of open and MIE cases within
the ECCG and DUCA series, a recent study from
four European centers identified a mean of 119 cases
required in the MIE learning curve, with a reduction
in anastomotic leak from 29.5% to less than 5%
after the learning curve is complete, but an over 10%
leakage during this learning period. In light of this
learning curve, our series highlights a major modern
dilemma for this Center and probably for many
surgeons internationally who are intending to or are
transitioning to MIE or robot-assisted approaches.26
8 Diseases of the Esophagus
Conversely, a recent report from Toronto of 383
patients, where sequentially there was a transition
from open to MIE approaches, with approximately
a 50:50 ratio, reported similar leak rates of 12.4
versus 8.9% and 90-day mortality of 6.2 and 4.6%
in open and MIE, respectively, highlighting that a
transitioning experience in a major specialist Center
could be undertaken with no significant added risk.27
Major respiratory complications, in particular
severe pneumonia or ARDS, are the most common
cause of mortality postesophagectomy. Moreover,
a reduction in respiratory complications provides
the main evidence-base supporting MIE or hybrid
approaches in RCTs compared with open surgery. The
TIME trial reported reduced pulmonary infections
with MIE, and the MIRO trial reported markedly
reduced overall respiratory complications with a
hybrid abdominal laparoscopic and open thoraco-
tomy approach.28,29 The ECCG consensus utilizes the
Center for Disease Control (CDC) definition classi-
fication, which is based on the following: progressive
infiltrates, consolidation, or cavitation on chest
radiography; either fever, leukocytosis or delirium;
and sputum changes suggesting infection, worsening
cough or dyspnea, bronchial breath sounds, or
worsening gas exchange.30,31 The classification was
developed for hospital-acquired pneumonia, includ-
ing ventilator-associated pneumonia, without valida-
tion in postoperative pneumonia, and this may be
particularly an issue in patients who have undergone
one lung anesthesia, and where some infiltrates may
not necessarily indicative of pneumonia. The Utrecht
group developed the Uniform Pneumonia Score to
define respiratory complications, which were treated
with antibiotics.32,33 This may represent an advance,
but conversely it may just serve to highlight the
overutilization of antibiotics where pneumonia does
not truly exist, and research needs to be done to define
grading and severity of respiratory complications that
have clinical importance short of ARDS, respiratory
failure and the need for reintubation.
Notwithstanding these caveats, a pneumonia rate
of 18.2% was observed in this series based on CDC
criteria, with 30% having proven pulmonary infec-
tions. All surgeries were open, the ECCG being almost
50:50 open: MIE, and 86% of patients in the DUCA
study were MIE. Of note, all series reported simi-
lar pneumonia and ARDS rates. A reintubation was
more frequent in this series, at 10%, compared with
7%, and 5.2% in the ECCG and DUCA reports,
respectively, and the drainage of pleural effusions was
higher in addition. In DUCA, the clearance of mucus
plugs via bronchoscopy was more common, perhaps
highlighting a preferred intervention protocol rather
than reintubation for which the threshold is low at
the INC. Paradoxically, in view of lower leak rate,
and mortality, and similar pneumonia rates, sepsis as
per CDC criteria was more commonly documented
in this series, at 5%, compared with 1.9 and 1.1%
rate in the ECCG and DUCA series, respectively.
These latter rates appear very low and inconsistent
with the reported leak rates and complication severity,
perhaps raising broader questions about data docu-
mentation across a large national or international net-
work? A THE is selectively used at this Center, partic-
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ularly in high-risk patients, an approach supported by
the HIVEC RCT comparing THE with transthoracic
surgery, and our own published experience.34,35 In this
series, comparing TTE and THE, respectively, pneu-
monia was documented in 18% versus 16%, ARDS at
4% versus 0%, and re-intubation at 11% versus 5%.
New onset postoperative atrial dysrhythmia was the
most common single complication in this series, at
22.8%, compared with 14.5 and 13.9% for ECCG and
DUCA, respectively. This may be multifactorial, but
the incidence in INC of obesity and cardiovascular
disease may be relevant, and, as previously reported,
there is a significant association with postoperative
pneumonia.36
This study highlights the value of such an audit
using agreed definitions and its clear potential
in clinical research and trials. Its strength is the
uniform approach to esophageal cancer surgery at the
INC from two experienced specialist surgeons, with
standardized anastomotic and surgical technique, and
perioperative approach to complications, and under-
pinned by hospital and national internal audit. A
limitation is the smaller sample size and comparison
with many centers of varying infrastructure providing
common datasets to a national or international
database, wherein some centers may have superior
outcomes to the INC. A broader comment of the
ECCG benchmark data in general is that it is not
risk stratified and represents averages rather than
agreed targets.37,38 A 75th percentile of the median
outcome parameters has been proposed. In a study
of 334 patients with low comorbidity undergoing
MIE in 13 centers, benchmark values based on the
75th percentile at 30 days after hospital discharge
were ≤55.7 and ≤30.8% for overall and major compli-
cations, ≤18% for readmission, <8% for anastomotic
leak rate, and for mortality ≤1 and ≤ 4.6% for 30-day
and 90-day mortality, respectively.39 Hence, even in
a highly selected MIE series, targeted benchmarks
are similar to the unselected cohort treated by
open surgery at this Center, with markedly higher
anastomotic leak rate, highlighting the importance
of strict consistent definitions to enable comparisons
across series in the future. Accordingly, it is likely that
targeted benchmark data, and risk assessment, will
merge in future iterations of ECCG.
In conclusion, this evaluation from a National
Center reports data similar to the ECCG and DUCA
reports in terms of overall complication rates, and
severity of complications, but significantly less with
respect to anastomotic leaks, and a mortality rate

of less than 1%. The study highlights the value of
the ECCG definitions and Esodata project for com-
parative analysis, and the clear potential to use the
large contemporaneous ECCG dataset to enable audit
and quality improvement at institution, national, and
international level. It also creates an opportunity
to increase knowledge and to improve standards
through research of key modifiable complications,
in particular, anastomotic leaks and pneumonia.
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