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Clinical Imaging 51 (2018) 23–29

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Clinical Imaging
journal homepage: www.elsevier.com/locate/clinimag

Diagnosing conduit leak after esophagectomy for esophageal cancer by T


computed tomography leak protocol and standard esophagram: Is old school
still the best?

Diana Palacioa, ,1, Edith M. Maromb, Arlene Corread, Sonia L. Betancourt-Cuellarc,
Wayne L. Hofstetterd
a
Department of Medical Imaging, The University of Arizona, Banner Medical Center, Tucson, AZ 85724, United States
b
Department of Diagnostic Imaging, The Chaim Sheba Medical Center, Ramat Gan, Israel affiliated with the Tel Aviv University, Tel Aviv, Israel
c
Department of Radiology, Diagnostic Imaging Division, The University of Texas MD Anderson Cancer Center, 1515 Holcombe Blvd, Houston, TX 77005, United States
d
Department of Surgery, Cardiothoracic Surgery Division, The University of Texas MD Anderson Cancer Center, 1515 Holcombe Blvd, Houston, TX 77005, United States

A R T I C L E I N F O A B S T R A C T

Keywords: The imaging modalities available to evaluate anastomotic leak complicating esophagectomy include
Esophageal leak CT-Esophageal Protocol (CTEP) and esophagram. The purpose of this study was to compare the performance of
Esophagectomy these two modalities, alone or in combination, with the final diagnosis of leak established by endoscopy, surgery
Esophagram and/or the clinical course and evaluate management implications.
CT esophagram
Esophageal cancer

1. Introduction 2. Materials and methods

Esophageal conduit leak is a major complication after esopha- In this retrospective study, we reviewed the charts of 382 con-
gectomy and can result in serious morbidity, prolonged intensive care, secutive patients who had undergone esophagectomy for esophageal
longer hospital admissions, and increased mortality [1–3]. In the past cancer between September 1, 2005, and August 30, 2009 [5] from the
decade, patient outcome after conduit leak has improved as a result of Thoracic Surgery database. There are 6 different types of esophageal
prompt diagnosis and appropriate management [4–8] and effective resections performed at our institution; decision for each is based on
therapy relies heavily on early diagnosis. Standard Esophagram (SE) tumor location, patient co-morbidities, and surgeon preference. Based
has traditionally been used to evaluate conduit leaks. The use of SE in on the database from our thoracic surgery department, the incidence of
the evaluation of a conduit leak has been validated in studies with small leak at our institution is statistically similar at all levels of anastomosis
numbers of patients [9–13]. Conduit leak after esophagectomy poses a and all techniques (data not shown). In order to focus on the char-
different clinical and imaging scenario than that of esophageal per- acteristics and performance of the imaging studies we left the surgery
foration. In this regard, SE early after esophagectomy can be difficult to descriptions out of this paper. We searched for the patients with clinical
perform as patients have limited mobility and may be unable to suspicion of conduit leak, which then formed the study group. We re-
swallow the large amounts of contrast needed for evaluation. Since vised the imaging studies pertinent to the suspected conduit leak and
2005 a CT esophageal conduit leak protocol (CTLP) has been im- conducted a longitudinal review of clinical and hospital discharge notes
plemented at our institution to diagnose esophageal conduit leaks. The pertaining to the first 31 days after esophagectomy.
purpose of this study was to review the role of CTLP and SE in the
diagnosis and treatment of patients with a clinical suspicion for a 2.1. Definition of conduit leak
conduit leak after esophagectomy for esophageal cancer.
Since there is no universal consensus on how to define anastomotic
leak after esophagectomy [14], the presence of conduit leak, for the
purposes of this study was defined and established retrospectively in


Corresponding author.
E-mail address: dpalacio@radiology.arizona.edu (D. Palacio).
1
Present address: 1515 N Campbell Ave., Tucson, AZ 85724, United States.

https://doi.org/10.1016/j.clinimag.2018.01.010
Received 17 November 2017; Received in revised form 17 January 2018; Accepted 19 January 2018
0899-7071/ © 2018 Elsevier Inc. All rights reserved.
D. Palacio et al. Clinical Imaging 51 (2018) 23–29

Fig. 1. a) Delayed SE view and b) CTELP axial image: Two sequential cone down axial images at the level of the pulmonary arteries. A small well sealed pocket of extravasated oral
contrast on the left side of the mediastinum, is seen in both studies, near the anastomosis, in keeping with a small contained leak (arrows).

Fig. 2. Delayed SE, demonstrating a leak into the right pleural space, being drained by a
chest tube, in keeping with a small contained leak.

Fig. 3. CTELP, cone down axial images at the right lung base (a–c), demonstrating the
collaboration with the Thoracic Surgery Service at our institution, as trajectory of the chest tube (arrows). There is radiodense material within the tube lumen
two or more of the following: positive imaging reports confirmed by (b–c), evidencing a small contained leak. No spillage of oral contrast was identified in the
endoscopic evaluation, surgical findings, longitudinal follow-up data pleural fluid.
consistent with the suspected development of a conduit leak or any
combination. We then classified the patients with a conduit leak ac-
cording to the type of treatment implemented: Patients with type I

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D. Palacio et al. Clinical Imaging 51 (2018) 23–29

Fig. 4. Delayed SE. (a, b). Orthogonal views demonstrating large extravasation of oral contrast on the right side of the mediastinum (thin arrows). Note moderate distention of the gastric
conduit (short arrows) associated with some degree of stenosis distally within the pyloric region (arrowhead in a).

conduit leak required no specific treatment; patients with type II con- posterior and bilateral anterior oblique fluoroscopic cine images in the
duit leak received conservative treatment (such as antibiotics, oral diet full upright position to various degrees of inclination depending on
withholding, or supplemental nutrition) or had undergone minimally patient tolerance were obtained. Bilateral posterior oblique views as
invasive procedures, such as esophageal stent, mediastinal drain, or well as postero-anterior views, in the prone position complemented the
chest tube placement; patients with type III conduit leak underwent study, depending on the patient's condition.
surgical management; patients with type IV conduit leak had surgical
management and conduit necrosis.
2.3. Conduit leak classification by imaging
Describing leak with some level of agreement between clinicians has
been historically difficult. A recent multi-national Delphi process con-
Based on the CTLP and SE reports, patients with positive results
ducted by a group known as ECCG (Esophagectomy Complications
were subdivided into two groups: those with small or contained conduit
Consensus Group) has published on a version of the categories defined
leaks and those with large or uncontained conduit leaks. Small or
in this paper. We feel that this is the best method to categorize leaks
contained conduit leaks (Figs. 1–3) had a blind ending track or a sealed-
currently [15].
off collection of oral contrast within the mediastinum with or without
drainage into the pleural space but with evidence of appropriate drai-
2.2. Imaging techniques nage by a chest tube in close proximity to the fluid collection. Large or
uncontained conduit leaks had large, diffuse, or free spillage of oral
2.2.1. CTLP technique contrast in the mediastinum and/or pleural space, with no adequate
All of the CTLP studies were conducted with use of 64 multidetector direct drainage by a chest tube (Figs. 4,5).
light-speed VCT Scanners (GE Medical Systems Milwaukee, WI). The
CTLP was acquired with the patient in supine position, at 2.5-mm slice
2.4. Imaging data collection
thickness, and with axial images reconstructed in a standard algorithm
before and after administration of 120 cm3 of IV iohexol or iodixanol
We reviewed the reports of all diagnostic CTLP and SE studies
(Omnipaque and Visipaque respectively, GE Healthcare, Cork, Ireland)
performed within the first month after esophagectomy. A diagnostic
and oral iohexol (Omnipaque, GE Healthcare) at 15 cm3 diluted in
CTLP or SE was considered the initial study performed to investigate a
100 cm3 of water given immediate before the scan or on the table.
clinical suspicion of conduit leak that was not previously diagnosed.
Coronal and sagittal reformatted images were available for interpreta-
Therefore, CTLP and SE studies conducted for conduit leak surveillance
tion.
were excluded from the analysis, as were conventional CT studies re-
quested for other purposes during the immediate postoperative period.
2.2.2. SE technique The overall individual CTLP and SE performance for diagnosis of
Under fluoroscopic examination, patients initially swallowed un- conduit leak was correlated with positive imaging reports, endoscopic
diluted iohexol (Omnipaque, GE Healthcare). If no conduit leak was evaluation, surgical findings, or longitudinal follow-up data. We also
identified, the patient was given liquefied full-strength barium. Antero- compared performance of CTLP and SE in patients who had both studies

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D. Palacio et al. Clinical Imaging 51 (2018) 23–29

Table 1
Patient distribution according to the clinical management of the conduit
leak.

Leak severity grade No. (%) of patients

I 7 (16.6)
II 9 (21.4)
III 21 (50)
IV 5 (11.9)
Total 42 (100)

Table 2
Distribution of patients diagnosed with conduit leak by imaging and type of leak.

Leak Diagnosis Diagnosis Diagnosis Diagnosis Diagnosis Total


type per by CTELP by SE (no by both by CTELP by SE but
Imaging (no SE CTELP CTELP but not SE not CTELP
performed) performed) and SE

Small 5 3 7 3 7 25
Large 6 1 4 11
Total 11 3 8 3 11 36

Table 3
Correlation of conduit leak type per imaging and management classification of the leak.

Conduit leak diagnosis Leak type per imaging Total

Small/contained Large/uncontained

I–II 13 0 13
III 10 8 18
IV 2 3 5
Total 25 11 36

Fig. 5. CTELP axial images at the level of the main pulmonary arteries (a) and at the level
of the inferior pulmonary veins (b showing a large uncontained leak (arrows). Note high
density of the pleural fluid (*), explained by spillage of oral contrast into the pleural
The remaining 121 patients were imaged to assess for conduit leak:
space.
17 underwent CTLP, 36 had SE, and 68 underwent both studies within
the first month after esophagectomy.
performed within the first month after esophagectomy. Recognizing
that a time bias may be introduced in doing so, we decided to extract a
subgroup of patients who underwent both CTLP and SE within 3 days of 3.1. Clinical information
one another and similarly analyzed performance for both diagnostic
modalities. A cross-match was obtained between the clinical classifi- The 125 patients who were suspected to have a conduit leak pre-
cation of the conduit leak according to severity and the imaging conduit sented with a variety of somewhat specific signs and symptoms, such as
leak characteristics independent of whether the diagnosis was made change in character or appearance of drain output, tachycardia, atrial
with CTLP, SE, or a combination of both. fibrillation but also more generic findings, such as chest pain, fever, and
We performed a Cox regression analysis of conduit leak-free prob- signs of sepsis including unexplained confusion, fatigue, malaise,
ability as a function of time and investigated how these findings could nausea/vomiting or any combination, without a clear cause.
affect the diagnostic value of the CTLP studies. Information regarding
alternative diagnoses offered by CTLP studies was also recorded.
3.2. Conduit leak type by imaging
3. Results
On imaging, 36/121 (29.7%) patients were positive for a conduit
Between September 1, 2005, and August 31, 2009, a total of 382 leak and 2 patients with proven conduit leaks, one by endoscopy and
patients underwent esophagectomy for esophageal cancer. The proce- another at surgery had false negative CTLP and SE studies. Both pa-
dures were performed by the thoracic surgery team members, with a tients were status post Ivor Lewis esophagectomy. One of the patients
minimum of 10 years of experience. The records of 125 patients, in- demonstrated anastomotic dehiscence at subsequent surgery measuring
dicated symptoms and/or signs concerning for esophageal leak during about 1.2 × 0.8 cm. The second patient showed a 5 mm defect at en-
the first month after surgery. At the cut-off time of 31 days post-pro- doscopy, approximately 1 cm distal to the anastomosis. Independent of
cedure, 42 patients were diagnosed with true leaks 42/125 following the imaging method used, 69.4% (n = 25) were small/contained con-
the previously stated criteria. The distribution of patients according to duit leaks and 30.5% (n = 11) were large/uncontained conduit leaks.
type of conduit leak is shown in Table 1. The diagnosis of conduit leak Table 2 displays the distribution of patients by diagnostic modality. Of
after surgery was made at a median of 11 days (range, 6–21 days). the patients with a small/contained conduit leak, 12/25 (48%) required
Of the 125 patients demonstrating concern for a potential leak, four surgical intervention and all 11 patients with a large/uncontained
patients did not have any pertinent imaging study and three of them conduit leak required surgical intervention. The correlation of conduit
were finally classified as having grade III conduit leaks whereas one was leak type per imaging and management classification are shown in
classified as a grade II conduit leak. Table 3.

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D. Palacio et al. Clinical Imaging 51 (2018) 23–29

Table 4 Table 6
Total of patients who underwent SE only. Comparison of report results with the final Patients who underwent CTELP and SE within the first month after esophagectomy.
diagnosis of conduit leak. Report result correlation with the final diagnosis of leak and management.

SE leak report Conduit leak diagnosis Total Conduit leak Conduit leak diagnosis Total

No Yes No Yes

No 31 0 31 CTELP leak report No 43 13 56


Yes 2 3 5 Yes 3 9 12
Total 33 3 36 Total 46 22 68
SE report No 45 4 49
Yes 1 18 19
Total 46 22 68
Table 5
Total of patients who underwent CTELP only. Result report correlation with the final
diagnosis of conduit leak.
Table 7
CTELP leak report Conduit leak diagnosis Total
Total of patients who underwent CTELP and SE within 3 days from one another in the first
month after esophagectomy. Correlation with the final diagnosis of leak and management
No Yes
classification.
No 4 1 5
Conduit leak report Conduit leak diagnosis Total
Yes 1 11 12
Total 17
No Yes

CTELP No 19 3 22
Yes 1 7 8
3.3. SE report analysis Total 20 10 30
SE No 19 2 21
Yes 1 8 9
Of the 125 patients, 36 (28.8%) with a clinical suspicion of conduit
Total 20 10 30
leak underwent SE. The median day for SE was postoperative day 9
(range, 4–27 days). The SE report distribution compared with that of
the management classification is shown in Table 4. The performance accuracy of 86.6%. SE studies performance resulted in a sensitivity of
screening of SE for this group resulted in a sensitivity of 84%, specificity 80%, specificity of 95%, PPV of 88.8%, NPV of 90.4%, and accuracy of
of 97.4%, positive predictive value (PPV) of 87.5%, negative predictive 90%. There was concordance between CTLP and SE in 76.7% of the 30
value (VPN) of 96.2%, and accuracy of 93.2%. cases (p = 0.032).

3.4. CTLP report analysis


3.6. CTLP accuracy as a function of time

Of the 125 patients, 17 (13.6%) with a clinical suspicion of conduit


The Cox regression test depicted the cumulative conduit leak free
leak underwent CTLP. CTLP studies were performed at a median of
probability as a function of time performance of the CTELP studies
9 days postoperatively (range, 1–31 days). The patient distribution ac-
(measured in weeks from the date of the esophagectomy). The results
cording to the examination reports and correlation with the manage-
showed that when the CTELP reports within the first 14 days are ne-
ment classification are listed in Table 5. The screening values in this
gative, the reliability of these results is low; in other words, a sub-
group for CTLP resulted in a sensitivity of 58.8%, specificity of 87%,
stantial number of patients were proven to have a conduit leak in spite
PPV of 83.3%, NPV of 87%, and accuracy of 78.8%.
of the negative results, whereas the negative results delivered after
14 days were more likely to represent true absence of conduit leak
3.5. CTLP and SE report performance in patients who underwent both
(Table 8).
studies for clinical suspicion of conduit leak

A total of 68 patients underwent both CTLP and SE during the first 3.7. Other findings on CTLP
month after surgery. The median timeframe between studies was 4 days
(range, 0–23 days). A total of 43 patients (63.2%) underwent CTLP Eight patients were reported to have complex pleural effusions, four
before SE with a median timeframe of 6 days (range, 1–23 days); 19 of whom required tube drainage and one who underwent decortication;
patients (27.9%) underwent CTLP after SE, with a median timeframe of the remaining three had chylothorax, one requiring open drainage, a
2 days (range, 1–12 days); and 6 patients (8.8%) underwent the studies second requiring a redo thoracotomy for thoracic duct ligation, and a
within the same day. The CTLP and SE report result distribution for this third requiring pleurodesis. Four other patients were diagnosed as
patient group is shown in Table 6. In this group, the performance values having multifocal pneumonia. One additional patient had pulmonary
for CTLP resulted in a sensitivity of 40.95%, specificity of 93.4%, PPV embolism, another had an omental infarction, and one had an infected
of 75%, NVP of 76.7%, and accuracy of 76.4%. Performance values for mediastinal seroma.
SE revealed a sensitivity of 81.8%, specificity of 97.8%, PPV of 94.7%,
NVP of 91.8%, and accuracy of 92.6%. Recognizing that there would be 4. Discussion
a significant time bias regarding results comparing CTLP and SE that
are separated by many days, we elected to evaluate a subgroup of 30 In clinical practice, the occurrence of “leak” after esophagectomy,
patients (100%) who underwent both CTLP and SE within 3 days of one can take several forms, including anastomotic dehiscense, focal defects
another: Nine patients had CTLP before SE, 15 had CTLP after SE, and 6 distal to the anastomosis and conduit necrosis. On imaging, the loca-
had both studies within the same day. The distribution of patients lization of a leak is challenging and often, this differentiation can be
compared with the management classification for CTLP and SE is dis- difficult to discern even on endoscopy. Since management does not per
played in Table 7. In this group, CTLP performance resulted in a sen- se depend as much on location and final diagnosis of anastomotic
sitivity of 70%, specificity of 95%, PPV of 87.5%, NPV of 86.3%, and versus conduit leak is unobtainable data in many situations, we elected

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Table 8
Leak free probability by CTELP report results: CTELP+ (positive for conduit leak) and CTELP− (negative for conduit leak). (a) studies performed < 7 days (b) between 7 and 14 days and
(c) later than 14 days after esophagectomy. After 7 days following esophagectomy, the hazard of leak was lower when the reports were negative than when they were positive (a,b).

to report “conduit leaks” rather than any specific type of leak. Our study basis of extraluminal air, fluid, and/or contrast material in the med-
was specifically focused on the SE and CTELP imaging performance, in iastinum were falsely positive and a result of surgical resection. Our
the setting of clinical suspicion for a conduit leak. results showed were 4/85 (4.7%) false positive conduit leaks diagnosed
The results showed that the absolute values in the screening analysis on CTLP. In a study by Strauss et al. [19], in which conduit leaks were
for SE reports were slightly better than were results for CTLP, and this suspected on CT performed between 3 and 7 days after esophagectomy
was statistically significant (p < 0.04). In the group of 68 patients in on the basis of mediastinal air alone, 15 of 16 patients had no conduit
whom both CTLP and SE studies were performed, we noted a significant leak by endoscopy and/or surgery. To complicate matters, the post-
number of false-negative results for the CTLP studies (13 of 68). This operative finding of oral contrast within chest tube drains, an obvious
analysis did not consider the exact time at which the diagnosis of sign of a conduit leak on CTLP, is easily overlooked in patients with a
conduit leak was made. Because of that, this large number of false- conduit leak. The addition of prone images to the CTLP studies could
negative results is probably not inherent to limitations of the diagnostic potentially improve sensitivity. There were 14/85 (16.4%) patients
modality itself, but simply related to the dynamic nature of conduit with a false negative CTLP. Our study, similar to that of Strauss et al.
leaks. Many of the studies may have been performed when the conduit [19], shows that when a conduit leak is suspected clinically in the first
leak was too early to become evident, as patients may be symptomatic two weeks after esophagectomy, a negative CT is not reliable in ex-
secondary to an area of infection or early ischemia that has not com- cluding a conduit leak and further imaging and/or endoscopy or even
pletely opened up as a leak. In fact, in up to 64% of patients, the CTLP surgical intervention may be considered depending on the level of
studies were performed before the SE examinations were conducted, concern. Furthermore, serial surveillance imaging may be a good al-
with a median timeframe of 6 days (range, 1–23 days) after surgery. ternative in relatively stable patients and may increase the diagnostic
The CTLP values significantly improved in the subgroup of 30 patients value of the imaging modality selected. As stated earlier, given the
who had both the CTLP and SE studies performed within a short period design of our study it was not possible to address the possibility of silent
of time of one another, which we arbitrarily selected to be 3 days. leaks, since we excluded all patients that were asymptomatic. However,
Identifying a conduit leak after esophagectomy can be difficult in accordance to previous studies, predictably these would typically be
when using any imaging modality, taking into account that the CT signs leaks without significant clinical consequence [13,20]. Therefore rou-
of a conduit leak differ from the typical appearance of a perforated tine imaging studies in all patients at some point after esophagectomy
esophagus. In this regard, a small amount of fluid and/or air in the may not be necessary or best practice. Several complications unrelated
mediastinum is suggestive of an esophageal perforation but can be a to conduit leak were diagnosed with CTLP and is potentially a benefit
normal finding in the early post-operative period after esophagectomy over SE in the evaluation of patients who have undergone an esopha-
[16,17]. Accordingly, it can be difficult to differentiate between an gectomy.
early sign of conduit leak and a result of surgical resection. In a recent Although our study shows that SE is reliable for the detection of
study by Lantos [18], 40% of conduit leaks on CT diagnosed on the conduit leaks, the postoperative appearance of the conduit poses

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D. Palacio et al. Clinical Imaging 51 (2018) 23–29

interpretative difficulties. The irregular anatomy of the anastomotic site of CTLP was lower in all of the groups analyzed, CTLP was as efficient
accounted for 6 false-positive studies in the SE group and this pitfall for in diagnosing clinically significant conduit leaks and has the ability to
conduit leak diagnosis has also been described in other studies [18]. diagnose other co-existing findings related on unrelated to leak.
This is particularly true when side-to-side anastomosis is performed, Because of the limitations of SE and CTLP in the evaluation of suspected
where the appearance is similar to a small-contained conduit leak. conduit leaks, the clinical status of the patient is a major factor de-
Additionally, redundancy of the anastomosis may be confused with a termining further investigation of a suspected conduit leak after eso-
small contained conduit leak, especially if asymmetric. phagectomy.
An important observation is that both CTLP and SE were able to
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