Delayed gastric emptying after esophagectomy: a single centre experience—comparison of the international expert consensus definition to the local definition
Highlight box
Key findings
• No significant difference in the numbers of patients diagnosed with early delayed gastric emptying (DGE) when considering both definitions.
• The sensitivity and specificity of the international expert consensus (IEC) definition was significantly lower in identifying patients requiring pyloric balloon dilatations.
What is known and what is new?
• IEC agreed on a diagnostic criterion in 2020.
• University Hospital Plymouth definition is comparable to the IEC definition of early DGE.
What is the implication, and what should change now?
• Regular chest radiographs allow assessment of the conduit to identify and treat DGE proactively specially after nasogastric tube removal.
Introduction
Background
The terms gastric outlet obstruction and delayed gastric emptying (DGE) have been interchangeable in describing delayed emptying of the gastric conduit after esophagectomy (1). Symptoms include dysphagia, vomiting, reflux and early satiety. There is currently no uniform definition in the literature for DGE post esophagectomy. Arya et al. looked at 25 studies and reported that DGE was defined based on clinical, radiological or a combination of both, in the range of 2.2–47% (2). With such a heterogeneity, it is difficult to compare outcomes of different studies and objectively measure the effects of preventative or therapeutic interventions.
An international consensus group agreed on a definition of early DGE in 2020. The criteria required are high nasogastric output (>500 mL) or dilated gastric conduit on chest radiograph (100% increase from baseline) within 14 days of surgery (3).
Rationale and knowledge gap
The degree of adoption of this definition worldwide and how it compares to well established definitions locally with subtle, yet significant differences is unknown. In University Hospital Plymouth (UHP) early DGE is defined using an algorithm. A 24-hour nasogastric output greater than 50% of total oral fluid intake on the morning of day 4 post op leads to suspicion of DGE. If this continues with conduit dilation greater than 50% of the right hemi-thorax after day 4 post Ivor Lewis gastro-oesophagectomy (ILGO), a diagnosis of DGE is confirmed (4). After the removal of the nasogastric tube (NGT), daily chest radiographs are performed routinely until discharge. If the conduit is dilated greater than 50% of the right hemithorax in any of those days, a diagnosis of early DGE is made. This algorithm is used only in oesophagectomy patients at UHP. It has been used since 2011. Treatment options include conservative, medical and definitive endoscopic management [pyloric balloon dilatation (PBD)]. Dilatation is carried out no earlier than day 7 postoperatively to reduce the potential risk to the anastomosis. This definition is used in all studies conducted at this unit. At UHP 90-100 oesophagectomies are carried out annually.
Objective
The aim of this study was to compare the definition at our institution to that of the international consensus to determine which definition is better at identifying patients with DGE following esophagectomy. We present this article in accordance with the STROBE reporting checklist (available at https://aoe.amegroups.org/article/view/10.21037/aoe-24-3/rc).
Methods
Patient selection
Consecutive patients who underwent an esophagectomy at UHP between April 2019 to August 2020 were studied retrospectively. Diagnosis of esophageal cancer is confirmed with endoscopy and histology. Patients with a pre-operative TNM staging of T2 and above underwent chemotherapy (FLOT) or chemo-radiotherapy (CROSS). The operative approach was either hybrid (laparoscopic abdomen/open right thoracotomy) or open. The conduit diameter was 4–5 cm. Only six patients underwent pyloroplasty. No other pyloric procedure was performed at the index procedure.
Post-operative protocol
An ERAS protocol was implemented (4). Patients are encouraged to mobilise early with intensive physiotherapy.
Diagnosis of DGE
Table 1 outlines both the IEC definitions of early DGE. The IEC definition was applied retrospectively to define early DGE (3). The UHP definition is used in all the studies done at this unit. The baseline X-ray used for further comparison is the one done on day 0 post-operatively in recovery. Figure 1 shows how a dilated conduit is defined on chest radiograph. A contrast swallow was not used in patients post operatively. Once DGE is established, an NGT is inserted if it wasn’t already in. If the NGT is spigotted, it is put on free drainage. No X-ray is done until after the dilatation to check conduit.
Table 1
| Early delayed gastric emptying (DGE) | International expert consensus (IEC) (3) | University Hospital Plymouth (UHP) (4) |
|---|---|---|
| Clinical definition | >500 mL diurnal nasogastric tube output measured on the morning of postoperative day five or later (but within 14 days of surgery) OR | 24-hour nasogastric output greater than 50% of total oral fluid intake in that period measured on morning of day four on wards post-surgery AND |
| Radiological definition | >100% increased gastric tube width on frontal chest X-ray projection (in comparison to baseline chest X-ray taken on the day of surgery) together with the presence of an air-fluid level | Conduit dilation greater than 50% of the right hemi-thorax at day four post-surgery (patients have daily X-rays apart from day 2 post-surgery) |
Treatment of DGE
Figure 2 outlines the treatment flow chart of patients with DGE. Patients diagnosed with DGE underwent endoscopy and PBD (5). Medical therapy with prokinetics such as domperidone is employed, but all patients with diagnosed DGE were treated with PBD. This was done no earlier than seven days after surgery to avoid harm to the anastomosis. Endoscopic pyloric dilatation was carried out under general anaesthetic, with a 30 mm CRETM Fixed Wire Balloon Dilator (Boston Scientific, Hertfordshire, United Kingdom), which had a total length of 90 cm. Once the pylorus is traversed with an endoscope, a guide wire is inserted via the working channel. Under X-ray guidance, the balloon is passed over the wire and dilated fully for 2 minutes. The position is confirmed with a paper clip put on the patient.
Follow-up
Patients are reviewed after discharge at 2 weeks, then 3 monthly for the first year. Thereafter they are reviewed every 6 months to complete an overall 5-year follow-up.
Statistical analysis
Grouped data were expressed as median (range) and comparison was carried out using non-parametric methods. χ2 test was used for comparison of categorical variables. Comparison of continuous variables was carried out with the Mann-Whitney U-test. A level of statistical significance was set at P value of <0.05. The Statistical Product and Service Solutions software (SPSS, IBM Corp, Armonk, NY, USA) was used to perform statistical analysis.
Ethical consideration
The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). As this was a retrospective study, institutional review board approval was gained which waived the requirement for ethics review or patient consent.
Results
Demographic details of all patients undergoing Ivor-Lewis oesophagectomy between April 2019 and August 2020 are shown on Table 2. The incidence of DGE was 27% (27/100) vs. 20% (20/100) according to the UHP and IEC definition respectively (χ2=1.363, P=0.24). Twelve patients satisfied both definitions.
Table 2
| Characteristics | Overall | UHP DGE | IEC DGE | P |
|---|---|---|---|---|
| Total number | 100 | 27 | 20 | 0.24 |
| Age, years, median [range] | 70 [45–84] | 71 [45–81] | 72 [48–78] | 0.35 |
| Gender, n (%) | 0.38 | |||
| Male | 74 (74.0) | 17 (63.0) | 15 (75.0) | |
| Female | 26 (26.0) | 10 (37.0) | 5 (15.0) | |
| Tumour type, n (%) | 0.67 | |||
| ACA | 80 (80.0) | 21 (77.7) | 15 (75.0) | |
| SCC | 17 (17.0) | 5 (18.5) | 3 (15.0) | |
| Other adenocarcinoma | 3 (3.0) | 1 (3.7) | 2 (10.0) | |
| Operative approach, n (%) | 0.05 | |||
| Hybrid | 71 (71.0) | 26 (96.3) | 13 (65.0) | |
| Open | 29 (29.0) | 1 (3.7) | 7 (35.0) | |
| Pathological T stage, n (%) | 0.34 | |||
| pT0 | 22 (22.0) | 6 (22.2) | 3 (15.0) | |
| pT1 | 11 (11.0) | 7 (25.9) | 5 (25.0) | |
| pT2 | 13 (13.0) | 1 (3.7) | 4 (20.0) | |
| pT3 | 48 (48.0) | 12 (44.4) | 8 (40.0) | |
| pT4 | 6 (6.0) | 1 (3.7) | 0 (0) | |
| Pathological N stage, n (%) | 0.98 | |||
| N0 | 45 (45.0) | 16 (59.2) | 12 (60.0) | |
| N1 | 27 (27.0) | 5 (18.5) | 4 (20.0) | |
| N2 | 17 (17.0) | 5 (18.5) | 4 (20.0) | |
| N3 | 11 (11.0) | 1 (3.7) | 0 (0) | |
| ASA, n (%) | 0.50 | |||
| 2 | 55 (55.0) | 18 (66.7) | 16 (80.0) | |
| 3 | 45 (45.0) | 9 (33.3) | 4 (20.0) | |
| BMI, kg/m2, median (range) | 26 (15.2–43.8) | 25.9 (15.2–38.6) | 25 (15.2–36) | 0.48 |
UHP, University Hospital Plymouth; DGE, delayed gastric emptying; IEC, International expert consensus; ACA, adenocarcinoma; SCC, squamous cell carcinoma; ASA, American Society of Anesthesiologists Classification; BMI, body mass index.
Overall, 29 of 100 patients underwent PBD for DGE. Seventeen patients underwent early dilatation (within 14 days post-operatively). These patients had a 30 mm balloon dilatation once and no further future interventions. Twelve patients underwent late dilatations (>14 days post op). All of the forementioned patients presented with symptoms of DGE ranging from early satiety to vomiting. The median time to dilatation was 3 months (0–13 months). Four patients did not meet any criteria of early DGE on either definition during their index admission (true late DGE). The UHP and IEC definition identified 75% (n=8) and 17% (n=2) respectively (P=0.52). Despite meeting the criteria for early DGE and therefore PBD during their index admission, these patients were treated conservatively and did not undergo PBD dilatation as their conduit dilatation were either just slightly greater than 50% of the hemithorax or improved during their inpatient stay.
Sensitivity and specificity
Out of the 29 patients, 25 satisfied the UHP definition of early DGE. The sensitivity and specificity therefore were 86.2% and 97.2% respectively. When the IEC definition of early DGE was applied, 11 out of the 29 patients satisfied this definition. The sensitivity and specificity of the IEC definition were 37.9% and 87.3% respectively.
Anastomotic leak and pneumonia
Eight patients developed an anastomotic leak, of which four were managed conservatively. Three of the eight had early DGE. Pneumonia was clinically and radiologically diagnosed in 28 patients, two of whom were admitted to the high dependency unit for organ support. Of the 27 diagnosed with early DGE under UHP’s definition, six patients had pneumonia. Seven out of 20 patients with early DGE (under the IEC definition) had pneumonia.
Pyloroplasty
Six patients (6%) underwent intraoperative pyloroplasty (surgeon preference). These patients were not considered for pyloric dilatation. Four patients developed early DGE (two under IEC definition, one under UHP definition and one under both definitions). These six patients did not develop late DGE.
Discussion
Key findings
The uncertainty surrounding the aetiology of DGE after esophagectomy coupled with the varied definitions have led to numerous prophylactic and management strategies (2,6-10). Although the consensus definition was published in 2020, its acceptance and application worldwide are unknown. Various units use well established clinical and radiological definitions of early DGE (2,6) including our institution here at UHP (4). This study was therefore important to determine whether IEC definition of early DGE should be adopted. Although there was no significant difference in the numbers of patients diagnosed with early DGE when considering both definitions, the sensitivity and specificity of the UHP definition was significantly higher compared to the IEC definition.
Strengths and limitations
The main strength of both definitions and this study is the attempt to give a standardised definition of DGE post esophagectomy. This not only helps in reporting incidence of DGE but also allows comparison of treatment management. There are limitations to this study and both definitions of early DGE. The overall number of patients is relatively small. This can account for the lack of significant difference between the two definitions when assessing the population of this study. The IEC definition of early DGE gives a static confirmation of DGE with regards to NGT output. This is important in assessing outcome and reporting it however early DGE is a dynamic diagnosis. The use of chest radiographs for assessment is imperative after eating and drinking to ascertain who has early DGE.
Comparisons with similar research
Preventative measures of DGE have been employed. Some surgeons routinely perform a prophylactic pyloroplasty or pyloromyotomy. However, there are a few complications associated with this such as leakage from the repair, secondary bile reflux and dumping syndrome (11). A significant proportion of patients who would not have developed DGE would be exposed to a prophylactic procedure, with the associated risk. The uptake of this approach is variable as reviews from Arya et al. and Akkerman et al. showed that pyloroplasty or pyloromyotomy had no significant effect on decreasing DGE rates post operatively (2,6). Intra-operative pyloric Botox injection was found to have no effect as a preventative measure (4). We have shown in a systematic review and meta-analysis that prophylactic PBD can decrease post operative DGE rates (7). This was an analysis of observational studies and all studies had variable definitions of DGE (8-10). PBD was shown to be an effective and safe treatment of DGE post oesophagectomy (5).
Explanation of findings
There are both advantages and disadvantages of the UHP definition compared to the IEC consensus. Part of the UHP definition considers oral fluid input and NGT output (NGT output greater than 50% of oral intake on day 4 onwards post op) when defining early DGE (4). The IEC early DGE definition on the other hand only considers NGT output (>500 mL on day 5) (3). This arbitrary value does not consider input and therefore, if a patient drinks more than 1 L in 24 hours, they could be misdiagnosed with early DGE even though more than half of their input has been absorbed. There was a group of patients with high NGT output that settled between 5–7 days post operatively. Their chest radiographs were normal and so were not labelled as early DGE. This however played part in our unit modifying the ERAS protocol for the future, having learned from the IEC paper. The change of management being NGT removal on day 5 (if no evidence of DGE) rather than day 4 post operatively. Moreover, the UHP definition of early DGE considers daily chest radiographs to check conduit size, which allows early recognition of a dilated conduit, thus facilitating treatment with pyloric dilatation.
The UHP definition does require the conduit to occupy 50% of the right hemi-thorax to define early DGE. On initial assessment this favours the IEC definition of early DGE (100% increase in conduit size, even if less than 50% of hemithorax). However, none of the patients in the study met the radiographic definition of early DGE as proposed by the IEC group as none had 100% increase in conduit size.
Both definitions did identify a different cohort of patients. Only 12 patients matched both UHP and IEC definitions of early DGE. We therefore studied the population of 29 patient who had balloon dilatations to assess which of them satisfied the UHP and IEC definitions as predictors of dilatation in the early phase (within 14 days post op) or late phase. Of the 29 patients 17 had dilatations within 14 days post op. The UHP definition of early DGE had a sensitivity of 86.7% and specificity of 97.2% for predicting those needing a dilatation. This is expected as it is what we use to diagnose patients to have a dilatation. What was surprising however regarding the IEC definition of early DGE, is the sensitivity and specificity for predicting dilatation were 37.9% and 87.3% respectively. Those patients missed by the IEC definition of early DGE were diagnosed with DGE after NGT removal as their radiographs showed a conduit size greater than 50% of the right hemithorax. This further supports the practice of carrying out daily radiographs to assess DGE especially after NGT removal.
There appears to be a group of patients who just about met the criteria for early DGE according to the UHP criteria (50% of hemithorax) during their index admission but were treated conservatively as they settled clinically and developed late DGE requiring dilatation. It is unknown whether this group of patients would have benefited from PBD during their index admission which may have improved their quality of life.
Implications and actions needed
The diagnostic criteria serve to guide management of early DGE to prevent complications. It’s imperative however to recognise importance of the overall clinical picture. The purpose of the consensus definition was to facilitate collaborative research in preventing and treating early DGE. The uptake of this is consensus is unknown. The challenges of collaborative research in this subject are numerous, as different units vary depending on postoperative protocols on fluid intake, duration of NG tube placement and use of routine imaging.
Conclusions
Although there was no significant difference in the number of patients diagnosed with DGE between the two definitions, the sensitivity and specificity of the UHP definition was significantly higher compared to the IEC definition. The UHP definition also identified a group requiring late dilatation. Regular chest radiographs allow assessment of the conduit to identify and treat DGE proactively.
Acknowledgments
Funding: None.
Footnote
Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://aoe.amegroups.org/article/view/10.21037/aoe-24-3/rc
Data Sharing Statement: Available at https://aoe.amegroups.org/article/view/10.21037/aoe-24-3/dss
Peer Review File: Available at https://aoe.amegroups.org/article/view/10.21037/aoe-24-3/prf
Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://aoe.amegroups.org/article/view/10.21037/aoe-24-3/coif). The authors have no conflicts of interest to declare.
Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). As this was a retrospective study, institutional review board approval was gained which waived the requirement for ethics review or patient consent.
Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.
References
- Konradsson M, Nilsson M. Delayed emptying of the gastric conduit after esophagectomy. J Thorac Dis 2019;11:S835-44. [Crossref] [PubMed]
- Arya S, Markar SR, Karthikesalingam A, et al. The impact of pyloric drainage on clinical outcome following esophagectomy: a systematic review. Dis Esophagus 2015;28:326-35. [Crossref] [PubMed]
- Konradsson M, van Berge Henegouwen MI, Bruns C, et al. Diagnostic criteria and symptom grading for delayed gastric conduit emptying after esophagectomy for cancer: international expert consensus based on a modified Delphi process. Dis Esophagus 2020;33:doz074. [Crossref] [PubMed]
- Tham JC, Nixon M, Ariyarathenam AV, et al. Intraoperative pyloric botulinum toxin injection during Ivor-Lewis gastroesophagectomy to prevent delayed gastric emptying. Dis Esophagus 2019;32:doy112. [Crossref] [PubMed]
- Maus MK, Leers J, Herbold T, et al. Gastric Outlet Obstruction After Esophagectomy: Retrospective Analysis of the Effectiveness and Safety of Postoperative Endoscopic Pyloric Dilatation. World J Surg 2016;40:2405-11. [Crossref] [PubMed]
- Akkerman RD, Haverkamp L, van Hillegersberg R, et al. Surgical techniques to prevent delayed gastric emptying after esophagectomy with gastric interposition: a systematic review. Ann Thorac Surg 2014;98:1512-9. [Crossref] [PubMed]
- Abdelrahman M, Ariyarathenam A, Berrisford R, et al. Systematic review and meta-analysis of the influence of prophylactic pyloric balloon dilatation in the prevention of early delayed gastric emptying after oesophagectomy. Dis Esophagus 2022;35:doab062. [Crossref] [PubMed]
- Swanson EW, Swanson SJ, Swanson RS. Endoscopic pyloric balloon dilatation obviates the need for pyloroplasty at esophagectomy. Surg Endosc 2012;26:2023-8. [Crossref] [PubMed]
- Hadzijusufovic E, Tagkalos E, Neumann H, et al. Preoperative endoscopic pyloric balloon dilatation decreases the rate of delayed gastric emptying after Ivor-Lewis esophagectomy. Dis Esophagus 2019;32:doy097. [Crossref] [PubMed]
- Decker C, Burke C, Olutola O, et al. Gastric emptying after esophagectomy: comparing single therapy versus dual therapy method for pyloric drainage. Shanghai Chest 2020;4:37. [Crossref]
- Zhang R, Zhang L. Management of delayed gastric conduit emptying after esophagectomy. J Thorac Dis 2019;11:302-7. [Crossref] [PubMed]
Cite this article as: Abdelrahman M, Fu K, Tham J, Emslie K, Ariyarathenam A, Berrisford R, Humphreys L, Sanders G, Wheatley T, Chan DSY. Delayed gastric emptying after esophagectomy: a single centre experience—comparison of the international expert consensus definition to the local definition. Ann Esophagus 2024;7:9.
