Abstract
Introduction
Anastomotic leakage (AL) is a severe complication after esophagectomy. Intraluminal oxygen delivery at the anastomosis site might improve the viability of the tissue and thereby reduce the incidence of AL. We present a feasibility study of intraluminal oxygen delivery after esophagectomy.
Methods
Eighteen patients scheduled for robot-assisted minimally invasive esophagectomy with an intrathoracic anastomosis were selected to receive an additional manometry catheter for intraluminal oxygen delivery at the anastomosis site. The primary endpoint was the feasibility of placing the catheter in the correct position and staying in situ for five days postoperatively. Intraluminal pressure was monitored during oxygen delivery at flow rates of 0 (control group), 1, 2, or 4 ml/min. Patients were questioned on the comfort of the catheter.
Results
In two patients, intraoperative placement of the catheter was unsuccessful. Two others replaced these patients according to the study protocol. 16 patients were analyzed. In five patients, the catheter was accidentally removed before the end of the study. The primary endpoint was successful in 11/16 patients (69 %). Intraluminal pressure in the 1 ml/min group did not differ from the control group. Intraluminal pressure in the 2 ml/min group increased substantially compared to the control group. Patients reported comfort rates that decreased over time.
Conclusion
This study shows that it is feasible to administer intraluminal oxygen in the first five days after esophagectomy and that a flow rate of 1 ml/min is not associated with increased intraluminal pressure. Future studies are required to study the effectiveness of intraluminal oxygen delivery in preventing AL.
Keywords: Anastomotic leakage, Esophagus resection, Complication reduction
Highlights
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Local ischemia is one of the main reasons for anastomotic leakage.
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Intraluminal oxygen at the anastomosis site could reduce anastomotic leakage.
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Intraluminal oxygen delivery is feasible and safe after an esophagus resection.
Introduction
Anastomotic leakage (AL) is a severe complication after esophagectomy for esophageal cancer, with incidence rates reported between 5 and 20 % [[1], [2], [3]]. AL significantly increases mortality from 3.1 to 6.2 % to 7.2–18.2 % [4,5]. In addition, it increases in morbidity, hospital and intensive care unit stay, and subsequent reinterventions. Furthermore, AL has a detrimental effect on quality of life, hospital resources, and costs [[5], [6], [7], [8]]. AL can result from various causes, all of which involve mechanisms of tissue ischemia, such as poor blood supply, tension on the anastomotic site, impaired healing due to local tissue hypoxia or malnutrition. During the healing process, the anastomotic site undergoes a series of events, including inflammation, cell proliferation, and tissue remodeling. If any of these processes are disrupted, it can impair the healing of the anastomotic site and increase the risk of leakage.
Several risk factors for developing AL have been suggested, including high body mass index, smoking behavior, comorbidities such as heart failure, hypertension, renal failure, longer operation duration, and certain types of anastomosis [5,9]. Unfortunately, it is difficult or unfeasible to modify some of these risk factors to lower the risk of AL [10,11]. Data suggests local conduit ischemia and necrosis at the anastomosis site can lead to anastomotic dehiscence [[12], [13], [14], [15]]. A partial oxygen pressure below 40 mmHg shows impaired healing of the anastomosis [16]. Schroder et al. measured postoperative partial CO2 pressure at the anastomosis site. The authors concluded that the microcirculation is most impaired 24 h after surgery and has almost recovered after four days [17].
Preventing AL is an essential goal of the surgical team. Various methods have been tested to reduce the rate of AL, such as preoperative ischemic conditioning of the stomach [18,19], alternative surgical techniques [[20], [21], [22]], intraoperative determination of an optimal site for anastomosis on the conduit [19], and peri-operative patient optimization [23]. It is important to note that while these methods have proved promising in reducing the risk of AL, they are not always effective or appropriate for every patient.
This study is the first step in exploring a novel method that might reduce the incidence of anastomotic leakage through postoperative intraluminal oxygen delivery at the anastomosis site. It investigates the feasibility of positioning a naso-esophageal tube for oxygen delivery, measuring intraluminal pressure, and maintaining this tube for several days postoperatively. We hypothesize that intraluminal oxygen diffuses through the mucosa and submucosa, complementing and perhaps even compensating for any deficits in the vascular oxygen supply, thereby mitigating tissue ischemia. We expect this to contribute to increased tissue regeneration and strengthening the anastomosis, decreasing the risk of AL.
Methods
This study was designed as a feasibility intervention study in patients undergoing a minimally invasive esophagectomy with an intrathoracic anastomosis at the University Medical Center Groningen (UMCG). The UMCG's institutional Review Board approved the study (NL69801.042.19).
Study setup
The inclusion criteria consisted of patients scheduled for a robot-assisted minimally invasive esophagectomy for esophageal cancer with an intrathoracic gastric conduit reconstruction in the UMC Groningen, aged 18 years or older and signed written informed consent. Exclusion criteria were known nasopharyngeal abnormalities preventing naso-esophageal tube insertion, salvage surgery after ‘definitive chemo-radiotherapy’, inability to provide informed consent, and illiteracy.
The study design consisted of four groups of patients. The first group (N = 3) is the zero-oxygen control group used to test the feasibility of the study setup but without oxygen delivery. In the second group, 10 patients were included and received 1 ml of oxygen per minute. The third and fourth groups comprised of three patients receiving 2 and 4 ml of oxygen per minute. The four study groups (0, 1, 2, 4 ml/min oxygen flow) were tested consecutively. After each study group, an interim safety evaluation was performed before progressing to the next study group. These safety checks are depicted in Table 1. Severe esophageal bleeding studies show that a pressure of 25–30 mmHg will lead to esophageal ischemia [24,25]. Therefore, a cutoff value of 20 mmHg persisting for more than 1 h was chosen. Fig. 1 shows the flow diagram of the study procedure.
Table 1.
Used safety checks before advancing to the next study group.
| Number | Safety checks |
|---|---|
| 1 | Impossible to advance the oxygen delivery tube at the site of the anastomosis during surgery in more than 60 % of the patients in the group. |
| 2 | Intolerance or accidental removal of the oxygen delivery tube in more than 60 % of the patients in the group. |
| 3 | Gastric tube dilation on the chest X-ray in the first 5 days in more than 60 % of the patients in the group. |
| 4 | Anastomotic leakage in more than 60 % of the patients in the group. |
| 5 | If the intraluminal pressure is above 20 mmHg for a longer period (>1 h) in more than 50 % of the patients in the group. |
Fig. 1.
General flow diagram of the study procedure.
Oxygen was delivered through an additional naso-esophageal tube inserted intraoperatively concurrent with the insertion of the regular nasogastric tube but in the other nostril. After creating the side-to-side stapled anastomosis, the tube is positioned under direct vision (Fig. 2) [26]. If insertion of the interventional naso-esophageal tube failed, another patient would replace the subject. The measurement setup was connected after surgery and the intraluminal oxygen delivery tube intended to remain in situ for five days for the zero‑oxygen control group and the 1 ml/min group. The study duration for the 2 and 4 ml/min groups was reduced to three days after evaluation of the level of comfort of the study setup in the group of 1 ml/min.
Fig. 2.
Schematic overview of the oxygen delivery tube near the anastomosis. The oxygen delivery lumens are 2 cm apart from each other. The pressure relieve lumen is located most near the anastomosis in between the second and the third oxygen delivery lumen. On the right-hand side a zoom in impression of the cross section of the nasogastric multilumen tube is depicted (not to scale). The nasogastric tube has an overall diameter of 4.7 mm and the 24 lm each have a diameter of 0.43 mm. The center lumen has a diameter of 1.65 mm.
The oxygen flow rates were determined by expert opinion and supported by a porcine animal study in which a section of the small bowel was cut off from blood supply and only supplied with 5 ml of intraluminal oxygen per minute [27]. After 2 h, the treated small bowels appeared macro and microscopically viable, while the control was not viable. Here, we have chosen the relatively low flow rates of 1, 2, and 4 ml/min and applied these in increasing order as a safety measure. In the previously mentioned porcine model, the section of the small intestine was cut off from all blood supply. In contrast, in our study, an esophagectomy anastomosis is still supplied with blood via the vascular bed in the surrounding tissue. Therefore, flow rates up to 4 ml/min may already be sufficient to prevent ischemia in the anastomotic site. Moreover, we expected that this relatively low flow would not lead to a higher pressure in the gastric tube and that more oxygen delivery would benefit anastomotic healing.
Daily chest x-rays were performed to check for gastric dilation, in which case the oxygen supply was stopped, and low suction was started from the naso-esophageal tube for 4 h (Fig. 1).
The level of comfort of the setup was evaluated using a daily visual analog scale (VAS) from 0 to 100. The level of comfort and practicality of the setup did not have safety cutoffs, but were used in the safety evaluation between groups.
Measurement setup
A measurement setup was created to deliver oxygen intraluminally near the anastomosis site. Fig. 3 displays an overview of the measurement setup. A multi-lumen esophageal pressure catheter delivered the oxygen, MMS G-90510 high-resolution esophageal manometry catheter (Mui Scientific, Mississauga, ON, Canada). The catheter contained 24 separate channels for manometry and 1 center lumen. The oxygen was delivered at four different outlet positions surrounding the anastomosis. The distance between the chosen outlets was 2 cm, resulting in an oxygen delivery region of 8 cm surrounding the anastomosis.
Fig. 3.
Overview of the measurement setup.
The outflow of each channel was regulated by an MPP-FR0.15T flow resistor (Laborie Europe/International, Enschede, The Netherlands). The flow resistor contains a metal inner tube with a diameter of 75 μm. Due to the resistance of this metal inner tube, a constant pressure is translated to a constant flow from the outlet of the flow resistor.
A small 1-liter oxygen tank supplied the flow resistors at a constant pressure. Before every oxygen administration, the flow of oxygen from the catheter was measured, and if needed, the pressure of the oxygen tank was adapted to ensure the correct oxygen flow.
Pressure transducers (Meritrans DTX plus disposable transducer) were attached to the oxygen delivery lumens. This pressure transducer enabled measurement of the pressure in the gastric tube at a sample rate of 1 Hz. To log the date, the pressure transducer was attached to an MMS wireless patient module (Laborie Europe/International, Enschede, The Netherlands).
As a safety measure, a pressure relief valve was added to a lumen centered on the anastomosis but was not used for oxygen delivery. If the pressure of the oxygen surrounding the anastomosis exceeded 20 mmHg, the oxygen could dissipate through this lumen and thus lower the pressure surrounding the anastomosis.
Statistical analysis
Data were expressed as mean ± standard deviation (SD) or numbers (%). We performed a paired Student's t-test to analyze the VAS score. The first 5 h of the intraluminal pressure measurements were not used for analysis, as the pressure was still stabilizing during this period. The pressure measurements are depicted as average pressure, maximum pressure, percentage of pressure above 20 mmHg, and most prolonged period above 20 mmHg. All analyses were performed using Matlab (R2020b, The MathWorks Inc., Natick Massachusetts) and GraphPad Prism (version 9, GraphPad Software, La Jolla, California, United States).
Results
Feasibility of the study
Sixteen patients were included in the study, three in the control group, 10 in the 1 ml/min oxygen group, and three in the 2 ml/min oxygen group. The 4 ml/min study group was not performed due to a failed safety evaluation check of the 2 ml/min group, which will be explained in the following sections. During surgery, in two patients, placement of the naso-esophageal oxygen delivery tube failed, resulting in the inclusion of two additional patients in the 1 ml/min group, and these patients were excluded from further analysis. One patient of the 1 ml/min group had a dilated gastric conduit on the chest x-ray. However, this occurred after the naso-esophageal tube was removed and recovered without any intervention needed. Eleven of the studied naso-esophageal tubes were inserted for the full duration of the study, the naso-esophageal tube was prematurely accidentally removed in five patients. Three of these five accidental removals were after day 3 and two after day 2. Due to these accidental removals, we improved the fixation of the tube at the nose by adding glue to improve the fixation of the lace to the catheter and again securing the strings on the forehead and nose. After this intervention we observed fewer accidental dislocations (2/3; 67 % vs 3/13; 23 %) (see Fig. 4). Table 2 summarizes patient characteristics and postoperative complications.
Fig. 4.
Flow diagram of the included patients and primary endpoint.
Table 2.
Patient characteristics.
| Control zero flow group | 1 ml/min oxygen group | 2 ml/min oxygen group | |
|---|---|---|---|
| Patient characteristics | |||
| Number of patients | 3 | 10 | 3 |
| Female sexa | 0 (0 %) | 2 (20 %) | 1 (33 %) |
| Age (years)a | 67.3 (4.5) | 66.1 (7.5) | 68.7 (11.1) |
| BMI (kg/m2)a | 24.7 (0.5) | 27.8 (5.1) | 28.0 (2.3) |
| ASA scorea | |||
| I–II | 3 (100 %) | 6 (60 %) | 2 (67 %) |
| III | 0 (0 %) | 4 (40 %) | 1 (33 %) |
| IV–V | 0 (0 %) | 0 (0 %) | 0 (0 %) |
| Tumour characteristics | |||
| Adenocarcinomab | 3 (100 %) | 9 (90 %) | 3 (100 %) |
| Squamous cell carcinomab | 0 (0 %) | 1 (10 %) | 0 (0 %) |
| Received neoadjuvant chemoradiotherapyb | 2 (67 %) | 9 (90 %) | 2 (67 %) |
| Comorbidities | |||
| Cardiaca | 1 (33 %) | 6 (60 %) | 1 (33 %) |
| Pulmonarya | 1 (33 %) | 3 (30 %) | 0 (0 %) |
| Vasculara | 1 (33 %) | 3 (30 %) | 3 (100 %) |
| Neurologica | 1 (33 %) | 1 (10 %) | 1 (33 %) |
| Diabetes mellitusa | 0 (0 %) | 1 (10 %) | 1 (33 %) |
| Complications | |||
| Anastomotic leakagea | 1 (33 %) | 2 (20 %) | 0 (0 %) |
| Pneumoniaa | 1 (33 %) | 1 (10 %) | 0 (0 %) |
| Atrial fibrillationa | 2 (67 %) | 1 (10 %) | 0 (0 %) |
| Chyle leaka | 0 (0 %) | 2 (20 %) | 0 (0 %) |
| Respiratory insufficiencya | 0 (0 %) | 1 (10 %) | 0 (0 %) |
| Re-admission Intensive carea | 0 (0 %) | 1 (8 %) | 0 (0 %) |
| Gastric dilatationa | 0 (0 %) | 1 (10.0 %) | 0 (0 %) |
| Surgical reinterventiona | 0 (0 %) | 0 (0 %) | 1 (33 %) |
Number (percentage).
Average (standard deviation).
Comfort of the study setup
The discomfort of the naso-esophageal tube was measured daily using a visual analog score, which can be seen in Fig. 5 (a lower score represents a lower level of comfort). The comfort score was relatively high on the first day, with an average of 80. In the following days, it showed a non-significant decline.
Fig. 5.
Daily comfort ratings of the study naso-esophageal tube assessed by a visual analog scale. The data is shown as average measurements along with the standard deviation.
Safety checks: intraluminal pressure recordings and gastric dilatation
Three intraluminal pressure recordings failed due to technical errors, one in the zero-control group, one in the 1 ml/min group, and one in the 2 ml/min group. Most of the intraluminal pressure recordings followed a similar pattern. Fig. 6 shows an exemplary pressure recording. An initial pressure spike can be seen, after which the pressure stabilizes and has minor variability. Table 3 shows the combined intraluminal pressure recordings of the different oxygen flow groups. The individual measurements are presented in Supplementary Table 1. The average and maximum pressure measurements of the zero-oxygen control group were slightly lower than the 1 ml/min group recordings but were comparable. One 1 ml/min group patient slightly exceeded 20 mmHg for shorter periods. The average and maximum pressure recordings of the 2 ml/min group were higher than the other groups and had a higher standard deviation. One of the patients in this group had an intraluminal pressure of more than 20 mmHg for a prolonged period, with the most extended period above 20 mmHg being almost 9 h. As a result, this met the conditions of safety check evaluations, and we did not proceed to the 4 ml/min group, thus stopping the study.
Fig. 6.
A representative intraluminal pressure recording of multiple days. An initial spike in pressure can be seen, after which the pressure stabilizes.
Table 3.
Intraluminal pressure measurements for the different study groups.
| Control zero flow group | 1 ml/min oxygen group | 2 ml/min oxygen group | |
|---|---|---|---|
| Patient characteristics | |||
| Average pressure (standard deviation) | 4.7 (1.0) mmHg | 7.8 (2.2) mmHg | 14.1 (8.0) mmHg |
| Maximum pressure | 14.1 mmHg | 19.1 mmHg | 53.5 mmHg |
| Percentage above 20 mmHg | 0.0 % | 1.3 % | 21.0 % |
| Longest period above 20 mmHg | 0.0 h | 0.9 h | 8.9 h |
Discussion
To our knowledge, this is the first study to investigate the feasibility of intraluminal oxygen delivery at the site of the anastomosis after esophagectomy. We designed a setup that makes it feasible to deliver oxygen intraluminal at the site of the anastomosis and have shown that an oxygen delivery of 1 ml/min is expected to be safe.
Feasibility of catheter placement and changes in the study setup
The general feasibility of the setup was good. Insertion of the naso-esophageal catheter was successful in most patients; in two patients (11 %), the insertion was unsuccessful. If the catheter could not be inserted in two attempts, the insertion was aborted, and the placement was deemed unsuccessful. We did not use a guidewire while inserting the catheter; using this might improve the catheter placement procedure.
At the start of the study, the catheter was secured to the patient by tying a lace around the catheter and fixating this with a plaster on the nose and forehead, as this is our routine for the fixation of naso-esophageal tubes. However, this proved insufficient, as we observed two accidental premature catheter removals in the first three patients. We improved the security of the catheter by adding glue to improve the fixation of the lace to the catheter and again securing the strings on the forehead and nose. After improved fixation, we observed fewer accidental dislocations (3/13; 23 %).
Comfort of the setup
The initial comfort scores of the setup were good (Fig. 4). The average VAS comfort score on day 1 was 73. However, this dropped to a score of 63 on day five, indicating decreased comfort during prolonged use. After observing this drop in comfort scores upon completion of the 1 ml/min group, the decision was made to shorten the duration of the oxygen delivery by the naso-esophageal tube from five to three days in the 2 ml/min group. The stiffness of the naso-esophageal tube likely contributed to the additional discomfort of the intervention. In some instances, patients noticed this immediately after removing the intervention tube. They reported more movements of the tube during swallowing and talking.
Safety measures
In the 1 ml/min group, one of the patients barely exceeded the pressure level of 20 mmHg. One patient had a dilatated gastric conduit. This was noticed after the removal of the study catheter and recovered without intervention. This gastric dilatation was not harmful. However, the peaks of the pressure measurements of the 2 ml/min group did exceed 20 mmHg for a prolonged period of time. This exceeded our safety level and was deemed unsafe. Even though the difference in measured pressure was not statistically significant, our opinion is that the maximum oxygen delivery should not exceed 2 ml/min.
We had originally planned to also include a 4 ml/min group, however, after the safety checks of the 2 ml/min group were exceeded, this group was not included.
Lessons learned and possible improvements to the setup
The current setup can be improved on several aspects. Firstly, the naso-esophageal tube was a multi-lumen esophageal manometer catheter with 24 lm. We utilized only five of these lumens. A majority of the available lumens were not needed for this application. In future studies, a specifically tailored naso-esophageal tube could be created with fewer lumens, reducing the thickness and improving the flexibility of the catheter. Another option could be to incorporate the oxygen delivery lumens into the standard nasogastric tube so that no additional naso-esophageal tube needs to be inserted. Secondly, the catheter could be outfitted with additional sensors. An option would be the addition of a pulse oximeter sensor to measure the tissue oxygen levels at the site of the anastomosis.
Future possibilities
This study investigated the feasibility and acceptable flow rates of intraluminal oxygen administration. More studies need to be conducted to assess whether intraluminal oxygen administration effectively reduces AL after esophagectomy. This study is the first step to improving wound healing of the anastomosis by delivering local oxygen, potentially decreasing the incidence of AL. In gastrointestinal surgery, AL is still one of the most severe complications, with significant impact on patient outcomes and resources.
Conclusion
To conclude, we showed that intraluminal oxygen delivery near the site of the anastomosis is feasible and safe with an oxygen flow of 1 ml/min. The use of intraluminal oxygen could potentially reduce AL incidence and, therefore, improve patient survival and clinical practice. Further studies are needed to investigate this.
The following is the supplementary data related to this article.
Intraluminal pressure measurements for all the individual patients.
CRediT authorship contribution statement
Douwe van der Steen: Conceptualization, Formal analysis, Investigation, Writing – original draft. Anne M. Leferink: Conceptualization, Writing – review & editing, Visualization, Methodology. Frederieke A. Dijkstra: Conceptualization, Writing – review & editing. Boudewijn van Etten: Conceptualization, Writing – review & editing. Eric Keus: Conceptualization, Writing – review & editing. Rutger J. Spruit: Conceptualization, Writing – review & editing. Roy J.J. Verhage: Conceptualization, Writing – review & editing. Jeroen J. Kolkman: Conceptualization, Writing – review & editing, Methodology. Jan Willem Haveman: Conceptualization, Investigation, Methodology, Supervision, Writing – review & editing.
Statement of ethics
The UMCG's institutional Review Board approved the study (NL69801.042.19). All patients were asked to provide written consent and were given more than 24 h to decide whether to participate in the study.
Funding sources
The esophagus pressure catheters were donated in kind by Laborie/Medical Measurement Systems B.V. (Enschede, Overijssel, The Netherlands). They had no say in the design of the study or draft of the manuscript. No further funding has been obtained for this study.
Declaration of competing interest
The authors report no proprietary or commercial interest in any product mentioned or concept discussed in this article.
Acknowledgements
We sincerely thank Jakob Hut for his valuable technical advice and dedicated assistance with the equipment, which contributed significantly to this work.
Glossary
- AL
Anastomotic leakage
- UMCG
University Medical Center Groningen
- VAS
Visual analog scale
- SD
Standard deviation
Data availability
The datasets used and/or analyzed during the current study are not publicly available due to them containing privacy sensitive information. The data is available from the corresponding author upon reasonable request.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Intraluminal pressure measurements for all the individual patients.
Data Availability Statement
The datasets used and/or analyzed during the current study are not publicly available due to them containing privacy sensitive information. The data is available from the corresponding author upon reasonable request.