Abstract
Background and Aim: Anastomotic leakage, the most common major complication after esophagectomy, is an important early postoperative complication that results in reoperation, delayed discharge, and psychological and financial distress. The current study focused on gastric conduit blood flow and investigated the relationship between gastric conduit temperature and anastomotic leakage. Patients and Methods: Between July 2015 and December 2017, a total of 51 patients aged 38 to 84 years who underwent esophagectomy followed by esophagogastric anastomosis with gastric conduit reconstruction were enrolled. Thermography was then used to measure the temperature of the intact stomach and gastric conduit before anastomosis. Results: The temperature of the planned site of gastric conduit anastomosis was significantly inversely correlated with anastomotic leakage, with the receiver operator characteristic curve showing a cutoff point of 27.6°C for predicting anastomotic leakage. Conclusion: The temperature of the planned gastric tube anastomosis line should be kept at 27.6°C or higher to reduce anastomotic leakage.
Although improved perioperative care and development of novel surgical technologies and techniques have greatly improved postoperative survival, surgical interventions have continued to be associated with significant morbidity and mortality. Anastomotic leakage, the most common major complication after esophagectomy, is a particularly important early postoperative complication that results in reoperation, delayed discharge, and psychological and financial distress. Hall et al. reported that prolonged operative time, increased preoperative white blood cell count, pre-existing diabetes, and perioperative transfusion were independently associated with anastomotic leakage in esophageal cancer (1). Moreover, Gao et al. reported that high postoperative drainage amylase content and low pre-albumin concentration might be potential risk factors for anastomotic leakage in patients who underwent minimally invasive McKeown esophagectomy (2), while Park J et al. revealed that the C-reactive protein level on the third postoperative day was a significant independent predictor of anastomotic leakage while identifying a significant diagnostic cutoff value for the development of anastomotic leakage after esophagectomy (3). Furthermore, Sato et al. reported that the sternum–trachea distance/sternum–vertebral body distance ratio was associated with cervical anastomotic leakage after retrosternal gastric conduit reconstruction following esophagectomy (4). Multiple technical parameters have been proposed to ensure the formation of an ideal esophagogastric anastomosis. Although several studies and meta-analyses have individually examined such parameters, none have shown a single approach or technique to be the most successful. Sheraz et al. reported that the cervical group developed anastomotic leakage more frequently than the thoracic group after examining numerous cases of esophagogastric anastomosis (5). Several facilities have implemented measures and examinations for the prevention of anastomotic leakage. Accordingly, Hu et al. reported that retrosternal tunnel expansion, gastric tube widening, sternothyroid muscle resection, and gastric tube fixation reduce the incidence of cervical anastomotic leakage after esophagectomy (6). Moreover, blood supply to the gastric conduit has traditionally been evaluated by inspecting the gastric serosa. Koyanagi et al. reported that intraoperative evaluation of blood flow speed through indocyanine green (ICG) fluorescence in the gastric conduit wall was a useful method for predicting the risk of anastomotic leakage after esophagectomy (7). Moreover, Campbell et al. reported that intraoperative vascular evaluation using ICG fluorescence imaging and Doppler examination of the gastric conduit may reduce anastomotic leakage after esophagectomy (8).
Apart from the aforementioned studies, Nishikawa et al. reported that intraoperative thermal imaging of the gastric tube surface can be utilized as a noninvasive and reliable technique for assessing blood flow and gastric tube viability (9). Moreover, they were the first to suggest that thermal imaging could be used to delineate the area of good perfusion in the gastric conduit for esophageal reconstruction and that it was superior to ICG in the quantitative assessment of viability after prospectively evaluating 263 patients who had undergone esophagectomy with gastric conduit reconstruction (10). The current study similarly performed blood flow evaluation using thermography to evaluate gastric conduit blood flow and determine whether such assessments remained clinically relevant for some time, although our results somewhat differ from those previously published. The present study provides novel findings regarding the evaluation of gastric conduit blood flow for the purpose of reducing anastomotic leakage that are highly likely to be utilized clinically.
Patients and Methods
This single-center retrospective study was conducted between July 2015 and December 2017 and included 45 males and six females aged 38 to 84 years [mean age±standard deviation (SD), 66.8±8.1 years]. Patients underwent transthoracic or video-assisted esophagectomy followed by esophagogastric anastomosis with gastric conduit reconstruction at the Department of General Surgical Science, Gunma University Graduate School of Medicine, Japan. All patients were preoperatively diagnosed using routine endoscopic examination with biopsy, endoscopic ultrasonography, computed tomography, and positron-emission tomography. Clinical staging and pathological examination for resected specimens were performed in accordance with the Guidelines for Clinical and Pathological Studies on Carcinoma of the Esophagus of the Japanese Society for Esophageal Diseases (11). Furthermore, tumor stage was classified according to the seventh edition of the tumor-node-metastasis classification system developed by the International Union Against Cancer (12). This study was approved by the Institutional Review Board of our hospital (HS2020-104), while all patients provided written informed consent for the use their data. Regarding the definition of anastomotic leakage, cases diagnosed by endoscopy and esophageal contrast examination were included, and minor leakage cases that were improved by antibiotic treatment were also included.
Evaluation of intact stomach and gastric conduit blood flow using thermographic imaging. Gastric conduit temperature was measured using an infrared thermographic camera (Testo Company®, Yokohama, Japan) at two time points: (i) After cutting the treated blood vessel, and (ii) after creating the gastric conduit (before anastomosis). Blood flow was measured at the vestibular site, gastric body, and planned site of anastomosis of the stomach (Figure 1), while absolute values for the planned anastomotic temperature and vestibular temperature, as well as their ratio, were used as parameters for evaluating blood flow. Total measurement time was approximately 20 s per patient. Thereafter, the correlation between temperature measurements and the presence or absence of anastomotic leakage was examined.
Temperatures of the intact stomach and gastric conduit using thermographic imaging. Average absolute values (mean±standard deviation) of each measurement site (vestibular site, gastric body, and planned anastomosis site) at the whole stomach stage (A) and at the gastric conduit stage (B) are shown.
Statistical analysis. All statistical analyses were performed using JMP Pro Version 14 software (SAS Institute Japan, Tokyo, Japan). An average of three sites A to C was used to analyze this study. Continuous data were analyzed using Student’s t-test or the Mann–Whitney U-test, while categorical data were analyzed using Person’s chi-squared test, Fisher’s exact test, or the Mann–Whitney U-test, as appropriate, with p<0.05 indicating statistical significance.
Results
Table I shows the correlation between patient characteristics and anastomotic leakage. No significant correlation was observed between patient characteristics, including preoperative comorbidity, preoperative treatment, and reconstruction route, and the presence or absence of anastomotic leakage. The average values (mean±SD) of each site of temperature measurement in the intact stomach and gastric conduit are summarized in Figure 1. As expected, the temperature decreased slightly from the vestibular site toward the cardiac region or tip of the gastric conduit. Figure 2 shows the correlation between the temperature of the planned anastomosis site and the presence or absence of anastomotic leakage in the whole stomach and gastric conduit. Significant inverse correlation was noted between the temperature of the planned site of the gastric conduit anastomosis and anastomotic leakage (p=0.007) (Figure 2B), although no significant correlation was found between the temperature of the planned anastomosis site of whole stomach and anastomotic leakage (Figure 2A). Moreover, Figure 3 shows the correlation between the temperature ratio for the planned anastomosis site/vestibular site and anastomotic leakage in the whole stomach and gastric conduit. No significant correlation was noted between these aforementioned temperatures and anastomotic leakage, although a higher temperature ratio led to fewer anastomotic leakages.
Correlation between patient characteristics and anastomotic leakage.
Correlation of the temperature of the planned anastomosis site for the intact stomach (A) and gastric conduit (B) according to anastomotic leakage.
Correlation of the temperature ratio for the planned anastomosis site/vestibular site for the intact stomach (A) and gastric conduit (B) according to anastomotic leakage.
Receiver operator characteristic curve analysis revealed a cutoff temperature of 27.6°C at the planned site of gastric conduit anastomosis for predicting anastomotic leakage (Figure 4), such that temperatures ≥27.6°C led to significantly less anastomotic leakage.
Rate of anastomotic leakage according to temperature using the receiver operator characteristic curve cutoff point for temperature in the gastric conduit. The rate of anastomotic leakage was 11.4% in the group with an anastomotic site temperature of 27.6°C or higher but was 50% in the group with a temperature below 27.6°C.
Discussion
A large multicenter study revealed that severe anastomotic leakage after esophagectomy in esophageal cancer adversely affects cancer prognosis and increases local recurrence (13). Given that anastomotic leakage after esophagectomy has remained a serious complication associated with prognosis, esophageal surgeons need to at least attempt to address such a problem. After measuring the gastric conduit temperature using thermography, the current study revealed that the temperature at the site planned for gastric conduit anastomosis was inversely associated with anastomotic leakage. Our findings are consistent with those reported by Nishikawa et al. (9, 10) and may indirectly indicate that the measuring gastric conduit temperature using thermography reflects the blood flow therein. Moreover, our results showed that anastomotic leakage was less likely to occur at planned gastric conduit anastomotic sites with temperatures of 27.6°C or higher as measured using thermography. Several factors have been reported to cause anastomotic leakage after esophageal cancer surgery (1-6), and it remains unclear whether only a single factor is involved or not. Nonetheless, direct temperature measurements have been shown to reflect blood flow, which is also considered a major factor. Moreover, as a matter of course, our results demonstrated that performing anastomosis on the pylorus side, where the temperature was highest, was preferable in order to prevent anastomotic leakage. Therefore, the current study highlights the need for measuring gastric conduit temperature and utilizing various measures to increase the temperature of the gastric tube and anastomosis site to over 27.6°C in cases exhibiting lower temperatures at these sites. Similarly, one study showed that ICG can be used for observing gastric conduit blood flow during surgery (7). However, ICG may promote allergic reactions, albeit rarely (14), and requires a longer examination time. Conversely, measuring the temperature of the gastric conduit surface is simpler and safer given that it carries a shorter evaluation time and does not require direct contact with the gastric conduit surface.
Given that all cases included herein underwent end-to-side anastomosis using a circular stapler, other anastomosis methods might have provided slightly difference results. Moreover, the type of thermograph used, differences in the operating room temperature setting at each facility, differences in the patient’s body temperature, and the effect of drugs during surgery might introduce some errors in the measurement of absolute temperature values. Further studies should therefore be conducted in the future, with the current one serving only as a guide. Numerous problems need to be considered when identifying at which gastric conduit site temperature should be measured, such as (i) identifying the most suitable site for predicting anastomotic leakage, (ii) determining the size of the gastric conduit, (iii) whether or not anastomosis is to be conducted at the planned site, and (iv) whether or not it is better to carry out temperature measurement after the anastomosis. Furthermore, this study did not evaluate gastric conduit congestion, a concern that needs to be addressed. In addition, given the insufficient number of cases included herein, future studies need to include a larger number of cases.
The current study showed that the temperature of the planned gastric conduit anastomosis line was inversely correlated with the onset of anastomotic leakage following esophagectomy with gastric conduit reconstruction. Considering the simplicity and safety of evaluating gastric tract blood flow using thermography, we would like to conduct further examinations after appropriately establishing the necessary conditions. Despite the considerable effort exerted by esophageal surgeons and the difficulty in modifying current policies, we believe that any effort directed towards eliminating suture failure after esophageal cancer would be a step in the right direction. Hence, esophageal surgeons should continue working towards reducing anastomotic leakage as much as possible, which would in turn contribute to improved prognosis.
Acknowledgements
The Authors would like to thank Enago (www.enago.jp) for English language review.
Footnotes
Authors’ Contributions
Makoto Sohda and Tatsuya Miyazaki: Substantial contributions to the conception or design of the work. Takayoshi Watanabe, Nobhiro Nakazawa, Yasunari Ubukata, Kengo Kuriyama, Keigo Hara, Makoto Sakai, Akihiko Sano and Takehiko Yokobori: Acquisition of data. Hiroomi Ogawa: Interpretation of data. Ken Shirabe: Interpretation of data and advice. Hiroshi Saeki: Interpretation of data and overall advice.
Conflicts of Interest
The Authors have no financial conflicts of interest to disclose concerning this study.
- Received November 4, 2020.
- Revision received November 22, 2020.
- Accepted November 24, 2020.
- Copyright© 2021, International Institute of Anticancer Research (Dr. George J. Delinasios), All rights reserved.
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