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Ann Thorac Surg 2002;74:1917-1922
© 2002 The Society of Thoracic Surgeons

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Original article: general thoracic

Does continuous mucosal partial carbon dioxide pressure measurement predict leakage of intrathoracic esophagogastrostomy?

^a Department of Visceral and Vascular Surgery, University of Cologne, Cologne, Germany

Accepted for publication July 2, 2002.

* Address reprint requests to Dr Schröder, Department of Visceral and Vascular Surgery, University of Cologne, Joseph-Stelzmann Str 9, 50931 Cologne, Germany.
e-mail: wolfgang.schroeder{at}uni-koeln.de

	Abstract

Top Abstract Introduction Patients and methods Results Comment References

 
BACKGROUND: Gastroplasty after esophagectomy is associated with relevant morbidity due to anastomotic leakage of the esophagogastrostomy. The aim of this study was to find out whether continuous partial carbon dioxide pressure (pCO₂) measurement of the gastric mucosa is an adequate method of monitoring the gastric tube during the postoperative course and of detecting patients with an anastomotic leakage.

METHODS: Forty-seven patients with esophageal cancer underwent esophagectomy and gastric tube formation with intrathoracic esophagogastrostomy. Postoperatively, mucosal pCO₂ of the gastric tube (pCO₂i) was measured using continuous tonometry (TONOCAP, Datex Ohmeda). pCO₂i was related to the arterial pCO₂ (pCO₂ = pCO₂i - pCO₂a).

RESULTS: A total of 4,338 pCO₂ measurements were recorded. On average, the pCO₂i of each patient was monitored over a period of 92 hours. In 5 patients an anastomotic leakage of the esophagogastrostomy developed. The mean pCO₂ of this group was 31.7 mm Hg (±19.3 SD) and significantly higher (p < 0.0001) than that of patients without anastomotic leakage (20.7 mm Hg ± 12.8 SD). With a pCO₂ cut-off point of 56 mm Hg measured for 5 hours, the sensitivity was 0.8, the specifity 0.9, and the positive predictive value 0.5. In patients with anastomotic leakage, the peak pCO₂ preceded clinical symptoms. False positive pCO₂ measurements (n = 4) were mainly due to severe pneumonia with long-term ventilation.

CONCLUSIONS: Mucosal pCO₂ measurement of the gastric tube can be used as an early indicator of a complicated postoperative course predicting anastomotic leakage of the esophagogastrostomy.

	Introduction

Top Abstract Introduction Patients and methods Results Comment References

 
The standard reconstruction after esophagectomy is the formation of a gastric tube with cervical or intrathoracic esophagogastrostomy [1]. This type of reconstruction is associated with a considerable morbidity and mortality due to anastomotic leakage of the esophagogastrostomy [2, 3]. The main cause of anastomotic leakage is the partial devascularization of the lesser curvature with ligature of the left gastric artery, which results in an impaired microcirculation in the anastomotic region of the gastric fundus [4]. Several clinical studies could prove these intraoperative changes after gastric tube formation [5–8]. Although almost all patients demonstrate these intraoperative changes, only a few of them develop an anastomotic leakage during the postoperative course. Therefore the monitoring of the gastric conduit has to focus on the postoperative course in order to detect patients in whom reduced perfusion results in impaired anastomotic healing with consecutive leakage. Only a few studies have addressed this clinical problem and monitored the interponate postoperatively [9, 10].

Tonometry is defined as measurement of the partial carbon dioxide pressure in the gastric mucosa (pCO₂i, in mm Hg), and has been used as an index of splanchnic perfusion in critically ill patients [11–13]. Two intraoperative studies could demonstrate that continuous pCO₂i measurement is a valid method of detecting microcirculatory changes during formation of a gastric tube after esophagectomy [7, 8].

Therefore the question of this study was whether continuous pCO₂i measurement can be used to monitor microcirculation of the gastric conduit during the postoperative course and to detect those patients who develop an anastomotic leakage.

	Patients and methods

Top Abstract Introduction Patients and methods Results Comment References

 
Patients
From April 1999 to November 2001, 47 consecutive patients with an esophageal carcinoma were included in this prospective protocol. Forty-one patients were male, 6 were female. The mean age was 60.5 years (range 27 to 75). In 32 patients (68.1%), the carcinoma was classified as adenocarcinoma and 15 patients (31.9%) had a squamous cell carcinoma. Because of a locally advanced tumor 14 patients (31.9%) received neoadjuvant radiochemotherapy according to a standardized protocol. In 25 patients histopathologic examination of the specimen demonstrated a tumor confined to the muscularis (pT1/2). In 22 patients the primary tumor extended the muscularis (pT3). The American Society of Anesthesiologists (ASA) classification was used to analyze patients’ preoperative condition. The distribution of ASA scores was as follows: ASA 1: n = 3 (6.4%); ASA 2: n = 27 (54.4%); ASA 3: n = 17 (36.2%).

Surgery
In all 47 patients a standardized transthoracic esophagectomy with two-field lymphadenectomy of the abdominal and mediastinal compartment was performed [14].

After laparotomy and opening of the hiatus the resectability of the primary tumor and the absence of distant metastases were reconfirmed. The duodenum was mobilized by an extensive Kocher maneuver followed by dissection of the gastrocolic ligament with maintenance of the right gastroepiploic artery along the greater curvature. The right gastric artery was preserved. In addition, partial en-bloc lymphadenectomy of abdominal compartment II was performed. Before closure of the abdomen the pylorus was mechanically dilated and gastric tube formation was commenced by placing one linear stapler at the lesser curvature between the middle and distal third.

After moving the patient into a left lateral position, an anterolateral thoracotomy through the fifth intercostal space was performed, followed by an en-bloc resection of the esophagus with dissection of the azygos vein and thoracic duct. Lymph node dissection of the upper mediastinum included the paraesophageal and right-sided paratracheal nodes. The esophagus was transected in the upper mediastinum 5 cm above the azygos vein and the stomach was pulled into the chest. A stapler esophagogastrostomy was performed between the gastric fundus and esophageal stump using a circular stapler (CEEA 28 [Autosuture, Germany]) inserted through the lesser curvature. The procedure was completed by resection of the lesser curvature with the adherent esophagus using a linear stapler (TAA 90, Autosuture). After finishing the intrathoracic anastomosis, a 16F tonometry nasogastric tube with a silicone balloon at its distal end (Datex Ohmeda, Duisburg, Germany) was placed in the gastric conduit. The upper edge of the silicone balloon was positioned 2 cm below the anastomosis under bimanual palpation.

The mean operation time was 395 minutes (range 250 to 560). During the intraoperative and postoperative course, a mean 1.8 U (range 0 to 18 U) packed red blood cells was administered. Twenty-eight of 47 patients (59.6%) required no blood transfusion. In all patients a complete resection of the primary tumor could be achieved (R0 resection).

Postoperative management included treatment in the intensive care unit (ICU) followed by monitoring of the patient’s course in the intermediate care unit. For statistical analysis this was summarized as "ICU stay." Daily chest roentgenography was performed to check on the correct position of the nasogastric tube and to look for radiologic evidence of pneumonia. Any prolonged mechanical ventilation due to pneumonia was treated by systemic antibiotics and a puncture tracheostomy to ensure an adequate bronchial lavage. Depending on clinical symptoms and the time interval after the operation, endoscopy or contrast swallow, or both, was performed to detect an anastomotic leakage. Routine postoperative contrast radiology was not considered to be useful [17, 18]. A detailed documentation of all postoperative surgical and general complications was carried out.

Postoperative tonometry
Continuous tonometry is based on recirculating gas analysis with a TONOCAP device (Datex Ohmeda, Duisburg, Germany). Recirculating gas analysis requires a silicon balloon with a semipermeable membrane (16F tonometry tube; Datex Ohmeda), which is automatically filled with a defined CO₂ concentration by the TONOCAP. After a definite time of equilibration with the mucosal CO₂, the gas is automatically sucked out of the balloon. The TONOCAP indirectly measures the mucosal pCO₂ from the gradient between mucosal and balloon CO₂ concentration. The CO₂ concentration is expressed as partial pressure (mm Hg). This cycle is repeated at 15-minute intervals.

Immediately after admission to ICU, pCO₂i measurement commenced. According to the manufacturer’s instruction, calibration of the TONOCAP required three to four cycles of recirculating gas analysis so that pCO₂i measurement of the first hour was not included for further analysis. Thereafter, one pCO₂i value was documented each hour. An initial chest roentgenogram confirmed the correct position of the nasogastric tube with its silicone balloon below the intrathoracic anastomosis. According to international standards [17, 18], pCO₂i was related to the arterial pCO₂ (pCO₂ = pCO₂i - pCO₂a). Arterial pCO₂ was obtained by regular blood gas analysis performed at least every 6 hours. All patients received a daily dosage of 40 mg omeprazle intravenously until oral intake on postoperative day 7 to 9 was begun. Postoperative tonometry was performed for as long as the patient required the nasogastric tube for emptying the gastric tube or was treated in the ICU. The decision to remove the nasogastric tube was entirely based on clinical judgment and was not influenced by the study protocol.

The study protocol was approved by the local institutional human research committee (No. 99045, 28 April 1999).

Statistical analysis
Aggregated data are presented using the usual descriptive means. To describe differences between various pCO₂, Student’s t test for unpaired samples or analysis of variance was used as appropriate. Posthoc analysis of subgroup differences was done using the Scheffe method. A p < 0.05 was considered significant. For the variables "anastomotic leakage" and "septic syndrome," sensitivity, specifity, and predictive value of postoperative pCO₂ as a diagnostic test were calculated from receiver operating characteristics (ROC). The definition of the cut-off point based on the ROC curve included the measurement of the designated pCO₂ for at least 5 hours. All computations were done using SPSS statistical software (version 10; SPSS Inc, Chicago, IL).

	Results

Top Abstract Introduction Patients and methods Results Comment References

 
Surgical results
Postoperative complications are summarized in Table 1. In 5 patients (10.6%) an anastomotic leakage of the esophagogastrostomy developed during the postoperative course (Table 2). On clinical suspicion of a leak in 3 patients the diagnosis was confirmed endoscopically during the early postoperative course between the postoperative days 3 and 5. They all underwent rethoracotomy, which demonstrated a limited ischemia of the tip of the gastric conduit. The poorly perfused portion was resected and a mechanical reanastomosis performed. In 2 of these 3 patients anastomotic leakage was associated with a septic syndrome requiring long-term mechanical ventilation and hemodynamic support. In 2 other patients the anastomotic leakage was diagnosed by contrast radiology on postoperative days 11 and 14. Endoscopy revealed small leaks in an otherwise vital conduit. Both patients were treated endoscopically with fibrin glue [19]. Otherwise the postoperative course of these patients was uneventful.

View this table: [in this window] [in a new window]   Table 2. Clinical Data and pCO2 Measurements of 5 Patients With Anastomotic Leakage of the Esophagogastrostomy

Measurement of pCO₂
A total of 4,338 pCO₂ measurements with a mean pCO₂ of 22.0 mm Hg (±14.2 SD) was recorded and included for further analysis. Based on an hourly documentation of pCO₂ values the gastric conduit of each patient was monitored over an average period of 92.3 hours (range 17 to 159).

For 42 patients without anastomotic leakage 3,832 pCO₂ measurements were analyzed. The histogram of these pCO₂ measurements showed an ordinary distribution with a mean pCO₂ of 20.7 mm Hg (±12.8 SD; Fig 1). For 5 patients with anastomotic leakage a total of 506 pCO₂ values were recorded. The mean pCO₂ in this group was 31.7 mm Hg (±19.3 SD) and significantly higher (p < 0.0001) compared with patients without anastomotic leakage (Fig 1). The optimal cut-off point calculated from ROC curve was a pCO₂ of 56 mm Hg measured for 5 hours (Fig 2). For this pCO₂ value the sensitivity was 0.8, the specifity 0.9, and the positive predictive value 0.5. The area under the ROC curve was 0.83. For this cut-off point, 4 of 5 patients with anastomotic leakage were identified by continuous tonometry (Table 2). In all 4 patients the defined cut-off point was measured for at least 5 hours and observed within the first 48 hours after the operation. This was before the clinical diagnosis of an anastomotic leak was suspected (Table 2). One patient did not fulfill the pCO₂ criteria of anastomotic leakage and was considered to be falsely negative.

View larger version (45K): [in this window] [in a new window]   Fig 1. Distribution of partial carbon dioxide pressure (pCO2) measurements (in percent) for 42 patients without anastomotic leakage and 5 patients with anastomotic leakage.

View larger version (28K): [in this window] [in a new window]   Fig 2. Receiver operating curve for the variable anastomotic leakage.

In 22 patients who had radiologic or microbiologic evidence, or both, of pneumonia during the postoperative course, a total of 2,263 pCO₂ measurements with a mean of 22.3 mm Hg ± 14.2 SD was recorded. For 25 patients without postoperative pneumonia (2075 pCO₂ measurements), the mean pCO₂ was not different (21.7 mm Hg ± 14.2 SD). In 5 patients with a septic syndrome and multiple organ failure, the mean pCO₂ of 470 recorded pCO₂ measurements was 26.4 mm Hg ± 15.9 SD. This was significantly different (p < 0.0001) from the 42 patients who had no septic complication during the postoperative course (3868 pCO₂ measurements, mean pCO₂ 21.5 mm Hg ± 13.8 SD). For the variable "septic syndrome," the cut-off point of 56 mm Hg measured for 5 hours revealed a sensitivity of 0.6, a specifity of 0.88, and a positive predictive value of 0.36. The area under the ROC curve was calculated as 0.76.

For analysis of pCO₂ measurement before and after extubation, 5 of 47 patients had to be excluded as mechanical ventilation exceeded postoperative pCO₂ measurement, so that no pCO₂ values were obtained after extubation. In 42 patients all pCO₂ measurements obtained during postoperative mechanical ventilation (n = 819) were compared with the first 7 pCO₂ measurements after extubation (approximately 7 hours) during spontaneous ventilation (n = 294). In 27 of 42 patients (64.3%) there was a significant increase of pCO₂ measurement after extubation. The mean pCO₂ during mechanical ventilation (15.1 mm Hg ± 10.8 SD) was significantly lower (p < 0.0001) compared with the mean pCO₂ (23.4 mm Hg ± 14.9 SD) after extubation.

	Comment

Top Abstract Introduction Patients and methods Results Comment References

 
Anastomotic leakage of the esophagogastrostomy is still of major concern in esophageal surgery. In a recent meta-analysis it could be demonstrated that transthoracic esophagectomy is associated with a hospital mortality of 9% [3]. The main causes of postoperative morbidity and mortality after transthoracic esophagectomy with intrathoracic reconstruction are pulmonary complications and anastomotic leaks [3]. Anastomotic problems are mainly due to an impaired microcirculation in the anastomotic region of the gastric fundus, which is the result of partial devascularization of the lesser curvature with the dissection of the left gastric artery [4]. Several studies focused on the intraoperative deterioration of microcirculation but were not able to correlate intraoperative findings with the postoperative incidence of anastomotic leaks [5, 6]. At present only few investigations with a small number of patients aim to monitor the microcirculation of the gastric conduit during the postoperative course [9, 10]. In these studies the applied methods are of limited use for routine postoperative monitoring [9, 10]. In general any postoperative monitoring of the gastric tube must meet the criterion of early detection in order to justify the additional effort of monitoring and to achieve a clinical benefit for those patients developing an anastomotic complication.

This study was conducted to evaluate continuous pCO₂i measurement as a method of postoperative monitoring of the gastric conduit. In contrast to other methods [9] the simple clinical application of continuous tonometry is striking as it requires only the positioning of an intraluminal nasogastric tube—a procedure performed by most surgeons to splint the esophagogastrostomy and to empty the gastric tube postoperatively. From this point of view pCO₂i measurement appears to be a favorable method of monitoring that can also be applied outside of an ICU. In previous studies tonometry was used to predict the outcome of ICU patients with a broad variety of different clinical diagnoses [11–13]. The general principle of continuous tonometry is based on the indirect measurement of mucosal pCO₂, which is used as an index of splanchnic perfusion [17, 18]. Splanchnic hypoperfusion results in an increase of cellular pCO₂ by two mechanisms. First, hypoperfusion induces a switch from aerobic to anaerobic metabolism with increased production of mucosal pCO₂. Second, hypoperfusion reduces the "washout" of mucosal pCO₂, which then accumulates in the gastric mucosa. According to international standards adequate mucosal pCO₂ measurement is performed as automated recirculating gas analysis, which has proved to be more sensitive than gastric saline tonometry [17, 18]. Furthermore, pCO₂i measurement is related either to end-expiratory pCO₂ (pCO₂e) or arterial pCO₂ (pCO₂a) in order to exclude the influence of pulmonary or hemodynamic factors [17, 18]. This pCO₂ is known to be superior to the mucosal pH (pHi) calculation because it does not depend on intra and extracellular bicarbonate concentration [17, 18]. Because pCO₂ values also reflect the actual pCO₂a, the measurement of other variables such as mixed venous saturation or cardiac index seems to be unnecessary. All these requirements of adequate pCO₂i measurement are fulfilled in this clinical study. The influence of H₂ blockers or proton pump inhibitors on pCO₂i measurement is still not known and a matter of controversial discussion [17, 18].

In the case of gastric tube formation, hypoperfusion in the critical region of the gastric fundus is induced by partial devascularization of the lesser curvature. This surgical procedure also reduces the integrity of the intramural capillary network [4]. Two clinical studies demonstrated that continuous tonometry is a valid method of detecting pCO₂i changes associated with gastric tube formation [7, 8]. Both studies reported a remarkable increase of pCO₂i during the operative procedure.

This is the first clinical study that investigates continuous tonometry as a method of monitoring the gastric tube during the postoperative course. A large series of 47 patients with an esophageal carcinoma was included. All patients underwent a transthoracic esophagectomy. The reconstruction was performed by a standardized gastric tube with intrathoracic esophagogastrostomy. It is remarkable that in almost all patients—even patients with an uncomplicated postoperative course—the pCO₂i measurement was clearly elevated when compared with the arterial pCO₂. Such an obvious gap between arterial and mucosal pCO₂ has not been described for any other patient group of other studies, indicating that increased pCO₂ values are not a prognostic factor for ICU patients in general.

Another phenomenon detected with continuous tonometry is that microcirculation of the gastric conduit deteriorates during the time of extubation, which can be explained by two physiologic mechanisms. First, extubation is associated with the release of endogenous catecholamines, which might cause vasoconstriction and consecutive hypoperfusion of the splanchnic region. Secondly, extubation is associated with an increase in abdominal muscle tension, causing elevated abdominal pressure. This increases the duodenogastric reflux of alkaline juice so that bicarbonate neutralizes H+ ions, resulting in an increased concentration of luminal pCO₂. Since the gastric interponate is vagotomized, it is unlikely that gastric mucosa still generates H+ ions in the early postoperative course. Therefore the increase in mucosal pCO₂ after extubation seems to be a true accumulation resulting from endogenous vasoconstrictors and hypoperfusion. The clinical consequence is to be aware of the decreased perfusion in the gastric interponate during extubation and to reduce the patient’s postoperative stress by adequate administration of analgetics.

The high rate of pulmonary complications can be explained through a very detailed and thorough documentation, including even patients with radiologic suspicion of pneumonia. An early indication for tracheostomy is part of a consequent ICU management for these patients, resulting in overall low mortality. In this series 5 of 47 patients developed an anastomotic leakage during the postoperative course. This complication rate is comparable with that of other recent reports on intrathoracic esophagogastrostomy [16]. To identify patients with this complication the establishment of an appropriate pCO₂ cut-off point is important. Assuming that only a hypoperfusion of a longer period can cause an anastomotic leakage, the designated cut-off point had to be measured for at least 5 hours. Based on this time interval and ROC analysis a pCO₂ of 56 mm Hg identified 4 of 5 patients as having an anastomotic problem. It is of major interest that in all 4 patients identified with continuous tonometry the peak pCO₂ measurement occurred clearly before the clinical manifestation of the anastomotic leakage. This appears to be the real advantage of continuous pCO₂i measurement—that it serves as an early diagnostic indicator of anastomotic leakage. Therefore it may help to reduce morbidity and mortality associated with this surgical complication.

One patient with an early anastomotic leak on postoperative day 5 was not detected by mucosal pCO₂ measurement. At the time of diagnosis, endoscopy revealed a small leak but a well-perfused mucosa of the gastric interponate. This patient clearly demonstrates the limitations of continuous tonometry with false negative results in case of technically defective anastomoses of an otherwise well-perfused interponate. In addition, improper positioning of the silicon balloon in the antrum or even in the corpus can cause false negative results when pCO₂i measurement is obtained from well-perfused gastric regions and not the important anastomotic region in the fundus.

Four patients were classified as false positive without developing an anastomotic leakage during the postoperative course. Three of these patients had prolonged ICU treatment owing to pulmonary and septic complications. In this respect continuous tonometry fulfills its task as an index of splanchnic perfusion and predictor of the general outcome of ICU patients, as has been demonstrated in other studies [11–13]. It is of major importance that for patients with an anastomotic leakage as well as for the false positive patients the pCO₂ peak was measured within the first 48 hours. This means that postoperative continuous tonometry limited to this interval still detects the patients of interest.

In summary, the results of this study suggest that continuous tonometry helps to identify patients in the early postoperative stage who are at risk of developing an anastomotic leakage of esophagogastrostomy during the postoperative course. For clinical purposes the cut-off point can be chosen at pCO₂ 50 mm Hg. The clinical consequence for patients presenting pCO₂ values beyond this cut-off point needs to be discussed. As increased pCO₂ levels occur before clinical manifestation of the primary complication, diagnostic and therapeutic strategies can be modified in order to prevent secondary complications. Therefore an early diagnostic workup of these patients is recommended considering that partial ischemia of the gastric tube might cause a fatal outcome. This diagnostic procedure includes contrast swallow or endoscopy, or both, which can be safely performed even in the very early postoperative course [15, 16]. In case of an unremarkable gastric tube without evidence of any anastomotic problem, very careful clinical observation seems mandatory because pCO₂ levels beyond the cut-off point are associated with a complicated and prolonged postoperative course in almost all patients.

	References

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Schröder, W. Articles by Hölscher, A. H. Search for Related Content PubMed PubMed Citation Articles by Schröder, W. Articles by Hölscher, A. H. Related Collections Esophagus - other