Ann Thorac Surg 2008;86:266-272. doi:10.1016/j.athoracsur.2008.03.017
© 2008 The Society of Thoracic Surgeons
Original Articles: General Thoracic
Association of Perioperative Fluid Balance and Adverse Surgical Outcomes in Esophageal Cancer and Esophagogastric Junction Cancer
Shenhai Wei, MD, PhD,
Jintao Tian, MD*,
Xiaoping Song, MD,
Yan Chen, MD
Department of Thoracic Surgery, First Hospital of Tsinghua University, Beijing, China
Accepted for publication March 7, 2008.
* Address correspondence to Dr Tian, Department of Thoracic Surgery, First Hospital of Tsinghua University, No.6 Jiuxianqiao 1st Rd, Chaoyang District, Beijing 100016, China (Email: tjt8105{at}sina.com).
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Abstract
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Background: Perioperative fluid balance and its association with surgical outcomes in patients with esophageal and esophagogastric junction cancer have not been clearly elucidated. A retrospective study of this association is reported.
Methods: A retrospective study involving 99 patients undergoing transthoracic esophagectomy or esophagogastrectomy was conducted. The intraoperative and postoperative fluid inputs and outputs as well as postoperative morbidity and mortality were recorded. Univariate analysis and multivariate logistic regression analysis were performed to clarify the effect of fluid balance on postoperative outcomes.
Results: There were 78 men and 21 women with an average age of 61.1 ± 10.9 years in the study. Among them, 68 patients had esophageal cancer and 31 had esophagogastric junction cancer. The postoperative morbidity and mortality were 38.4% and 7.1%, respectively. Compared with favorable outcomes, adverse surgical outcomes were significantly related to larger fluid balance on postoperative day 1 and day 2, and to cumulative fluid balance from the intraoperative period to postoperative day 2 (605.0 ± 931.5 mL versus 200.1 ± 712 mL; p = 0.016; 607.8 ± 743.9 mL versus 200.1 ± 678.6 mL; p = 0.005; 2,818.5 ± 1,456.5 mL versus 1,797.1 ± 1,704.0 mL; p = 0.002, respectively). On multivariate logistic regression analysis, cumulative fluid balance from intraoperative period to postoperative day 2 was independently related to adverse surgical outcomes (odds ratio, 1.000; 95% confidence interval, 1.000 to 1.001; p = 0.014).
Conclusions: The cumulative fluid balance from the intraoperative period to postoperative day 2 is a good predictor of surgical outcomes. It can be used as a prognostic tool to evaluate the risk of adverse surgical outcomes.
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Introduction
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Despite improvements in preoperative evaluation, operation techniques, and postoperative care, performing resection of esophageal carcinoma or carcinoma at the esophagogastric junction is still associated with significant risk of high morbidity and mortality rate [1–5]. Many preoperative risk factors have been identified, such as advancing age, preoperative comorbidity, low body mass index (BMI) and decreased functional status [1–3, 6–10]. In addition to these preoperative risk factors, the early postoperative course also may help predict the short-term outcome.
Resection of the esophageal cancer or esophagogastric junction cancer induces stress responses involving profound changes in the endocrine, neuroendocrine, and immune system as well as significant changes in organ function [11, 12]. Trauma as a result of operative procedures causes severe inflammatory response syndrome. The release of inflammatory mediators causes severe capillary leakage, loss of protein, and a fluid shift from the intravascular space into the interstitium [4, 13]. All these stress and inflammatory responses can lead to intraoperative and postoperative accumulation of fluid in the body. Thus, perioperative fluid balance status may be a marker for postoperative trauma and underlying systematic immunoinflammation [13].
Fluid balance has been documented to be associated with survival of posttraumatic hemorrhagic shock [14] and recovery from acute lung injury [15]. Restrictions of intravenous fluid can reduce postoperative complications after colorectal resection [16]. Yet to date no studies have addressed perioperative balance as a predictor of postoperative morbidity and mortality after esophagectomy and esophagogastrectomy. In this study, the value of intraoperative and early postoperative fluid balance as a reliable marker of short-term outcomes after resection of esophageal or esophagogastric junction cancer is evaluated.
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Patients and Methods
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Ethical approval for this retrospective study was obtained from the ethics committee at First Hospital of Tsinghua University. The need for informed consent from all patients individually was waived by the ethics committee.
A total of 99 consecutive patients with carcinoma of the esophagus or esophagogastric junction, who underwent elective transthoracic esophagectomy or esophagogastrectomy in our hospital from January 1998 to November 2005, were involved in this study. All patients' relevant data were collected.
All the patients had a thorough preoperative evaluation to determine tumor stage and estimate operation risks. The preoperative medical comorbidities were recorded, as well as patients' percentage weight loss, body mass index, pulmonary function, blood analysis, cigarettes and alcohol consumption, and the duration of each operation.
General anesthesia with one-lung ventilation during the operation was performed. A total of 88 patients underwent esophagectomy or esophagogastrectomy through a left thoracotomy approach with anastomosis of the esophagus and stomach or jejunum. Left thoracotomy combined with a neck incision or right thoracotomy combined with neck and abdominal incision were performed in another 11 patients with upper esophageal cancer or recurrence of esophageal cancer. In these patients, the stomach tube or portion of the colon was used as a substitute through the posterior mediastinal route. All patients were extubated within 3 hours after operation.
The total fluid administered and eliminated through all routes including blood loss and insensible perspiration was calculated and recorded on the day of surgery and postoperative days 1 and 2. The day of surgery was composed of intraoperative time and postoperative day 0. The fluid balance was calculated by subtracting fluid eliminated from total fluid administered.
Data manipulation and statistic analysis was conducted using SPSS version 11.5 for Windows (SPSS Inc, Chicago, IL). Values for continuous data are shown with mean ± standard deviation. Univariate analysis was performed relating the demographic variables, laboratory data, preoperative comorbidities, and fluid balance to postoperative outcomes. Continuous variables were compared by Student's t test or by one-way analysis of variance in case of more than two groups. Categorical variables were examined by 
2 test. Multivariate logistic regression analysis with forward stepwise technique was used to identify independent risk factors for adverse surgical outcomes involving complications and deaths. Any candidate variables with a probability of less than 0.10 were entered into the model. The odds ratio with its respective 95% confidential interval was generated by the model. A receiver operating characteristic curve was used to assess the discriminative power of the model and determine the cutoff point value for fluid balance. All statistical tests were considered significant at a probability value less than 0.05.
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Results
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This study population consisted of 99 patients who received esophagectomy or esophagogastrectomy for malignancy. There were 78 men and 21 women, ranging in age from 28 to 82 years, with a mean age of 61.1 ± 10.9 years. Among them, 68 patients had esophageal carcinoma and 31 had esophagogastric junction carcinoma. Patients' characteristics and laboratory value are listed in Table 1.
Fluid input, fluid output, and fluid balance for the intraoperative period and postoperative days 0, 1, and 2 are shown in Table 2. All patients exhibited positive fluid balance during the operation, and most of them turned to negative fluid balance on postoperative day 0. In the subsequent 2 days, the average fluid balance returned to positive again (Fig 1). Fluid balance on postoperative day 0 was much less than that of any other period (p < 0.001).
There were 7 (7.1%) in-hospital deaths, and 38 (38.4%) other patients experienced postoperative complications (Table 3). The most common postoperative complication was non–sinus arrhythmia (11.1%). Pulmonary infection (8.1%) was the second most common one, which was followed by heart failure (7.1%).
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Table 3 Postoperative Mortality and Morbidity With Different Cumulative Fluid Balance From Intraoperative to Postoperative Day 2
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Most deaths were caused by cardiopulmonary complications. Two of the deaths were of heart failure, and two of respiratory failure accompanying severe arrhythmia. Empyema owing to pulmonary infection caused one death. The other two died separately of refractory pulmonary infection and severe infection caused by anastomotic leakage.
Fluid balance from the intraoperative period to postoperative day 2 in different groups of postoperative outcomes is shown in Table 4
and Figure 2. Compared with the group with no complications, the complications group was associated with a larger fluid balance on postoperative day 2 (598.7 ± 800.7 mL versus 200.1 ± 678.6 mL; p = 0.01).
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Fig 2. Fluid balance from intraoperative time to postoperative day 2 for different groups of postoperative outcomes. (POD = postoperative day.)
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Cumulative fluid balance from the day of operation (including the intraoperative period) to postoperative day 2 was calculated as a new variable. The average amount of the cumulative fluid balance in each separate group of postoperative morbidity and mortality is shown in Table 3. The cumulative fluid balance for patients with postoperative deaths was double that of those without postoperative morbidity and mortality (p = 0.005). Patients with postoperative complications also had larger cumulative fluid balance than those without complications (p= 0.014). Among the complications, pulmonary complication and heart complication both were associated with a larger cumulative fluid balance compared with no complications (p= 0.014 and 0.022, respectively).
Considering all the in-hospital deaths being caused by postoperative complications, we divided the patients into two groups according to postoperative outcomes. One group with adverse outcomes involved in-hospital deaths and postoperative complications, another group with favorable outcomes consisted of patients without postoperative complications or deaths.
All the variables were analyzed to screen the potential risk factors for adverse outcomes by univariate analysis (Table 5). The results indicated that adverse surgical outcomes were associated with larger fluid balance on postoperative days 1 and 2 and cumulative fluid balance from the intraoperative period to postoperative day 2 compared with favorable outcomes (605.0 ± 931.5 mL versus 200.1 ± 712 mL; p = 0.016; 607.8 ± 743.9 mL versus 200.1 ± 678.6 mL; p = 0.005; 2,818.5 ± 1,456.5 mL versus 1,797.1 ± 1,704.0 mL; p = 0.002). These three variables were entered into multivariate logistic regression model together with other variables with a probability value less than 0.1, including age, type of the carcinoma, smoking within 2 weeks, drinking, the percentage of the predicted value for the maximal voluntary ventilation, and duration of operation. Cumulative fluid balance from the intraoperative period to postoperative day 2 was identified as an independent risk factor for adverse postoperative outcomes (odds ratio, 1.000; 95% confidence interval, 1.000 to 1.001; p = 0.014), as was the percentage of the predicted value for the maximal voluntary ventilation (Table 6).
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Table 5 Patients' Characteristics, Laboratory Data, Duration of Operation, Different Period Fluid Balance, and Cumulative Fluid Balance From Intraoperative Period to Postoperative Day 2 Relating to Adverse Surgical Outcomes
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The receiver operating characteristic curve was plotted for the cumulative fluid balance (Fig 3). The area under the curve was 0.705 (standard error 0.054; 95% confidence interval 0.6 to 0.809; p = 0.000), and the cutoff value for the cumulative fluid balance was 1890.3 mL, with a sensitivity of 0.82 and specificity of 0.59.
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Fig 3. Receiver operating characteristic curve for cumulative fluid balance from intraoperative period to postoperative day 2 as a predictor of the adverse surgical outcomes.
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Comment
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Despite recent advances in preoperative evaluation and postoperative treatment for patients with esophageal and esophagogastric junction carcinoma, the overall morbidity and mortality after surgery for these patients remain high [1–5].Bailey and colleagues [1] reported 10% mortality and 50% morbidity in a series of 1,777 esophagectomies. Orringer and associates [2] reported a series of 1,085 patients who underwent transhiatal esophagectomy, with mortality of 4% and morbidity of 26%. In a series of 143 patients with gastroesophageal junction cancer undergoing esophagogastrectomy, the perioperative morbidity and mortality was 29% and 2.1%, respectively [3]. The most common and serious postoperative morbidity arises from pulmonary complications, including pneumonia, acute respiratory distress syndrome, and respiratory failure [4, 5]. This current study, which involved 68 esophageal cancer patients and 31 esophagogastric junction cancer patients resected transthoracically, demonstrated a 38.4% postoperative morbidity and a 7.1% postoperative mortality. The pulmonary complications in this study were the second most common complications (15.2%) after cardiac complications (18.2%).
Perioperative fluid balance was reported to be associated with postoperative complications and mortality after cardiothoracic surgery and nonthoracic surgery. Kalus and colleagues [17] reported that the risk of the atrial fibrillation after cardiothoracic surgery increased with an increase of fluid balance on postoperative day 2. Møller and associates [18] demonstrated that excess fluid balance during anesthesia was the strongest risk factor for postoperative pulmonary complications and in-hospital mortality after pneumonectomy. In a randomized study, Brandstrup and associates [16] pointed out that restricted intravenous fluid regimen with unchanged body weight can reduce complications after elective colorectal resection. However, to date few studies have been carried out to investigate the fluid balance in transthoracic esophagectomy and esophagogastrectomy and its associations with postoperative complications and deaths.
In this study, all patients were in a status of positive fluid balance during the operation, and most of the patients' urine began to increase after completion of surgery, which resulted in a negative fluid balance on postoperative day 0. Then the fluid balance turned to be positive again in the subsequent 2 days. Causes in the change of fluid balance are uncertain. Anesthesia effects [13], reservation of fluid in the body, and internal fluid redistribution caused by heavy stress and inflammatory responses elicited by surgical trauma [13, 19, 20] may be contributors to intraoperative positive fluid balance. We postulate that attenuation of vasodilation effects of anesthesia may have been the main contributor to the change in fluid balance from positive to negative on postoperative day 0. Also, increased capillary permeability as a result of inflammatory mediators as well as fluid conservation effects from neuroendocrine hormones, the result of stress responses, could be considered as influential factors in maintaining the positive fluid balance on postoperative days 1 and 2.
In this current study, the fluid balance of the intraoperative period and postoperative days 0, 1, and 2 had been compared with different surgical outcomes. Only fluid balance of postoperative day 2 was significantly different between patients with and without complications (p= 0.01). The fluid balances of other times have no associations with different outcomes. However, when the cumulative fluid balance from the intraoperative period to postoperative day 2 was calculated as a variable, it exhibited strong relations to postoperative morbidity and mortality.
Postoperative deaths and complications, especially heart and pulmonary complications, were related to larger cumulative fluid balance in this study compared with no complication. There was no association of cumulative fluid balance with incidence of anastomotic leakage, even though tissue healing would be inhibited by tissue hypoxemia owing to interstitial fluid accumulation [13, 16, 21]. Furthermore, no associations were observed between the cumulative fluid balance and pulmonary embolism, empyema and wound infection, acute gastric dilation, and recurrent laryngeal nerve palsy. These are attributed to different reasons and uncertain causes, but as for the anastomotic leakage and recurrent laryngeal nerve palsy, we agree with the idea that these two complications are related to surgical approaches or technique [22].
Adverse surgical outcomes in this study, including postoperative complications and deaths, were related to larger fluid balance on postoperative days 1 and 2 and cumulative fluid balance from the intraoperative period to postoperative day 2. However, on multivariate logistic regression analysis, only cumulative fluid balance from the intraoperative period to postoperative day 2 remained in the model and was identified as an independent variable associated with adverse surgical outcomes. Reasons for that might be attributed to the fact that surgical stress and inflammatory responses related to adverse postoperative outcomes were a continuous process from the intraoperative time to the early postoperative days. The cumulative fluid balance, rather than the fluid balance in one single period, was the reflection of the pathophysiologic process. Thus, excessive cumulative fluid balance from the intraoperative period to postoperative day 2 can be an important predictor for adverse surgical outcomes after esophageal cancer surgery or esophagogastric junction cancer operations. However, the excessive fluid balance may be a result of postoperative complications. For example, excessive fluid administered may increase demand on cardiac function and potentially increase postoperative cardiac morbidity, and cardiac dysfunction, at the same time, can affect fluid elimination from the body, thus, aggravating fluid retention in the body. So, it is difficult to distinguish exactly whether the fluid balance excess is a cause or a result of postoperative complications. It is unclear whether restriction of fluid administration or use of diuretics after surgery can reduce postoperative morbidity and mortality for patients with esophageal or esophagogastric junction cancer. Randomized controlled studies are needed to demonstrate these issues.
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Acknowledgments
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We would like to thank Hassan Dib, MD, for his contribution in proofreading this submitted retrospective study.
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References
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Abstract
Introduction
