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Ann Thorac Surg 2002;73:1704-1709
© 2002 The Society of Thoracic Surgeons

Original article: general thoracic

The influence of perioperative blood transfusion on survival after esophageal resection for carcinoma

Stephen M. Langley, MD, FRCS(CTh)*a, Christos Alexiou, FRCSa, Daniel H. Bailey, MBBSa, David F. Weeden, FRCS(CTh)a

a Department of Cardiothoracic Surgery, Southampton General Hospital, Southampton, Hampshire, United Kingdom

Accepted for publication February 8, 2002.

* Address reprint requests to Mr Langley, Department of Cardiothoracic Surgery, Southampton General Hospital, Southampton, Hampshire SO16 6YD, UK
e-mail: stephenlangley{at}dial.pipex.com


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 References
 
Background. There is evidence that perioperative blood transfusion may lead to immunosuppression. Our aim was to determine whether blood transfusion influenced survival after esophagectomy for carcinoma.

Methods. The study group comprised 234 consecutive patients (175 men and 59 women) with a mean age of 66 years who underwent esophagectomy for carcinoma by one surgeon between 1988 and 1998. The impact of 41 variables on survival was determined by means of univariate and multivariate analysis. Follow-up was complete (mean follow-up, 19.2 months; standard deviation, 16 months; range, 0 to 129 months).

Results. The operative mortality rate was 5.6% (13 deaths). Median operative blood loss was 700 mL (range, 150 to 7,000 mL). One hundred sixty-one patients (68.8%) received a blood transfusion postoperatively (mean transfusion, 2.6 units; range, 0 to 12 units). Overall actuarial 1-year, 3-year, and 5-year survival rates inclusive of operative mortality were 58.1%, 28.5%, and 16.1%, respectively. On univariate analysis, positive lymph nodes, pathological TNM stage, transfusion of more than 3 units of blood, incomplete resection, poor tumor cell differentiation, longer tumor, greater weight loss, male sex, and adenocarcinoma were significant (p < 0.05) negative factors for survival. On Cox proportional hazards regression analysis, after excluding operative mortality, lymph node involvement (p = 0.001), incomplete resection (p = 0.0001), poor tumor cell differentiation (p = 0.04), and transfusion of more than 3 units of blood (p = 0.04) were independent adverse predictors of late survival.

Conclusions. In addition to reaffirming the importance of completeness of resection and nodal involvement, this study demonstrates that blood transfusion (more than 3 units) may have a significant adverse effect on late survival after esophageal resection for carcinoma. Every effort should be made to limit the amount of transfused blood to the absolutely essential requirements.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 References
 
It is well established that transfusion of allogeneic blood can expose patients to bloodborne viruses such as hepatitis B and C and human immunodeficiency virus. In addition, there is increasing evidence to suggest that perioperative blood transfusion may have an immunomodulatory effect. This effect can be either beneficial or detrimental depending on the clinical setting. Kidney allograft survival, for example, is increased in recipients given transfusion before transplantation compared with those without transfusion [1, 2], and patients undergoing bowel resection for Crohn’s disease have been shown to have reduced recurrence rates if they receive a perioperative blood transfusion [3]. In contrast, perioperative blood transfusion has been associated with decreased survival in various types of cancer including colorectal, lung, liver, gastric, renal, and breast cancer [4–9]. Although there is mounting evidence suggesting a reduced survival after operation in these patients, this association has not been universally supported. A number of studies [10–12] have failed to demonstrate that perioperative blood transfusion influences long-term outcome.

The association between perioperative blood transfusion and prognosis after esophagectomy for carcinoma and the evidence of an immunosuppressive effect of blood transfusion after esophageal resection are less clear. Relatively few studies have previously addressed these issues, and the results are conflicting. One [13] of these studies concluded that the poorer outcome in patients receiving blood transfusion simply reflected the circumstances necessitating transfusion rather than any immunosuppressive effects. Others have suggested that the influence on survival is confined only to those patients receiving a large amount of transfused blood [14] or to select patients at short-term follow-up only [15]. Only one previous study [16] of patients undergoing esophageal resection for carcinoma has demonstrated a significantly worse prognosis for those receiving a blood transfusion independent of disease stage or the presence of major complications. The aim of the current study was to determine the influence of perioperative blood transfusion on survival in a consecutive series of patients undergoing esophageal resection for carcinoma by one surgeon over a recent 10-year period.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 References
 
Between February 1987 and November 1998, 234 consecutive patients underwent esophagogastrectomy for carcinoma by one of us (D.F.W.). There were 175 men (74.8%) and 59 women (25.2%) with a mean age of 66 years (standard deviation, 10.3 years; range, 26 to 90 years). Ninety patients (38.5%) were older than 70 years. Dysphagia was the main presenting symptom in 173 patients (73.9%) with a mean duration of 10.9 weeks (standard deviation, 13.2 weeks, range, 2 to 104 weeks). A history of weight loss was noted for 183 patients (78.2%), and the mean loss was 3.3 kg (standard deviation, 4.6 kg; range, 2 to 26 kg). The tumor was situated at the gastroesophageal junction in 132 patients (56.4%), the lower third of the esophagus in 67 (28.6%), middle third in 28 (12%), and upper third in 7 patients (3%). The mean tumor length was 4 cm (standard deviation, 1.6 cm; range, 1 to 12 cm). Histopathological examination of the resected specimen revealed the presence of adenocarcinoma in 160 patients (68.4%), squamous cell carcinoma in 66 (28.2%), and other cell types in 8 patients (3.4%). Tumors were staged after resection according to the American Joint Committee on Cancer guidelines [17]. Seven patients (3%) were found to have stage I disease; 69 (29.5%), stage IIA; 39 (16.7%), stage IIB; 100 (42.7%), stage III; and 19 (8.1%), stage IV disease. Positive lymph nodes were present in 152 patients (65%).

Operative technique
The standard operative approach was through a left thoracolaparotomy. For adenocarcinomas at the esophagogastric junction, initially a short, oblique left upper quadrant laparotomy was performed about 5 cm from the costal margin toward the umbilicus to assess operability. The nodes around the left gastric artery were examined, and tumor invasion into the crura or pancreas or the presence of liver metastases was assessed. Operability in patients with squamous cell carcinomas was evaluated through a left thoracotomy to judge the extent of any nodal disease or direct invasion into the aorta or the pericardium. All such patients underwent bronchoscopy prior to thoracotomy to exclude direct invasion into the left main bronchus or the trachea. In either case, if it was an operable tumor, the incision was extended to a full thoracolaparotomy through the bed of the seventh rib.

For adenocarcinomas, the esophagus was resected from the level of the aortic arch down to the mid-stomach. For squamous cell carcinomas, only a small amount of stomach was removed with the entirety of the esophagus up to within 3 cm of the cricopharyngeus. After mobilization of the stomach, a Kocher’s operation on the duodenum was carried out, and a temporary pyloromyotomy was performed using a Tubbs’ mitral dilator. For squamous cell carcinomas, the esophagus was mobilized into the neck to the right of the aortic arch. In the case of adenocarcinomas, the gastric remnant was passed through the hiatus, and the esophagogastric anastomosis was completed with interrupted Vicryl sutures below the aortic arch. For squamous cell tumors, a left oblique cervical incision was used, the proximal esophagus was excised, the stomach was drawn into the neck, and again the esophagogastric anastomosis was completed with interrupted Vicryl sutures.

After the operation, all patients were transferred to the intensive care unit for a short period to allow elective removal of the endotracheal tube before their return to the ward. Oral intake with water was commenced on the third postoperative day, followed by soft food on the fifth day. A contrast-medium swallow was performed only if there was clinical suspicion of a leak.

A left thoracoabdominal approach was used in 219 patients (93.6%) with a cervical anastomosis in 100 (42.7%) and an intrathoracic anastomosis in 119 (50.9%). Ten patients (4.3%) underwent an Ivor Lewis operation, and a transhiatal procedure was undertaken in 5 (2.1%).

Six patients were entered into a multicenter randomized phase III clinical trial of surgical treatment with or without chemotherapy (the Medical Research Council OEO2 trial). Of these, 3 received operation alone and 3, operation and neoadjuvant chemotherapy.

Follow-up
Patients were seen in the outpatient clinic every 3 months for the first postoperative year, every 6 months for the next 2 years, and then annually for life. Relevant information was collected from the patients’ medical records, direct communication with the patients’ general practitioners, and data supplied by the Office of National Statistics. Follow-up was complete (mean follow-up, 19.2 months; standard deviation, 16 months; range, 0 to 129 months).

Definitions and statistical analysis
Operative mortality includes all hospital deaths plus any death occurring after the patient was discharged from the hospital within 30 days of the operation. Survival time (± the standard error of the mean) was calculated from the time of operation until death or until the end of the study period using the Kaplan-Meier product-limit method. The survival estimate for the overall group includes operative mortality.

To identify independent predictors of survival, a total of 41 variables were analyzed (Appendix). On univariate analysis, categorical variables (eg, presence or absence of dysphagia, positive or negative lymph nodes, adenocarcinoma or squamous cell carcinoma) were tested with the log-rank test, and continuous variables (eg, duration of symptoms preoperatively, length of tumor) were screened with a Cox regression analysis. The variables that reached (p < 0.05) or approached (p = 0.05) significance on univariate analysis were entered into multivariate Cox proportional hazards regression models. A p value of less than 0.05 was considered significant on multivariate analysis. All statistical analyses were done using the statistical package SPSS (version 8.0) (SPSS Inc, Chicago, IL).


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
References
 
Blood transfusion
In regard to perioperative blood loss (losses in the operating theater plus losses down the drains prior to their removal), the median blood loss was 700 mL (interquartile range, 412 to 1,000 mL). One hundred fifty-five patients lost more than 350 mL of blood, 93 lost more than 700 mL, and 58 lost more than 1,000 mL.

Seventy-three patients (31.2%) did not require a blood transfusion in the perioperative period. The remaining 161 patients (68.8%) did receive blood, and the median amount transfused was 2 units (range, 1 to 12 units). Thirty-two patients (13.7%) received 1 unit of blood, 71 (30.3%) received 2 units, 21 (9%) received 3 units, and 37 (15.8%) received more than 3 units.

Survival
The operative mortality rate was 5.6% (13 patients). Six patients died of respiratory complications and 4, of an anastomotic leak. One patient each died of a myocardial infarction, a pulmonary embolism, and a cerebrovascular accident. The overall survival rates including operative mortality and all causes of death were 58.1% ± 3.4% at 1 year, 28.5% ± 3.3% at 3 years, and 16.1% ± 3.0% at 5 years (Fig 1).



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  		Fig 1. The overall survival rates including operative mortality and all causes of death at 1 year, 3 years, and 5 years were 58.1% ± 3.4%, 28.5% ± 3.3%, and 16.1% ± 3.0%, respectively.

 
On univariate analysis, pathological TNM stage, poorer tumor cell differentiation, greater weight loss, longer tumor, male sex, adenocarcinoma, positive lymph nodes, incomplete resection, and transfusion of more than 3 units of blood were significant adverse factors for survival (Table 1). On multivariate analysis, positive lymph nodes, incomplete resection, and transfusion of more than 3 units of blood remained independent negative factors for survival (see Table 1).


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  		TABLE 1. Adverse Predictors of Survival After Esophageal Resection for Carcinoma

 
To exclude the influence of any perioperative event on late survival and to determine the disease-specific survival, a further multivariate analysis (Cox proportional hazards regression model) was undertaken using data from hospital survivors. This demonstrated that the same variables, ie, incomplete resection (p = 0.0001), positive lymph nodes (p = 0.001), and transfusion of more than 3 units of blood (p = 0.04), plus poor tumor cell differentiation (p = 0.04) were significant independent adverse predictors of survival. At 2 years and 5 years, survival rates for patients having a complete resection were 42.2% ± 3.9% and 20% ± 3.6%, respectively (Fig 2). However, when the resection was incomplete, only 7.2% ± 4.9% were alive at 2 years and no patients were alive at 5 years (P = 0.0001). Patients with negative nodes had a 5-year survival rate of 29.6% ± 6.8% versus 10.1% ± 2.9% for those with positive nodes (P = 0.001) (Fig 3). Regarding the influence of transfused blood on survival, patients who received less than 3 units had a 5-year survival rate of 17.5% ± 3.3%, whereas those who received more than 3 units had a 5-year survival rate of only 10.0% ± 6.1% (P = 0.04) (Fig 4).



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  		Fig 2. Survival rates at 2 years and 5 years for patients having a complete resection (unbroken line) were 42.2% ± 3.9% and 20% ± 3.6%, respectively. None of the patients having an incomplete resection (broken line) were alive at 3 years (p = 0.0001).

 


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  		Fig 3. Patients with negative nodes (unbroken line) had a 5-year survival rate of 29.6% ± 6.8% versus 10.1% ± 2.9% for those with positive nodes (broken line) (p = 0.001).

 


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  		Fig 4. Patients receiving less than 3 units of blood (unbroken line) had a 5-year survival rate of 17.5% ± 3.3%, whereas those receiving more than 3 units (broken line) had a 5-year survival rate of only 10.0% ± 6.1% (p = 0.04).

 
Comment
The earliest reports of immunomodulation after blood transfusion in the 1970s were in the field of renal transplantation where transfusion prior to transplantation was accompanied with increased allograft survival [1]. Improved graft survival is associated with an increasing number of transfusions before transplantation [18], with a near maximal benefit after 5 units [19]. This suggests that there may be a threshold immunomodulatory effect related to volume of blood transfused. In the context of cancer surgery, a similar finding has been demonstrated in that the adverse influence of blood transfusion on survival is seen only after larger transfusions for both colorectal tumors and soft tissue sarcomas [20, 21].

The current study demonstrates a significant correlation between the use of more than 3 units of blood in the perioperative period and an adverse outcome in terms of survival for patients undergoing esophagectomy for carcinoma. This supports the suggestion of a threshold effect and is also consistent with the findings after esophageal resection for carcinoma in other series [13, 14, 16]. Although the evidence of an association between blood transfusion and poorer cancer prognosis is strong, it is not uniform, and some investigators [10–12] have not been able to demonstrate any influence of blood transfusion on survival. Furthermore, the correlation between blood transfusion and poorer survival does not prove a causal relationship.

It has been suggested that the immunosuppression induced by transfusion results from both an early unspecific immunosuppression mediated by monocytes and a later phase induced from increased suppressor T cell activity. Both effects are dependent on the number of transfusions. Blood transfusion has been shown to impair natural killer cell function [22] and to lower the CD4 to CD8 ratio [23]. In addition, prostaglandin E2 levels are increased after transfusion [24]. This may result in a direct inhibition of interleukin-2 production from CD4 cells with subsequent effect, as interleukin-2 is obligatory for natural killer cell activity. Although it is not clear at a molecular level which factors influence immunosuppression after allogeneic blood transfusion in cancer surgery, there is good evidence that leukocytes in the blood mediate the effects seen [25].

The two paramount functions of the immune system are to detect and kill malignant cells and to defend against invading infectious organisms. Not only may blood transfusion be detrimental regarding cancer recurrence, but also it has been shown to be an independent risk factor for postoperative bacterial infections [26]. Again, the detrimental effects of allogeneic blood transfusion in relation to infectious complications appear to be mediated through leukocytes [25]. The correlation between blood transfusion and infection is not evident when blood is depleted of leukocytes prior to transfusion. The patients in the current study did not have leukocyte-depleted transfusions; however, since 1999, all allogeneic blood for transfusion in our hospital has been leukocyte depleted. This is part of a nationwide policy in the United Kingdom aimed at minimizing the possibility of new-variant Creutzfeldt-Jakob disease being passed through transfusion of blood or blood products.

During the study period, there was not a strict blood transfusion policy, but care was taken to limit the amount of blood given perioperatively. As a result of the findings in this study, a more circumscribed policy has evolved, and, in general, we now try not to give a transfusion to a patient unless the hemoglobin level falls to less than 9 g/dL. However, other variables such as hemodynamic status and oxygen delivery are more important than an arbitrary hemoglobin concentration, and some patients will be symptomatic at higher hemoglobin levels and clearly will benefit from a transfusion.

Major blood loss may be unavoidable in operations for esophageal cancer, more so than with other tumors, because of the need to enter both the thoracic and abdominal cavities. As the results of the current study suggest a detrimental effect from transfusion, every effort should be made to reduce the amount of blood lost at the time of operation to an absolute minimum, and the importance of meticulous surgical technique cannot be overemphasized.

Other strategies that may limit the requirement of allogeneic transfusion include use of either predonated autologous blood or a Cell Saver. The use of a Cell Saver for transfusion of shed blood perioperatively should be avoided because of the risk of dissemination of malignant cells. Consideration should be given, however, to the use of autologous blood that has been predonated. A recent study [27] of patients undergoing predonation of autologous blood prior to resection of esophageal carcinoma demonstrated a significant reduction in the need of allogeneic transfusion. Only 3% of patients from the autologous group required such a transfusion compared with 34% in the control group. Furthermore, the use of allogeneic blood in this study was significantly related to postoperative infection.

Despite the limitations of the current study including its retrospective nature and the lack of a uniform transfusion policy, the results support previous reports that demonstrated an adverse effect on survival of patients undergoing esophagogastrectomy for carcinoma who receive an allogeneic blood transfusion. However, studies in this context have produced variable results. The earliest [13] showed that only high-volume blood transfusions (more than 8 units) were associated with a significant decrease in long-term survival. The amount of blood transfused in that study was high: 30% of patients required more than 5 units. The association between shorter survival and blood transfusion was probably related more to the circumstances necessitating transfusion rather than any immunosuppressive effect of the transfused blood. Subsequently, a separate study [15] demonstrated a significant connection between blood transfusion and decreased survival but only in the short term (at 1 year but not beyond) and only in patients with stage III disease. More recently, a clearer association between patients receiving an allogeneic transfusion of 4 or more units of blood and reduced survival after esophageal resection for carcinoma has been demonstrated [16].

In conclusion, this study reaffirms the importance of completeness of resection and the importance of lymph node involvement in esophageal resection for carcinoma. In addition, it shows that transfusion of more than 3 units of blood can adversely affect survival. Therefore, every effort should be made to limit the amount of blood transfused to the minimum requirement.


   Appendix
 

Variables Analyzed as Possible Predictors of Survival
Patient variables   Splenectomy
  Age (continuous variable)   Other concurrent procedures
  Age greater than 70 years   Duration of operation
  Age greater than 80 years   Blood loss (milliliters)
  Sex   Blood transfusion (yes or no)
  Year of operation   Blood transfusion of more than 1 unit
  Weight loss (yes or no)   Blood transfusion of more than 2 units
  Amount of weight loss   Blood transfusion of 3 units
  Dysphagia (yes or no) Tumor variables
  Duration of symptoms   Tumor length
  Urea clearance   Tumor site
  Creatinine level   T stage
  Aspartate aminotransferase value   N stage
  Alanine aminotransferase value   Pathological stage
  Alkaline phosphatase value   Tumor cell differentiation
  Bilirubin level   Status of resection margin
  Albumin level Postoperative variables
  Hemoglobin level   Intensive care unit stay
  Histological type   Duration of ventilation
Operative variables   Tracheostomy
  Type of incision   Anastomotic leak
  Site of anastomosis
   Adjuvant treatment


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 References
 

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