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10.1245/ASO.2005.12.018
Annals of Surgical Oncology 12:1017-1024 (2005)
© 2005 Society of Surgical Oncology
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Original Article

Evaluation of Intraoperative Autotransfusion Filtration for Hepatectomy and Pancreatectomy

Robert C. G. Martin, MD1, Samuel R. Wellhausen, PhD2, Dave A. Moehle, BS3, Alvin W. Martin, MD2 and Kelly M. McMasters, MD, PhD1

1 Division of Surgical Oncology, University of Louisville School of Medicine, 315 East Broadway, Room 313, Louisville, Kentucky 40202
2 Department of Pathology, University of Louisville School of Medicine, Louisville, Kentucky 40202
3 UES Inc., Louisville, Kentucky, 40292

Correspondence: Address correspondence and reprint requests to: Robert C. G. Martin, MD; E-mail: robert.martin{at}louisville.edu


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Background: Hepatectomy and pancreatectomy are often associated with significant in-traoperative blood loss leading to postoperative anemia, which has been demonstrated to lead to increased perioperative morbidity, a prolonged hospital stay, and decreased overall survival. Cancer has remained an absolute contraindication to autotransfusion because of the unproven concern about reinfusion of malignant cells. Thus, the aim of this study was to test for the presence of malignant cells in autotransfused filtered blood in patients undergoing major pancreatic and liver resection.

Methods: A prospective study of 20 consecutive patients evaluated the presence of malignant cells from autotransfusion filtered blood after resection by flow cytometric and immunohistochemical methods.

Results: Ten patients underwent major hepatectomy for metastatic colorectal cancer, with a median blood loss of 500 mL (range, 200–700 mL). Three patients received a total of six units of packed red blood cells. Ten patients underwent pancreaticoduodenectomy for adenocarcinoma with a median blood loss of 400 mL (range, 200–1300 mL). Five patients received a total of nine units of packed red blood cells. Flow cytometry did not demonstrate the presence of any cytokeratin-positive carcinoma cells in filtered blood.

Conclusions: Intraoperative autotransfusion for major hepatectomy in metastatic colorectal cancer and pancreatectomy for adenocarcinoma is safe and should begin to be evaluated in a phase II study for efficacy.

Key Words: Autotransfusion • Hepatectomy • Pancreatectomy • Surgical oncology • Liver neoplasms • Pancreatic neoplasms


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Major surgical resections, including esophagectomy, gastrectomy, pancreaticoduodenectomy, hepatectomy, and retroperitoneal sarcoma resection, are often associated with significant intraoperative blood loss (in the range of 750–1250 mL in most series).1–7 Intraoperative and postoperative anemia with subsequent homologous transfusion has been demonstrated to result in increased perioperative morbidity,2,8 prolonged hospital stay, and decreased overall survival.9

Homologous transfusion, the ability to transfuse blood from one individual to another, has been proven to be critical in modern surgery and medicine. However, maintaining adequate reserves of blood and its components is becoming more challenging with the shrinking donor population and the relatively short shelf life of components.10 Use of patients’ own blood, obtained and stored before surgery (autologous transfusion), has become popular in some centers for major surgical procedures. However, this mode of transfusion has several drawbacks, including the requirement of adequate planning, the ability of the patient to donate his or her own blood, and the expense of obtaining and storing the patient’s blood before use.

Another alternative has been to salvage the patient’s own blood at the time of operation and then reinfuse it during the operative procedure.11 This technique, , has become widely accepted in both cardiac surgery and vascular surgery. Historically, intraoperative autotransfusion has been contraindicated for patients with cancer. This contraindication has been based on the potential for reintroducing tumor cells, and this potential is based on the belief that surgery often "violates" the tumor during resection and, thus, that tumor cells are spilled in the operative field during resection. However, with en-bloc resection of most tumors, the concept that cancer cells are a routine contaminant in the lost blood during surgery may not be correct. Even if cancer cells are present, current techniques of autotransfusion may adequately prevent reinfusion of cancer cells along with red blood cells.

Although a few retrospective studies using auto-transfusion in both urological and gynecological surgery have failed to demonstrate an increase in disseminated malignancy,12–15 the hypothesized potential risk has led to the overall belief that intraoperative autotransfusion is not safe in oncological surgery.16–18 Thus, the aim of this study was to evaluate the presence of malignant cells in auto-transfusion filtered blood in patients undergoing pancreatectomy and hepatectomy to obtain initial data regarding the potential safety of autotransfusion in surgical oncological patients.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
This was a prospective institutional review board–approved study of 20 consecutive patients (10 for hepatectomy and 10 for pancreatectomy) that evaluated the presence of malignant cells from auto-transfusion filtered blood after resection. All intraoperative blood loss designated for waste from opening to closure was collected, filtered, and prepared for autotransfusion. A standard Haemonetics Cell Saver 5 autotransfusion system (Braintree, MA) was used for all patients.19 The standard technique for autotransfusion involves aspirating the blood that is lost during an operation into a disposable centrifuge bowl. It is in this bowl that the red blood cells are separated, concentrated, and washed. The bowl consists of two subassemblies: an inner one, which remains stationary, and an outer one, which rotates. The outer subassembly rotates primarily at 5650 rpm and provides the chamber in which centrifugal processing (washing) is accomplished. When blood solution is pumped into the spinning bowl from the patient through the inlet port, the red blood cells are centrifuged outward toward the bowl’s perimeter and recovered; if they are of an adequate hematocrit, they are given back to the patient either during or after the operation.

A single 5-mL aliquot of blood was also taken during the procedure that was not filtered, and it was evaluated for malignant cells to serve as a possible positive control. All samples were then immediately taken for flow cytometric and immunohistochemical analyses.

The flow cytometry evaluation technique removed all erythrocytes by hypotonic lysis with ammonium chloride. The remaining nucleated cells were then washed and resuspended in phosphate-buffered saline. Aliquots were then stained with fluorochrome-conjugated monoclonal antibodies and analyzed by flow cytometry for determination of lymphocyte and monocyte content. Cytospin preparations were made and stained with Wright-Giemsa for morphological evaluation. Additional cytospin preparations were also stained with anti-cytokeratin antibody for immunohistochemical evaluation of cytokeratin-positive carcinoma cells. The immunohistochemistry clone used in this study was AE1/AE3 (DakoCytomation, Fort Collins, CO), which recognizes multiple subtypes of cytokeratins and is used for routine use in surgical pathologic analysis when immunohistochemistry is used to screen for an epithelial origin in a poorly differentiated tumor. The cytokeratin subsets recognized by AE1/AE3 are present in both colon and pancreatic cancer.

Previous studies have demonstrated that flow cytometric analysis can detect 1 cytokeratin cell in 1000 nucleated cells, whereas immunohistochemical analysis can detect 1 cytokeratin cell in 1 x 106 nucleated cells.20 Immunohistochemical analysis further enables differentiation of benign from malignant cytokeratin-positive cells by a pathologist (in this study, A.W.M.).

A positive control experiment was also performed to ensure sensitivity and specificity of the flow cytometry technique. In this experiment, 100,000, 1,000, 100, and 10 malignant adenocarcinoma cells from pancreatic cell culture were put through a Cell Sorter device (Mo-Flo Cell Sorter; DakoCytomation) and were added to 250 mL of serum and then recovered by centrifugation. They were then stained by immunohistochemistry for cytokeratin and counterstained with Wright-Giemsa. Our results demonstrated that our detection protocol can reliably detect fewer than 100 cytokeratin-positive contaminant cancer cells in a unit of blood treated by Cell Saver. In addition, 250 mL of serum was spiked with 300,000 pancreatic cells and then filtered through a single leukofiltration filter. This experiment demonstrated that leukofiltration removed all of the added pancreatic cancer cells. Preoperative hemoglobin levels, comorbidities, intraoperative blood loss, transfusion requirements, type of procedure, and discharge hemoglobin levels were also recorded.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
From December 2002 to August 2003, 10 patients underwent major hepatectomy (4 bisegmentectomy, 2 extended right lobectomy, 3 right lobectomy, and 1 left lobectomy). Three men and seven women underwent major hepatic resection for metastatic colorectal cancer, with a median blood loss of 500 mL (range, 200–700 mL). The median admission hemoglobin level was 11.5 g/dL (range, 9.2–13.7 g/dL), with a median discharge hemoglobin level of 10.0 g/ dL (range, 7.3–12.8 g/dL; Table 1Go). Three patients received a total of six units of packed red blood cells. The median length of stay was 6 days (range, 5–24 days).


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  		TABLE 1. Perioperative results of 20 patients undergoing intraoperative autotransfusion analysis
 
During the same time interval, 10 patients underwent a standard pancreaticoduodenectomy with retroperitoneal lymph node dissection. Six women and three men underwent pancreaticoduodenectomy for adenocarcinoma, with a median blood loss of 400 mL (range, 200–1300 mL). The median length of stay was 7 days (range, 5–10 days). The median admission hemoglobin level was 13.7 g/dL (range, 12.5–15.6 g/ dL), with a median discharge hemoglobin level of 10 g/dL (range, 8.1–13.9 g/dL; Table 1Go). Five patients received a total of nine units of packed red blood cells.

Flow cytometric analysis of unfiltered blood revealed the presence of normally distributed leukocyte subsets (Fig. 1Go), as well as cytokeratin-positive cells in 6 of 20 specimens tested (Fig. 2Go). These six patients all had undergone pancreaticoduodenectomy, and the unfiltered aliquot was obtained after reconstruction. Immunohistochemical analysis demonstrated the presence of cytokeratin-positive cells in the unfiltered aliquot, but none was malignant (Fig. 3Go). These findings were also similar for the filter washings. After filtration, immunohistochemical detection of leukocyte depletion–filtered blood demonstrated no cytokeratin-positive cells or intact leukocytes (Fig. 4Go).


Figure 1
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  		FIG. 1. Light scatter graph of unfiltered blood treated by Cell Saver demonstrates the presence of normally distributed leukocytes. PMNs, polymorphonuclear neutrophils; SSC, side scatter; Monos, monocytes; Lymphs, lymphocytes; R2, the analytical gate for monocytes.

 

Figure 2
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  		FIG. 2. Plot of DNA of both control (left) and anti-cytokeratin fluorescent antibody (right) of unfiltered blood treated by Cell Saver. This sample contains cytokeratin-positive cells. FITC, fluorescein isothiocyanate; R2, the analytical gate for isotype control FITC antibody and anti-cytokeratin FITC antibody.

 

Figure 3
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  		FIG. 3. Cytokeratin positive cells (brown) detected with immunohistochemical staining in unfiltered blood.

 

Figure 4
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  		FIG. 4. Immunohistochemical detection of leukocyte depletion–filtered blood failed to detect cytokeratin-positive cells or intact leukocytes.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
Intraoperative hypotension and perioperative blood transfusion have been demonstrated to adversely affect the disease-free interval in patients undergoing complete resection for colorectal liver metastases.21 That study, published in 1991, most likely represented a selection bias in that the patients who received blood transfusions were those with the worst prognosis; i.e., they had large tumors or cirrhotic parenchyma and underwent nonstandard hepatectomy techniques. However, the risk of postoperative morbidity still remains significantly higher in patients who receive homologous blood transfusions. These immunomodulatory effects related to blood transfusions render the recipient more vulnerable to infection, recurrence, or reactivation of latent viruses (both known and unknown).22 The most recent evaluation of blood transfusion and hepatectomy did not demonstrate a difference in disease-free interval or overall survival, but it did demonstrate a significant increase in surgical morbidity.8 The overall blood transfusion rate, even from large-volume liver surgery centers, still remains at ≥50% in the surgical management of the liver.23

Similarly, the median estimated blood loss for patients undergoing pancreatectomy is 600 mL, with a range of 300 to 1500 mL.24 The overall complication rate for this difficult procedure remains in the 50% to 60% range, even at major centers.25 Similarly, large-volume blood loss (>750 mL) has been demonstrated in numerous studies to be a predictor of increased morbidity and mortality in patients undergoing pancreatectomy for malignant tumors. This is a significant problem, because the median overall survival for pancreatic adenocarcinoma ranges from 12 to 20 months.

Maintaining adequate reserves of homologous blood and its components is becoming more challenging with the shrinking of the donor population and the relatively short shelf life of its components.10 The shelf life of red blood cells and pooled cells remains a short 42 and 5 days, respectively. Continued seasonal shortages have required many institutions to adopt blood exchange programs across the country to keep ahead of the demand.26

In addition to the shortages, significant risks remain in the use of homologous transfusions. These include transfusion reactions,27 immune suppression, the risk of transmission of known infections, and the risk of possible transmission of unknown infections.28 Even with the improvement in screening over the last three decades, the risk of transfusion-transmitted diseases still remains. However, infectious transmission is not the primary risk in transfusion of blood products. Most transfusion-related deaths result from transfusion of ABO-incompatible blood.29 The incidence is estimated in 1 in 33,000 red blood cell transfusions. In the operating room, general anesthesia may delay the recognition of hemolytic reaction and, thereby, increase the risk of a fatal outcome. Common symptoms of hemolytic reaction—hypotension, tachycardia, hemoglobinuria, or microvascular bleeding—may be mistakenly attributed to other causes.30

The increased use of erythropoietin (epoetin {alpha}; Procrit [Ortho Biotech, Inc., Raritan, NJ]) has reduced the number of homologous transfusions, but only in the chronically anemic. Epoetin {alpha} has not been effective for intraoperative blood loss or for immediate perioperative recovery. Preoperative use of epoetin {alpha} has been found to be effective, but the cost and the need to delay surgery for up to 1 month to allow for an adequate response has limited its use in the surgical oncological patient population.

Preoperative blood donation before surgical resection has also been evaluated in large series to reduce the use of allogeneic transfusions. Limitations of this technique remain adequate hemoglobin to donate before surgery, cost of storage, and adequate planning to allow patients to undergo this technique. In a recent study of 359 patients who underwent hepatic resection for colorectal metastasis, only 32% (123 patients) had adequate hemoglobin levels to donate 1 or 2 units of their own blood, and 17% of these (61 patients) still required allogeneic blood transfusion.31

Intraoperative phlebotomy with resultant hemodilution to allow for autologous blood transfusion at the end of the procedure has also been used, primarily in patients undergoing hepatectomy. This technique has been successful in small number of series, primarily in cardiac and orthopedic procedures.32,33 The major limitations of this technique remain a suboptimal cardiovascular status and preoperative hemoglobin levels that are inadequate for the patient to tolerate hemodilution; anesthesiologists who are comfortable with and facile in this technique are also uncommon.

Intraoperative autotransfusion represents another option in the management of perioperative blood loss and postoperative anemia. This technique has been widely used in multiple surgical procedures, including vascular revascularization, coronary bypass grafting, and spine surgery.34–36 The successful use of intra-operative autotransfusion is based on a minimum amount of blood loss for a procedure. The minimum amount of blood or fluid that needs to be collected ranges from 400 to 600 mL, depending on the degree of hemolysis for the procedure. This amount will allow for a successful autotransfusion of 100 mL of blood.

The use of intraoperative autotransfusion in major surgical oncological procedures has been limited because of the absolute contraindication related to the hypothesized belief that tumor cells would be rein-fused into the patient and thus lead to a greater incidence of metastasis. The in vitro studies that established this belief lacked true clinical applicability. Prior research attempted to evaluate this by demonstrating the viability of three tumor cell lines after multiple passes through a cell processor and showing that these cell lines retained their viability.37 Most of these studies used nonstandard filtration systems or only standard red blood cell transfusion filters, unlike contemporary intraoperative auto-transfusion systems.38 More recent research demonstrated that a standard leukocyte depletion filter removed all tumor cells completely with a single filtration system.39 The viability of these cells was evaluated by the trypan blue exclusion test and by cell culture. This study suggested that the use of a leukocyte depletion filter during intraoperative auto-transfusion might reduce the potential for reinfusion of viable tumor cells.

At present, no study has evaluated actual intra-operative human blood loss that is filtered by standard intraoperative autotransfusion techniques and then evaluated for possible tumor viability. All of the previous studies have been on cancer cell lines and have used variable techniques, none of which is applicable to the surgical blood loss that occurs during a standard oncological procedure. Thus, the safety of intraoperative autotransfusion for oncological procedures has not been adequately evaluated until now. This study of 20 patients undergoing surgical resection for adenocarcinoma successfully demonstrated no evidence of suspicious or malignant cells in autotransfused filtered blood. This should help to dispel concerns regarding reinfusion of tumor cells and establish the possibility that intraoperative autotransfusion may be safe for patients undergoing oncological procedures.

The limitations of this study stem from the knowledge that flow cytometric immunohistochemical analyses may not be 100% accurate in identifying malignant cells. This limitation, however, is strengthened by the clinical studies, which have failed to demonstrate a significant increase in disseminated metastasis in patients who have undergone autotransfusion. At present, immunohistochemistry is the most sensitive test for detection of viable cells and is the most specific for detection of malignant cells. Other tests, such as reverse transcription-polymerase chain reaction, are not likely to be helpful because of the false-positive results, detection of nonviable cells, and lack of established clinical significance. Other studies, such as attempted cell culture, could demonstrate the viability of cells but, again, lack the established clinical significance. Further evaluation in an ongoing phase II trial demonstrating the safety of autotransfusion filtered blood in patients undergoing major surgical oncological procedures will help to establish new criteria for autotransfusion use.


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
Intraoperative autotransfusion for major hepatectomy in metastatic colorectal cancer and pancreatectomy for adenocarcinoma is safe and should begin to be evaluated in a phase II study for efficacy. This study has the ability to significantly expand the use of intraoperative autotransfusion in all aspects of oncology. Once this is proven safe for autotransfusion, the ability to minimize homologous blood transfusion in these and many other procedures would be significant. If this technique could decrease blood transfusion–related complications, both known and unknown, then this may translate into shorter hospital stays and, perhaps, an improved quality of life for these patients.


   ACKNOWLEDGMENTS
 
Supported by the Center for Advanced Surgical Technologies of Norton Hospital, Louisville, KY.

Received for publication December 17, 2004. Accepted for publication July 22, 2005.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

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