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J Thorac Cardiovasc Surg 2005;130:20-28
© 2005 The American Association for Thoracic Surgery

Surgery for Acquired Cardiovascular Disease

Safety, efficacy, and cost of intraoperative cell salvage and autotransfusion after off-pump coronary artery bypass surgery: A randomized trial

G.J. Murphy, MD, FRCS a , C.S. Rogers, PhD, a , W.B. Lansdowne, BSc b , I. Channon, BSc b , H. Alwair, MRCS a , A. Cohen, FRCA c , M. Caputo, MD a , G.D. Angelini, MD, FRCS a , *

a Bristol Heart Institute, University of Bristol, Bristol Royal Infirmary, Bristol, United Kingdom.
b Department of Clinical Perfusion, Bristol Royal Infirmary, Bristol, United Kingdom.
c Department of Anaesthetics, Bristol Royal Infirmary, Bristol, United Kingdom

Received for publication September 30, 2004; revisions received November 17, 2004; accepted for publication December 7, 2004.

* Address for reprints: G. D. Angelini, MD, FRCS, Bristol Heart Institute, Bristol Royal Infirmary, Bristol BS2 8HW, United Kingdom (Email: G.D.Angelini{at}bristol.ac.uk).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Discussion
 References
 
OBJECTIVE: We evaluated, in a randomized controlled trial, the safety and effectiveness of intraoperative cell salvage and autotransfusion of washed salvaged red blood cells after first-time coronary artery bypass grafting performed on the beating heart.

METHODS: Sixty-one patients undergoing off-pump coronary artery bypass grafting surgery were prospectively randomized to autotransfusion (n = 30; receiving autotransfused washed blood from intraoperative cell salvage) or control (n = 31; receiving homologous blood only as blood-replacement therapy). Homologous blood was given according to unit protocols.

RESULTS: The groups were well matched with respect to demographic and comorbid characteristics. Patients in the autotransfusion group had a significantly higher 24-hour postoperative hemoglobin concentration (11.9 g/dL; SD, 1.41 g/dL) than those in the control group (10.5 g/dL; SD, 1.37 g/dL) (mean difference, 1.02 g/dL; 95% confidence interval, 1.60-0.44 g/dL; P = .0007), as well as a 20% reduction in the frequency of homologous blood product use (11/31 vs 5/30; P = .095). Autotransfusion of washed red blood cells was not associated with any derangement of thromboelastograph values or laboratory measures of clotting pathway function (prothrombin time, activated partial thromboplastin time, and fibrinogen levels), increased postoperative bleeding, fluid requirements, or adverse clinical events. There was no statistical difference between groups in the total operation, hospitalization, and management costs per patient (median difference, $1015.90 [US dollars]; 95% confidence interval, –$2260 to $206; P = .11).

CONCLUSIONS: Intraoperative cell salvage and autotransfusion was associated with higher postoperative hemoglobin concentrations, a modest reduction in transfusion requirements, no adverse clinical or coagulopathic effects, and no significant increase in cost compared with controls. This study supports its routine use in off-pump coronary artery bypass grafting surgery.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Discussion
 References
 
Reinfusion of salvaged autologous blood after conventional coronary artery bypass grafting (CABG) with cardiopulmonary bypass (CPB) has been shown to reduce homologous blood exposure without any increase in adverse events, coagulopathy, or hospitalization costs. 1–3 Go It remains unclear, however, whether this is also true for CABG performed on the beating heart (off-pump CABG; OPCAB). In comparison to conventional CABG, OPCAB is associated with a significant reduction in perioperative blood loss, homologous blood and blood product use, and postoperative morbidity, 4–6 Go and this may reduce any benefit of cell salvage in this setting. It is also possible that any potential coagulopathic effects of autotransfused washed red blood cells, not evident against the background noise of the abnormal clotting evident after CPB, may be more clinically relevant after OPCAB surgery. The aim of this study was to assess the effects of intraoperative cell salvage and autotransfusion on postoperative hemostasis, homologous blood exposure, and cost in OPCAB surgery in a randomized controlled trial.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Discussion
 References
 
Study Population and Patient Allocation
Sixty-one patients admitted to our institution for CABG consented to enrollment in the study over a 16-month period. Male or female patients aged 18 years or more and who were undergoing nonemergency first-time CABG were eligible to take part. Exclusion criteria included patients who are prevented from receiving blood and blood products according to a system of beliefs (eg, Jehovah Witnesses); patients receiving preoperative warfarin, heparin, or other systemic anticoagulant drugs; patients with congenital or acquired platelet, red blood cell, or clotting disorders; patients with ongoing or recurrent systemic sepsis; and patients who were unable to give full informed consent for the study (eg, because of learning or language difficulties). The study received local ethics committee approval. Patients were assigned to 1 of 2 randomized groups, autotransfusion or control, in a 1:1 ratio by using block randomization. Allocations were generated by a card system and concealed in sealed opaque envelopes. Patients who had given consent were randomized immediately before surgery. Clinical outcome data were collected prospectively as part of our patient analysis and tracking system.

The study was powered to detect a significant effect of autotransfusion on postoperative clotting profiles. This was chosen in preference to the frequency of homologous blood usage, as using data derived from a previous study, 4 Go it was calculated that this would have required as many as 660 patients to achieve adequate power. Our previous studies of clotting profiles and hematologic and biochemical indices in OPCAB patients 4,7,8 Go had shown significant differences in outcomes with sample sizes of 20 patients in each group. Using these data, we predicted that a randomized study of 40 patients in total would allow a 90% chance of detecting a standardized difference of more than 1 in laboratory measures of clotting pathway function and hematologic indices with 95% confidence. For the purposes of this study, we recruited a total of 30 patients in each arm to allow for possible dropouts.

Cell-Salvage Protocol
Patients in the autotransfusion group underwent intraoperative cell salvage, with autotransfusion of washed, salvaged red blood cells at the completion of the operative procedure. All blood lost, from skin incision to skin closure, was salvaged via a single-lumen suction tube flushed with heparinized 0.9% saline (10 U/mL infused at 83 mL/h) and connected to the closed rigid collection chamber of a Dideco Compact autotransfuser device (Dideco, Gloucester, United Kingdom) at high-pressure suction. Before autotransfusion, the heparinized salvaged intraoperative blood underwent a washing process, with resuspension of the red blood cells in saline, to a hematocrit of approximately 0.6. This red blood cell suspension was then transferred to a sterile collecting bag that was disconnected from the autotransfuser and administered via a standard blood-giving set. Salvaged washed red blood cells were autotransfused at the time of skin closure.

In the control group, all blood spilled, from skin incision to skin closure, was aspirated with a high-pressure sucker and discarded. Perioperatively all patients were administered homologous, leukodepleted packed red blood cells as blood-replacement therapy, according to predefined unit protocols. The threshold for transfusion of homologous blood was hemoglobin less than 8 g/dL or hematocrit less than 0.23. In patients with excessive blood loss and cardiovascular instability, blood was given at the discretion of anesthetic or intensive care unit (ICU) staff. Clotting products and platelets were administered at the discretion of the ICU staff in response to bleeding in the presence of coagulopathy or diminished platelet count.

In both groups, after closure of the sternum, postoperative mediastinal drainage was achieved by 28F single-lumen rigid sump drains (n = 1-3) to a 1000-mL sterile collection chamber connected to 20 cm H2O wall suction via an underwater seal, from which all subsequent shed mediastinal fluid loss was then recorded. This collected blood was discarded.

Operative Technique
The anesthetic technique was standardized for all patients and has been reported previously. 4 Go Heparin (150 IU/kg) was administered before the start of the first anastomosis to achieve an activated clotting time greater than 300 seconds. On completion of all anastomoses, protamine was given (1:1 ratio) to reverse the effect of heparin and return the activated clotting time to preoperative levels. The method of exposure and stabilization used to perform the anastomoses has been described previously. 9–11 Go The target vessel was exposed and snared above the anastomotic site by using a 4-0 Prolene (Ethicon, Inc, Somerville, NJ) suture with a soft plastic snugger to prevent coronary injury. The coronary artery was then opened, and the anastomosis was performed. An intracoronary shunt (Anastoflo Intravascular Shunt; Research Medical Inc, Midvale, Utah) was used to perform each anastomosis, to reduce blood loss and regional ischemia. 11 Go No patient had predonated autologous blood for perioperative use.

Laboratory and Bedside Measurements of Clotting Pathway and Platelet Function
Hemoglobin concentration, hematocrit, platelet count, measurements of clotting pathway function (international normalized ratio of the prothrombin time, a measure of the extrinsic and common clotting pathways; and activated partial thromboplastin time [APTT], expressed as the APTT ratio to a normalized control value, a measure of the intrinsic and common clotting pathways), serum fibrinogen levels, and thromboelastograms (TEG; Thrombelastograph; Haemoscope Corp, Skokie, Ill) were performed before surgery, immediately after the administration of protamine, 1 hour after completion of the surgical procedure, and then at 24 hours after the procedure. TEG was performed on heparinized celite-activated whole blood drawn from the arterial line. As part of routine postoperative care, hemoglobin concentration and hematocrit were measured on arrival in the ICU and then at hourly intervals, or as clinically indicated, via the indwelling arterial cannula.

Cost Calculation
The outcome variable was the total cost for both operative and postoperative services. Professional fees, preoperative costs, operating room and perfusionist staff costs, and drug costs were excluded. Variable and fixed direct costs were obtained for each care area and included the cost of operating room materials, bed occupancy (which included nursing costs), transfusion products, and postoperative complication management. Indirect costs such as hospital administration, building, and maintenance costs were excluded. Patients transferred to an intermediate care facility before home discharge were censored at the time of discharge from the cardiothoracic unit. All costs are in US dollars with the exchange rate calculated as of June 2004.

Statistical Analysis
Continuous measurements were assessed for normality of distribution. If skewed, data are summarized as a median and interquartile range; otherwise, a mean and SD are given. Data for the 2 groups were compared by using the Mann-Whitney test, and effect sizes are expressed as a median difference or hazard ratio (time measurements). Categorical data are reported as the number and percentage and were compared by using the Pearson {chi}2 test or Fisher exact test (if expected frequencies were <5). The odds ratio was used to quantify the effect of autotransfusion. All effect sizes are reported with 95% confidence intervals (CIs). Postrandomization measurements of hemoglobin and platelet count and measures of clotting pathway function were compared by using a mixed regression model. All analyses were adjusted for prerandomization (baseline) readings. A variety of models describing the correlations between repeated measurements on the same patient were examined, and the structure that led to the lowest value for the Schwarz bayesian information criterion was chosen in each case. Platelet count and fibrinogen both followed a skewed distribution and were transformed to the logarithmic scale for analysis. Model adequacy was assessed graphically, and where outlying observations were indicated, the model was refitted with the outlier(s) excluded. Results are reported here with outliers excluded. Changes in treatment effect over time were assessed with the F-test, and, if statistically significant at the 10% level, the treatment difference is reported separately at that time point. Otherwise, an overall effect of treatment is given. Results are presented as least-squares means and as a difference in means with 95% CIs. For platelet count and fibrinogen, least-squares geometric means and the ratio of geometric means with 95% CIs are given. All data analysis was performed with SPSS for Windows, version 9.0 (SPSS Inc, Chicago, Ill) except for the mixed regression models, which were fitted by using SAS version 8.2 (SAS Institute, Cary, NC).


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Discussion
 References
 
Baseline Characteristics
Preoperative and operative characteristics are shown in Table 1. The 2 groups were balanced before surgery with respect to demographics and comorbidity apart from a higher frequency of unstable angina symptoms in the autotransfusion group. Parsonnet scores or EuroSCOREs were similar for the 2 groups. Intraoperative characteristics were also well matched. No patient received aprotinin during the study. Ten patients in the autotransfusion group had cells salvaged but had insufficient volume to merit processing (<150 mL). This blood was discarded; however, these patients were included in the analysis on the basis of intention to treat.


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  		TABLE 1. Patient characteristics
 
Efficacy and Safety of Cell Salvage and Autotransfusion Versus Control
Patients in the autotransfusion group received a median of 236 mL (interquartile range, 206–342 mL) of autotransfused red blood cells after surgery. There was a statistical trend toward a reduction in the frequency of exposure to homologous blood products in the autotransfusion group (P = .095; Table 2). There was no difference between groups in postoperative chest drainage, ventilation time, ICU stay, or the frequency of serious morbidity. One patient in the autotransfusion group required 29 days of vacuum-assisted drainage for a deep sternal wound infection that resolved without operation. One patient in the control group had sternal rewiring after a sternal dehiscence. Two patients in the control group required noninvasive ventilation after extubation, and postoperative pneumonia developed in another 2 patients.


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  		TABLE 2. Postoperative outcome and homologous blood product requirements
 
Effect of Autotransfusion on Hematologic Indices and Measures of Coagulation Pathway and Platelet Function
The postoperative hemoglobin concentration was significantly higher in the autotransfusion patients. Hemoglobin levels were similar in the 2 groups after protamine administration and at 1 hour (P = .71 and P = .60, respectively), but at 24 hours the mean level was, on average, 1.02 g/dL lower in the control group (95% CI, –1.60 to –0.44; P = .0007; Table 3). A similar difference was noted with hematocrit. At 24 hours, the mean hematocrit level was significantly lower (0.03 L/L) in the control group (95% CI, –0.049 to –0.013; P = .0008). There was no difference between groups in the level of intraoperative or postoperative hemodilution (Tables 2 and 3). There was no difference between groups for any of the laboratory clotting pathway indices or TEG parameters measured (Table 3) except for a possible time-related difference between the 2 treatment groups for APTT (P = .075). The APTT ratio was similar in the 2 groups after protamine administration and at 24 hours (P = .47 and P = .42, respectively), but at 1 hour, the mean ratio was, on average, 0.057 lower in the control group (95% CI, –0.004 to 0.12; P = .069).


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  		TABLE 3. Hemoglobin concentration, platelet count, and measures of clotting pathway function: response over time and effect sizes
 
Effects of Cell Salvage and Autotransfusion on Procedural Costs
There was a significant difference in the median operative cost per patient between the 2 groups (Table 4), and this was attributed to the increased cost of the cell salvage consumables in the autotransfusion group, although this effect was minimized by not processing small volumes of blood. There was no difference in bed and nursing costs or complication-management costs (Table 4). Transfusion costs were less in the autotransfusion group; however, this was not statistically significant. The increase in operative costs as a result of using the cell salvage device did not result in a statistically significant increase in overall costs.


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  		TABLE 4. Perioperative costs
 

   Discussion
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Discussion
References
 
In this randomized study, intraoperative cell salvage was associated with higher postoperative hemoglobin concentrations, a modest reduction in transfusion requirements, no adverse clinical or coagulopathic effects, and no significant increase in total cost compared with controls. The benefits of a higher postoperative hemoglobin are intuitive, because ultimately this will result in lower homologous transfusion rates. Cell salvage and autotransfusion of blood spilled during surgery resulted in higher postoperative hemoglobin concentrations. As a result, fewer autotransfused patients reached the transfusion trigger (hematocrit <0.23), and fewer received transfusions. The observed 19% reduction in overall homologous blood component use in the autotransfusion group, although not statistically significant (P = .095), seems to us clinically relevant, particularly when one considers the low-transfusion-risk patient cohort and surgical technique (OPCAB), which will both have contributed to low overall homologous blood requirements. 4,7,12 Go The observed effect size of cell salvage on homologous red blood cell use was a reduction of 10%. We calculated that for any future study to detect a difference of this magnitude, given a 23% transfusion rate in the control group, 90% power, and a 2-sided 5% level of statistical significance, a total of 660 patients (330 per group) would be required. It is also possible that the effect size would have been greater had patients at higher risk of bleeding, such as unstable patients receiving preoperative heparin or clopidrogrel, been enrolled in the study. These patients were excluded, however, because of the greater variability observed in their perioperative clotting profiles.

Avoidance of homologous blood transfusion is not the only benefit of higher postoperative hemoglobin concentrations. Low intraoperative and postoperative hematocrit has been associated with both significantly increased mortality and severe morbidity, including low cardiac output syndrome, intra-aortic balloon pump use, and renal failure requiring dialysis. 13,14 Go In contrast, one study has suggested that hyperviscosity might contribute to graft thrombosis. Spiess and colleagues 15 Go demonstrated an association between a high postoperative hematocrit (>0.34) and postoperative myocardial infarction in patients after conventional CABG with CPB. The validity of this analysis has subsequently been questioned, however, 16 Go and such a prothrombotic effect, if any, would have to be compared with the well-documented benefits of avoiding homologous blood transfusion.

Historically, autotransfusion has been associated with increased bleeding and coagulopathy, the so-called salvaged-cell syndrome. 17 Go This has been addressed by modern cell-salvage and -washing systems, which effectively remove activated leukocytes, platelets, and inflammatory mediators from salvaged blood. 18–20 Go Concern remains, however, that even washed cells may have a coagulopathic effect. A randomized study demonstrated that postoperative autotransfusion of washed red blood cells increased serum fibrinogen levels, as well as prothrombin and APTT times, after CABG with CPB. 3 Go Similarly, retransfusion of cell salvage-washed red blood cells from the residual extracorporeal circuit blood after coronary bypass has been shown to result in deranged coagulation on laboratory testing. 19,20 Go Interpretation of these studies in on-pump patients is made difficult because of the background noise from increased fibrinolysis, platelet activation, and clotting factor consumption associated with CPB, 21,22 Go and clinical studies do not support any clinically significant effect of these apparent changes on blood loss or transfusion requirements after washed red blood cell autotransfusion. 1–3 Go OPCAB results in reduced thrombin generation, reduced fibrinolytic activity, and better overall preservation of hemostasis compared with conventional CABG 22,23 Go and serves as a better template to assess any derangement of hemostasis resulting from autotransfusion. These data demonstrate that, on routine use in OPCAB patients, there was no detectable coagulopathic or thrombotic effect of intraoperatively salvaged, washed red blood cells. Furthermore, there was no increase in bleeding or thrombotic events. We therefore conclude that autotransfusion is safe and effective.

Cell salvage was not associated with any significant increase in total cost, and although the power of this study to exclude a type II error in this respect is limited, these findings are noteworthy for several reasons. First, in addition to these immediate costs, homologous blood transfusion has additional indirect long-term and remote costs that were not considered in this analysis. For example, the annual costs of routine medical care, excluding emergency admissions and liver transplantation, for a patient with transfusion-associated hepatitis C infection in the United States in 1995 was $12,000. 24 Go Although transfusion-associated hepatitis C transmission is now very rare, new bloodborne pathogens (prions, West Nile virus, and transfusion-transmitted virus) are continuously emerging, 24,25 Go and the relative cost benefit of avoiding homologous blood exposure will only increase. Second, cell salvage is a relatively inexpensive cell-conservation modality. Mechanical cell salvage in many of our patients resulted in only 13% of patients requiring red blood cell transfusion, compared with 10% in a randomized trial of aprotinin in OPCAB (2 x 106 KIU loading dose followed by continuous infusion of 0.5 x 106 KIU throughout the operation). 26 Go The cost of intraoperative cell salvage in our study was, however, less expensive per patient than aprotinin therapy ($118.30 vs $261.55, respectively). Cell salvage and autologous blood transfusion may also avoid thrombotic complications that have been attributed to aprotinin use. 27 Go Acute normovolemic hemodilution combined with intraoperative tranexamic acid administration and, on demand, intraoperative reinfusion of shed blood (in 39% of patients) reduced homologous blood use from 20% to 4% in a randomized trial. 28 Go Cell-saver use was operator dependent, however, and was therefore a potential source of bias. Also, although both acute normovolemic hemodilution and tranexamic acid are inexpensive, the use of cell salvage will have increased the cost considerably. The relative cost-effectiveness of this and other strategies merit further analyses.

A potential criticism of this study is that the ICU staff were not blinded to treatment allocation. There is a recognized tendency to avoid homologous blood in patients in whom cell salvage devices are used, 29 Go and the unblinded nature of the study may have led to bias. Intraoperative cell salvage is used routinely in OPCAB patients at our institution, however, and strict local guidelines are used to make decisions about perioperative clinical management, thus making this less likely.

In conclusion, intraoperative cell salvage and autotransfusion in OPCAB surgery is associated with a modest clinical benefit, without increased risk to patients or significantly increased costs. As homologous blood becomes more expensive, the relative cost-effectiveness of this technique will increase. This study supports its routine use in OPCAB surgery, although its precise role as part of a multimodality red blood cell conservation strategy in OPCAB remains to be defined.


   Acknowledgments
 
We are grateful to Dr Raimondo Ascione, Franco Ciulli, and Jon Hutter for permitting their patients to be enrolled in this study and for the assistance of the Departments of Perfusion, Cardiothoracic Anaesthesia, and Intensive Care.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Discussion
 References
 

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Eur. J. Cardiothorac. Surg., August 1, 2006; 30(2): 271 - 277.
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