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* From the Departments of Cardiopulmonary Surgery (Dr. Fransen, and Dr. Maessen), Pulmonology (Dr. Dentener), and Surgery (Drs. Senden and Buurman), University Hospital Maastricht, Maastricht, Netherlands.
Correspondence to: Jos Maessen, MD, PhD, Department of Cardiopulmonary Surgery, University Hospital Maastricht, P. Debyelaan 25, PO Box 5800, 6202 AZ Maastricht, Netherlands; e-mail: jma{at}scpc.azm.nl
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Abstract |
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Design: Prospective study.
Setting: Cardiopulmonary surgery department in a university hospital.
Patients: One hundred fourteen consecutive patients undergoing cardiac surgery.
Interventions: Blood samples were taken at induction of anesthesia, at the start of aortic cross-clamping, at aortic unclamping, and at 0.5, 4, 8, and 18 h thereafter.
Results: Thirty-six patients received PC intraoperatively. BPI levels in patients who received transfusions were significantly higher at 0.5 and 4 h after aortic unclamping than in patients without transfusions (p < 0.05), and increased with the number of PC administered. IL-6 levels at 0.5, 4, and 18 h after aortic unclamping were also significantly higher in patients who received transfusions (p < 0.01). BPI was found in all units of packed red cells tested at concentrations up to 15 times preoperative plasma levels in patients. However, PC IL-6 could be detected in none of the samples. Plasma levels of LBP and CRP were similar in both patient groups. LBP was found in very low concentrations in all PC. Patients who received intraoperative transfusions had a worse postoperative performance.
Conclusions: Intraoperative PC transfusions do contribute to the inflammatory response after cardiac surgery both by enhancing part of the response and by directly changing plasma concentrations of inflammatory mediators. Furthermore, these data show that intraoperative PC transfusion is associated with a worse postoperative performance.
Key Words: blood transfusions • cardiac surgery • inflammatory mediators
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Introduction |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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The administration of allogeneic blood transfusions is a common procedure in cardiac surgery. However, along with its beneficial effects, allogeneic blood transfusions have been reported to suppress the immune system, thereby contributing to patient morbidity during recovery.3 4 Previous studies5 showed that the plasma supernatant of blood transfusion products contain bioactive substances that cause febrile reactions. Therefore, we examined whether administration of packed red cells to patients undergoing cardiac surgery, during the course of the operation, affects the release of inflammatory mediators into plasma in these patients. In addition, we examined the correlation of intraoperative packed red cell transfusion and patient morbidity during postoperative recovery.
For this study, we measured bactericidal permeability increasing protein (BPI) levels as a marker of activation of polymorphonuclear leukocytes (PMN), interleukin 6 (IL-6), and the acute-phase proteins lipopolysaccharide binding protein (LBP) and C-reactive protein (CRP) in 114 patients undergoing cardiac surgery, of whom 36 received at least one allogeneic packed red cell unit (PC) during surgery. In addition, we checked for the presence of BPI, IL-6, and LBP in packed red cells that were administered to these patients. Furthermore, we documented variables of postoperative performance.
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Materials and Methods |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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Intraoperative Patient Management
Standard anesthetic (lorazepam, fentanyl citrate, sufentanil
citrate, alfentanil hydrochloride, midazolam hydrochloride, pancuronium
bromide) and monitoring techniques (ECG, arterial pressure monitoring,
urinary output, rectal and skin temperature monitoring) were used in
all patients. Cefuroxime was used for antibiotic prophylaxis; the first
dose was administered before sternotomy.
Before connection to the non-heparin-coated extracorporeal circuit for CPB, porcine heparin (300 IU/kg [Heparin Leo; Leo Pharmaceutical Products BV; Weesp, The Netherlands]) was administered to achieve an activated coagulation time > 480 s (Hemochron 400; International Technidyne; Edison, NJ). Details of the extracorporeal circulation circuit and perfusion procedures have been published previously.6 After initiation of CPB and reaching a blood temperature < 28°C, the heart was topically cooled with cold saline solution (0.9%) at 4°C. When fibrillation occurred, the aorta was cross-clamped, and a single dose of approximately 800 mL (600 to 1000 mL) of St. Thomas-I cardioplegic solution at 4°C was infused into the aortic root during a period of 4 min (3 to 5 min) to provide myocardial preservation. Hypothermic pulsatile perfusion was maintained throughout the period of aorta cross-clamping. After completion of all distal anastomoses, the aortic cross-clamp was removed, and proximal anastomoses were performed with a partial occlusion clamp after spontaneous or electrical defibrillation. Meanwhile, the rewarming of the patient to 37°C continued. Heparin was neutralized by 3 mg/kg protamine chloride (Hoffman/Laroche BV; Mijdrecht, The Netherlands). All pump blood, including shed blood, was returned to the patient without hemoconcentration through the aortic cannula or IV via infusion bags. Allogeneic blood transfusions were administered if hematocrit values were < 20% in patients undergoing coronary artery bypass grafting or < 25% in patients undergoing valve surgery (in both cases in combination with the measured intraoperative blood loss or the extent of hemodilution). Patients received standard (leukocyte-containing, buffy coat-free) saline-adenine-glucose-mannitol RBCs (Dutch Red Cross Bloodbank Zuid-Limburg; Maastricht, The Netherlands), 325 mL/U, hematocrit 60%. RBC units contained < 5 x 108 leukocytes/U and < 15 x 109 thrombocytes/U. RBC units were stored at 4°C. Postoperative patient treatment in the cardiac surgical care unit was standardized and similar for both groups. All packed red cells were administered before the final intraoperative blood sample was taken, eg, within 0.5 h after the release of the aortic cross-clamp.
Blood Sampling
Blood samples were taken at induction of anesthesia (baseline),
at the start of aortic cross-clamping, at the start of reperfusion, and
at 0.5, 4, 8, and 18 h thereafter. Samples were collected in
evacuated blood collection tubes (10 mL, Monoject; Sherwood Medical;
Ballymoney, Northern Ireland) containing ethylenediaminetetraacetic
acid. Immediately after sampling, the blood was cooled and centrifuged
at 3,500 rpm for 20 min, and plasma samples were stored at -70°C
until measurements were performed.
For measurement of inflammatory mediators in the units of allogeneic packed red cells, we randomly selected 12 U of packed red cells. Samples were collected in evacuated blood collection tubes (5 mL, Monoject) containing ethylenediaminetetraacetic acid. Samples were collected directly from the infusion bag in case packed red cells were included in the priming volume of the heart-lung machine, or at bedside just before infusion from a routinely used setup of four one-way stopcocks (Vygon; Ecouen, France), after which the samples were treated as described above for the plasma samples.
Measurements
Plasma levels of BPI, IL-6, and LBP were measured using sandwich
enzyme-linked immunosorbent assays (ELISA), which have been described
elsewhere.7
8
9
In short, 96-well plates
(Immuno-Maxisorp; Nunc; Roskilde, Denmark) were coated with the
appropriate antibodies. For BPI, IL-6, and LBP measurements, human
BPI-specific monoclonal antibody (MoAb) 4E3, murine MoAb 5E1, and
polyclonal anti-human LBP IgG, respectively, were used as coatings.
Free sites were blocked with 1% bovine serum albumin in
phosphate-buffered saline solution. Samples and standard dilution
series were added for 2 h. Human recombinant BPI (kindly provided
by M. Marra; Incyte; Palo Alto, CA), human recombinant IL-6 (a kind
gift from Prof. W. Sebald; Psychiologisch-Chemisches Institut der
Universität Würzburg; Germany), and human recombinant LBP
were used for standard titration curves. Human recombinant LBP was
obtained from supernatant of Chinese hamster ovary cells transfected
with cDNA of human LBP (kindly provided by Dr. P. Tobias; Scripps
Research Institute; La Jolla, CA). In case of the BPI and LBP ELISA,
washing and dilution buffers contained 80 or 40 mM magnesium chloride,
respectively, to prevent disturbance by lipopolysaccharide.
Biotinylated polyclonal rabbit anti-human BPI IgG, biotinylated
polyclonal rabbit anti-human IL-6 antiserum, and polyclonal rabbit
anti-human LBP IgG were used as detection antibodies. The detection
limits for the ELISAs were 200 pg/mL for the BPI-assay, 10 pg/mL for
IL-6, and 500 pg/mL for LBP. Biotinylated antibodies were detected with
peroxidase-conjugated streptavidin (Zymed; San Francisco, CA). Finally,
3,3',5,5'-tetramethylbenzidine (Kirkegaard & Perry Laboratories;
Gaithersburg, MD) was used as a substrate. Photospectrometry (450 nm)
was performed using a micro-ELISA autoreader. All plasma samples were
analyzed in the same run.
CRP concentrations were measured using a turbidimetric method. A CRP reagent (Beckman test kit number 445855), in conjunction with the Synchron CX Systems CX CRP Calibrator Set (Beckman, number 445915; Beckman Instruments; Brea, CA), was used for the quantitative determination of CRP in serum. CRP levels were determined on the day before surgery, and on days 1, 2, 4, and 6 after surgery.
Clinical Data
The following variables were recorded: type of surgery, time
until weaning from ventilation, postoperative stay in the ICU, diuresis
during the first 24 postoperative hours, total mediastinal fluid
drainage, length of postoperative hospitalization, incidence of
postoperative infection during hospitalization, and mortality. Centers
for Disease Control and Prevention definitions for nosocomial
infections were used for diagnosing postoperative
infections.10
All infections were diagnosed during
hospitalization.
Data Analysis
Repeated-measures analysis of variance was used to compare
changes in time between both patient groups. The Mann Whitney
U test was added to isolate significant differences between
both experimental groups at a single, predetermined time. A Wilcoxon
matched-pairs signed-ranks test was used for comparisons of values from
one variable between two times. Incidence of variables was analyzed by
a 
2 test. Independent predictive value of
variables was assessed by multiple regression analysis. Differences
were considered significant at p values < 0.05. All data are
presented as mean ± SEM.
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Results |
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Mean preoperative plasma levels of the acute-phase protein LBP were 32.4 ± 4 and 40.0 ± 5 µg/mL in the control group and transfusion group, respectively (Fig 1 , bottom left, C). In both groups, LBP plasma levels decreased during surgery (until 0.5 h after reperfusion; p < 0.01), and gradually increased between 0.5 and 18 h after reperfusion (p < 0.01).
Mean preoperative plasma levels of CRP were 11.5 ± 3 and 12.1 ± 4 mg/L in the control group and transfusion group, respectively (Fig 1 , bottom right, D). On the first postoperative day, CRP levels were significantly increased in both groups, to 86.9 ± 3 mg/L in the control group and 82.6 ± 7 mg/L in the transfusion group. CRP levels reached their highest mean plasma levels on day 2 after surgery and gradually decreased thereafter. All postoperative CRP levels were significantly elevated from baseline levels (p < 0.01). Both LBP and CRP levels did not significantly differ between both patient groups at any time.
Clinical Data
Preoperative hematocrit values and hemoglobin levels were
significantly lower in the transfusion group than in the control group,
32 ± 6% vs 38 ± 4% (p < 0.001), and 7.2 ± 0.1 vs
8.5 ± 0.1 mmol/L (p < 0.001), respectively. Hematocrit values and
hemoglobin levels decreased postoperatively without differences between
the patient groups. On the first postoperative day, hematocrit values
and hemoglobin levels were 29 ± 4% and 6.2 ± 0.1 mmol/L in the
transfusion group, and 30 ± 3% and 6.3 ± 0.1 mmol/L in the
control group. Both hematocrit values and hemoglobin levels did not
significantly differ between both patient groups at this time.
Time until weaning from ventilation was significantly longer in patients who received transfusions than in control patients: 42 ± 12 vs 22 ± 2 h (Table 2 ). Furthermore, postoperative length of stay on the cardiac surgical ICU until transportation to the ward was significantly longer in patients who received transfusions (Table 2) . Postoperative mediastinal bleeding and postoperative diuresis during the first 24 postoperative hours did not significantly differ between both groups (Table 2) . The incidence of postoperative infections in control patients and in patients who received transfusions was not significantly different (odds ratio = 2.12; 95% confidence interval, 0.70 to 6.36). However, the duration of postoperative hospitalization was significantly longer in patients who received transfusions than in control patients (Table 2) .
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Analysis of Risk Factors for Red Cell Transfusion and Postoperative
Morbidity
Using retrospective group stratification, we found significant
differences between control patients and patients who received
transfusions with respect to age, height, weight, the distribution of
sex (Table 1)
, and preoperative hematocrit and hemoglobin levels. A
stepwise multiple regression analysis including these variables as
independent variables and the administration of packed red cells during
surgery as the dependent variable revealed, as expected, that
preoperative hematocrit and hemoglobin levels are key determining
factors in intraoperative packed RBC transfusion requirements
(p < 0.001 and p = 0.023 for hematocrit and hemoglobin,
respectively). Furthermore, entering age, height, weight, sex, and the
intraoperative administration of packed red cells as independent
variables and postoperative BPI or IL-6 levels as the dependent
variable showed that the intraoperative administration of packed red
cells during surgery was the most important predictor of BPI levels at
aortic unclamping (p = 0.009) and 0.5 h thereafter
(p = 0.002), and IL-6 levels at 0.5 (p = 0.025) and 4 h after
aortic unclamping (p = 0.002). In addition, entering age, sex, and
the intraoperative administration of packed red cells as independent
variables and time until weaning from ventilation or postoperative stay
in the ICU as the dependent variable revealed that, in both cases, the
intraoperative administration of packed red cells was the most
important independent variable predicting time until weaning from
ventilation (p = 0.022) and postoperative stay in the ICU
(p = 0.011). Therefore, despite the differences in some preoperative
variables, the intraoperative administration of packed red cells during
cardiac surgery is found to be significantly associated with the
release of inflammatory mediators BPI and IL-6, and to coincide with
impaired postoperative performance.
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Discussion |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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In the present study, we measured BPI in plasma from patients as well as in PCs to evaluate whether cells that originate from transfusion units affect the presence of inflammatory mediators found in the recipient. BPI is a human neutrophil granule protein that has been shown to bind to lipopolysaccharide and both exerts bactericidal effects on Gram-negative bacteria and neutralizes the activities of lipopolysaccharide.1 In plasma, BPI is released after activation of PMNs and therefore can be used as a marker of PMN activation. In the PCs, large amounts of BPI may be released from the azurophilic granules because of PMN activation by the plastic infusion bag or PMN disintegration as a result of cold storage (4°C).11
Transfusions and PMN Activation
In our study, we showed a perioperative increase in BPI plasma
levels, which was identical to levels that we found in previous
studies,1
12
with higher levels at 0.5 and 4 h after
aortic unclamping in patients who received transfusions (p < 0.05).
In addition, BPI was present in all packed red cells with higher levels
in units that had been stored longer. These data suggest that part of
the higher BPI levels at 0.5 and 4 h after aortic unclamping in
the patients who intraoperatively received transfusions may originate
from the transfusion units. Indeed, calculations revealed that in
patients receiving 2 U of packed red cells, approximately 15% of the
total amount of BPI in plasma at 0.5 h after aortic unclamping can
originate from the transfusion products (based on an estimated plasma
volume of 4,500 mL). Alternatively, the BPI increase can be explained
by either donor or recipient leukocytes becoming activated on
transfusion, and at this time releasing their BPI from the azurophilic
granules.
Several studies have shown that leukocytes present in allogeneic cellular blood components are associated with adverse effects in the recipient.3 13 The proposed immunosuppressive effects of donor leukocytes might be beneficial for some patients, eg, for the maintenance of kidney allografts.13 In patients undergoing cardiac surgery, however, these effects may be undesirable inasmuch as these patients are already immunosuppressed by the surgical trauma. Although it is generally assumed that these effects are caused by the interaction of anti-leukocyte alloantibodies in the recipient’s plasma and WBCs in the transfusion product, Heddle et al5 recently reported that unidentified bioactive substances in the plasma supernatant produced or released by platelet products mediate reactions on transfusion.5 Our present data are in support of this view inasmuch as they confirm the presence of large amounts of BPI in packed red cells. The transfusion of BPI by giving packed red cells to a patient actually leads to increased circulating plasma levels of BPI. It cannot be deduced from our present data that higher BPI levels cause an increased postoperative morbidity.
Transfusions and Acute-Phase Response
In agreement with previous studies,1
14
increased
plasma IL-6 levels were observed in all patients in the present study.
Neutrophil- and mononuclear phagocyte-derived IL-6 is released in
response to a variety of stimuli, including infection, major surgery,
and thermal injury.15
IL-6 is a pleiotropic cytokine that
stimulates the adhesive interaction between neutrophils and cardiac
myocytes and induces the acute-phase response, and therefore it is a
sensitive marker of the inflammatory response. In this study, the
enhancement of IL-6 levels in control patients was significantly
delayed and also lower compared with those of patients who received
transfusions, although the pattern of IL-6 release was similar in both
patient groups. Unlike BPI, we did not detect IL-6 in PCs, which is in
agreement with findings by others.16
Interestingly, IL-6
was found by several authors in stored platelet
concentrates.5
17
18
19
Heddle et al5
found low
concentrations of IL-6, even when the concentrate was filtered before
storage to remove contaminating leukocytes. In addition, they showed
that IL-6 levels in the platelet concentrates progressively increased
during storage and were positively correlated with the leukocyte count
in the platelet product. Importantly, in their study, the platelet
concentrates were stored at 22°C (vs 4°C for the packed red cells
in our study), which may have affected the production and release of
IL-6 in these concentrates. Although others reported that the
production of proinflammatory cytokines is one of the immune functions
that is depressed by allogeneic blood transfusions,20
the
findings of the present study suggest that the significantly higher
IL-6 plasma levels in the patients who received transfusions result
from an increased IL-6 release by the recipient. Whether substances in
stored blood induce this increased IL-6 release has yet to be
established.
Plasma levels of CRP and LBP, two acute-phase proteins, were similar in both patient groups. CRP is the prototypal acute-phase reactant and can activate the classic pathway of complement.21 Our data support the acute-phase nature of the LBP response as well as the CRP response. Because LBP is produced by hepatocytes and was found in all PCs, the LBP in these units probably originates from the donor and is not produced or released during cold storage. This finding is supported by the fact that, unlike BPI levels, LBP levels did not increase with the length of storage. LBP levels in the PCs were low compared with LBP plasma levels and presumably did not substantially affect plasma levels (Fig 1 , bottom left, C).
Interestingly, the rise of LBP and CRP in the systemic circulation was identical in both study groups, despite the fact that we found significant differences in plasma cytokine levels (Fig 1 , bottom, C and D). Thus, the present data suggest that, in patients undergoing cardiac surgery, the amount of circulating IL-6 in the systemic circulation does not necessarily reflect the amount of acute-phase proteins produced.21 22
Patient Morbidity
In patients undergoing cardiac surgery, the surgical trauma
induces a noninfectious systemic inflammatory response, which is
considered to play a role in the development of postoperative
complications.23
Thus, in patients receiving allogeneic
packed red cells, bioactive substances might serve as a second
inflammatory insult, which amplifies the initial inflammatory response.
This results in a further imbalance between proinflammatory and
counterregulatory influences, which may lead to damage of otherwise
healthy cells and organs, and thus leads to an impaired postoperative
recovery. Our data support the findings by others showing that patients
who received packed red cells during cardiac surgery have more
complications during the postoperative course.24
A
multiple regression analysis identified the intraoperative transfusion
of packed red cells as the most important independent variable
significantly associated with worse postoperative performance, among
the classic risk factors, age and female sex. However, the direct link
between packed red cell transfusion and increased postoperative
morbidity has yet to be established.
Concluding Remarks
The findings of the present study are important for several
reasons. This study shows for the first time that intraoperatively
transfused units of packed red cells affect the perioperative release
of inflammatory mediators in patients undergoing cardiac surgery. These
transfusions affect the well-known systemic inflammatory response to
cardiac surgery both by enhancing part of the response and by direct
transfusion of bioactive substances into the circulation. Thus, our
data suggest that the findings of previous studies on the release of
inflammatory mediators in response to cardiac surgery and/or the CPB
procedure that did not take the intraoperative administration of packed
red cell transfusions into account need to be reconsidered.
In addition, we show that the intraoperative administration of allogeneic packed red cells in cardiac surgery coincided with increased postoperative morbidity. Because packed red cells contain considerable amounts of BPI, as was demonstrated in this study, other neutrophil granule proteins, such as elastase, cathepsin G, and highly toxic defensins, may also be present in transfusion products. Future studies should reveal whether the administration of these bioactive substances through blood transfusions directly affects postoperative morbidity.
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Footnotes |
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Abbreviations: BPI = bactericidal permeability increasing protein; CPB = cardiopulmonary bypass; CRP = C-reactive protein; ELISA = enzyme-linked immunosorbent assay; IL-6 = interleukin-6; LBP = lipopolysaccharide binding protein; PC = packed red cell unit; PMN = polymorphonuclear leukocytes
Abstract was winner of the "ACCP Young Investigator Award," CHEST 1998, November 8–12, 1998, Toronto, Canada.
Received for publication December 8, 1998. Accepted for publication April 16, 1999.
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