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* From the Critical Care Division (Drs. Leal-Noval, Rincón-Ferrari, Herruzo-Avilés, Camacho-Laraña, Garnacho-Montero, and Amaya-Villar) and the Microbiology Division (Dr. García-Curiel), Hospital Universitario "Virgen del Rocío," Seville, Spain.
Correspondence to: Santiago Ramón Leal-Noval, MD, Servicio de Cuidados Críticos y Urgencias. Hospital Universitario "Virgen del Rocío," Avda Manuel Siurot s/n, 41013. Seville, Spain; e-mail: sramon{at}cica.es
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Abstract |
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 TOP Abstract IntroductionMaterials and MethodsResultsDiscussionAppendix 1References |
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Setting: The postoperative ICUs of a tertiary-level university hospital.
Design: A cohort study.
Methods: During a 4-year period, 738 patients, classified as patients with SPIs and patients without SPIs (non-SPI patients), were included in the study. We studied the influence of 36 variables on the development of SPI in general and individually for pneumonia, mediastinitis, and/or septicemia. The influence of the blood derivatives on infections was assessed for RBC concentrates, RBC and plasma, and RBC and platelets.
Results: Seventy patients (9.4%) were
classified as having SPIs, and 668 (90.6%) were classified as not
having SPIs. After multivariate analysis, the variables
associated with SPI (incidence, 9.4%) were reintubation, sternal
dehiscence, mechanical ventilation (MV) for 
48 h, reintervention,
neurologic dysfunction, transfusion of 4 U RBCs, and systemic
arterial hypotension. The variables associated with nosocomial
pneumonia (incidence, 5.9%) were reintubation, MV for 48 h,
neurologic dysfunction, transfusion of 4 U blood components, and
arterial hypotension. The variables associated with mediastinitis
(incidence, 2.3%) were reintervention and sternal dehiscence, and
those associated with sepsis (incidence, 1.6%) were reintubation, time
of bypass 110 min, and MV for 48 h. The mortality rate
(patients with SPI, 52.8%; non-SPI patients, 8.2%; p < 0.001) and
mean (± SD) length of stay in the ICU (patients with SPI,
15.8 ± 12.9 days; non-SPI patients, 4.5 ± 4.4 days; p < 0.001)
were greater for the infected patients. The transfused patients also
had a greater mortality rate (13.3% vs 8.9%, respectively;
p < 0.001) and a longer mean stay in the ICU (6.1 ± 7.2 days vs
3.7 ± 2.8 days, respectively; p < 0.01) than those not
transfused.
Conclusion: The administration of blood derivatives, mainly RBCs, was associated in a dose-dependent manner with the development of SPIs, primarily nosocomial pneumonia.
Key Words: cardiac surgery • nosocomial pneumonia • postoperative infection • transfusion
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Introduction |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAppendix 1References |
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Blood transfusions are a frequent therapy in the ICUs. Patients received an average of 0.2 U/d in a multidisciplinary ICU, which increased to 1.3 U in cardiac surgery patients.7 Blood transfusions appear to increase the susceptibility to infection in surgical patients. Seventeen of 19 retrospective studies found transfusion to be a significant factor and, frequently, the single best predictor of postoperative infection.8 In a number of studies, transfusion has been considered a risk factor for the development of mediastinitis,5 9 early bacteremia,6 increased mortality rate, and the length of stay in hospitals10 after cardiac surgery. There are, however, many other uncontrolled, confounding, or circumstantial variables that impede the adequate assessment of the role of transfusions in the development of postoperative infections.
To our knowledge, few studies have been designed to assess the
influence of blood transfusions on the development of postoperative
infections in patients undergoing cardiac surgery.10
Recent data suggest that these patients are transfused
excessively11
; therefore, a decreased number of
transfusions could contribute to a reduction in morbidity and
mortality. In a 1998 randomized controlled trial12
carried
out in patients undergoing cardiac surgery, nosocomial pneumonia was
the most frequent infection and was found only when transfused RBC
concentrates accounted for 3 U. In our hospital, a case control
study13
demonstrated that the transfusion of 4 U blood
components was independently associated with the acquisition of
nosocomial pneumonia. Intraoperative RBC transfusion may contribute to
the inflammatory response after cardiac surgery and is associated with
a worse postoperative recovery.14
This cohort study was designed to establish the influence of blood transfusions (ie, RBC, plasma, and/or platelets) on the development of severe postoperative infections (SPIs) in 738 patients undergoing cardiac surgery. Our working hypothesis was that blood transfusions contribute to the development of SPI.
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Materials and Methods |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAppendix 1References |
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In most cases, patients received MV for < 8 h and were extubated when hemodynamically stable, with a Ramsay score of 2 to 3, arterial oxygen saturation of > 95% with a fraction of inspired oxygen of < 0.4, and no significant bleeding. Gastric protection was carried out routinely with famotidine (20 mg IV q12h) during the first 24 h after admission to the ICU, and if a patient required further treatment, famotidine was replaced by sucralfate (1 g po or by nasogastric tube q8h). When patients were in clinically stable condition, they were transferred from the ICU to a surgical ward, without any intermediate stay at a subacute unit.
Study Design
This study is a unicentric, cohort study in that all the data
have been collected and stored in a specially designed database
(Access, version 7 for Windows 95; Microsoft; Redmond, WA). All
patients undergoing cardiac surgery were initially evaluable.
Univariate and multivariate statistical analyses were performed using a
statistical software package (SPSS, version 7.5; SPSS; Chicago, IL).
Patients with any of the following characteristics were excluded from the study: (1) a stay in the ICU of < 24 h; (2) infection before admission to the ICU; (3) cardiac surgery without cardiopulmonary bypass; (4) cardiac transplant recipients and patients receiving immunosuppressive therapy; (5) age < 16 years; and (6) hemoglobin level of < 11 g/dL and/or disorders of coagulation before surgery.
The principal aim of the study was to determine whether a relationship exists between the transfusion of blood components and SPI. Other variables that can adversely affect the final results also were included in the statistical analysis in order to differentiate the effect of the variable transfusion from the remaining variables.
Consequently, the influence of 36 variables, including transfusion, on the acquisition of SPI was assessed in those subjects with at least one of the following infections: nosocomial pneumonia; mediastinitis; and/or sepsis of unknown origin. Subsequently, the influence of the same variables on the development of nosocomial pneumonia, mediastinitis, and sepsis of undetermined origin was assessed on an individual basis. These variables were as follows.
2 mg/dL), previous surgery, New York Heart
Association (NYHA) preoperative score III, acute myocardial
infarction before surgery (registered in the patients’ clinical
records), and a cardiac ejection fraction before surgery of 
40%
(assessed by echocardiography and/or hemodynamic evaluation). 48 h, the use of
inotropic drugs (first used in the operating room or in the ICU), CNS
dysfunction (focal or diffuse motor deficits without depressor
medication of the CNS), postoperative cardiac failure (requiring
inotropic drugs and/or vasodilator therapy in continuous perfusion),
the transfusion of blood components (RBC concentrates, plasma, and
platelets), the need for reintubation, the amount of mediastinal
bleeding, arterial hypotension in the immediate postoperative period
(mean arterial BP < 65 mm Hg for at least 1 h), fever during the
first 24 h after surgery (temperature, > 38.5°C), sternal
dehiscence, and an APACHE II score at admission to the ICU of 12.
All these variables were considered before the development of
nosocomial infection.
Infectious Surveillance and SPI
First-generation cephalosporins were used for antibiotic
prophylaxis just before the onset of the surgical intervention and
treatment was discontinued after the patient had been in the ICU for
24 h. Radial artery, pulmonary artery, and bladder catheters were
discontinued in the ICU within the first 24 h, whereas mediastinal
and pleural drainage was removed 48 h after admission to the ICU.
Patients received a daily chest radiograph. Tracheal secretions (before
extubation) and the tips of all intravascular catheters as well as an
exudate of the sternotomy wound were systematically cultured. If the
patient became febrile (body temperature, > 38°C), cultures of
blood, urine, and tracheal secretions were taken. In addition, venous
catheters were removed and cultured. If the origin of fever remained
unknown, a CT scan was carried out to rule out mediastinitis or
sinusitis as the cause of infection.
In the present study, only the following SPIs were considered: pneumonia; mediastinitis; or sepsis of unknown origin. In our experience, urinary tract infections and catheter-related bloodstream infections had a very low incidence because of our premature removal of bladder and venous catheters.
Five groups of patients were considered:
38°C, leukocytosis 12,000 cells/µL, or leukopenia
3,000 cells/µL, and purulent endotracheal secretion with a
Gram’s stain showing > 25 neutrophils and < 10 epithelial cells
per field. In all patients with a clinical suspicion of nosocomial
pneumonia, bronchial secretion was collected for culturing, obtained
with a protected pulmonary specimen brush (PSB), introduced by
fiberoptic bronchoscopy through the endotracheal tube. The results of
the brush culture were expressed in colony-forming units per
milliliter. The diagnosis of nosocomial pneumonia was made when at
least one of the following criteria was fulfilled: (1) positive
quantitative culture of a sample of the lower respiratory tract
obtained by PSB ( 103 colony-forming units per
milliliter); (2) blood culture positive for the same microorganisms
isolated in an approximate 48-h interval in samples obtained from the
respiratory tract (by PSB); and (3) pleural culture positive for the
same microorganisms isolated, in an approximate 48-h interval, in
samples obtained from the respiratory tract (by PSB); and
Allogeneic Blood Transfusion Criteria for Transfusion
The criteria for transfusion were based on previously published
regulations5
16
17
acknowledged by the anesthesiologists,
intensive care specialists, and surgeons involved in the care of these
patients, and adapted by our institution (see "Appendix"). However,
the decision on the transfusion requirement depended ultimately on the
physician in charge of the patient.
The number of units of blood components related to the development of postoperative nosocomial infection was calculated in an ascendant and stepwise fashion, first for all blood components (ie, any combination of RBCs, plasma, and platelets) and subsequently for each blood component in particular. These variables underwent successive division in order to determine the value at which the differences were found to be significant.
Statistical Analysis
A univariate analysis was performed to identify those risk
factors (36 in general, including transfusion) associated with SPI
(ie, nosocomial pneumonia, mediastinitis, and/or sepsis of
unknown origin). Subsequently, the influence of the same variables on
the development of nosocomial pneumonia, mediastinitis, and sepsis of
unknown origin was analyzed on an individual basis. The
2 test was used for the comparison of
dichotomized variables. The continuous variables, with a normal
distribution, were compared applying Student’s t test and,
if not normally distributed, they were compared using a Wilcoxon test.
The comparisons were unpaired and two tiered for all the tests with
statistical significance. The variables with p values 0.05 were
included in a logistic regression model with stepwise elimination. The
results of the univariate analysis were expressed as relative risk and
confidence intervals. The results of the four multivariate analyses
(ie, severe infection in general, nosocomial pneumonia,
mediastinitis, and sepsis of unknown origin) were expressed as adjusted
odds ratio and confidence intervals.
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Results |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAppendix 1References |
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III, 29.6%; and a preoperative ejection fraction
< 40%, 7.1% (Table 1
).
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Influence of the Variables on the Acquisition of SPI
Seventy patients (9.4%) fulfilled the requirements to be included
in the infected group vs 668 patients (90.6%) in the noninfected
group. In the univariate analysis, 17 variables showed a positive
influence on the development of postoperative infection (Table 2
). A logistic regression model was developed with these variables,
pointing out seven of the following variables as being independently
related to infection: reintubation; sternal dehiscence; MV for 48
h; reintervention; neurologic dysfunction; arterial hypotension; and
the transfusion of 4 U blood components (Table 3
).
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48 h; transfusion of 4 U RBC concentrates;
transfusion of 4 U blood components; arterial hypotension;
reintervention; and transfusion of 2 U plasma. Only the following
five variables continued in the multivariate analysis: reintubation; MV
for 48 h; neurologic dysfunction; transfusion of 4 U blood
components; and arterial hypotension (Table 3)
.
Influence of the Variables on the Acquisition of Mediastinitis
Seventeen patients (2.3%) received diagnoses of mediastinitis. In
the univariate analysis, a total of seven variables showed positive
influence on the development of mediastinitis: sternal dehiscence;
reintervention; reintubation; female sex; MV 48 h; postoperative
cardiac failure; and transfusion 4 U of RBC concentrates. Only two
variables appeared in the model of logistic regression: reintervention
and sternal dehiscence (Table 3)
.
Influence of the Variables on the Acquisition of Sepsis of Unknown
Origin
Twelve patients (1.6%) received diagnoses of sepsis of unknown
origin. The univariate analysis encountered the following five
variables with positive influences on the development of postoperative
sepsis from an undetermined origin: reintubation; MV for 48 h; time
of ischemia of 75 min; time of cardiopulmonary bypass circulation
of 110 min; and APACHE II score 12. A logistic regression model
was developed with the following three discriminating variables
independently related to sepsis: reintubation; time of cardiopulmonary
bypass circulation of 110 min; and MV for 48 h (Table 3)
.
Transfusion
Of the 738 patients, 592 patients (80.2%) underwent transfusion
and received RBC concentrates. One hundred fifty-eight patients
(21.4%) underwent transfusion with at least 1 U of plasma, and 89
patients (12%) underwent transfusion with at least 1 U of platelets.
All the transfusions were performed before the development of
nosocomial infection.
The transfusion of 4 U blood components (ie, any
combination of RBC concentrates, plasma, or platelets) was associated
with infection and pneumonia in the univariate analysis and only with
infection in the multivariate analysis. The transfusion of 4 U RBC
concentrates was associated with infection, nosocomial pneumonia, and
mediastinitis (univariate analysis) and was significant only for
infection and nosocomial pneumonia in the multivariate analysis. The
transfusion of 2 U plasma or 1 U platelets is related to the
development of infection and nosocomial pneumonia in the univariate
analysis but not in the multivariate analysis.
A direct relationship (Fig 1
) was established between the number of units transfused and the general
rates of infections, pneumonia, and mediastinitis. The rates of
infection, pneumonia, and APACHE II score increased considerably after
the transfusion of 4 U blood components.
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Outcome
Ninety-two patients died, for a crude mortality rate of 12.5%.
The mortality rate was 52.8% (37 of 70 patients) in the SPI group and
8.2% (55 of 668 patients) in the non-SPI group (p < 0.001). The
mean length of stay in the ICU was 15.8 ± 12.9 days in the SPI group
vs 4.5 ± 4.4 days in the non-SPI group (p < 0.001).
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Discussion |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAppendix 1References |
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In critically ill patients, it has been hypothesized that measures
aimed toward a maximal transportation of oxygen to the tissue aid in
avoiding oxygen debt. When transfusions, fluids, or drugs increase
oxygen delivery, the survival rate of high-risk surgical patients
improves markedly.18
19
However, this has not been
verified by a number of studies, in that the increase of oxygen
delivery to supranormal levels did not improve survival rates and,
moreover, had deleterious effects.20
A 1999 randomized
controlled trial21
was designed to determine whether a
restrictive strategy of RBC concentrate transfusion (to maintain
hemoglobin levels at 7 to 9 g/dL) and a liberal strategy RBC
concentrate transfusion (to maintain hemoglobin levels at 10 to 12
g/dL) could produce equivalent results in critically ill patients.
Results showed that death rates from all causes at 30 days were similar
in the two groups. However, the rates were significantly lower with the
restrictive transfusion strategy among patients who were less severely
ill (APACHE II score, 20) and were < 55 years of age. Moreover,
the restrictive strategy resulted in a relative decrease of 54% in the
number of transfusions, and 33% of the patients assigned to this
strategy did not receive any RBC transfusions. A study performed with
patients undergoing bypass surgery did not find differences between the
transfusion strategies.22
In fact, transfusion abuse could
lead to adverse results.23
24
However, anemia also can
increase the risk of death in critically ill patients with cardiac
disease.25
These results have led to a considerable
variation in transfusion policies among institutions in regard to
patients who are undergoing cardiac surgery,6
11
with a
high percentage of transfusions considered to be inappropriate. The
implantation of transfusion criteria could decrease the rate of the
patients who are transfused.5
The adverse effects of blood transfusions may be important, because they have been involved in the development of postoperative infections in patients undergoing cardiac surgery. Miholic et al3 studied the risk factors for the development of severe bacterial infections (ie, mediastinitis, pneumonia, septicemia, and prosthetic valve endocarditis) in 246 patients undergoing cardiac surgery. Many variables, such as the duration of surgery, reintervention because of bleeding, urgent surgery, intra-aortic balloon pumping, age, sex, and the professional status of the surgeon, were collected in the logistic regression model. The following three variables were found to be significant in the logistic regression analysis: the restoration of > 2,500 mL blood; reintervention; and the duration of the cardiopulmonary bypass. A similar study4 demonstrated that allogeneic transfusions were involved in the sternal infection of 2,579 patients undergoing cardiac surgery. Other studies have confirmed the relationship of the allogeneic transfusion with postoperative infection, mainly mediastinitis26 27 and pneumonia.13 It has been acknowledged28 that transfusions can be related to early bacteremia. In a case control study of 7,928 patients undergoing cardiac surgery, the logistic regression analysis established that pulmonary hypertension, diabetes, inotropic infusions, and the number of units of blood that were transfused were related to early bacteremia during the first 96 h after cardiopulmonary bypass.
In our study, RBC concentrate transfusions were involved in the development of infection in general (multivariate analysis), pneumonia (multivariate analysis), and mediastinitis (univariate analysis). Plasma or platelet transfusions were related to infection and mediastinitis (univariate analysis).
The effect that a blood transfusion can have on the immune system is called immunomodulation and may have very important repercussions. It is estimated that the death rate due to a postoperative infection caused by this immunomodulation may exceed the death rate caused by the combination of all the other transfusion risks.29 Measures directed toward decreasing the deleterious effects of immunomodulation could save between $6 and $12 billion dollars in hospital expenses, while reducing the number of postoperative infections.30 The mechanism of allogeneic transfusion-induced immunomodulation may involve altered cytokine regulation that contributes to the down-regulation of macrophage and T-cell functions and to the up-regulation of humoral immunity. Allogeneic transfusions decrease the cellular immune function of the monocytes, macrophages, T cells, and natural killer cells, down-regulating the antigen-presenting cells and T-cell function.29 This impaired cellular immune response is the mechanism that is proposed as being responsible for the high incidence of postoperative infections.31 The leukocytes present in transfused blood seem to have a primordial role in the suppression of cellular immunity.29 30
As in other studies, the association of transfusion with
infection was dose dependent with a threshold of 1 U for platelets,
2 U for plasma, 4 U for RBC concentrates, and 4 U for all
blood components (ie, any combination of RBC concentrates,
plasma, or platelets). Although excessive bleeding (ie,
800 mL) and severity of disease in the patient on admission to the
ICU (ie, APACHE II score of 12) were implicated in the
development of postoperative infection in the univariate analysis
(Table 2)
, they were not involved in the multivariate analysis,
suggesting that the association of the allogeneic transfusion with
postoperative nosocomial infection is independent of bleeding and
severity of disease in the patient. When the number of units
transfused increased, the infection rate and the APACHE II score did
also. The increase in the infection rate was, however, greater than
that in the APACHE II score (Fig 1)
.
The transfusion of RBC concentrates was related fundamentally to the development of nosocomial pneumonia. This relationship has been documented previously.2 3 12 13 In our study, the incidence of mediastinitis (2.3%) and of sepsis (1.6%) was low and the number of risk factors considered was high. So, it is probable that the number of patients necessary to demonstrate an association between allogeneic blood transfusion and mediastinitis and/or allogeneic blood transfusion and sepsis must be higher.
This study has important limitations. With an observational design, researchers can only control the effects of confounding factors that are known and are measurable, which can be introduced in the multivariate analysis.32 Unfortunately, this type of study does not measure the effects of other unknown modalities that can affect the final results. Therefore, it has been suggested that the immunomodulatory effects of allogeneic blood transfusion were not related to the transfusion itself,32 but to other clinical variables not measured in the study. That led to the blood transfusion and, hence, dictated the final outcome. Transfusion would only be a marker of uncontrolled confounding factors. For these same reasons, the possible influence of transfusions on mortality may suffer important misinterpretations. A low number of patients transfused with plasma or platelets exist. The transfusion of these components always has been accompanied by the transfusion of RBC concentrates. Hence, it is difficult to assess whether the transfusion of plasma and/or platelets influences the acquisition of postoperative infection. Although APACHE II severity scoring performs well to predict mortality after cardiac surgery,33 34 other severity scorings could be more appropriate for use with these patients. Other multiple factors relatedto the difficulty of surgery, personnel, equipment, manipulation, and length of stay may have been discarded involuntarily.
The practical consequences may be important. The perioperative transfusion of RBC concentrates is associated with nosocomial pneumonia. Our data also suggest that other blood components commonly used in patients undergoing cardiac surgery, such as plasma and/or platelets, could be involved. Until verification by new prospective studies, blood transfusions should be considered as a possible risk factor for postoperative infection.
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Appendix 1 |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAppendix 1References |
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8 g/dL; Fresh Frozen Plasma Patients with severe hemorrhaging and:
1.5 times
that of control subjects; Platelets Patients with severe hemorrhaging and:
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Acknowledgements |
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Footnotes |
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Received for publication December 7, 1999. Accepted for publication October 10, 2000.
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References |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAppendix 1References |
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