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Ann Thorac Surg 1998;66:870-875
© 1998 The Society of Thoracic Surgeons

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Original articles: Cardiovascular

Association between age and blood loss in children undergoing open heart operations

^a Department of Anesthesiology, Children’s Hospital and Regional Medical Center, University of Washington School of Medicine, Seattle, Washington, USA

Accepted for publication May 1, 1998.

Address reprint requests to Dr Williams, Department of Anesthesia and Critical Care, Children’s Hospital and Regional Medical Center, PO Box 5371/CH-05, Seattle, WA 98105-0371
e-mail: (jwilli{at}chmc.org)

	Abstract

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
Background. Although recent studies indicated young children are at risk for increased perioperative hemorrhage after open heart operations, the associations between patient age, blood loss and blood product transfusions have not been fully defined in children.

Methods. Perioperative blood loss and blood product transfusion data were recorded for 414 consecutive children undergoing open heart procedures. The children were in the following age groups: 1 month or younger, group 1; older than 1 month to 12 months, group 2; older than 1 year to 5 years, group 3; and older than 5 years, group 4.

Results. Postoperative blood loss and blood product transfusions were inversely related to age and differed significantly between the four age groups. Multiple preoperative and intraoperative factors that possibly influence hemostasis also differed significantly between age groups. Median units transfused within 72 hours differed significantly with age (p < 0.0001): group 1, 8 units (range, 1 to 19 units); group 2, 6 units (range, 0 to 21 units); group 3, 2 units (range, 0 to 23 units); and group 4, 0 units (range, 0 to 38 units).

Conclusions. Blood loss and transfusions vary inversely with age. Per kilogram of body weight, neonates bled more and received more donor products than any other age group.

	Introduction

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There is morbidity and mortality associated with excessive perioperative hemorrhage after cardiac operations [1, 2]. Although a substantial research effort has been focused on hemostasis in adults undergoing cardiac surgical procedures, the same is not true for children [3]. Collectively, children undergoing open heart operations are very heterogeneous with a wide age distribution. Increased blood loss has been noted in younger patients [4–8], but there are no reports specifically relating age to perioperative blood loss and blood transfusion therapy.

Age can influence hemostasis during pediatric cardiac surgical procedures through several mechanisms, including immaturity, disease pathology, and complexity of the operative procedure [9]. The relationship between age or size and bleeding deserves examination because patients at increased risk of bleeding can be identified, thereby assisting physicians in their selection of appropriate hemostasis management strategies and providing parents with information about the transfusion risk to their child.

The aims of this study of children undergoing open heart operations were to investigate whether age is associated with perioperative blood loss and transfusion requirements and to identify age groups at increased risk for bleeding.

	Material and methods

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After institutional review board approval, data pertaining to perioperative hemostasis and its management were obtained prospectively on consecutive children 18 years of age or younger who underwent an open heart operation at Children’s Hospital and Regional Medical Center, Seattle, from January 1996 to June 1997. Parental or patient consent was not required. Children receiving prophylactic antifibrinolytic therapy were excluded. Patient sex, age, weight, and height were noted, as were preoperative medications and details of anesthesia, surgical, and cardiopulmonary bypass (CPB) technique.

Anesthesia, anticoagulation, and cardiopulmonary bypass
Patients received fentanyl (25 to 100 µg/kg), midazolam hydrochloride (0.1 to 0.4 mg/kg), and muscle relaxants (vecuronium bromide, 0.1 mg/kg, pancuronium bromide, 0.1 mg/kg, or both). Anticoagulation was established with an initial bolus (infants 1 year of age, 400 U/kg, and children >1 year of age, 300 U/kg) of porcine heparin (Elkins-Sinn, Inc, Cherry Hill, NJ); additional heparin was administered during CPB to maintain celite activated clotting time higher than 480 seconds. Initial protamine sulfate dose was 3 to 5 mg/kg. Nonpulsatile CPB was performed with a hollow-fiber membrane oxygenator (Terumo Corp, Tokyo, Japan). The CPB circuit was primed with lactated Ringer’s, 5% albumin, 8.5% sodium bicarbonate, and heparin (3.0 ± 1.0 U/mL, dose depended on prime volume). The CPB circuit prime volumes ranged from 420 to 1,950 mL, depending on the patient’s size. When necessary, whole blood was added to maintain a hematocrit of about 20% during CPB. The extent of hemodilution by CPB was calculated as , where EBV is estimated blood volume (milliliters) and PV, measured prime volume (milliliters). Hypothermia was induced in all patients and the minimum core temperature was recorded. By surgical protocol, blood conservation techniques included modified venovenous ultrafiltration for infants younger than 1 year and red blood cell salvage for all other children. After bypass, residual blood in the CPB circuit was processed by cell salvage.

Laboratory tests
Perioperative laboratory tests included hematocrit, prothrombin time, activated partial thromboplastin time, platelet count, fibrinogen concentration, thrombin time, D-dimers, and thromboelastography. Thromboelastograms (TEGs) were obtained using recalcified citrated whole blood in a metal cuvette (Thromboelastograph Coagulation Analyzer; Haemoscope Corp, Skokie, IL). If the sample was taken during CPB, 10 µL (5 µg) of protamine sulfate solution was added to neutralize the heparin effect [10]. Five values were measured from the TEG: R (reaction time), K (coagulation time), (angle), MA (maximum amplitude), and A30 (amplitude 30 minutes after MA). An A60 to MA ratio of less than 0.85 has been used to define increased fibrinolysis [11]. In this study, increased fibrinolysis was conservatively defined as a TEG A30 to MA ratio of less than 0.85 because our institution’s laboratory does not report A60.

Blood loss
Total blood loss represented the sum of intraoperative and postoperative blood loss. Intraoperative blood loss per kilogram of body weight was calculated from sponge weights, discarded suction volumes, chest tube output, and volume of salvaged washed red cells. Postoperative blood loss per kilogram of body weight was calculated as running totals from the chest tube output at 6, 12, 24, and 48 hours after the patient’s arrival in intensive care.

Blood product transfusions
Blood components were administered to treat excessive microvascular (coagulopathic) bleeding. The decision to transfuse was based on measured blood loss and intraoperative visual assessment of the surgical field. Component therapy was guided by hematocrit and laboratory coagulation tests. During the early period after CPB, platelet transfusion (1 U/10 kg) was considered if the platelet count on CPB was less than 100,000/µL, and fresh frozen plasma (10 to 20 mL/kg) or cyroprecipitate transfusion (1 U/5 kg) was considered if the fibrinogen concentration on CPB was lower than 100 mg/dL. Further administration of blood products was guided by results of coagulation tests after transfusion (prothrombin time, activated partial thromboplastin time, platelet count, fibrinogen concentration, thrombin time, D-dimers, and thromboelastography) and followed previously published recommendations [9]. Postoperative minimum acceptable hematocrit values ranged from 20% to 45%, depending on the presence of cyanosis and the complexity of the surgical repair. Whole blood (> 48 hours since donation) was used in the early period after CPB. Packed red blood cells were transfused if whole blood was not available or the volume of blood to be administered was a concern. The volume (milliliters per kilogram) of blood products transfused intraoperatively (including blood added to the CPB prime) and during the first 72 hours after operation was noted.

Data analysis
Factors that possibly could be related to blood loss were examined to determine their distribution by patient age. The preoperative risk factors analyzed included coagulation tests (prothrombin time, activated partial thromboplastin time, thromboelastography fibrinogen concentration, and platelet count), polycythemia (hematocrit > 46%, an indirect indicator of cyanotic heart disease), congestive heart failure, and anticoagulation therapy. Congestive heart failure was defined as preoperative therapy with at least two of the following medications: digoxin, diuretics, vasodilators, or intravenous inotropic agents; anticoagulation was defined as administration of Coumadin (crystalline warfarin sodium), aspirin, or heparin therapy or continuous heparin flush to maintain vessel patency. Intraoperative risk factors considered included repeat sternotomy, complexity of operation [5], duration of CPB, duration of aortic cross-clamping, duration of deep hypothermic circulatory arrest, minimum core temperature on CPB, type of CPB prime, increased fibrinolysis, and coagulation tests during CPB.

Patients who required reoperation for surgical bleeding were excluded from blood loss and transfusion analysis. Continuous independent data were analyzed with the t test and analysis of variance. The Tukey B adjustment was used for multiple post hoc comparisons. Median donor exposure was compared using the Kruskal-Wallis test. Categorical data were analyzed with the ² and ² for Trend tests. A multivariate analysis of variance test was used to analyze serial chest tube drainage over 48 hours. Significance was defined as a p value of less than 0.05. Data were analyzed with a commercial statistical package, SPSS for Windows (SPSS Inc, Chicago, IL) and are reported as the mean ± the standard deviation unless stated otherwise.

	Results

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Demographics
There were 414 patients (55% male) in the study, and their age-group distribution is shown in Table 1. Data are presented for four age groups that were formulated to be clinically relevant and accurately illustrative of the associations between age and blood loss: 1 month or younger, group 1; older than 1 month to 12 months, group 2; older than 1 year to 5 years, group 3; and older than 5 years group 4. Twenty patients (5%) were reexplored for bleeding; large-vessel (surgical) hemorrhage was identified or suspected to be a contributory cause in 11 children, and microvascular hemorrhage was considered the most likely cause in the others. Twelve of the 20 patients were in group 1, and the incidence of reexploration was significantly greater in infants than in older children. Thirty-nine patients (9%) died (of all causes), and their age-group distribution was as follows: group 1, 66%; group 2, 20%; group 3, 9%; and group 4, 5%. Mortality in infants was significantly greater than in older children.

Blood loss and blood product transfusion therapy
Postoperative chest tube output was inversely related to age. Blood loss at 24 hours differed between the four age groups (Table 3). For all time points, neonates (1 month of age) had the greatest postoperative blood loss, and children older than 5 years experienced the least loss. Age-related differences for intraoperative blood loss were significant only in the neonatal group. Table 4 lists published blood loss data for different pediatric age groups.

	Comment

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Blood loss and transfusion requirements: relationship to age and size
This prospective study in children undergoing open heart operations found postoperative blood loss (milliliters per kilogram) was inversely related to age and differed significantly between four age groups (1 months, >1 month to 12 months, >1 year to 5 years, and >5 years). These age-related differences were apparent at 6, 12, 24, and 48 hours after operation. Total products and the individual components administered (milliliters per kilogram) were likewise inversely related to age, with significant differences demonstrated between the four age groups. Median number of units transfused per patient also differed inversely with age.

The coagulopathy associated with CPB is recognized in children [3, 23–25], but the heterogeneity of children with congenital heart disease complicates their hemostasis management. Surgical repair of congenital heart defects in newborns and infants has become standard practice, and in the present study, 38% of patients were less than 1 year old. There are only a few reports of the association of age or size and blood loss. Two prospective studies of children after open heart operations found that patients less than 2 years of age (n = 161) [5] and children weighing less than 8 kg (n = 75) [8] bleed more than older or bigger children. Similarly, children weighing less than 10 kg (n = 12) had greater blood loss than children weighing 13 to 19 kg (n = 12) [13], and a retrospective study [6] of 73 patients reported neonates had greater blood loss and donor exposure than children more than 1 month to 12 months old. A retrospective analysis [26] of perioperative blood product use during 126 pediatric cardiac operations noted infants less than 4 months of age required greater numbers of blood product units, but average number of components transfused did not correlate with age.

Our study findings have several implications. First, as shown in Table 4, investigations reporting blood loss during congenital heart operations sometimes group together children ranging in age from neonates to adolescents. Researchers should recognize that age and size are associated with blood loss. Second, our study confirmed that small infants incur the greatest hemostatic derangement and quantified their impressive transfusion requirements. Autologous transfusion is not realistic for this age group. In addition to risk from multiple donor exposures [1], small children are more prone to complications related to infusion rate and volume [27] because large volumes of blood products, in excess of the patient’s blood volume, are often administered.

Risk factors for bleeding: relationship to age and size
Examination of the relationships between patient age and risk factors for bleeding was undertaken to gain insight into the association between patient age and blood loss in children. Our study showed neonates were more likely to have abnormal preoperative laboratory coagulation test results (eg, prothrombin time), a finding consistent with a previous report [24]. Polycythemia (a surrogate measure of cyanotic heart disease), treatment of congestive heart failure, and anticoagulant administration were inversely related to age and have been associated with impaired coagulation [28, 29]. Older children were more likely to undergo reoperation, a risk factor for bleeding in adults [1]. Infants less than 1 year old were more likely to undergo complex operations, had a longer duration of CPB, and were subjected to a greater degree of hemodilution, hypothermia, a period of deep hypothermic circulatory arrest, or both. On-CPB values for platelet count, fibrinogen concentration, and TEG MA were most abnormal in group 1 (1 month). Hemodilution has a major influence on coagulation tests during CPB and is an important contributor to the coagulopathy associated with CPB in children [3, 23]. Complexity of operation, age younger than 2 years, weight less than 8 kg, polycythemia, prolonged CPB, deep hypothermic circulatory arrest, and hematocrit after CPB have been reported as risk factors for bleeding in children after open heart procedures [5, 6, 20]. Young children were identified as the age group most likely to become hyperfibrinolytic during CPB. There is evidence for increased fibrinolysis in children undergoing open heart operation [3, 25]. Excessive fibrinolysis in adults has been linked to hemorrhage [11], but the contribution of fibrinolysis to bleeding in children after open heart procedures is unclear [3].

Age and size are correlated in pediatric patients, but this study has not determined if they are independent risk factors for bleeding. As discussed already, we and others have shown that many important hemostatic factors also correlate with age and bleeding, thus confounding the actual effect of age or size on bleeding during open heart operations. However, age is easily measured and can be employed clinically as a useful indicator of blood loss and transfusion requirements.

Magnitude of blood loss
For both children [6, 8] and adults [1], blood loss and transfusion practices after cardiac surgical procedures vary widely between institutions (see Table 4). Lack of availability of fresh whole blood in the present study may have had an adverse impact on the number of donor exposures [5], although component therapy (after priming the CPB circuit with fresh blood) has been advocated [6]. Both modified ultrafiltration and cell separation have been reported to be useful methods of blood conservation in children, although there is a potential for reheparinization [30]. Comparison of efficacy of the two techniques was problematic because modified ultrafiltration was reserved by surgical protocol for infants.

Like others [26], we have found blood product utilization data of value in modifying our clinical practice. Stratification of donor exposure by age groups has also helped parents understand the likelihood of their child requiring a perioperative blood product transfusion.

The reexploration rate (5%) was within the reported range for adults [2]. In this study, young children were found at increased risk of reexploration for excessive bleeding. This population was also the age group most likely to die after operation. Hemostasis after cardiac operations remains problematic [9], but any reduction in blood loss may help stabilize the clinical status of these critically ill children and contribute to improved survival.

In summary, this study in children after open heart operations demonstrated that hemorrhage and volume (per kilogram of body weight) of administered blood products were inversely related to age and size. Infants 1 month of age or less were at the greatest risk for blood loss and donor exposure, and they received a median of 8 units of blood products during a 3-day perioperative period. Several factors that may contribute to increased blood loss were found to be age associated; these included preoperative clinical status and drug therapy, results of coagulation tests before and during CPB, CPB duration and technique, and complexity of operation. Infants were more likely to require reexploration for bleeding. Knowledge of the association between patient age and blood loss can facilitate appropriate allocation of blood bank resources and blood conservation techniques.

	Acknowledgments

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We thank Mary Kay Nespeca, RN, Nancy Nielsen, RN, and Patsy Thomas, RN, for their assistance with data collection and Jeff Morray, MD, and Anne Lynn, MD, for reviewing the manuscript.

	References

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Williams, G. D. Articles by Ramamoorthy, C. Search for Related Content PubMed PubMed Citation Articles by Williams, G. D. Articles by Ramamoorthy, C.