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Fibrinolytic System in Adolescents: Response to Venous Occlusion Stress Tests

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Fibrinolytic System in Adolescents: Response to Venous Occlusion Stress Tests 0031-3998/03/5302-0333 PEDIATRIC RESEARCH Vol. 53, No. 2, 2003 Copyright © 2003 International Pediatric Research Foundation, Inc. Printed in U.S.A. Fibrinolytic System in Adolescents: Response to Venous Occlusion Stress Tests PAUL MONAGLE, ANTHONY K.C. CHAN, MANUELA ALBISETTI, PATRICIA VEGH, MAUREEN ANDREW, AND LESLEY MITCHELL Division of Laboratory Services, Royal Children’s Hospital, Department of Paediatrics, University of Melbourne, Melbourne Australia [P.M.]; Hamilton Civic Hospitals Research Center, Hamilton, Ontario, Canada [A.K.C.C., M.Al., P.V.]; Population Health Sciences, Hospital for Sick Children, Toronto, Canada [M.An., L.M.] ABSTRACT Recent studies indicate that the incidence of thromboembolic increased plasminogen activator inhibitor-1 activity levels after events is increasing as a secondary complication in children with venous occlusion, resulting in significantly prolonged euglobulin serious underlying diseases. The mechanism to eliminate these lysis times. The results of our study confirm developmental thrombi via the thrombolytic system in children is unknown. The differences in the fibrinolytic response to venous occlusion stress baseline fibrinolytic system is age dependent, with significant testing. The age-related differences in fibrinolytic response to variation between children and adults. Adult studies would sug- venous occlusion of younger children and the significance of gest that the fibrinolytic response to venous occlusion has more these differences on the pathophysiology of thromboembolic clinical relevance than the baseline fibrinolytic system. The aim events in children require further studies. (Pediatr Res 53: of this study was to determine whether the fibrinolytic response 333–337, 2003) to venous occlusion stress testing in healthy adolescents differs from the response in healthy adults. Healthy adolescents (13–18 Abbreviations y) from a school population and normal adults were recruited. TE, thromboembolic events Pre- and postvenous occlusion blood samples were collected tPA, tissue plasminogen activator using standard techniques. Plasma tissue plasminogen activator, PAI, plasminogen activator inhibitor ␣ ␣ ␣ plasminogen activator inhibitor-1, plasminogen, 2-antiplasmin, 2-AP, 2-antiplasmin ␣ ␣ ␣ 2-macroglubulin, D-dimers, euglobulin lysis time, and fibrino- 2-M, 2-macroglobulin gen were measured on each sample. Adolescents had signifi- ELT, euglobulin clot lysis time cantly decreased tissue plasminogen activator antigen levels and CI, confidence interval Thromboembolic events occur relatively rarely during child- wall in the young and the role that these physiologic differ- hood, even in the presence of acquired or congenital risk ences may have in protecting children from TE. These studies factors (1, 2). In contrast, TE occur in approximately 5% of the have shown that there is a decreased capacity to generate adult population, and may be idiopathic, or secondary to thrombin, a key enzyme in coagulation, enhanced regulation of ␣ congenital or acquired disorders. The profound difference in thrombin by inhibitors such as 2-M, a circulating anticoagu- incidence of TE in children suggests that there are protective lant with antithrombin activity at birth, and increased amounts mechanisms in place in the young. Recent studies have focused of proteoglycans with antithrombin activity in the vessel wall on physiologic differences in the coagulation system and vessel of the young (3–6). Although extensive information on the coagulation system in the young is available, specifically on the regulation of Received June 18, 2001; accepted September 26, 2002. Correspondence: Lesley Mitchell, The Hospital for Sick Children, Population Health thrombin, there is little information on the fibrinolytic system Sciences, 555 University Avenue, Toronto, ON, M5G 1X8, Canada; e-mail: and its potential role in preventing TE during childhood. At [email protected] birth, all components of the fibrinolytic system are present but Supported by a grant from the Heart and Stroke Foundation of Canada. P.M. is supported by a research fellowship from the Murdoch Children’s Research Institute. with differing plasma concentrations of key components, and A.K.C.C. is supported by a fellowship from the Heart and Stroke Research Foundation of evidence of significant, transient activation (7). Throughout Canada. M.A. is a Career Investigator for the Heart and Stroke Foundation of Canada. childhood, the ratio of tPA to PAI-1 is reversed compared with L.M. is a research scholar of the Canadian Institutes of Health Research. M.Al. is the recipient of a Stipendium zur Foerderung des Akademischen Nachwuchses of the Uni- adults, suggesting that the fibrinolytic system may be relatively versity of Zurich, Switzerland. suppressed and may not provide increased protection from TE DOI: 10.1203/01.PDR.0000047644.97422.F2 in the young (1). 333 334 MONAGLE ET AL. Although the incidence of TE in children is reduced com- hematocrit after occlusion, and Bd ϭ 0.9 when blood and pared with adults, recent population-based studies in Canadian anticoagulant are mixed in a ratio of 9:1 (8). children have shown that the incidence of TE is increasing as a secondary complication in children with serious underlying Assays diseases such as cancer and congenital heart disease (2). Per- sistent thrombi result in obstruction of the venous system with The following assays were performed on all pre- and the associated risk of recurrent TE and postphlebitic syndrome. postvenous occlusion samples: tPA antigen (Imubind, tPA, To date, there is no information in the literature on the devel- American Diagnostica); tPA activity (Spectrolyse tPA/PAI, opmental differences in the overall fibrinolytic capacity of American Diagnostica); PAI-1 antigen (Imubind, PAI-1, children using tests sensitive to in vivo responses such as American Diagnostica); PAI-1 activity (Spectrolyse PAI, venous occlusion. Therefore, the objective of the current study American Diagnostica); plasminogen antigen (ELISA: Imu- was assess the in vivo response of the fibrinolytic system to clone, American Diagnostica); plasminogen activity (Ac- ␣ venous occlusion in healthy adolescents. Adolescents are a tichrome PLG, American Diagnostica), and 2-AP activity particularly relevant population to assess as they are the second (Actichrome American Diagnostica) using an Automated Co- ␣ most common age group in which TE occur in pediatric agulation Laboratory (ACL, Milan, Italy); 2-M antigen by patients (2). radial immunodiffusion using commercially available antibody (Cedarlane Laboratories Limited, Hornby, Ontario, Canada); D-dimer (Dimertest Gold EIA, American Diagnostica); ELT METHODS [modified from Bucknell (9)]; and fibrinogen (functional) by semiautomated Clauss method (ST4, Diagnostica Stago, Study Population Asnières, France). Hematocrits were measured on a Coulter Healthy adolescents on no medications (including the oral STK-S (Coulter Canada, Burlington, ON, Canada). The D- contraceptive pill) between 13 and 18 y of age attending a dimer assay was chosen over fibrinogen degradation products school in Oakville, Ontario, Canada, were approached to par- (FDP) as D-dimers are specific to plasmin degradation of ticipate in the study. Informed consent was obtained from both cross-linked fibrin only, whereas FDP detect plasmin proteol- the adolescents and their parents before participation. Healthy ysis of either fibrinogen or fibrin (10). adults aged 20–50 y on no medications (including the oral tPA/PAI-1 ratios. The ratio represents a measure of the contraceptive pill) were used as controls. The study was ap- fibrinolytic capacity in patients by assessing the relative rela- proved by the ethics review board at Chedoke McMaster tionship of plasma levels of tPA to plasma levels of tPA’s main University, Hamilton, Ontario, Canada. inhibitor, PAI-1. An increased ratio (i.e. increased tPA and/or decreased PAI-1) would be characterized as a hyper fibrino- lytic state. The converse, a decreased ratio (i.e. decreased/ Sample Collection normal tPA and increased PAI-1), would be characterized as a Subjects and controls fasted from 0000 h before the morning hypofibrinolytic state. The tPA/PAI-1 ratios were calculated of testing. All blood collections were performed between 0800 using the antigen levels for both proteins. and 1000 h. On arrival, patients had local anesthetic cream applied to both antecubital fossae. After 15 min resting supine, Statistical Analysis pre-stress test samples were collected via a single, clean veni- The mean values for pre- and postocclusion results with 95% puncture from the antecubital fossa of a non-occluded arm. CI were calculated for each variable. Preocclusion and postoc- Ͻ Tourniquet use was avoided or kept to a minimum ( 1 min). clusion were compared for adult controls and adolescents using Ten milliliters of blood were collected into 3.2% sodium citrate t test. Between-gender differences were assessed using one- (nine parts blood: one part citrate) for tPA antigenic assay, way ANOVA with posthoc comparisons. p Values Ͻ 0.05 ␣ PAI-1 functional and antigenic assays, plasminogen, 2-AP, were considered statistically significant. ␣ 2-M, D-dimer, ELT, and fibrinogen. A further sample was collected into acidified sodium citrate tubes (pH 4.3) (Stabilyte RESULTS tubes, American Diagnostica, Greenwich, CT, U.S.A.) for tPA functional assays, and 0.5 mL into EDTA for hematocrit Samples were collected from 15 adolescent girls, mean age determination. A blood pressure cuff appropriate to the size of
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