Referrals for abnormal coagulation profiles are common
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- Walter Grant Robbins
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1 A Practical Approach to Pediatric Patients Referred With an Abnormal Coagulation Profile Monica Acosta, MD; Rachel Edwards, BS; E. Ian Jaffe, MD; Donald L. Yee, MD; Donald H. Mahoney, MD; Jun Teruya, MD, DSc Context. Workup for prolonged prothrombin time (PT) and activated partial thromboplastin time (PTT) is a frequent referral to a Hematology and Coagulation Laboratory. Although the workup should be performed in a timely and cost-effective manner, the complete laboratory assessment of the coagulation state has not been standardized. Objective. To determine which clinical and laboratory data are most predictive of a coagulopathy and to formulate the most efficient strategy to reach a diagnosis in patients referred for abnormal coagulation profiles. Design. Retrospective case review. Medical records of 251 patients referred for prolonged PT and/or PTT to our Hematology Service between June 1995 and December 2002 were reviewed. Results. The study included 135 males and 116 females with a mean age of 7.0 years. A personal history of bleeding was reported in 137 patients, and a family history of bleeding was reported in 116 patients. Fifty-one patients (20%) had a coagulopathy (ie, a bleeding risk). Factors predictive of a bleeding risk were a positive family history of bleeding (P.001) and a positive personal history of bleeding (P.001). Of 170 patients with findings of normal PT and PTT values on repeat testing, 14 were subsequently diagnosed with a coagulopathy. Two of these patients reported no positive personal or family history of bleeding. Conclusions. Coagulopathy was identified in 20% of the children referred for abnormal PT and/or PTT. In the absence of a personal or family history of bleeding, a normal PT and/or PTT on repeat testing has a negative predictive value of more than 95%. (Arch Pathol Lab Med. 2005;129: ) Referrals for abnormal coagulation profiles are common challenges for pediatric hematology/oncology sections. Prothrombin time (PT) and activated partial thromboplastin time (PTT) are commonly used screening tests to assess hemostasis. 1 Patients may present with little or no significant personal or family history of bleeding. Initial screening coagulation studies may have been performed at inopportune times or with preanalytic process problems. During these studies, patients may not be at baseline health conditions 2 ; furthermore, different storage conditions may alter the reproducibility of PT and PTT. 3 The Clinical and Laboratory Standards Institute (formerly NCCLS) guidelines should be followed on the collection of blood specimens for coagulation testing: the allowable time interval between obtaining the specimen and performing the test is 24 hours for PT and 4 hours for PTT, and the ratio in the collecting tube for whole blood citrate Accepted for publication April 1, From the Department of Pediatrics, Cancer Center & Hematology Service (Drs Acosta, Yee, Mahoney, and Teruya), and the Department of Pathology (Drs Acosta, Jaffe, and Teruya and Ms Edwards), Texas Children s Hospital, and the Department of Medicine, Thrombosis Research Section (Dr Teruya), Baylor College of Medicine, Houston, Tex. The authors have no relevant financial interest in the products or companies described in this article. Portions of this work were presented at the American Society of Pediatric Hematology/Oncology annual meeting, Seattle, Wash, May Reprints: Jun Teruya, MD, DSc, Texas Children s Hospital, MC , Baylor College of Medicine, 6621 Fannin St, Houston, TX ( jteruya@bcm.tmc.edu). should be 9:1. 4 On referral, authorization for confirmatory assays may be blocked or delayed by health maintenance organizations/managed care organizations. 5 There are 3 types of referrals: patients with recurrent and persistent bleeding symptoms only, patients with prolonged PT and/or PTT with bleeding symptoms, and patients with an incidental finding of prolonged PT and/or PTT. The third type is typically seen before elective surgery. 6 Commonly reported bleeding symptoms include epistaxis, menorrhagia, easy bruising, gum bleeding, and bleeding from the gastrointestinal tract. In some reviews, approximately 30% of the patients with frequent epistaxis 7 and 10% of the patients with menorrhagia 8 have a coagulopathy. To assess if the patient has a hereditary bleeding tendency, an accurate yet concise personal and family history of bleeding must be obtained. Occasionally, patients may require repeated and additional tests to resolve the diagnosis. Workup for prolonged PT and/or PTT may include mixing studies, individual factor assays, von Willebrand factor assay, lupus anticoagulant assay, and special tests such as prekallikrein and high-molecular-weight kininogen. Performing the most efficient and cost-effective evaluation of a patient with a prolonged PT and/or PTT is a challenge for hematologists and clinical pathologists. The objective of this retrospective review was to determine the characteristics of children referred with abnormal coagulation profiles, to assess which clinical and laboratory data best predict a coagulopathy, and to formulate the most efficient strategy to reach a diagnosis. Arch Pathol Lab Med Vol 129, August 2005 Pediatric Patients With Coagulopathy Acosta et al 1011
2 MATERIALS AND METHODS Patients We retrospectively reviewed the medical records of 251 consecutive patients referred for evaluation of a prolonged PT, prolonged PTT, or prolonged PT and PTT to the outpatient clinic of the Hematology Service between June 1995 and December 2002 for a coagulation problem. Patients were initially identified from the database by obtaining a list of all consecutive patients coded for rule out coagulopathy. Coagulopathy is defined as a disease affecting the coagulability of the blood and, specifically, causing a bleeding tendency. Therefore, we did not include lupus anticoagulant and factor XII deficiencies, which are not risk factors for bleeding. A random number was given to each medical record for statistical analysis. Patients with thrombocytopenia were excluded. The following data were collected from each patient s medical record when available: age, sex, race, and the indication for performing coagulation tests during a previous evaluation, which led to patient referral to our institution. In addition, we recorded personal bleeding information, with site specification, duration, and frequency of bleeding symptoms reported in the chart, family history of bleeding in first- and second-generation family members, personal history of surgery, and any findings of abnormal bleeding during or following surgery. Observations of bleeding during or after surgery were considered abnormal if bleeding lasted longer than expected for a specific surgery or if the patient unexpectedly required a red blood cell transfusion during or after a surgery. We reviewed all laboratory test results ordered at our institution relevant to an evaluation for coagulopathy, including PT (reference range, seconds); PTT (reference range, seconds); complete blood count with platelets; fibrinogen (reference range, g/dl [ mol/l]); von Willebrand panel, including factor VIII (reference range, U/mL); von Willebrand factor antigen (reference range, U/mL); Ristocetin cofactor activity (reference range, U/mL); von Willebrand multimer analysis; other individual coagulation factors (reference ranges, U/mL); and lupus anticoagulant panel, including a dilute Russell viper venom test screen and confirmatory ratio (reference value, 1.25) and a hexagonalphase phospholipid neutralization test (reference value, 8.0 seconds). All factor assays were performed with a 1-stage clotting assay method using factor-deficient plasma. The specific coagulation profile initially recommended for each patient varied according to presenting bleeding history and outside laboratory results. The Institutional Review Board at Baylor College of Medicine approved this study protocol, H13910, with an exemption for informed consent, as all patient data were masked for these analyses. Statistical Analysis A 2 test, t test, or Fisher exact test was used to assess the individual effect of factors such as a personal history of bleeding, family history of bleeding, history of abnormal intra- or postoperative bleeding, and abnormal PT/PTT on the final diagnosis of a coagulopathy. Logistic regression analysis was used to simultaneously assess the effect of a personal history of bleeding, family history of bleeding, and the interactions among these factors on the probability of a diagnosis of coagulopathy. RESULTS Demographic characteristics are shown in Table 1. The mean age was 7.0 years, with a range from 0.01 to 17 years. There was a slight predominance of boys over girls, with a ratio of 1.16:1. A total of 137 patients (55%) were referred after experiencing bleeding symptoms with subsequent prolonged PT and/or PTT on previous evaluation. Of 251 patients, 114 (45%) had an abnormal coagulation profile on routine preoperative coagulation screening Table 1. Characteristics of the Patients* Mean age (range), y 7.0 ( ) Sex Female Male Race White Hispanic African American Asian Native American Undetermined Coagulation profiles at referral Prolonged PTT Prolonged PT 116 (54) 135 (46) 91 (36) 59 (24) 30 (12) 5 (2) 1 (0.4) 65 (26) 180 (72) 42 (17) Both prolonged PT and prolonged PTT 29 (11) Personal history of bleeding Family history of bleeding History of surgery Abnormal bleeding during surgery 114 (45) 137 (55) 135 (54) 116 (46) 143 (57) 108 (43) 108 (94) 7 (6) * Values are number (percent), unless otherwise indicated. PT indicates prothrombin time; PTT, activated partial thromboplastin time. tests. Tonsillectomy and adenoidectomy were the most frequent surgeries planned in these patients. Three patients were referred for an isolated positive family history of bleeding, and 1 patient was referred for abnormal coagulation test results in a family member. A prolonged PTT was the most frequent laboratory observation, leading to a referral in 180 patients (72%), followed by a prolonged PT in 42 patients (17%) and both a prolonged PT and a prolonged PTT in 29 patients (12%). Among patients with personal histories of bleeding, 50 (40%) had isolated epistaxis, and 30 (22%) had bruising, which were the most commonly reported symptoms (Figure 1). A positive family history of bleeding was reported in 116 patients (46%). A positive history of abnormal bleeding during surgery was found in only 7 (6%) of 108 patients who reported having previous surgery. On initial evaluation at our institution, PT and PTT were performed in all patients, and hemoglobin values were recorded in 213 of 251 patients (85%). Abnormal PT, PTT, or both were confirmed in 74 patients (29%), and both normal PT and normal PTT values were found in 177 (71%) patients. A total of 180 (72%) of 251 patients were eventually discharged from our clinic with no evidence of a primary coagulopathy. This group of patients without a coagulopathy included 3 persons with factor XII deficiency (1.2%) and 6 persons with positive lupus anticoagulant (2.4%). A specific diagnosis of a coagulopathy was eventually made in 51 patients (20%) (Table 2). A personal history of bleeding, family history of bleeding, and history of surgical bleeding were compared in patients with and without a coagulopathy (Table 3, A). The 2 most significant historical factors associated with coag Arch Pathol Lab Med Vol 129, August 2005 Pediatric Patients With Coagulopathy Acosta et al
3 Figure 1. Bleeding symptoms of patients with a positive personal history of bleeding (N 251). * Percentage of females aged 11 or older who have menorrhagia (5/14). Table 2. Hemophilia A Factor VII deficiency von Willebrand disease Factor XI deficiency Hemphilia B Factor X deficiency Factor V deficiency Dysfibrinogenemia Total Final Diagnosis of Patients With a Coagulopathy* Diagnosis No. (%) 15 (29.4) 12 (23.5) 11 (21.6) 6 (11.8) 4 (7.8) 1 (2.0) 1 (2.0) 1 (2.0) 51 (100.0) * This category of coagulopathy does not include 3 cases of factor XII deficiency and 6 cases of lupus anticoagulant. It is not known if it is congenital deficiency or acquired isolated deficiency. ulopathy were a positive family history of bleeding (P.001) and a positive history of abnormal surgical bleeding (P.001). A positive personal history of bleeding was also associated with a final diagnosis of a coagulopathy (P.001). The patients with a coagulopathy had a lower hemoglobin level than the patients without a coagulopathy (P.001). Children with a coagulopathy had a longer mean PT and PTT than did those without a coagulopathy, 13.3 seconds versus 12.5 seconds (P.001) and 39.4 seconds versus 30.5 seconds (P.001), respectively (Table 3, B). A confirmatory PTT value greater than 35.0 seconds or a PT value greater than 14.5 seconds was associated with a coagulopathy (P.001). Patients with and without a coagulopathy showed no difference in the platelet counts, although thromocytopenic patients had been excluded from the study. A simultaneous assessment of the effects of personal and family history of bleeding on the final diagnosis of a coagulopathy in all patients indicated that a family history of bleeding was a significant independent predictor of coagulopathy (P.001). The odds ratio of having a diagnosed coagulopathy was 4.4 (95% confidence interval, , P.001) with a positive family history of bleeding. On the other hand, the odds ratio of persons with a positive personal history to have a coagulopathy was 3.0 (95% confidence interval, , P.002). Of note, all 19 patients with hemophilia A or B had a positive Table 3. Final Diagnosis of Coagulopathy or No Coagulopathy Clinical Features A. Bleeding History No Coagulopathy, n 180, No. (%) Coagulopathy, n 51, No. (%) P Value personal bleeding history 85 (47.2) 37 (72.5).001 family bleeding history 72 (40.0) 38 (74.5).001 History of abnormal surgical bleeding 1 (0.6) 5 (9.8).001 B. Laboratory Data Laboratory Values* No Coagulopathy Coagulopathy P Value Hemoglobin, g/dl 12.6 (n 150) 12.0 (n 46).001 PT, s 12.5 (n 177) 13.3 (n 47).001 PTT, s 30.5 (n 179) 39.4 (n 50).001 * Reference range: PT, seconds; PTT, seconds. PT indicates prothrombin time; PTT, activated partial thromboplastin time. Arch Pathol Lab Med Vol 129, August 2005 Pediatric Patients With Coagulopathy Acosta et al 1013
4 Table 4. Final Diagnosis of Coagulopathy or No Coagulopathy With Bleeding History in Patients With Normal Prothrombin Time/Activated Partial Thromboplastin Time (n 177) Family History Family History Personal Personal Personal Personal Coagulopathy 2 (3.4)* 1 (2.4) 5 (16.7) 6 (15.0) 14 No coagulopathy 56 (96.6) 41 (97.6) 25 (83.3) 34 (85.0) 156 No final diagnosis 0 (0) 2 (4.5) 1 (3.2) 4 (9.1) 7 Total * Two patients had type 1 von Willebrand disease. One patient had heterozygous factor VII deficiency. Three patients had low factor VII, and 2 patients had type 1 von Willebrand disease. Two patients had von Willebrand disease, 2 patients had factor XI deficiency, 1 patient had mild hemophilia A, and 1 patient had mild hemophila B. Total personal history of bleeding, but 4 patients (2 mild and 2 severe) had no family history of bleeding. Among the group of 177 patients with normal PT and normal PTT values, 14 were eventually diagnosed with a coagulopathy (Table 4). Von Willebrand disease was the most frequent diagnosis (6 patients), followed by heterozygous factor VII deficiency (4 patients), heterozygous factor XI deficiency (2 patients), mild hemophilia B (1 patient), and mild hemophilia A (1 patient). Seven of those 14 patients had a positive personal history of bleeding, and 11 had a positive family history of bleeding. Only 2 of the 14 patients with a diagnosed coagulopathy and normal values for PT and PTT had no positive personal or family history of bleeding. COMMENT This study presents some limitations, since it is a retrospective review of medical records. Although the information about the personal and family histories of bleeding was recorded in the chart, the data were not obtained with a standard questionnaire, and we were unable to retrieve any missing information. Additionally, this institution is a tertiary care hospital, and the high number of patients diagnosed with factor deficiencies does not reflect the prevalence of coagulopathy in the general population. Our retrospective analysis shows that among 251 patients referred for prolonged PT and/or PTT, 51 children (20%) had a coagulopathy. The same proportion of patients with coagulopathies has been diagnosed in other studies of bleeding symptoms. 7 The high prevalence of coagulopathies can be attributed to the fact that our institution is a tertiary care hospital to which patients are referred from different places. The most common coagulopathy diagnosed was hemophilia A. The severity of the disease and family history may influence the age of diagnosis in hemophilia, and a great disparity in the median age at diagnosis according to severity has been described. 9 Low factor VII level ( 0.50 U/mL) was the second most common coagulopathy and was more common than von Willebrand disease. The number of patients with low factor VII was unexpectedly high; however, this was a retrospective review, and the nature of the deficiency (ie, congenital or transient) could not be effectively addressed. Low factor VII can be accounted for by chronic mild vitamin K deficiency, which is not unusual and is underdiagnosed among patients with cerebral palsy. 10 A positive family history of bleeding and a positive surgical history of abnormal bleeding were the 2 most important historical factors associated with the presence of a coagulopathy. A prolonged PT, PTT, or both on repeated evaluation were useful laboratory variables in predicting a coagulopathy. A total of 36 patients (49%) with repeat abnormal PT and/or PTT had a coagulopathy. We found that a PT and PTT in the reference range on repeat testing appeared to have a negative predictive value of more than 95% in patients without a personal or family history of bleeding. A total of 56 of 58 patients with a normal PT and a normal PTT on repeat testing and no personal or family history of bleeding had no evidence of coagulopathy (Table 4). The 2 exceptions were 1 patient with type 1 von Willebrand disease and 1 patient with an unknown type of von Willebrand disease. It is already well known that changes in PTT value may be observed in von Willebrand disease because of the fluctuation of the von Willebrand factor in response to stress, similar to other acutephase reactants. 11,12 The finding of a normal PT and a normal PTT in the presence of a coagulopathy can be secondary to a lower factor sensitivity of the PT and/or PTT reagents used at the time of the evaluation. Mild deficiencies of factor VIII, IX, and XI can occur with a normal PTT; specific assays may therefore be required. 13 A factor VIII as low as 0.13 U/mL as well as a factor X of 0.03 U/mL with a normal PTT have been described. 14 The only patient with a normal PT and a normal PTT with a positive personal but a negative family history of bleeding who had a coagulopathy had a low factor VII level of 0.35 U/mL. With the current PT reagents, a prolonged PT value in this patient would be expected, as the use of more sensitive reagents increased the diagnosis of mild coagulopathies. 15 Proposed Strategy for Prolonged PT and/or PTT Workup in the Pediatric Setting Children with an abnormal coagulation profile are frequently referred to pediatric hematology clinics. The strategy of workup for a prolonged PT and/or PTT in children is not the same as in adult patients because the quantity of the specimen is usually limited, and the prevalence of the lupus anticoagulant among children is lower than in adults. 16,17 As stated earlier, however, patients may or may not be old enough to have a bleeding history. In addition, it is not uncommon to see patients with both lupus anticoagulant and factor deficiency at the same time. Since many variables exist among patients, depending on the purpose of the prolonged PT/PTT workup, such as presurgical assessment or an abnormal PT or PTT without any signifi Arch Pathol Lab Med Vol 129, August 2005 Pediatric Patients With Coagulopathy Acosta et al
5 Figure 2. Request for prolonged prothrombin time/activated partial thromboplastin time (PT/PTT) consultation form. cant symptoms, reflex testing policy cannot uniformly apply. If the repeat PT and PTT values are normal and the patient is not anemic and has no personal or family history of bleeding, no further workup is required; however, in the presence of a positive personal or family history of bleeding, the case should be further evaluated. An additional workup may be required, since some mild coagulopathies exist that may not prolong PT and PTT. 14 If the repeat PTT is prolonged and the specimen was collected through a venous access device, there is a possibility of heparin contamination. Heparin should subsequently be removed from the specimen. This step, however, is not necessary for most PT reagents, since they contain a heparin inhibitor. If the patient has bleeding symptoms, factor assays should be performed regardless of the mixing study results. A mixing study for PTT is performed at our institution only if PTT is prolonged for more than 3 seconds above the reference range. A mixing study is a screening test for a circulating inhibitor. 18 However, its utility is limited as a guide for the performance of individual factor assays or lupus anticoagulant assays. A PT mixing study has very limited utility, as factor VII inhibitor is extremely rare. If the PT is prolonged due to a lupus anticoagulant or a factor II, V, or X inhibitor, the PTT is also usually prolonged. On the other hand, if the PT is prolonged within 2.0 seconds above the reference range and the patient does not have significant bleeding symptoms or will not have any invasive procedure, we recommend that the performed PT be repeated in 3 months. If the PT is prolonged 2.0 seconds or longer and/or the patient requires surgery, extrinsic factor assay testing, which includes factors VII, X, V, and II and fibrinogen, should be performed. It is known that PTT is less sensitive to the deficiency of common pathway factors than PT. 14 Since prolonged PT and/ or PTT is a frequent indication for referral for pediatric patients, no uniform algorithm may apply to all the cases; therefore, we have implemented a prolonged PT/PTT consultation using a specific request form (Figure 2). Clinicians send specimens for coagulation testing, and laboratory assays start with PT and PTT. If both assays are within the reference range, no further workup is performed unless the patient has bleeding symptoms or a positive family history of bleeding. If the patient has bleeding symptoms, a von Willebrand panel will be performed. If a further workup is indicated, a quantitative factor XIII assay, an 2 -antiplasmin assay, a thromboelastography, and a platelet function analysis using a PFA-100 or whole blood aggregation study will be performed. Using this strategy, we have found many advantages for patients, clinicians, and the laboratory. Patients do not need to return for additional laboratory testing on the basis of the results. Additionally, appropriate tests are prioritized in the laboratories in instances in which a limited amount of specimen is present. We gratefully acknowledge the assistance of E. O Brien Smith, PhD, in the statistical analysis of this work and Jorge Karam, MD, for his technical assistance. References 1. Lusher JM. Screening and diagnosis of coagulation disorders. Am J Obstet Gynecol. 1996;175: Plebani M, Carraro P. Mistakes in a stat laboratory: types and frequency. Clin Chem. 1997;43: Rao LV, Okorodudu AO, Petersen JR, et al. Stability of prothrombin time and activated partial thromboplastin time tests under different storage conditions. Clin Chim Acta. 2000;300: Clinical and Laboratory Standards Institute (formerly NCCLS). Collection, Transport, and Processing of Blood Specimens for Coagulation Testing and General Performance of Coagulation Assays. 3rd ed. Wayne, Pa: NCCLS; Approved guideline H21-A2. 5. Mahoney DH, Steuber CP, Hurwitz R, et al. Impact of managed care practices on the evaluation of children with suspected bleeding disorders. J Pediatr Hematol Oncol. 1999;21: Patel RI, DeWitt L, Hannallah RS. Preoperative laboratory testing in children undergoing elective surgery: analysis of current practice. J Clin Anesth. 1997;9: Sandoval C, Dong S, Visintainer P, et al. Clinical and laboratory features of 178 children with recurrent epistaxis. J Pediatr Hematol Oncol. 2002;24: Arch Pathol Lab Med Vol 129, August 2005 Pediatric Patients With Coagulopathy Acosta et al 1015
6 8. Dilley A, Drews C, Miller C, et al. Von Willebrand disease and other inherited bleeding disorders in women with diagnosed menorrhagia. Obstet Gynecol. 2001;97: Chambost H, Gaboulaund V, Coatmelec B, et al. What factors influence the age of diagnosis of hemophilia? Results of the French hemophilia cohort. J Pediatr. 2002;141: Krashinki SD, Russell RM, Furie BC, et al. The prevalence of vitamin K deficiency in chronic gastrointestinal disorders. Am J Clin Nutr. 1985;41: Pottinger BE, Read RC, Paleolog EM, et al. Von Willebrand factor is an acute phase reactant in man. Thromb Res. 1989;53: Nichols WC, Ginsburg D. von Willebrand disease. Medicine. 1997;76: Sham RL, Francis CW. Evaluation of mild bleeding disorders and easy bruising. Blood Rev. 1994;8: Teruya J, Oropeza M, Ramsey G. A normal aptt does not guarantee adequate coagulation factor levels. Anesthesiology. 2001;94: Wojtkowski TA, Rutledge JC, Matthews DC. The clinical impact of increased sensitivity PT and APTT coagulation assays. Am J Clin Pathol. 1999;112: Male C, Lechner K, Eichinger S, et al. Clinical significance of lupus anticoagulants in children. J Pediatr. 1999;134: Shi W, Krilis SA, Chong BH, et al. Prevalence of lupus anticoagulant and anticardiolipin antibodies in a healthy population. Aust N Z J Med. 1990;20: Taylor LJ. Laboratory management of the bleeding patient. Clin Lab Sci. 2003;16: Arch Pathol Lab Med Vol 129, August 2005 Pediatric Patients With Coagulopathy Acosta et al
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