Clinical Chemistry 47: 1204-1211, 2001;
(Clinical Chemistry. 2001;47:1204-1211.)
© 2001 American Association for Clinical Chemistry, Inc.
Discontinuation of the Bleeding Time Test without Detectable Adverse Clinical Impact
Christopher M. Lehman1,3a,
Robert C. Blaylock1,3,
Donald P. Alexander4 and
George M. Rodgers1,2,3
1
Department of Pathology, Division of Clinical Pathology,
2
Department of Medicine, Division of Hematology, and
4
Department of Pharmacy Services, University of Utah Health Sciences Center, Salt Lake City, UT 84132.
3
ARUP Laboratories, Inc., 500 Chipeta Way, Salt Lake City, UT 84108
aAddress correspondence to this author at: Department of Pathology, University of Utah Health Sciences Center, 5C124 SOM, 50 N. Medical Drive, Salt Lake City, UT 84132. Fax 801-585-6666; e-mail lehmanc{at}arup-lab.com
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Abstract
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Background: The bleeding time (BT) test predicts a higher bleeding complication rate in populations at risk for inherited or acquired platelet dysfunction, but it is of limited assistance in evaluating individual patients. There are no reports of clinical outcomes after discontinuation of the BT test.
Methods: Interviews with a subset of the physicians who had ordered the BT test before discontinuation of the test were conducted. The total number of platelet-aggregation tests, the mean number of monthly, unmodified platelet units transfused, the incidence of kidney biopsy complications, and the number of doses of 1-deamino-8-D-arginine vasopressin (DDAVP) administered 5 months before and after discontinuation of the BT test were compared. We recorded the rates of bleeding complications in the Major Surgery Risk Pool during the 12 months before and the 5 months after the discontinuation of the BT test.
Results: Clinicians reported they did not significantly change their preprocedural work-ups, postpone an invasive procedure, experience an increase in bleeding complications, or increase their use of blood products after discontinuation of the BT test. Platelet-aggregation tests (n = 9, before and after), platelet transfusions (P = 0.958), and DDAVP administration (before = 24; after = 10) did not increase after discontinuation of the BT test. The rate of postprocedural bleeding complications did not increase significantly in either Major Surgery Risk Pool cases (<3
deviation from the mean rate) or in patients undergoing renal biopsies (P = 0.225 for decrease in hematocrit; P = 1.000 for the percentage of patients transfused) after discontinuation of the BT test.
Conclusions: Our study failed to identify a clinically significant, negative impact of discontinuing the BT test.
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Introduction
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Excessive bleeding may complicate medical procedures when a patient has an acquired or inherited disorder of platelet function (1). Bleeding time (BT)
1
tests were developed in the hope that quantifying the length of time a patient bled after incising or puncturing the skin would aid in the diagnosis of platelet dysfunction disorders and would predict the risk of abnormal bleeding from internal organs during and/or after an invasive procedure (2)(3). Unfortunately, the BT test became popularized in clinical practice without sufficient peer-reviewed evidence supporting its use, probably under the assumption that an in vivo test was needed and no other test was available. By the early 1990s, sufficient data questioning the utility of the BT test as a predictor of clinical bleeding had accumulated to prompt the publication of two review articles opposing routine preoperative use of the BT test, and suggesting that the BT test might be of limited use under any circumstances (4)(5). The College of American Pathologists and the American Society of Clinical Pathologists later published a position article (6) concluding that the BT test was not effective as a screening test in patients lacking a history of excessive bleeding, including patients who had recently taken aspirin or nonsteroidal antiinflammatory agents (NSAIDs). Nonetheless, the BT test is still commonly recommended for use in assessing the risk of bleeding in patients taking drugs or herbs or suffering from inherited or acquired disorders known to adversely affect platelet function (7)(8)(9)(10)(11)(12).
In recent years, the frequency in ordering the BT test at our institution had gradually decreased to the point that its use was confined to patient populations with impending invasive procedures who were presumed to be at risk for acquired platelet function disorders. The decreased volume of testing made it difficult to train new personnel, to document continuing competency of existing personnel, and to perform proficiency testing as required by good laboratory practice and the Clinical Laboratory Improvement Act of 1988. Consequently, our Hospital Laboratory Committee, composed of diverse clinicians and administrators, reevaluated the efficacy of the BT test in contemporary clinical practice and decided to discontinue offering the test to our clinicians. Although other institutions have reportedly limited or eliminated the BT test (13)(14), we are unaware of any reports of clinical outcomes after discontinuation of the test. This report summarizes our experiences after removal of the BT test from the repertoire of clinical laboratory tests at a busy, tertiary care, university medical center.
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Materials and Methods
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Clinicians with admitting privileges to the Hospital were notified by mail of discontinuation of the BT test as approved by a multidisciplinary Hospital Laboratory Committee in January 1999. The memo included background information on the BT test, as well as a discussion of its limitations and citations of the literature supporting its discontinuation. An algorithm for evaluating the risk of a bleeding disorder in patients with a personal or family history of bleeding (Fig. 1
) was also included in the mailing, along with phone numbers of two physician laboratorians who were available for consultation. The University of Utah Health Sciences Center is a tertiary care center with active adult Hematology/Oncology, Nephrology, Transplant (renal, heart, heart/lung, kidney, bone marrow), Gastroenterology and Neurosurgery programs. The Newborn Intensive Care and Well Baby Units represent the only pediatric patient care units. The clinical specialties represented on the Hospital Committee at that time included Family Practice, Hematology, Pulmonary Medicine, General Surgery, Obstetrics/Gynecology, Anesthesiology, Pathology and Emergency Medicine.
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Figure 1. Algorithm for evaluating the risk of excessive bleeding in patients with a personal or family history of bleeding, which was distributed to clinicians before discontinuation of the BT test.
PT, prothrombin time; PTT, partial thromboplastin time.
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Indications for platelet transfusions administered to patients with normal platelet counts in the first 4.5 months after discontinuation of the BT test were determined by reviewing patient medical records. The mean number of nonirradiated, nonleukocyte-reduced apheresis and pooled platelet units transfused during the 5 months (February 1999 through June 1999) after discontinuation of the BT test was compared with the mean number transfused in the 5 months immediately before discontinuation of the BT test and with the mean number transfused during the same 5-month interval of the preceding year (February 1998 through June 1998), using the Student t-test (SPSS 9.0.1; SPSS). The unmodified platelet products were chosen for analysis because they would be used for nonimmunosuppressed patients, the primary patient population to undergo BT testing at our institution. The number of platelet-aggregation tests ordered by clinicians during the same 5-month intervals described above were also compared. To assess the potential effect of discontinuation of the BT test on surgical procedures, the summary statistics for the overall rate of postprocedural hemorrhage or hematoma in patients in the Major Surgery Risk Pool (University HealthSystem Consortium Clinical Performance Measure 2947) for the 12 months before and the 5 months after discontinuation of the BT test were reviewed. The Major Surgery Risk Pool consists of 126 surgical procedures including gastrointestinal, cardiovascular, oncologic, transplant, urologic, orthopedic, plastic, gynecologic, and endocrine procedures. Bleeding complications are identified by reviewing bleeding-related ICD-9 codes reported in association with Major Surgery Risk Pool procedures. Complication rates are calculated as the number of patients experiencing postprocedural hemorrhage or hematoma divided by all eligible surgical patients. The monthly complication rates were compared through the use of a Shewart control chart for attributes (15). Complication rates for the 12 months before and 5 months after discontinuation of the BT test were plotted on a "fraction-defective" or "P" control chart with standard upper and lower control limits of ± 3, based on a binomial distribution (SPSS 9.0.1). Complication rates exceeding the mean rate by 3 are an indication of a process that is statistically out of control (15).
To assess the possible impact of discontinuation of the BT test on bleeding complications in a patient population known to be predisposed to abnormal platelet function and who undergo invasive diagnostic procedures, we chose to evaluate the complication rate of kidney biopsy procedures performed during the 5 months immediately before and the 5 months immediately after discontinuation of the BT test. Demographic characteristics (age, sex), the origin of the biopsied kidney (native vs allograft), and pertinent laboratory values [prebiopsy BT test, blood urea nitrogen (BUN), creatinine, hematocrit, platelet count, prothrombin time, partial thromboplastin time, and the postbiopsy hematocrit] were summarized for each 5-month interval. The percentage of patients with abnormal coagulation values (prothrombin time >15.0 s; partial thromboplastin time >40 s), an abnormally low platelet count (<140 x 109/L), or a hematocrit <0.300 (30%) was calculated. The incidence of red blood cell transfusions secondary to postbiopsy bleeding, documented by abdominal computed tomography, was also assessed for the two intervals. Continuous variables were tested with the Kolmogorov–Smirnov test to determine whether observed values came from a gaussian distribution. All variables followed a gaussian distribution except for creatinine and BUN. Mean values were compared using the two-sided Student t-test. Median values were compared using the Mann–Whitney test. Frequencies were compared using the Pearson 
2 test unless the expected value of any cell was <5, in which case the Fisher’s exact test was used. Potential correlations between variables were evaluated using the Spearman’s 
coefficient. All statistical tests were performed using SPSS 9.0.1. A probability of P <0.05 was considered statistically significant.
Use of the BT test during a 5-month period preceding discontinuation of the test was quantified and summarized by the specialty and ordering physicians. Questionnaires for surgical and nonsurgical specialists were constructed and acted as the basis for interviews with a subset of the physicians who had ordered the BT test during the 5 months before discontinuation of the BT test (Table 1
). To assess the reliability of the clinicians’ perceptions, and to assess the potential impact of a change in use of hemostatic agents after discontinuation of the BT test on bleeding complications, we reviewed the use of the drug 1-deamino-8-D-arginine vasopressin (DDAVP) during the 5 months immediately before and after discontinuation of the BT test. Administration of DDAVP represents the primary intervention taken by clinicians at our institution to counteract platelet function defects (e.g., uremia, Von Willebrand’s disease) in patients who are at risk and are scheduled to undergo invasive procedures, or who are actively bleeding. The total number of patients who received platelet-active doses of DDAVP (
0.3 µg/kg), as well as the number of DDAVP-treated patients with coincidental renal insufficiency, and the fraction of patients who received DDAVP before renal biopsy were recorded for the two 5-month intervals.
This study was conducted under a protocol approved by the University of Utah Institutional Review Board. Interviews were conducted with the written consent of the clinicians.
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Results
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The algorithm for evaluating the risk of excessive bleeding in patients with a personal or family history of bleeding is presented in Fig. 1
. Note that, in the absence of a carefully elicited bleeding history, no further work-up was recommended. The number of procedures, and the clinical services ordering them, in the 5 months before discontinuation of the BT test, are summarized in Table 2
. The primary services ordering the BT test were Nephrology, Obstetrics/Gynecology, Hematology (primarily one clinician), Pulmonary (transplant), and Neurosurgery. The predominance of subspecialty services requesting BT tests reflects a relatively conservative use of the BT test. Evaluation of platelet function in patients before kidney biopsy (n = 19), before liver biopsy (n = 10), or with a history of NSAID ingestion (n = 5) included >40% of the indications for a BT test. Before discontinuation of the BT test, only one clinician (Neurosurgery) contacted the Laboratory after the notification memo was distributed. A second clinician (Neurosurgery) contacted the Laboratory 12 months after discontinuation, asking for a BT test. In both cases, the concern was related to determining the risk for excessive bleeding in patients taking NSAIDS. These were the only inquiries regarding the BT test fielded by the Laboratory in the 24 months since discontinuation of the test.
An evaluation of the ordering frequency of platelet-aggregation tests revealed no increase during the 5 months after discontinuation of the BT test compared with either the 5-month period immediately before discontinuation or the same 5-month interval (February through June) in 1998 (Table 3
). Likewise, there was no significant difference in the number of nonirradiated, nonleukocyte-reduced platelet units transfused in the 5 months before discontinuation of the BT test vs the 5 months after, nor for the months of February through June of 1998 vs 1999 (Table 3
). A review of the indications for platelet transfusions administered to patients with platelet counts in the reference interval over the first 4.5 months after discontinuation of the BT test revealed only cardiopulmonary bypass as an indication related to a known, acquired platelet function defect. BT tests had not historically been ordered for this group of patients before discontinuation of the test. In addition, no clinicians have specifically requested a platelet transfusion to correct an acquired platelet function defect in a patient undergoing a procedure.
The rate of postprocedural hemorrhage or hematoma in patients in the Major Surgery Risk Pool has remained in statistical control (<3) in the 5 months since discontinuation of the BT test (Fig. 2
). In fact, the monthly variation in complication rates has remained within 2 of the mean. Therefore, there is no evidence that discontinuation of the BT test has led to an increase in bleeding complications. In addition, the Laboratory has not been notified of any cases of excessive bleeding in surgical patients where discontinuation of the BT test was thought to play a significant role in the clinical outcome.
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Figure 2. Rate of postprocedural hemorrhage or hematoma for patients in the Major Surgery Risk Pool for the 12 months before and 5 months after discontinuation of the BT test.
Data are plotted as a "P" control chart with standard upper and lower control limits of ± 3. The months during which the BT test was no longer available are indicated by an asterisk and by BT Discontinued on the graph. •, observed monthly rate; - - -, standard upper and lower confidence limits; ——, mean rate.
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To assess the possible impact of discontinuation of the BT test on bleeding complications in a nonsurgical patient population known to be predisposed to abnormal platelet function, and who undergo invasive diagnostic procedures, we evaluated the complication rate of kidney biopsy procedures immediately before and after discontinuation of the BT test. Demographic variables and potentially significant risk factors were compared for patients undergoing biopsy in the before and after 5-month intervals. BUN was higher in the patients biopsied after discontinuation of the BT test, but did not correlate with the decrease in the postbiopsy hematocrit (rs = 0.154; P = 0.224). On the other hand, significantly more renal allografts were biopsied after the BT test was no longer available (Table 4
); and an analysis of the mean decrease in hematocrit for allografts vs native kidneys, for all eligible patients (n = 66), revealed a significantly larger mean decrease in the hematocrit (P = 0.008) for allograft kidneys (mean ± SD = 0.96 ± 2.31; n = 31) vs native kidneys (mean ± SD = 2.68 ± 2.72; n = 35). This probably accounts for the lower mean decrease in hematocrit demonstrated by the patients biopsied after discontinuation of the BT test, although the difference did not reach statistical significance (Table 4
). There was no significant difference in the incidence of RBC transfusion after biopsy between the two time intervals (Table 4
). Three of the transfused patients were female, and three had a native kidney biopsied. In addition, three of the four patients had prebiopsy prothrombin time and/or platelet count values that were abnormal. A BT test was not performed on any of the four patients.
Because clinicians might not have actively reported bleeding complications in patients thought to have had a platelet-function disorder, 18 (35%) physicians who had ordered a BT test in the 5 months before discontinuation of the test were interviewed using the questionnaires presented in Table 1
. Of the 4 surgeons interviewed [General/Trauma, Neurosurgery (2), Ear Nose and Throat], none had changed his or her practice as a result of discontinuation of the BT test. They reported that they did not significantly change their preoperative work-ups (with the exception of elimination of the BT test), postponed a surgical procedure, experienced an increase in bleeding complications, or increased the use of blood products. However, the concern about preoperative evaluation of neurosurgical patients taking NSAIDs or aspirin was raised again.
The responses from the nonsurgical clinicians were consistent with those of the surgical faculty. They reported that they had not modified their practices or noted an increase in bleeding complications, except for one physician who would consider the use of DDAVP in lung transplant patients requiring a lung biopsy when the patient’s BUN was >16.1 mmol/L. This clinician reported one episode of excessive bleeding associated with a lung biopsy in a transplant patient with uremia. The clinician stated that a preprocedural BT test would normally have been ordered, but would not have affected the timing of the biopsy.
A review of the administration of therapeutic (i.e., platelet-active) doses of DDAVP to patients before and after discontinuation of the BT test failed to show an increase in the overall use (Table 3
), the use in patients with renal disease (Table 3
), or the administration immediately before renal biopsy (Table 4
). This is consistent with the clinicians’ perception of their practices. Administration of DDAVP represents the primary intervention taken by clinicians at our institution to counteract platelet function defects (e.g., uremia, Von Willebrand’s disease) in patients who are at risk for bleeding because of scheduled invasive procedures or who are actively bleeding.
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Discussion
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The role of the BT test in defining the risk of pathologic bleeding in "susceptible" populations remains controversial. Most literature surveys that have objectively evaluated the performance of the BT test have found no clinical utility for this test (4)(5)(6). Our study failed to identify a clinically significant, negative impact of discontinuing availability of the test at our Medical Center. Objective measures of complication rates validated the clinicians’ perceptions of unchanged patient outcomes. The rate of postoperative bleeding in patients undergoing procedures in the Major Surgery Risk Pool before and after discontinuation of the BT test did not change. This suggests that there was not a dramatic increase in bleeding episodes attributable to unidentified platelet dysfunction. However, a minor increase cannot be ruled out because ICD-9 codes do not allow stratification of events by root cause. Likewise, we were unable to identify an increase in bleeding complications after renal biopsy, whether measured by a decrease in hematocrit or a requirement for RBC transfusions. These findings must be tempered, however, by the potential bias of an increased proportion of allograft kidneys in the cohort of patients after discontinuation of the BT test. It is interesting to note that our finding of a smaller decrease in the postprocedural hematocrit in transplant patients is at odds with other reports of greater arteriovenous fistula formation (16) and a greater decrease in the hematocrit of biopsied transplant kidneys (17). Transplantation may have been acting as a surrogate for an unmeasured variable because renal transplant patients did not differ significantly from nontransplant patients for any other characteristic that was assessed (data not shown).
Because clinical outcomes could have been influenced by a change in clinician behavior after discontinuation of the BT test, we attempted to assess potentially significant changes in clinical practices. Interviews with physicians who had previously ordered the BT test failed to identify an impact of discontinuation of the test on their clinical practice and/or patient outcomes. None believed he or she had significantly altered preprocedural work-ups or periprocedural transfusion practices as a result of discontinuation of the BT test; and, with one exception, none could recall a case where he or she felt a BT test might have led to an improved outcome. This included 60% of the practicing nephrologists, many of whom had frequently used the BT test before kidney biopsy. In fact, the Nephrology Division did not oppose discontinuation of the BT test when they were surveyed before elimination of the test. Their consensus opinion was that the questionable utility of the test did not justify the necessary maintenance. Consistent with the clinicians’ perceptions of their practice, utilization of platelet-aggregation tests, administration of DDAVP, and mean monthly platelet transfusions did not increase after discontinuation of the BT test. In addition, an evaluation of the indications for platelet transfusion in patients with normal counts at the time of transfusion failed to identify increased platelet utilization in patients at risk for acquired platelet dysfunction. Therefore, we found no evidence of significant changes in clinician practice that could have biased our assessment of patient outcomes before and after discontinuation of the BT test.
Although our neurosurgeons expressed concerns about their ability to identify patients at risk for bleeding among those taking NSAIDs, they did not use platelet-aggregation tests as a substitute and did not prescribe platelet transfusions for patients on NSAIDs. The lack of reported bleeding complications in their patients may suggest that the actual risk attributable to platelet dysfunction is less than that perceived. The degree of risk of bleeding complications in patients undergoing invasive procedures who have ingested aspirin or NSAIDs is somewhat controversial, even in neurosurgical patients, where even a small bleed may be catastrophic (18)(19)(20)(21). A review of the literature revealed very few case reports of presumed NSAID-induced bleeding episodes in patients undergoing neurological procedures, and no true prospective studies could be found (22)(23)(24)(25). In fact, one author recently concluded that there was insufficient evidence of increased risk of bleeding complications in patients who received aspirin therapy before central neural blockade to recommend a routine preprocedural BT test (20). In addition, two experimental studies have demonstrated that the skin template BT is, in fact, not predictive of visceral BTs in subjects treated with aspirin. Treatment of healthy human volunteers with aspirin prolonged the skin BT test, but did not prolong a gastric mucosal BT test performed during endoscopy (26); and an animal model of neurosurgical bleeding found that aspirin prolonged the skin BT test, but not a brain BT test induced by a standard incision (27).
Use of the BT test in clinical medicine relies on the premise that clinically relevant bleeding episodes, during or after invasive procedures, can be predicted a priori in susceptible patients, leading to appropriate preventative action. Whereas the BT test may predict a higher bleeding complication rate in populations at risk, it is of limited assistance in evaluating an individual patient, because of low sensitivity and specificity. In fact, Lee and Lamila (13) suggest that more harm, in the form of delayed surgery or administration of unnecessary or inappropriate blood products, may be incurred as a result of false-positive BT tests. The almost uniform lack of clinician concern about discontinuation of the BT test at our institution suggests that the test was not considered to be essential for practice, and possibly, unnecessarily obstructive. Many clinicians stated that they had ordered the test because it was available or because it was how they were trained.
The apparent lack of clinically significant adverse events attributable to discontinuation of the BT test would suggest the following: (a) in the absence of a personal or family history of bleeding, excessive bleeding attributable solely to platelet dysfunction must be relatively uncommon [e.g., in 10 years, Lee and Lamila (13) detected only two mild cases of von Willebrand’s disease through the use of routine preoperative BT tests], and (b) the BT test does not add significant positive predictive values to routine coagulation parameters and a platelet count, even in patients with the potential for undiagnosed, clinically significant platelet dysfunction (e.g., renal failure, liver failure). This may be attributable, in part, to relatively recent changes in the clinical management of these patients. For example, patients suffering from chronic renal failure commonly receive erythropoietin therapy, causing an increase in their hematocrit, which is thought to improve primary hemostasis (28). Administration of conjugated estrogens, DDAVP, or cryoprecipitate before procedures performed on uremic patients can correct a prolonged BT test, and presumably acquired platelet dysfunction (29)(30)(31)(32), although a cause-and-effect relationship with decreased hemorrhage has never been established. For patients with hepatic failure, wider availability of the transjugular (vs percutaneous) route for hepatic biopsies in patients with coagulopathies and/or thrombocytopenia may have reduced the risk of serious bleeding complications resulting from this procedure (33)(34).
Our assessment of the impact of discontinuation of the BT test could have missed infrequent events of bleeding that might have been avoided by performing the test. In fact, one of the four patients who required RBC transfusions after renal biopsy had normal coagulation values, as well as a normal platelet count. A BT test was not performed, although it was available at the time. It is interesting to speculate whether performance of a BT test would have impacted the clinical outcome. However, because these episodes are rarely, if ever fatal (17)(35)(36)(37)(38)(39), and because the clinical effectiveness of the interventions routinely taken to correct an abnormal BT have never been rigorously tested, the cost and significant effort required to maintain competency in the face of dwindling test numbers, and the repercussions of numerous false-positive BT test results, are not clinically justified.
In conclusion, our study failed to identify a clinically significant, negative impact of discontinuing availability of the BT test at a busy, tertiary-care, university medical center serving adult and neonatal patient populations. The role for new in vitro methods for assessing platelet function needs to be well defined, and the tests must be clinically validated before clinical acceptance is attained (40).
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Footnotes
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1 Nonstandard abbreviations: BT, bleeding time; NSAID, nonsteroidal antiinflammatory agent; BUN, blood urea nitrogen; and DDAVP, 1-deamino-8-D-arginine vasopressin. 
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References
|
|---|
-
Bick RL. Platelet function defects associated with hemorrhage or thrombosis [Review]. Med Clin North Am 1994;78:577-607.[Web of Science][Medline]
[Order article via Infotrieve]
-
Duke WW. The relation of blood platelets to hemorrhagic disease. Description of a method for determining the bleeding time and coagulation time and report of three cases of hemorrhagic disease relieved by transfusion. JAMA 1910;55:1185-1192.[Abstract/Free Full Text]
-
Ivy AC, Nelson D, Bucher G. The standardization of certain factors in the cutaneous "venostasis" bleeding time technique. J Lab Clin Med 1941;26:1812-1822.[Web of Science]
-
Rodgers RPC, Levin J. A critical reappraisal of the bleeding time. Semin Thromb Hemost 1990;16:1-20.[Web of Science][Medline]
[Order article via Infotrieve]
-
Lind SE. The bleeding time does not predict surgical bleeding [Review]. Blood 1991;77:2547-2552.[Free Full Text]
-
Peterson P, Hayes TE, Arkin CF, Bovill EG, Fairweather RB, Rock WA, et al. The preoperative bleeding time test lacks clinical benefit [Review]. Arch Surg 1998;133:134-139.[Abstract/Free Full Text]
-
Fugh-Berman A. Herb-drug interactions [Review]. Lancet 2000;355:134-138.[Web of Science][Medline]
[Order article via Infotrieve]
-
Mcdonald R. Bleeding time. Br J Anaesth 1992;69:329.[Free Full Text]
-
Sutor AH. The bleeding time in pediatrics [Review]. Semin Thromb Hemost 1998;24:531-543.[Web of Science][Medline]
[Order article via Infotrieve]
-
Mattix H, Singh AK. Is the bleeding time predictive of bleeding prior to a percutaneous renal biopsy [Review]?. Curr Opin Nephrol Hypertens 1999;8:715-718.[Web of Science][Medline]
[Order article via Infotrieve]
-
Boberg KM, Brosstad F, Egeland T, Egge T, Schrumpf E. Is a prolonged bleeding time associated with an increased risk of hemorrhage after liver biopsy? [Review]. Thromb Hemost 1999;81:378-381.[Web of Science][Medline]
[Order article via Infotrieve]
-
Messmore HL, Godwin J. Medical assessment of bleeding in the surgical patient [Review]. Med Clin North Am 1994;78:625-634.[Web of Science][Medline]
[Order article via Infotrieve]
-
Lee S, Lamila CM. Reducing the number of routine preoperative screening bleeding time tests [Letter]. Arch Pathol Lab Med 1991;115:1088-1089.[Web of Science][Medline]
[Order article via Infotrieve]
-
Rodgers RPC, Levin J. Reducing the number of routine preoperative screening bleeding time tests [Letter]. Arch Pathol Lab Med 1991;115:1089.[Web of Science]
-
Swift JA. Introduction to modern statistical quality control and management. Delray Beach, FL: St Lucie Press, 1995:350pp..
-
Stiles KP, Yuan CM, Chung EM, Lyon RD, Lane JD, Abbott KC. Renal biopsy in high-risk patients with medical diseases of the kidney [Review]. Am J Kidney Dis 2000;36:419-433.[Web of Science][Medline]
[Order article via Infotrieve]
-
Mendelssohn DC, Cole EH. Outcomes of percutaneous kidney biopsy, including those of solitary native kidneys. Am J Kidney Dis 1995;26:580-585.[Web of Science][Medline]
[Order article via Infotrieve]
-
Belisle S, Hardy JF. Hemorrhage and the use of blood products after adult cardiac operations: myths and realities. Ann Thorac Surg 1996;62:1908-1917.[Abstract/Free Full Text]
-
Self DD, Bryson GL, Sullivan PJ. Risk factors for post-carotid endarterectomy hematoma formation. Can J Anaesth 1999;46:635-640.[Web of Science][Medline]
[Order article via Infotrieve]
-
Wildsmith JAW, McClure JH. Aspirin, bleeding time and central neural block [Letter]. Br J Anaesth 1993;70:112.[Free Full Text]
-
Ferraris VA, Gildengorin V. Predictors of excessive blood use after coronary artery bypass grafting. A multivariate analysis. J Thorac Cardiovasc Surg 1989;98:492-497.[Abstract]
-
Merriman E, Bell W, Long DM. Surgical postoperative bleeding associated with aspirin ingestion. Report of two cases. J Neurosurg 1979;50:682-684.[Web of Science][Medline]
[Order article via Infotrieve]
-
Heye N. Is there a link between acute spinal epidural hematoma and aspirin?. Spine 1995;20:1931-1932.[Web of Science][Medline]
[Order article via Infotrieve]
-
de Swiet M, Redman CW. Aspirin, extradural anaesthesia and the MRC Collaborative Low-dose Aspirin Study in Pregnancy (CLASP). Br J Anaesth 1992;69:109-110.[Free Full Text]
-
Palmer JD, Sparrow OC, Iannotti F. Postoperative hematoma: a 5-year survey and identification of avoidable risk factors. Neurosurgery 1994;35:1061-1064.[Web of Science][Medline]
[Order article via Infotrieve]
-
O’Laughlin JC, Hoftiezer JW, Mahoney JP, Ivey KJ. Does aspirin prolong bleeding from gastric biopsies in man?. Gastrointest Endosc 1981;27:1-5.[Web of Science][Medline]
[Order article via Infotrieve]
-
MacDonald JD, Remington BJ, Rodgers GM. The skin bleeding time test as a predictor of brain bleeding time in a rat model. Thromb Res 1994;76:535-540.[Web of Science][Medline]
[Order article via Infotrieve]
-
Anand A, Feffer SE. Hematocrit and bleeding time: an update [Review]. South Med J 1994;87:299-301.[Web of Science][Medline]
[Order article via Infotrieve]
-
Boyd GL, Diethelm AG, Gelman S, Lagner R, Laskow D, Deierhoi M, Barber WH. Correcting prolonged bleeding during renal transplantation with estrogen or plasma. Arch Surg 1996;131:160-165.[Abstract/Free Full Text]
-
Weigert AL, Schafer AI. Uremic bleeding: pathogenesis and therapy [Review]. Am J Med Sci 1998;316:94-104.[Web of Science][Medline]
[Order article via Infotrieve]
-
Mannuccio PM, Remuzzi G, Pusineri F, Lombardi R, Valsecchi C, Mecca G, Zimmerman TS. Deamino-8-D-arginine vasopressin shortens the bleeding time in uremia. N Engl J Med 1983;308:8-12.[Abstract]
-
Janson PA, Jubelirer SJ, Weinstein MJ, Deykin D. Treatment of the bleeding tendency in uremia with cryoprecipitate. N Engl J Med 1980;303:1318-1322.[Abstract]
-
Sawyer AM, McCormick PA, Tennyson GS, Chin J, Dick R, Scheuer PJ, et al. A comparison of transjugular and plugged-percutaneous liver biopsy in patients with impaired coagulation. J Hepatol 1993;17:81-85.[Web of Science][Medline]
[Order article via Infotrieve]
-
Bonnard P, Vitte R, Barbare J, Denis J, Stepani P, Di Martino V, et al. Is bleeding time measurement useful for choosing the liver biopsy route? The results of a pragmatic, prospective multicentric study in 219 patients [Letter]. J Clin Gastroenterol 1999;29:347-349.[Web of Science][Medline]
[Order article via Infotrieve]
-
Mahal AS, Knauer MC, Gregory PB. Bleeding after liver biopsy. West J Med 1981;134:11-14.[Web of Science][Medline]
[Order article via Infotrieve]
-
Piccinino F, Sagnelli E, Pasquale G, Giusti G. Complications following percutaneous liver biopsy. A multicenter retrospective study on 68,276 biopsies. J Hepatol 1986;2:165-173.[Web of Science][Medline]
[Order article via Infotrieve]
-
Little AF, Ferris JV, Dodd GD, Baron RL. Image-guided percutaneous hepatic biopsy: effect of ascites on the complication rate. Radiology 1996;199:79-83.[Abstract/Free Full Text]
-
Benfield MR, Herrin J, Feld L, Rose S, Stablein D, Tejani A. Safety of kidney biopsy in pediatric transplantation: a report of the Controlled Clinical Trials in Pediatric Transplantation Trial of Induction Therapy Study Group. Transplantation 1999;67:544-547.[Web of Science][Medline]
[Order article via Infotrieve]
-
Hergesell O, Felten H, Andrassy K, Kuhn k, Ritz E. Safety of ultrasound-guided percutaneous renal biopsy-retrospective analysis of 1090 consecutive cases. Nephrol Dial Transplant 1998;13:975-977.[Abstract/Free Full Text]
-
Carr ME, Jr. In vitro assessment of platelet function [Review]. Transfus Med Rev 1997;11:106-115.[Web of Science][Medline]
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G. Lippi and M. Franchini
Laboratory Screening for Abnormalities of Primary Hemostasis: What's Next?
Clin. Chem.,
November 1, 2001;
47(11):
2071 - 2071.
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- Christopher Lehman
- Clinical Chemistry Online, 20 Aug 2001
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Abstract
Introduction
