A prolonged bleeding time may be indicative of

The major conclusions of this position article are as follows: (1) In the absence of a history of a bleeding disorder, the bleeding time is not a useful predictor of the risk of hemorrhage associated with surgical procedures. (2) A normal bleeding time does not exclude the possibility of excessive hemorrhage associated with invasive procedures. (3) The bleeding time cannot be used to reliably identify patients who may have recently ingested aspirin or nonsteroidal anti-inflammatory agents or those who have a platelet defect attributable to these drugs. The best preoperative screen to predict bleeding continues to be a carefully conducted clinical history that includes family and previous dental, obstetric, surgical, traumatic injury, transfusion, and drug histories. A history suggesting a possible bleeding disorder may require further evaluation; such an evaluation may include performance of the bleeding time test, as well as a determination of the platelet count, the prothrombin time, and the activated partial thromboplastin time. In the absence of a history of excessive bleeding, the bleeding time fails as a screening test and is, therefore, not indicated as a routine preoperative test.

Historically, the bleeding time test has been used to evaluate the integrity of primary hemostasis. The undocumented, but widespread, assumption is that the bleeding time correlates better with a hemorrhagic tendency in disorders of platelet function than any other in vitro test. As a consequence, the bleeding time is often determined prior to invasive procedures in an attempt to predict the risk of hemorrhagic complications. Recently, the indications for the clinical use of the bleeding time have come under closer scrutiny, resulting in an increase in the controversy regarding the appropriate use of the bleeding time test.1-4 Some of the underlying issues in this controversy include a desire to have a test that accurately predicts the risk of procedure-associated hemorrhage, fear of litigation in the event of a major hemorrhage, lack of understanding of the limitations of the bleeding time test, efforts to control rising health care costs, and increasingly limited laboratory resources. The goal of this position article is to generate a consensus that a routine preoperative bleeding time test is not warranted in the patient who does not have a history of a bleeding disorder.

The bleeding time is an indicator of in vivo primary hemostasis.5 It is prolonged in patients with quantitative or qualitative platelet disorders or both and in patients with abnormalities of vascular wall integrity. The bleeding time test assesses the formation of a platelet plug in a skin wound and reflects complex pathophysiological mechanisms that are not completely understood. In general, the bleeding time test is performed by making a small incision in the skin and then determining how long it takes for blood flow to cease.

Historically, the bleeding time test has been plagued with problems of reproducibility. Numerous modifications have resulted in a more standardized format and instrumentation for performing the test. More than 50 years ago, Ivy et al6 advocated incising the lateral aspect of the volar surface of the forearm and using a sphygmomanometer to elevate capillary pressure and maintain a constant capillary tone, thereby controlling a major variable—collapse of the vessel wall. Almost 25 years ago, Mielke et al7 introduced the template technique to address standardization of the length and the depth of the incision. More recently, disposable devices based on the approach by Mielke et al have been introduced.8,9 Recent work suggests that these modifications to the Ivy technique have not notably improved the reproducibility, sensitivity, or specificity of this procedure.10,11 Despite these attempts to standardize technique, the bleeding time test continues to be affected by numerous technical variables and clinical conditions (Table 1). 1,5,12-45

There is a relationship between the platelet count and the bleeding time that was shown in the classic study of Harker and Slichter.20 Their study of clinically stable, nonmedicated subjects with pure platelet production defects showed that the bleeding time is normal when the platelet count is greater than 100×109/L. However, the results of their study cannot be generalized because the patient population they examined is not representative of the patients for whom the bleeding time might be used to make clinical decisions.1 There are clinical conditions, such as systemic lupus erythematosus and uremia, for which the bleeding time may be prolonged with mild thrombocytopenia and for which bleeding problems are more likely a reflection of dysfunctional platelets rather than mild thrombocytopenia. Furthermore, there are conditions, such as idiopathic thrombocytopenic purpura, for which the bleeding time may be shorter than would be expected based on the platelet count. Because the correlation between the bleeding time and the platelet count may vary markedly, the bleeding time should not be used as an estimate of the platelet count.

Studies concerning the preoperative use of the bleeding time test

One to 2 million bleeding time procedures are performed each year in the United States, making it one of the most widely used tests of hemostasis.4,46 Most of these bleeding time tests are probably performed in anticipation of surgery or other invasive procedures.47 The bleeding time test was introduced in an era when clinical tests were not scrutinized for their predictive value, quickly became established as a "routine" test, and has been promoted as an aid to diagnosis, prognosis, and the monitoring of therapy.1,2 It was assumed to be an effective screening test for congenital disorders of platelet function and a predictor of the risk of bleeding. Despite its widespread clinical use, the bleeding time test is not a good preoperative screening tool for the general population.1,2,47,48

Preoperative Evaluation of Risk of Bleeding

Excessive perioperative bleeding secondary to a preexisting hemorrhagic disorder in a patient with no history of excessive bleeding is a rare event.1,2,46-48 When a test is used to screen a low-risk population for an uncommon event, a positive result is often a false positive. In other words, the predictive value of a positive test in such a situation is poor. Barber et al47 reviewed 1941 consecutive template bleeding times, approximately 95% of which were used for a preoperative screen. Only 110 (6%) of the patients were found to have an abnormal bleeding time. Eighty-three (75%) of these patients could have been predicted to have an abnormal bleeding time from an adequate clinical history. No obvious cause for the prolonged bleeding time could be found in the other 27 patients. Seventeen of these 27 patients later underwent a second bleeding time test; of these tests, the results for 12 were normal, suggesting that most of these long bleeding times were false positives due to technical artifact.

There are insufficient data to accurately calculate the sensitivity, specificity, or predictive value of the bleeding time regarding perioperative or postoperative hemorrhage.1,2 Rodgers and Levin1 were able to identify only 2 published studies with sufficient data to prepare receiver operating characteristic curves. The receiver operating characteristic curves from these studies indicated that the bleeding time behaved like a noninformative test in predicting the risk of bleeding.

Recent reviews have highlighted the inability of the bleeding time to predict excessive surgical bleeding.1,2,4 Multiple studies have found no relationship between the preoperative bleeding time and the amount of blood loss associated with cardiopulmonary surgery.29,49-54 In one double-blind study, the hemostatic integrity of 101 consecutive patients was evaluated preoperatively by 2 hematologists.55 They stratified the patients into 3 groups according to the anticipated risk of bleeding; 7 of 8 high-risk patients were classified as such based on a prolonged bleeding time. Only 2 of the 17 patients who experienced excessive bleeding were prospectively classified as high risk. Two patients died as a result of excessive intraoperative hemorrhage; neither had been classified as high risk. Ferraris and Swanson56 prospectively evaluated the conditions of 129 patients requiring urgent, unplanned, general surgical procedures. Eight of these patients had a prolonged bleeding time preoperatively; none of these 8 patients had excessive bleeding. Handler et al57 observed 38 patients with postoperative bleeding in a series of 1445 patients undergoing tonsillectomy; there was no difference in the mean bleeding time between patients with (5.46-minutes) and without (5.34-minutes) postoperative bleeding. In a subsequent study, they identified 3 of 1603 patients with a long bleeding time prior to tonsillectomy. The results of a subsequent bleeding time test were abnormal in only one of these patients; this patient had von Willebrand disease and also had a prolonged activated partial thromboplastin time.30

There is little information regarding the efficacy of the bleeding time test in predicting hemorrhagic risk associated with specialized surgery or other invasive procedures. In a prospective study of 139 patients undergoing cataract extraction, hyphema developed in 3 (19%) of 16 patients with a prolonged bleeding time compared with 10 (9.5%) of 105 patients with a normal preoperative bleeding time.58 Although these data suggest a trend towards an increased risk of hyphema with a long bleeding time, the difference was not statistically significant. Furthermore, the relationship between aspirin ingestion and prolongation of the bleeding time was not addressed. Amrein et al59 addressed the effect of perioperative administration of aspirin on bleeding in patients undergoing hip surgery. While there was a slight increase in blood loss associated with the administration of aspirin, there was no association between the preoperative bleeding time and surgical blood loss.

Hematoma formation is a rare, but feared, complication of epidural and spinal anesthesia.60-64 The potential association between the common use of nonsteroidal anti-inflammatory drugs, abnormalities of platelet function, and hematoma formation have led some to recommend that a bleeding time test be performed before epidural anesthesia and that a bleeding time in excess of 10 minutes is a relative contraindication for epidural anesthesia.64 There are inadequate data to support this conclusion.58 Horlocker et al65 found that 39% of the patients undergoing spinal or epidural anesthesia were exposed to antiplatelet medications in the preoperative period. Neurologic complications in association with the procedure did not develop in any of these patients. Odom and Sih66 reported their experience with 1000 cases of epidural anesthesia given to patients receiving oral anticoagulants. They observed no complications that could be related to bleeding or hematoma formation in the extradural space. There are anecdotal cases of spinal subdural bleeding in association with the use of antiplatelet medications; however, the preoperative bleeding time has not been uniformly prolonged in these cases.31,32 Finally, as discussed in the section on "Evaluation of Risk of Bleeding in Patients Taking Aspirin or Nonsteroidal Anti-inflammatory Drugs," the bleeding time is not a sensitive test when used to detect the preoperative use of aspirin. Thus, even if there is a slight association between the preoperative use of aspirin and hematoma formation following epidural or spinal anesthesia, the bleeding time is not an adequate test to identify patients who have taken aspirin.

Evaluation of Risk of Bleeding in Patients Taking Aspirin or Nonsteroidal Anti-inflammatory Drugs

The bleeding time is also often misused to identify patients who may have recently ingested a drug, usually aspirin, known to interfere with platelet function. A history of aspirin ingestion has been associated with increased blood loss in some clinical settings, including open heart surgery, hip surgery, delivery of a neonate, and gastrointestinal bleeding.33-36 The clinical desire to identify such patients is easy to understand. However, there are 2 basic problems with using the bleeding time for this purpose: (1) the bleeding time is not effective in identifying such patients and (2) the correlation between bleeding and prolongation of the bleeding time is poor in such patients.

The ingestion of 650 mg of aspirin by volunteers resulted in a method-dependent mild increase in the bleeding time compared with the individual's baseline bleeding time.7,26 However, in most of the individuals studied, the bleeding time remained within the normal range. In a study of patients receiving long-term aspirin therapy, the mean (±SD) bleeding time in patients receiving 300 mg of aspirin a day was 217± 69 seconds; in patients receiving 1200 mg of aspirin a day, it was 240± 60 seconds; and in patients receiving placebo, it was 217± 63 seconds.37 In a case-control study, Bashein et al33 found that the preoperative bleeding time (±SD) in patients taking aspirin within 7 days of open heart surgery was 5.5± 2.2 minutes compared with 4.9± 1.1 minutes in those not taking aspirin during this period. Although the difference in mean bleeding time was significant, there was too much overlap between the 2 groups to make the bleeding time a clinically useful procedure. In a study of patients requiring unexpected surgery, Ferraris and Swanson56 found that the bleeding time was prolonged in only 8 of 22 patients with a history of recent aspirin ingestion, documented by suppression of thromboxane B2 levels. These studies indicate that the bleeding time cannot be used to reliably identify patients who have recently received aspirin.

Although a history of aspirin ingestion has been associated with bleeding in patients with some conditions, there is little evidence that increased blood loss in such patients can be predicted by the bleeding time. In their evaluation of the effect of aspirin ingestion on bleeding associated with hip surgery, Amrein et al59 found no correlation between increased bleeding and a bleeding time of greater than 10 minutes or an aspirin-induced prolongation of 4 minutes over baseline. As noted previously, Ferraris and Swanson56 found no relationship between surgical bleeding and either preoperative bleeding time or history of aspirin ingestion in their study of patients requiring urgent surgical procedures. The relationship between a history of aspirin ingestion, preoperative bleeding time, and perioperative blood loss has also been examined in patients undergoing cardiopulmonary bypass surgery.33,37,39 These studies have shown that there is an association between a history of aspirin ingestion and blood loss but that there is no relationship between the preoperative bleeding time and blood loss. Finally, O'Laughlin et al40 found that while the skin bleeding time was prolonged after aspirin ingestion, the gastric bleeding time following a gastric biopsy was normal, suggesting that a long skin bleeding time may not accurately predict the response to vascular injury at other sites.

Therefore, the most effective method of identifying patients who may be at risk because of aspirin ingestion is the clinical history. The critical period for exposure to aspirin seems to be approximately 3 days prior to an invasive procedure. A recent study67 documented that platelet function, as measured by thromboxane A2 production and aggregation studies, returned to normal 4 days after the cessation of aspirin therapy. Another study68 showed that aspirin-induced prolongation of the bleeding time lasts no longer than 48 hours. The prolonged bleeding time in patients taking aspirin may be shortened after the administration of desmopressin acetate; however, there is no evidence that this translates into decreased perioperative blood loss.41

Evaluation of Risk of Bleeding in Patients With Uremia

Uremia is a complex metabolic disorder that has deleterious effects on hemostasis. The hemostatic defect associated with uremia is complex and multifactorial and has not yet been fully delineated.69 In recent years, it has become evident that a low hematocrit is associated with a prolonged bleeding time in patients with uremia and that correction of the hematocrit by transfusion or use of recombinant erythropoietin is associated with normalization of the bleeding time in most patients.70-72 Uncontrolled studies have suggested that the normalization of the bleeding time with increasing hematocrit is associated with a decreased incidence of bleeding.71-74 This effect seems to be due to improved interaction between circulating platelets and the vessel wall, as well as alteration of a plasma defect associated with uremia.75

The bleeding time has also been used to assess other forms of intervention in patients with uremia. Several studies have shown that the bleeding time decreases following the intravenous or subcutaneous administration of desmopressin acetate within 4 to 6 hours.76 The bleeding time has also been used to monitor the response to cryoprecipitate or conjugated estrogens.42,77,78 In all these reports, there is anecdotal evidence that correction of the bleeding time was associated with decreased clinical bleeding. Indeed, it has been suggested that the bleeding time may be the best indicator of bleeding risk in patients with uremia.43 Other studies evaluating the relationship between bleeding of widely varying severity and prolongation of the bleeding time have failed to establish the use of the bleeding time for the prediction of clinically severe bleeding in advance of its occurrence.44,45,79,80 In particular, the study by Eknoyan et al44 showed that a decline in prothrombin consumption was more predictive of bleeding than any other parameter studied, including the bleeding time. Although some studies have shown a reasonable correlation between the bleeding time and "clinical" bleeding (as distinguished from "surgical" bleeding) in patients with uremia, no controlled study has shown that patients with prolonged bleeding times have more clinically significant complications than those with normal bleeding times.1,2,22,43 Thus, the bleeding time may be useful for monitoring the response to therapy in patients with uremia. However, there is little direct evidence indicating that the bleeding time can be used to predict the risk of bleeding in these patients, particularly in a patient undergoing an invasive procedure.

In addressing the issues of concern regarding this laboratory test, we conclude the following:

1. In the absence of a clinical history of a bleeding disorder, the bleeding time is not a useful predictor of the risk of hemorrhage associated with surgical procedures.

2. A normal bleeding time does not exclude the possibility of excessive hemorrhage associated with invasive procedures.

3. The bleeding time cannot be used to reliably identify patients who may have recently ingested aspirin or nonsteroidal anti-inflammatory agents, or who have a platelet defect attributable to these drugs.

The best preoperative screen to predict bleeding continues to be a carefully conducted clinical history, which includes family and previous dental, obstetric, surgical, traumatic injury, transfusion, and drug histories. A patient with a history suggesting a possible bleeding disorder may require further examination. In the absence of a history of excessive bleeding, the bleeding time fails as a screening test and is, therefore, not indicated as a routine preoperative test.

This study was supported by the College of American Pathologists, Northfield, Ill, and by the American Society of Clinical Pathologists, Chicago, Ill.

Reprints: College of American Pathologists, 325 Waukegan Rd, Northfield, IL 60093-2750.

1.

Rodgers  RPCLevin  J A critical reappraisal of the bleeding time.  Semin Thromb Hemost. 1990;161- 20Google ScholarCrossref

2.

Lind  SE The bleeding time does not predict surgical bleeding.  Blood. 1991;772547- 2552Google Scholar

3.

Triplett  DA The bleeding time: neither pariah or panacea.  Arch Pathol Lab Med. 1989;1131207- 1208Google Scholar

4.

Burns  ERLawrence  C Bleeding time: a guide to its diagnostic and clinical utility.  Arch Pathol Lab Med. 1989;1131219- 1224Google Scholar

5.

Mielke  CH Measurement of the bleeding time.  Thromb Haemost. 1984;52210- 211Google Scholar

6.

Ivy  ACNelson  DBuchet  G The standardization of certain factors in the cutaneous ‘venostasis' bleeding time technique.  J Lab Clin Med. 1941;261812- 1822Google Scholar

7.

Mielke  CHKaneshiro  MMMaher  IAWiener  JMRapaport  SI The standardized normal Ivy bleeding time and its prolongation by aspirin.  Blood. 1969;34204- 215Google Scholar

8.

Babson  SRBabson  AL Development and evaluation of a disposable device for performing simultaneous duplicate bleeding time determinations.  Am J Clin Pathol. 1978;70406- 409Google Scholar

9.

Smith  C Surgicutt: a device for modified template bleeding times.  J Med Technol. 1986;329- 31Google Scholar

10.

Koster  TCaekebeke-Peerlinck  KMJBriet  E A randomized and blinded comparison of the sensitivity and the reproducibility of the Ivy and Simplate II bleeding time techniques.  Am J Clin Pathol. 1989;92315- 320Google Scholar

11.

Sramek  RSramek  AKoster  TBriet  ERosendaal  FR A randomized and blinded comparison of three bleeding time techniques: the Ivy method, and the Simplate II method in two directions.  Thromb Haemost. 1992;67514- 518Google Scholar

12.

Göbel  UVoss  HVJürgens  HLauber  AVolkner  HP The reproductiveness of bleeding time tests.  Minerva Pediatr. 1978;301391- 1396Google Scholar

14.

Chen  H-ITang  Y-RWu  H-JJen  CJ Effects of acute exercise on bleeding time, bleeding amount and blood cell counts: a comparative study.  Thromb Res. 1989;55503- 510Google ScholarCrossref

15.

Sutor  AHBowie  EJWThompson  JH  et al.  Bleeding from standardized skin punctures automated technic for recording time, intensity, and pattern of bleeding.  Am J Clin Pathol. 1971;55541- 550Google Scholar

16.

Bain  BForster  T A sex difference in bleeding time.  Thromb Haemost. 1980;43131- 132Google Scholar

17.

Macpherson  CRJacobs  P Bleeding time decreases with age.  Arch Pathol Lab Med. 1987;111328- 329Google Scholar

18.

Small  MLowe  GDCameron  EForbes  CD Contribution of the haematocrit to the bleeding time.  Haemostasis. 1983;13379- 384Google Scholar

19.

Rao  AK Congenital disorders of platelet function.  Hematol Oncol Clin North Am. 1990;465- 86Google Scholar

20.

Harker  LASlichter  SJ The bleeding time as a screening test for evaluation of platelet function.  N Engl J Med. 1972;287155- 159Google ScholarCrossref

21.

Janson  PAJubelirer  SJWeinstein  MJDeykin  D Treatment of the bleeding tendency in uremia with cryoprecipitate.  N Engl J Med. 1980;3031318- 1322Google ScholarCrossref

22.

Livio  MGotti  EMarchesi  DMecca  GdeGaetoma  G Uraemic bleeding: role of anaemia and beneficial effect of red cell transfusions.  Lancet. 1982;21013- 1015Google ScholarCrossref

23.

George  JNShattil  SJ The clinical importance of acquired abnormalities of platelet formation.  N Engl J Med. 1991;32427- 39Google ScholarCrossref

24.

Mielke  CHKaneshiro  MMMaher  IAWiener  JMRapaport  SI The standardized normal Ivy bleeding time and its prolongation by aspirin.  Blood. 1969;34204- 215Google Scholar

25.

Jorgensen  KADyerberg  JOlesen  AS  et al.  Acetylsalicylic acid, bleeding time, and age.  Thromb Res. 1980;19799- 805Google ScholarCrossref

26.

Mielke Jr  CH Aspirin prolongation of the template bleeding time: influence of venostasis and direction of incision.  Blood. 1982;601139- 1142Google Scholar

27.

Milner  PCMartin  JF Shortened bleeding time in acute myocardial infarction and its relation to platelet mass.  Br Med J (Clin Res Ed). 1985;2901767- 1770Google ScholarCrossref

28.

O'Brien  JREtherington  MDJamieson  S  et al.  Blood changes in atherosclerosis and long after myocardial infarction and venous thrombosis.  Thromb Diath Haemorrh. 1975;34483- 497Google Scholar

29.

DeCaterina  RLanza  MManca  G  et al.  Bleeding time and bleeding: an analysis of the relationship of the bleeding time test with parameters of surgical bleeding.  Blood. 1994;843363- 3370Google Scholar

30.

Burk  CDMiller  LHandler  SDCohen  AR Preoperative history and coagulation screening in children undergoing tonsillectomy.  Pediatrics. 1992;89691- 695Google Scholar

31.

Greensite  FSKatz  J Spinal subdural hematoma associated with attempted epidural anesthesia and subsequent continuous spinal anesthesia.  Anesth Analg. 1980;5972- 73Google ScholarCrossref

32.

Mayumi  TDohi  S Spinal subarachnoid hematoma after lumbar puncture in a patient receiving antiplatelet therapy.  Anesth Analg. 1983;62777- 779Google Scholar

33.

Bashein  GNessly  MLRice  ALCounts  RBMisbach  GA Preoperative aspirin therapy and reoperation for bleeding after coronary artery bypass surgery.  Arch Intern Med. 1991;15189- 93Google ScholarCrossref

34.

Stuart  MJGross  SJElrad  HGraeber  JE Effects of acetylsalicylic acid ingestion on maternal and neonatal hemostasis.  N Engl J Med. 1982;307909- 912Google ScholarCrossref

35.

Laporte  JRCarne  XVidal  XMoreno  VJuan  J Upper gastrointestinal bleeding in relation to previous use of analgesics and non-steroidal anti-inflammatory drugs: Catalan Countries Study on Upper Gastrointestinal Bleeding.  Lancet. 1991;33785- 89Google ScholarCrossref

36.

Levy  MMiller  DRKaufman  DW  et al.  Major gastrointestinal tract bleeding: relation to the use of aspirin and other nonnarcotic analgesics.  Arch Intern Med. 1988;148281- 285Google ScholarCrossref

37.

Frith  PAWarlow  CP A study of bleeding time in 120 long-term aspirin trial patients.  Thromb Res. 1988;49463- 470Google ScholarCrossref

38.

Taggart  DPSiddiqui  AWheatley  DJ Low-dose preoperative aspirin therapy, postoperative blood loss, and transfusion requirements.  Ann Thorac Surg. 1990;50424- 428Google ScholarCrossref

39.

Woodman  RCHarker  LA Bleeding complications associated with cardiopulmonary bypass.  Blood. 1990;761680- 1697Google Scholar

40.

O'Laughlin  JCHoftiezer  JWMahoney  JPIvey  KJ Does aspirin prolong bleeding from gastric biopsies in man?  Gastrointest Endosc. 1981;271- 5Google ScholarCrossref

41.

Kobrinsky  NLIsrael  EDGerrard  JM  et al.  Shortening of the bleeding time by 1-deamino-8-D-arginine vasopressin in various bleeding disorders.  Lancet. 1984;11145Google ScholarCrossref

42.

Shemin  DElnour  MAmarantes  BAbuelo  JGChazan  JA Oral estrogens decrease bleeding time and improve clinical bleeding in patients with renal failure.  Am J Med. 1990;89436- 440Google ScholarCrossref

43.

Steiner  RWCoggins  CCarvalho  ACA Bleeding time in uremia: a useful test to assess clinical bleeding.  Am J Hematol. 1979;7107- 117Google ScholarCrossref

44.

Eknoyan  GWacksman  SJGlueck  HIWill  JJ Platelet function in renal failure.  N Engl J Med. 1969;280677- 681Google ScholarCrossref

46.

Not Available, Clinical Laboratories: Opportunities and Threats 1982-1990.  Northfield, Ill J Lloyd Johnson Associates1984;990- 92

47.

Barber  AGreen  DGalluzzo  TTs'ao  C The bleeding time as a preoperative screening test.  Am J Med. 1985;78761- 764Google ScholarCrossref

48.

Gewirtz  ASMiller  MLKeys  TF The clinical usefulness of the preoperative bleeding time.  Arch Pathol Lab Med. 1996;120353- 356Google Scholar

49.

Simon  TLAkl  BFMurphy  W Controlled trial of routine administration of platelet concentrates in cardiopulmonary bypass surgery.  Ann Thorac Surg. 1984;37359- 364Google ScholarCrossref

50.

Dieter  RANeville  WEPifarre  RJasuja  M Preoperative coagulation profiles posthemodilution cardiopulmonary bypass hemorrhage.  Am J Surg. 1971;121689- 693Google ScholarCrossref

51.

Installe  EGonzalez  MSchoevaerdts  JCTremouroux  J Prevention by ticlopidine of platelet consumption during extra-corporeal circulation for heart surgery and lack of effect on operative and postoperative bleeding.  J Cardiovasc Pharmacol. 1981;31174- 1183Google ScholarCrossref

52.

Ramsay  GArvan  DAStewart  SBlumberg  N Do preoperative laboratory tests predict blood transfusion needs in cardiac operations?  J Thorac Cardiovasc Surg. 1983;85564- 569Google Scholar

53.

Salzman  EWWeinstein  MJWeintraub  RM  et al.  Treatment with desmopressin acetate to reduce blood loss after cardiac surgery: a double-blind randomized trial.  N Engl J Med. 1986;3141402- 1406Google ScholarCrossref

54.

Burns  ERBillett  HHFrater  RWSisto  DA The preoperative bleeding time as a predictor of postoperative hemorrhage after cardiopulmonary bypass.  J Thorac Cardiovasc Surg. 1986;92310- 312Google Scholar

55.

Eika  CHavig  OGodal  HC The value of preoperative haemostatic screening.  Scand J Haematol. 1978;21349- 354Google ScholarCrossref

56.

Ferraris  VASwanson  E Aspirin usage and perioperative blood loss in patients undergoing unexpected operations.  Surg Gynecol Obstet. 1983;156439- 442Google Scholar

57.

Handler  SDMiller  LRichmond  KHBaranak  CC Post-tonsillectomy hemorrhage: incidence, prevention and management.  Laryngoscope. 1986;961243- 1247Google Scholar

58.

Gorman  MRittersbach  GHEliason  JARosenthal  AR Preoperative prediction of hyphemas.  Ophthalmic Surg. 1986;17490- 492Google Scholar

59.

Amrein  PCEllman  LHarris  WH Aspirin-induced prolongation of the bleeding time and perioperative blood loss.  JAMA. 1981;2451825- 1828Google ScholarCrossref

60.

Wildsmith  JAWMcClure  JH Anticoagulant drugs and central nerve blockade.  Anaesthesia. 1991;46613- 614Google ScholarCrossref

61.

Sage  DJ Epidurals, spinals and bleeding disorders in pregnancy: a review.  Anaesth Intensive Care. 1990;18319- 326Google Scholar

63.

Tekkok  IHCataltepe  OTahta  KBertan  V Extradural haematoma after continuous extradural anaesthesia.  Br J Anaesth. 1991;67112- 115Google ScholarCrossref

65.

Horlocker  TTWedel  DJOfford  KP Does preoperative antiplatelet therapy increase the risk of hemorrhagic complications associated with regional anesthesia?  Anesth Analg. 1990;70631- 634Google ScholarCrossref

66.

Odom  JASih  IL Epidural analgesia and anticoagulant therapy.  Anaesthesia. 1983;38254- 259Google Scholar

67.

Jiminez  AHStubbs  METofler  GH  et al.  Rapidity and duration of platelet suppression by enteric-coated aspirin in healthy young men.  Am J Cardiol. 1992;69258- 262Google ScholarCrossref

68.

Fiore  LDBrophy  MTLopez  AJanson  PDeykin  D The bleeding time response to aspirin: identifying the hyperresponder.  Am J Clin Pathol. 1990;94292- 296Google Scholar

70.

Fernandez  FGoudable  CSie  P  et al.  Low hematocrit and prolonged bleeding time in uraemic patients: effect of red cell transfusions.  Br J Haematol. 1985;59139- 148Google ScholarCrossref

71.

van Geet  CHauglustaine  DVerresen  LVanrusselt  MVermylen  J Haemostatic effects of recombinant human erythropoietin on chronic haemodialysis patients.  Thromb Haemost. 1989;61117- 121Google Scholar

72.

Moia  MVizzotto  LCattaneo  M  et al.  Improvement in the haemostatic defect in uraemia after treatment with recombinant human erythropoietin.  Lancet. 1987;21227- 1229Google ScholarCrossref

73.

Zwaginga  JJIjsseldijk  MJWdeGroot  PG  et al.  Treatment of uremic anemia with recombinant erythropoietin also reduces the defects in platelet adhesion and aggregation caused by uremic plasma.  Thromb Haemost. 1991;66638- 647Google Scholar

74.

Mannucci  PMRemuzzi  GPusineri  F  et al.  Deamino-8-D-arginine vasopressin shortens the bleeding time in uremia.  N Engl J Med. 1983;3088- 12Google ScholarCrossref

75.

Vigano  GLMannucci  PMLattuada  AHarris  ARemuzzi  G Subcutaneous desmopressin (DDAVP) shortens the bleeding time in uremia.  Am J Hematol. 1989;3132- 35Google ScholarCrossref

77.

Janson  PAJubelirer  SJWeinstein  MJDeykin  D Treatment of the bleeding tendency in uremia with cryoprecipitate.  N Engl J Med. 1980;3031318- 1322Google ScholarCrossref

78.

Livio  MMannucci  PMVigano  G  et al.  Conjugated estrogens for the management of bleeding associated with renal failure.  N Engl J Med. 1986;315731- 735Google ScholarCrossref

80.

Willoughby  MLNCrouch  SJ An investigation of the hemorrhagic tendency in renal failure.  Br J Haematol. 1961;7315- 326Google ScholarCrossref

What does bleeding time indicate?

Which conditions affect the bleeding time?