Veterinary Clinical Pathology ISSN 0275-6382
ORIGINAL ARTICLE
Comparison of the buccal mucosal bleeding time in dogs using 3
different-sized lancet devices
Marcel Aumann, Valentina Rossi, Kevin Le Boedec, Armelle Dique
Internal Medicine, Department of Clinical Sciences, Universite
Key Words
Dogs, hemorrhage, mucosa, platelets, primary
hemostasis
Correspondence

lou, Internal Medicine, Ecole
Dr. Armelle Dique
nationale Veterinaire de Toulouse, 23 chemin
des Capelles, BP 97614, 31076 Toulouse
Cedex France
E-mail a.diquelou@envt.fr
DOI:10.1111/vcp.12087
Introduction
Disorders of primary hemostasis, including thrombo-
cytopenia, thrombocytopathia, von Willebrand disease
(vWD) and vascular disorders such as Ehlers-Danlos
syndrome, may result in internal and external superfi-
cial bleeding as well as excessive hemorrhage follow-
ing surgery or trauma.1 The bleeding time (BT) has
been used in people, dogs, and cats as a point of care
test to evaluate primary hemostasis in vivo.1–6 In dogs,
a prolongation of the buccal mucosal bleeding time
(BMBT) above the published upper limit of 210 s7 in
light of a normal Plt count may be due to vWD,
thrombocytopathia, or vascular disorders.1–3,7 Reports
in people and dogs indicate that BT is prolonged with
thrombocytopenia at concentrations < 100 9 109/L
and < 20 9 109/L, respectively.1,3,8 Human studies
Vet Clin Pathol 42/4 (2013) 451–457 ©2013 American Society for Veterinary Clinical Pathology

lou

de Toulouse, INPT, ENVT, Toulouse, France
Background: The buccal mucosal bleeding time (BMBT) evaluates primary
hemostasis in vivo. Three different-sized lancet devices designed for people,
Adult (A), Junior (J), and Newborn (N), can be used to perform the BMBT
in dogs.
Objectives: The aim was to compare BMBT using 3 different-sized human
lancet devices in dogs with varying platelet counts and hematocrits.
Methods: The BMBT was measured in 46 client-owned dogs (2 healthy,
44 suffering from various disorders) with varying platelet (Plt) counts and
hematocrits, using the 3 devices successively in each dog, in a randomly
determined order, over a 10- to 30-minute period. Statistical analysis
(ANOVA, Mann–Whitney U-test) was performed using commercial
software.
Results: BMBTs were significantly different between devices
(P < .00001), and shorter with devices N and J compared with device A
(P < .01). The BMBT was prolonged (> 210 s) in 10 dogs with device A and
in 7 dogs each with devices J and N, respectively. Sixteen dogs had a Plt
count < 200 9 109/L (Reference interval 200–500 9 109/L). Nine of these
dogs had prolonged BMBT with device A, and 6 dogs with device J and
device N, respectively. BMBT was longer in thrombocytopenic dogs with
devices A and J (P < .016). Anemia without thrombocytopenia did not
affect BMBT with any device.
Conclusions: The BMBT is influenced by the size of the used device, with
A resulting in the longest BMBT. Therefore, the type of device used to
obtain the BMBT has to be specified for standardized results.
have also demonstrated a relationship between a
decrease in HCT and a prolongation of the BT,9 and a
study of dogs with experimentally induced renal fail-
ure, anemia, and a prolonged BMBT demonstrated
temporal normalization of BMBT after a blood transfu-
sion and a consequent increase in the HCT.10
In people, evaluation of different methods to mea-
sure the cutaneous BT4,11 have shown the influence of
length and depth of the incision,12,13 location, and
direction of the incision,4 and the degree of venosta-
sis.4,5,14 To enhance the reproducibility of the results
and thereby the clinical usefulness of the BT, the
template or standardized BT has been introduced in
people.4 A spring-loaded device is used to make a stan-
dardized skin incision on the ventral aspect of the fore-
arm in an area devoid of large veins and hair. A blood
pressure cuff is applied above the incision and inflated
451
Comparison of bleeding time in dogs using 3 devices
to a constant pressure of 40 mmHg to provide venosta-
sis.4,5 In dogs and cats, cutaneous, toenail, and BMBT
have also been employed to assess primary hemosta-
sis.2,6,15–17 The cutaneous template BT technique used
in people has not been effective to evaluate primary
hemostasis in domestic animals3 because of the wide
variety in skin thickness, hair coat, and depth of subcu-
taneous fat.15 Measuring the BT in dogs after clipping
off a toenail does not differentiate adequately between
primary and secondary hemostasis.18 The BMBT is cur-
rently the preferred method to measure the BT in dogs3
and cats.6 The technique to determine the BMBT in
dogs has been described in detail in the veterinary liter-
ature;2,3,6,15–17 however, standardization of the
method has not been established to the same degree as
in people. Three different-sized lancet devices designed
for human BT assessment and resulting in variable
length and depth of the incision can be used to assess
the BMBT in dogs.
The aim of this study was to compare the BMBT
measured with 3 different-sized human lancet devices
in dogs with varying Plt count and HCT.
Material and Methods
Dogs
Dogs that were presented to the Teaching Hospital of
the National Veterinary School of Toulouse between
June 2009 and July 2010, and November–December
2011 for routine vaccination or for evaluation of vari-
ous diseases were consecutively recruited in this study.
After informed owner consent, dogs were included in
the study if they had a CBC (Sysmex XT2000iV hema-
tology analyzer, Sysmex, Roissy, France) including
HCT (reference interval [RI] 0.37–0.55) and Plt count
(RI 200–500 9 109/L) performed on the day of BMBT
assessment, and if the BMBT was performed with all 3
devices as described below. The Plt count was con-
firmed by evaluation of a blood smear by exclusion of
platelets clumps and rough estimation of the count
(averaging the number of platelets in at least 5 oil-
immersion fields in the monolayer of the smear, and
multiplying this number by 15). Anemia was defined
as a HCT < 0.37 and thrombocytopenia as a Plt count <
200 9 109/L based on the laboratory-specific RIs.
BMBT
The BMBT measurements were performed in con-
scious un-sedated dogs according to a standardized
protocol previously described.15 Briefly, dogs were
restrained in lateral recumbency. The upper lip was
452 Vet Clin Pathol 42/4 (2013) 451–457 ©2013 American Society for Veterinary Clinical Pathology
Aumann et al
everted to expose the buccal mucosa and a strip of
gauze 2 cm in width was tied around the maxilla and
the mandible to hold the lip in place and to cause con-
gestion of the superficial mucosal vessels. The strip of
gauze stayed in place until all 3 successive measure-
ments of the BMBT were completed.
Three different-sized commercially available BT
devices (Surgicutt Adult, Junior and Newborn, Kitvia,
Labarthe-Inard, France) containing a spring-loaded
blade were used. The device was placed against the
buccal mucosa in a horizontal position avoiding large
mucosal vessels. Activation of the trigger mechanism
resulted in a standardized incision with the length and
depth depending on the device used (Adult [A]
5 mm 9 1 mm, Junior [J] 3.5 mm 9 1 mm, New-
born [N] 2.5 mm 9 0.5 mm). Every 5–10 s, blood was
carefully removed with filter paper by blotting 1–
2 mm away from the incision to avoid disruption of
clot formation. The stopwatch was started at the time
of device activation resulting in the initiation of the
incision. It was stopped when blood no longer stained
the filter paper. If the BMBT was longer than 480 s,
the stopwatch was stopped and gauze was applied to
the incision to stop bleeding.
For each dog, the 3 consecutive BMBT measure-
ments were performed by the same operator (MA, VR,
or AD) successively over a period of 10–30 minutes.
Operators varied between different dogs. The order in
which devices A, J, and N were used was randomly
determined (http://www.randomization.com).
Statistical analysis
Statistical analysis was performed using commercial
software (Stata 9.1 software [Statacorp, College Sta-
tion, TX, USA]; Excel [Microsoft France, Les Ulis,
France]; and Analyze-It software Add on for Excel
[Microsoft France]).
An ANOVA was used to compare the BMBT
among the 3 different devices. A logarithmic transfor-
mation was necessary to provide normality and
homogeneity of variance (homoscedasticity) of residu-
als, and both were assessed graphically and by the
Shapiro–Wilk, and the Breusch–Pagan and Cook–
Weisberg tests, respectively. Distribution and residual
were considered as normal and homoscedastic, respec-
tively, when P > .05 for the Shapiro–Wilk and the
Breusch–Pagan/Cook–Weisberg tests. A Bonferroni
correction of the a-value from 0.05 to 0.016 was applied
to compare the different pairs of devices, using 3 paired
t-tests (level of significance P < .016). Spearman corre-
lation coefficients, Bland–Altman Difference plots and
Passing–Bablok equations were also evaluated. The
Aumann et al
Mann–Whitney U-test was used to compare the
BMBT determined with each device between throm-
bocytopenic and nonthrombocytopenic dogs.
Results
Signalments of dogs studied and results of the CBC
Forty-eight dogs were enrolled in the study. Two
dogs were excluded because BMBT measurements
could not be acquired, leaving the results of the
remaining 46 dogs for analysis. There were 20 intact
males and 20 females each, 4 spayed females and 2
castrated males, the age ranged from 0.3 to
15.5 years (median 7.25 years). A total of 24 breeds
were represented, including 9 mixed breeds, 6 Labra-
dor Retrievers, 5 Brittany Spaniels, 3 Rottweilers, 2
Akita Inus, 2 Bernese Mountain Dogs, 2 German
Shepherds, 2 Boxers, and 2 Fox Terriers. Forty-four
dogs suffered from various disorders including infec-
tious (n = 10), respiratory (n = 7), musculoskeletal,
neoplastic, gastrointestinal and urogenital (n = 4
each), reproductive and neurologic (n = 3 each), car-
diovascular and endocrine (n = 2 each), and derma-
tologic (n = 1) diseases.
A CBC was performed in 45 dogs. The HCT ranged
from 0.12 to 0.53 (median 0.41, RI 0.35–0.52) and the
Plt count from 10 to 625 9 109/L (median 251 9 109/
L, RI 200–562 109/L). Sixteen dogs were anemic (range
0.12–0.36, median 0.27) and 16 dogs were thrombocy-
topenic (range 10–198 9 109/L, median 55.5 9 109/
L). Ten dogs had a Plt count < 100 9 109/L, including
8 dogs with a Plt count < 50 9 109/L. Eleven dogs were
diagnosed with both anemia and thrombocytopenia.
Table 1. Comparison of the buccal mucosal bleeding time (BMBT) of all dogs, dogs with and without thrombocytopenia, dogs with and without ane-
mia, and dogs with anemia but without thrombocytopenia, using 3 different-sized lancet devices: A = Adult, J = Junior, N = Newborn.
Number of Dogs
All Dogs
Dogs without
Thrombocytopenia
Dogs with
Thrombocytopenia
Dogs with Anemia
Dogs without Anemia
Dogs with Anemia but
without Thrombocytopenia
The values represent mean [range].
*Significantly shorter than device A, P < 0.016.
†Significantly shorter than device J, P < 0.016.
‡Significantly longer than without thrombocytopenia, P < 0.016.
Vet Clin Pathol 42/4 (2013) 451–457 ©2013 American Society for Veterinary Clinical Pathology
Comparison of bleeding time in dogs using 3 devices
BMBT results
All dogs tolerated the BMBT procedure without chemi-
cal sedation. The median BMBT for all dogs
was 104.5 s (range 45–480 s) with device A, 99.5 s
(range 37–480 s) with device J, and 72.5 s (range 18–
480 s) with device N (Table 1). A total of 12 dogs had a
BMBT above the published upper limit of 210 s, 4 of
which had a BMBT > 210 s with all 3 devices. Two dogs
had a BMBT > 210 s with devices A and J, and 2 dogs
had a BMBT > 210 s with devices A and N (Table 2).
Comparison of BMBT results using the different
devices
The BMBT was significantly shorter using device N
compared with device A (P < .00001) or J (P < .01),
and using device J compared with device A (P < .015,
Figure 1, Table 1). A similar difference was observed
in dogs without thrombocytopenia (P < .01, Table 1).
The correlation of the BMBT results was
moderate-to-good between A and J devices (rho =
0.72, 95% confidence interval [CI] 0.54–0.84,
P < .0001), and weak-to-moderate between A and N
devices (rho = 0.54, CI 0.29–0.72, P < .001) and J
and N devices (rho = 0.49, CI 0.23–0.68, P < .001).
Scatter plots, Passing – Bablok equations as well as
Bland–Altman plots demonstrated that there were
constant and proportional biases between the BMBT
obtained with the different devices (Figure 2). The
BMBT tended to be longer with the A device compared
to the 2 other devices and with the J device compared
to device N. The importance of this bias tended to
increase proportionally as BMBT was prolonged.
BMBT (Seconds)
A J N
45 104.5 [45–480] 99.5* [37–480] 72.5* † [18–480]
,
29 88 [45–267] 86* [43–226] 65*,† [25–266]
16 244‡ [58–480] 188‡ [66–480] 113.5 [44–480]
16 178.5 [45–480] 155 [50–480] 85.5 [18–480]
29 88 [50–480] 86 [37–480] 67 [25–266]
5 90 [45–150] 100 [50–114] 62 [51–71]
453
Comparison of bleeding time in dogs using 3 devices
Table 2. Numbers of dogs with different platelet counts and with pro-
longed buccal mucosal bleeding time (BMBT) using 3 different-sized lan-
cet devices grouped: A = Adult, J = Junior, N = Newborn.
BMBT > 210 Seconds
9
Platelet Count (10 /L) Number of Dogs A J N more superficial than with devices A and J, and the
< 100 9 109/L (n = 10) 8 8 5 6
100 9 109/L ≤ 200 9 109/L (n = 6) 2 1 1 0
≥ 200 9 109/L (n = 29) 2 1 1 1
Figure 1. Comparison of buccal mucosal bleeding times (BMBT) mea-
sured in 45 dogs using 3 different-sized lancet devices: Adult, Junior, and
Newborn. The solid horizontal line indicates the median, the dotted line
indicates the published upper limit of the BMBT,7 * = P < 0.015,
** = P < 0.00001.
Platelet count, HCT, and results of the BMBT
Twenty-nine dogs had a normal Plt count. The BMBT
of 2 of these dogs was increased (Table 2). In one of
these dogs, the BMBT was only increased with the N
device. In the other dog, which was suffering from
bronchitis due to Streptococcus equi, it was increased
with devices A and J. Ten of the 16 thrombocytope-
nic dogs had an increased BMBT with at least one of
the devices (Table 2), with 4 of these dogs having an
increase with all 3 devices. BMBT measurements
obtained in thrombocytopenic dogs were higher than
in nonthrombocytopenic dogs with devices A and J
(P < .016); significance was not reached with device
N (P = .0214, Table 2). Eleven of the 16 anemic dogs
had concurrent thrombocytopenia. Eight of these
dogs had an increased BMBT with at least one
device. None of the 5 dogs with anemia and normal
Plt count had a prolonged BMBT (Table 1).
Discussion
In the current study, the BMBT was shortest with
device N compared with devices A and J, and shorter
454 Vet Clin Pathol 42/4 (2013) 451–457 ©2013 American Society for Veterinary Clinical Pathology
Aumann et al
with device J compared with device A. This confirms
previous reports in people that both length and depth
of the incision influence the length of BT.12,13 In dogs,
the incision resulting from device N is both shorter and
incision obtained with device J is of the same depth as
that of, but shorter than that with, device A.
Two of the 29 dogs with a normal Plt count and
normal HCT had a BMBT > 210 s. Surprisingly, in one
of these dogs, the BMBT was only prolonged with
device N. A technical error was suspected in this case,
but not confirmed. The second dog, with infectious
bronchitis due to S equi, had a prolonged BMBT with
devices A and J. No evidence for hemostatic abnormal-
ities was identified on clinical examination and a diag-
nostic evaluation of primary hemostasis by further
laboratory testing was declined by the owner.
The results of our study confirm previous reports
in people and dogs that the BT is prolonged in the pres-
ence of thrombocytopenia (< 100 9 109/L in people
and < 20 9 109/L in dogs).1,3,8 Specifically, 9 of 16
thrombocytopenic dogs had a prolongation of the
BMBT with the A device and 6 with the J or N device,
respectively. All 8 dogs with a Plt count < 50 9 109/L
had a prolonged BMBT with device A, whereas only 5
and 6 of these highly thrombocytopenic dogs had pro-
longed BMBT with J and N devices, respectively, sug-
gesting that the A device may be better suited to
identify dogs with primary defective hemostasis attrib-
utable to severe thrombocytopenia. One dog with a Plt
count of 77 9 109/L had a normal BMBT with all 3
devices. A direct relationship between the degree of
thrombocytopenia and the degree of prolongation of
the BT was suggested in a study of thrombocytopenic
people;8 however, the results of this study have never
been confirmed.14 It has been shown that the hemostat-
ic effect of platelets does depend not only on the Plt
count but also on platelet size and activation efficacy.14
For instance, people with thrombocytopenia due to
immune-mediated thrombocytopenic purpura may
have normal BTs in spite of severe thrombocytopenia.19
Only 2 of the 6 dogs with a Plt count between 100
and 200 9 109/L had a BMBT > 210 s with one of the
devices (device A or J, respectively). Both of these dogs
were anemic suggesting that the effect of thrombocy-
topenia on the BMBT may be enhanced by concurrent
anemia. Human studies have demonstrated a relation-
ship between a decrease in HCT and a prolongation of
the BT.9 The impairment of primary hemostasis in peo-
ple with anemia may be due to altered distribution of
cells in flowing blood resulting in decreased contact of
platelets with blood vessel walls and decreased release
of ADP by disrupted red blood cells.20,21 In people with
Aumann et al Comparison of bleeding time in dogs using 3 devices

Figure 2. Scatter plots, Passing Bablok equations, and Bland Altman difference plots of buccal mucosal bleeding time (BMBT) measured in 45 dogs,
comparing (A) Adult to Junior devices (A), (B) Adult to Newborn devices and (C) Junior to Newborn lancet devices.

Vet Clin Pathol 42/4 (2013) 451–457 ©2013 American Society for Veterinary Clinical Pathology 455
Comparison of bleeding time in dogs using 3 devices
anemia and uremia, correction of the anemia through
blood transfusions improved the BT even if the Plt
count remained stable.22 In a study of dogs with experi-
mentally induced renal failure, anemia and a prolonged
BMBT, the BMBT normalized temporarily after a blood
transfusion increased the HCT.10 In the current study,
7 of the 16 dogs with anemia had a prolonged BMBT,
but all of these dogs were also thrombocytopenic.
The median BMBT for dogs without thrombocyto-
penia (Device A 88 s, device J 86 s, device N 65 s) was
lower than the mean BMBT published previously
(163 s),15 or (157 s);3 however, in these studies, the
BMBT was measured with a different device (Simplate
II). The Simplate II device makes 2 incisions of 6 mm
length and 1 mm depth, compared to the 5, 3.5, and
2.5 mm length, and 1, 1, and 0.5 mm depth for the A,
J, and N devices, respectively. The correlation between
the BMBT and plasma von Willebrand factor concen-
tration using the Surgicutt device (without specifying
A, J, or N device) was studied in 61 Greyhounds. The
mean and median BMBT were 129.5 s and 130 s,
respectively, but results of normal dogs and dogs with
vWD were not analyzed separately.2
Our study has several limitations. As each dog
served as its own control, potential confounding effects
of signalment and disease states on differences in
BMBT measurements using the different devices were
limited. Thrombocytopenia has been associated with a
prolongation of the BT in people and dogs1,3,8 and ane-
mia with a prolongation of the BT in people.9 Although
our study was designed based on the methods recom-
mended by Jensen and Kjelgaard–Hansen23 and
included 46 patients covering the entire working range
of the method investigated, the number of anemic dogs
was not large enough to assess the influence of anemia
on the BMBT performed with the 3 different devices.
For practical and ethical reasons, the current study
did not assess the repeatability of the method because
this would have required a duplication of the measure-
ments of the BMBT with each device resulting in 6
BMBT measurements in each dog. Intra- and interob-
server variability in BMBT measurements in dogs per-
formed with the lancet device used in our study has
been published previously and the repeatability of the
measurements was low.2 Interobserver variability
could have been eliminated from our study by one and
the same investigator performing all BMBT measure-
ments instead of 3 main, albeit experienced, investiga-
tors (MA, VR, and AD). We also adhered to an
established protocol as the repeatability of the BT has
been said to improve with standardization,2,4 even
though, in people, the beneficial effect of standardiza-
tion of the BT technique has been questioned.11
456 Vet Clin Pathol 42/4 (2013) 451–457 ©2013 American Society for Veterinary Clinical Pathology
Aumann et al
Standardization of the length of the incision is eas-
ier than the depth of the incision. The depth of the inci-
sion does depend not only on the device but also on
the operator pressure applied to the site. In people,
variations in incision depth due to nonstandardization
of operator pressure may influence the BT.24 In the
current study, variations in operator pressure may
have contributed to interobserver variability; how-
ever, it was unlikely to have contributed to intraob-
server variability as BMBT measurements in a
particular dog were performed by the same operator.
Variation in the degree of venostasis may have
influenced the duration of the BMBT in the dogs in our
study. The degree of venostasis has been standardized
in people, but not in animals.7 In people, a cuff pres-
sure of 40 mmHg is applied to the arm where the BT is
performed.4,5 The BT tends to be shorter if venostasis is
not applied.4 Although a strip of gauze was tied around
the muzzle to provide venostasis in the dogs in our
study, the degree of venostasis was difficult to stan-
dardize and may have varied significantly among dogs.
The 3 consecutive BMBT measurements were per-
formed within a period of 10–30 minutes. Even
though the gauze was not adjusted or removed
between the 3 measurements, the degree of venostasis
could have changed during this time period. The order
in which the different devices were used was random-
ized, minimizing the influence of changes in the
degree of venostasis on the comparison of the BMBT.
The number of dogs included in our study was not
large enough to establish reference intervals for BMBT
measurements with the different devices, nor was the
study designed to calculate diagnostic sensitivity and
specificity. Reference intervals for the BMBT using the
lancet device still have to be established.
In conclusion, the results of the current study indi-
cate that the duration of the BMBT in dogs with and
without thrombocytopenia is influenced by the device
used. Determination with the A lancet device results in
a longer BMBT than with J and N devices. Therefore,
for standardized BMBT, the type of device has to be
specified.
Acknowledgments
The authors thank Michelle Ingelbach for technical assis-
tance and Pr Jean Pierre Braun for assisting with the revi-
sion of the manuscript.
Disclosure: The authors have indicated that they have
no affiliations or financial involvement with any organiza-
tion or entity with a financial interest in, or in financial
competition with, the subject matter or materials discussed
in this article.
Aumann et al
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