Standardized capillary refill time and relation to clinical parameters in hospitalized dogs

Abstract

Objective
To assess the relationship between various physical and clinicopathologic parameters and the capillary refill time (CRT) using a standard method; to evaluate the influence of emergency room (ER) versus ICU hospital location on CRT; and to identify latent subgroups among the CRT distribution.

Design
Prospective, observational study.

Setting
University teaching hospital.

Animals
Client‐owned dogs in the ER (n = 40) and ICU (n = 71).

Interventions
The CRT was defined as the duration required for the oral mucosa of the upper lip to return to its original color after blanching for 4 seconds. The CRT was recorded in seconds to the 10ths place by a single observer using an automated recording device.

Measurements and Main Results
Median CRT for all dogs was 1.1 seconds (ER, 1.2 s; ICU, 1.1 s; P = 1.000). The CRT was significantly associated with rectal temperature (P = 0.004), systolic blood pressure (P = 0.028), body weight (P = 0.031), mucous membrane color (P = 0.007), skin turgor (P = 0.039), and acute patient physiologic and laboratory evaluation mentation score (P = 0.019) for all dogs. The CRT was related to a greater number of variables in the ER than in the ICU patient population. In general, the total population of dogs had CRTs belonging to 1 of 2 groups: either ≤1.2 or ≥1.7 seconds. A statistically significant association was found between body weight CRT ≥1.3 seconds (P = 0.02).

Conclusions
A CRT following blanching for 4 seconds may provide insight into the hydration status and hemodynamic stability of canine patients. Further research into its clinical application is warranted.

Full text

Received: 3 May 2019 Revised: 3 November 2019 Accepted: 7 December 2019
DOI: 10.1111/vec.13088
ORIGINAL STUDY
Standardized capillary refill time and relation to clinical
parameters in hospitalized dogs
Nolan V. Chalifoux DVM Carl F. Spielvogel VMD Darko Stefanovski PhD, MS
Deborah C. Silverstein DVM, DACVECC
Department of Clinical Sciences and Advanced
Medicine, University of Pennsylvania School of
Veterinary Medicine, Philadelphia,
Pennsylv ania, USA
Correspondence
Deborah C. Silverstein, Department of Clinical
Studies, School of VeterinaryMedicine, Uni-
versity of Pennsylvania, 3800 Spruce Street,
Philadelphia, PA19104, USA.
Email: dcsilver@vet.upenn.edu
Abstract
Objective: To assess the relationship between various physical and clinicopathologic
parameters and the capillary refill time (CRT) using a standard method; to evaluate the
influence of emergency room (ER) versus ICU hospital location on CRT; and to identify
latent subgroups among the CRT distribution.
Design: Prospective, observational study.
Setting: University teaching hospital.
Animals: Client-owned dogs in the ER (n=40) and ICU (n=71).
Interventions: The CRT was defined as the duration required for the oral mucosa of
the upper lip to return to its original color after blanching for 4 seconds. The CRT was
recorded in seconds to the 10ths place by a single observer using an automated record-
ing device.
Measurements and Main Results: Median CRT for all dogs was 1.1 seconds (ER, 1.2
s; ICU, 1.1 s; P=1.000). The CRT was significantly associated with rectal temperature
(P=0.004), systolic blood pressure (P=0.028), body weight (P=0.031), mucous mem-
brane color (P=0.007), skin turgor (P=0.039), and acute patient physiologic and lab-
oratory evaluation mentation score (P=0.019) for all dogs. The CRT was related to a
greater number of variables in the ER than in the ICU patient population. In general, the
total population of dogs had CRTs belonging to 1 of 2 groups: either ≤1.2 or ≥1.7 sec-
onds. A statistically significant association was found between body weight CRT ≥1.3
seconds (P=0.02).
Conclusions: A CRT following blanching for 4 seconds may provide insight into the
hydration status and hemodynamic stability of canine patients. Further research into
its clinical application is warranted.
KEYWORDS
canine, dehydration, hypovolemia, shock
Abbreviations: APPLE, acute patient physiologic and laboratory evaluation; BE, base excess;CI, confidence interval; CRT, capillary refill time; ER, emergency room; LAE, left atrial enlargement;
OR, odds ratio; SIRS, systemic inflammatory response syndrome; SpO2, arterial blood hemoglobin oxygen saturation bypulse oximetry; TPP, total plasma protein concentration
© Veterinary Emergency and Critical Care Society 2021
JVetEmergCritCare. 2021;31:585–594. wileyonlinelibrary.com/journal/vec 585

586 CHALIFOUX ET AL.
1INTRODUCTION
Capillary refill time (CRT) is broadly defined as the time for color
to return to a capillary bed that has been blanched by the appli-
cation of direct pressure.1Originally rooted in World War II, CRT
was subjectively assessed as “normal,” “definite slowing,” and “very
sluggish” in severely wounded Allied soldiers as part of the initial
assessment of shock.2Decades later, the normal range, optimal pres-
sure application, and anatomic location for CRT are debated,3–15
and numerous confounding factors such as patient3,9,11,12,16
and ambient temperature,3,9,12 lighting conditions,17 gender,3,16
age,3,16 and interobserver variability11,12,17–22 have been identified.
Although CRT has been reported in some instances to correlate with
dehydration7,13,23–27 and hemodynamic measures11,15,24,28–30 in
children and adults, the overall validity and reliability of CRT as a
measure of circulatory status remains controversial throughout the
literature.3,6,10,11,13,14,16,20,21,28,31–39
In cats and dogs, CRT is measured by pressing the oral mucous mem-
branes with a finger, and a 2 seconds upper limit of normal is tradi-
tionally used.1,40–42 Surprisingly, the history of the CRT’s implementa-
tion into small animal medicine is unclear, and there exists a paucity
of evidence-based data investigating the correct methods and clinical
utility of the CRT for use in animals. Veterinary emergency and crit-
ical care medicine relies on the assumption that CRT is representa-
tive of a patient’s cardiovascular status, and traditionally the CRT is
regarded as an indicator of intravascular volume rather than intersti-
tial hydration.1,41–43 However, no studies to date have evaluated the
use of CRT as an indicator of perfusion, hemodynamic, or hydrationsta-
tus in dogs.1Despite a recent report proposing the use of an optical
device for automated CRT measurement in dogs,44 manual assessment
remains the most practical and widely accessible method to perform
CRT. There is a need for clinical and experimental research investigat-
ing this globally accepted physical examination parameter.
The objectives of this study were to quantitatively assess the rela-
tionship of various physical and clinicopathologic parameters of known
hemodynamic relevance to CRT using a standard method; to evaluate
the potential role of hospital location (emergency room [ER] vs. ICU) on
the parameters associated with CRT; and to use finite mixture model-
ing to look for latent populations within the distribution of the CRT. The
goal of the last was to investigate potential reference values for CRT
that may have clinical significance. Based on the mean CRT reported
by Obiorah et al.45 in apparently healthy dogs, potential associations
between hemodynamic variables of interest and a dichotomized vari-
able of a CRT of either <1.3 or ≥1.3 seconds were also investigated.
The authors hypothesized that published physical indicators of hemo-
dynamic stability such as heart rate and blood pressure, in addition to
clinicopathologic indicators such as base excess (BE) and plasma lac-
tate, would be associated with the CRT.
2MATERIALS AND METHODS
This prospective observational study was conducted from March to
December 2017 at the Matthew J. Ryan Veterinary Hospital at the
TAB L E 1 Method used to assess capillary refill time in dogs
∙A single observer was be used.
∙A single location, the inner lip oral mucosa, was used and care was
taken not to restrict mucosal blood flow when everting the lip.
∙A pressing time of 4 seconds was applied to the site with moderate
direct pressure.
∙The use of a stopwatch was used to record the time for color to
return to the capillary bed.
∙Immediate (within 2 min) reassessment was avoided at the same site.
University of Pennsylvania. The University of Pennsylvania’s Institu-
tional Animal Care and Use Committee waived the requirement for
informed owner consent because the study design did not deviate from
conventional standard of care.
2.1 Inclusion criteria
All dogs admitted to the ER and ICU were eligible for enrollment.
Aggressive dogs or those receiving vasopressor therapy were excl-
uded.
2.2 Measurements and recorded data
2.2.1 Intraoral CRT measurement
Intraoral CRT was measured once by a single observer for all patients
and was defined as the duration required for the oral mucosa of the
inner lip to return to original color after blanching for 4 seconds
(Table 1). The upper lip overlying a canine tooth was everted with the
nondominant hand of the observer, using care to not restrict mucosal
blood flow in the process. Subsequently, the index finger of the
observer’s dominant hand applied firm pressure to the oral mucosa of
the inner lip for 4 seconds. The dominant (blanching) hand held a stop-
watch deviceathat counted down to indicate 4 seconds of manually
applied blanching with an audible beep, followed by then automatically
counting up at the end of blanching to measure the CRT. The CRT was
visually assessed and measured to the 100th of a second but recorded
as rounded to the nearest 10th of a second. Examination gloves were
worn by the investigator for all patient interactions. All dogs were in
a climate-controlled environment with an ambient temperature of
22 ±2◦C.
2.2.2 Procedures
At the time of each CRT measurement, the patient’s age, hospital loca-
tion (ER or ICU), time since hospital admission, and reproductive status
were recorded from the medical record. The ER population was com-
posed of both primary first opinion and tertiary referral cases admit-
ted to the hospital for transfer to a specialty service. The ICU pop-
ulation was located in a separate area of the hospital and was com-

CHALIFOUX ET AL.587
posed of critically ill dogs transferred to the ICU for primary case
management, case oversight, and intensive postoperative monitoring
and care. Mucous membrane color (too pale to blanch, pale, normal,
hyperemic), skin turgor (normal, decreased), severity of dental disease
(no dental disease, mild, moderate, severe), body condition (under-
weight, normal, overweight), body weight, rectal temperature, heart
rate, femoral pulse quality and rhythm (synchronous vs pulse deficits),
systolic blood pressure (Dopplerbor oscillometricc), arterial blood
hemoglobin oxygen saturation by pulse oximetry (SpO2), and the pres-
ence or absence of systemic inflammatory response syndrome (SIRS)
(see below) were also recorded at the time of CRT measurement. Due
to the observational nature of the study, left atrial enlargement (LAE),
PCV, total plasma protein concentration (TPP), and blood gas data
were extracted from the medical record at the time point nearest to
CRT measurement (maximum ±5 h) as long as the patient’s cardio-
vascular state at the time of data acquisition was deemed unequivo-
cal. Data from the medical record were not included if any new inter-
ventions expected to affect the dog’s cardiovascular state, such as fluid
therapy, had been implemented between the time of data acquisition
and CRT measurement. When data acquisition was limited by ongo-
ing treatments or an inability to interact with the dog, additional infor-
mation was extracted from treatment sheets provided it was an accu-
rate representation of the patient’s cardiovascular status at the time
of CRT measurement (as previously described). LAE was defined as a
left atrium-to-aortic root ratio >1.546,47 on thoracic ultrasound per-
formed by the attending clinician or definitive LAE reported on thoracic
radiographic study by a board-certified radiologist. PCV and TPP were
assessed following routine centrifugationdand refractometry.e
2.2.3 Blood gas analysis
Arterial or venous blood gas pH, lactate concentration, and extracellu-
lar BE were recorded. Venous blood gas samples were obtained during
placement of a peripheral IV catheter in the ER, whereas the majority
of ICU patients had blood drawn from a centrally placed catheter lumen
or sampling catheter. All arterial blood gas samples were obtained from
the dorsal pedal artery. Two separate analytical machines were used in
the ERfand ICU.g
2.2.4 Acute patient physiologic and laboratory
evaluation mentation score
The previously published mentation score extrapolated from the com-
plete acute patient physiologic and laboratory evaluation (APPLE)
score outlined by Hayes et al.48 was applied to the patient population
at the time of CRT assessment. Dogs were assigned an ordinal score
ranging from 0 to 4, where 0 was defined as normal mentation; 1 was
defined as being able to stand unassisted, responsive but dull; 2 was
defined as only being able to stand when assisted, responsive but dull; 3
was defined as unable to stand, responsive; and 4 was defined as unable
to stand, unresponsive.
2.2.5 SIRS criteria
In order to qualify for SIRS, patients had to meet at least 2 of 4
of the following criteria: (1) body temperature <37.8 or >39.4◦C
(<100.0 or >102.9◦F); (2) heart rate >140/min; (3) respiratory rate
>20/min; and (4) white blood cell count: leukocytosis (>16 ×109/L
[>16 ×103/µL]), leukopenia (<6×109/L [<6×103/µL), or band neu-
trophilia (>3% bands).49,50
2.3 Statistical analysis
Statistical analysis was performed with a commercially available com-
puter program.hContinuous variables were assessed for normality
using the Shapiro–Wilk test. As the majority of the data were nonnor-
mally distributed, descriptive statistics of continuous variables were
reported as median and range. Frequency data were reported as the
count and percentage (%).
Potential associations between CRT and dichotomous (sex, repro-
ductive status, hospital location, LAE, and SIRS status), continuous (age,
weight, time since hospital admission, rectal temperature, heart rate,
systolic blood pressure, SpO2, PCV, TPP, pH, plasma lactate concentra-
tion, and BE), and ordinal (mucous membrane color,mucous membrane
moistness, femoral pulse quality, femoral pulse rhythm, dental disease,
body condition, and APPLE mentation score) variables of interest were
obtained using the Spearman’s rank correlation. All variables show-
ing trend for association (P<0.2) were included in subsequent anal-
ysis. The relationship between select potentially significant variables
and CRT was then quantified using univariate binomial logistic regres-
sion for dichotomous outcomes, linear regression for continuous out-
comes, and ordinal logistic regression for ordinal outcomes. Finally, the
influence of hospital location (ER or ICU) on the associations with CRT
was assessed by repeating variable selection and respective regression
analyses for the separate ER and ICU populations. Results are reported
as the coefficient or odds ratio (OR), 95% confidence interval (CI), and
respective P-value.
Finite mixture modeling was used to evaluate the presence of poten-
tial subgroups of CRTs among the total population of dogs in the study.
Following the identification of latent groups among the total popula-
tion, the continuous CRT variable was categorized and dogs were clas-
sified according to their respective groups. Subsequently, Spearman’s
rank correlation was used to identify potentially significant associa-
tions (P<0.2) between dichotomous, ordinal, and continuous vari-
ables of interest and the categorized CRT groups to determine whether
potential subgroups represented ranges of normal or abnormal CRTs.
Based on the mean CRT reported by Obiorah et al.45 in apparently
healthy dogs, potential associations with the dichotomized variable of
a CRT of either <1.3 or ≥1.3 seconds were also investigated. Univari-
ate ordinal or binomial logistic regression modeling was then used to
determine associations between potentially significant variables and
an ordinal or dichotomous variable defined by cutoff points for latent
groups within the CRT distribution. Significance was set at P<0.05 for
all statistical modeling.

588 CHALIFOUX ET AL.
3RESULTS
A total of 111 cases from the ER (n=40) and ICU (n=71) were included
in the study. Fifty-three (48%) dogs were neutered females, 47 (42%)
dogs were neutered males, 6 (5%) dogs were intact males, and 5 dogs
(5%) were intact females. The median age and body weight of all dogs
was 8.7 years (range, 5.0 mo to 15.9 y) and 17.5 kg (range, 2.9–84 kg),
respectively. Twenty-nine (26%) were classified as mixed breed dogs
and 82 (74%) were classified as purebreds. Notable breeds included 7
(5%) Golden Retrievers, 6 (5%) Labrador Retrievers, and 4 (4%) each of
American Pit Bull terriers, Boxers, and Yorkshire Terriers.
Median time from hospital admission to CRT measurement for all
dogs was 12 hours (range, 0–4.9 d). Dogs in the ER had a median time
since hospital admission of 29 minutes (range, 0–21 h) compared to
20 hours (range, 0–4.9 d) for dogs in the ICU. There was no significant
association between the time since hospital admission at CRT assess-
ment and the CRT in any population of dogs.
Physical examination and clinicopathologic data are summarized in
Table 2. Median CRT of all dogs was 1.1 seconds and ranged from unde-
tectable to 5.6 seconds. Median rectal temperature of all dogs was
38.2◦C and ranged from 33.9 to 40.8◦C (93.0 to 105.4
◦F). Seven (6%)
dogs had a temperature >39.4◦C(>102.9◦F) and 29 (26%) dogs had a
temperature <37.8◦C(<100.0◦F).
No potentially significant associations between the CRT of all
dogs and dichotomous variables of interest (sex, reproductive sta-
tus, hospital location, LAE, SIRS status) were identified following
exploratory statistical analysis. However, Spearman’s correlation anal-
ysis revealed multiple continuous and ordinal factors potentially asso-
ciated with CRT. Subsequent linear and ordinal logistic regression mod-
eling revealed that rectal temperature (P=0.004), systolic blood pres-
sure (P=0.028), body weight (P=0.031), mucous membrane color
(P=0.007), skin turgor (P=0.039), and APPLE mentation score
(P=0.019) were significantly associated with CRT for all dogs. No sta-
tistically significant associations were identified between CRT of all
dogs and the severity of dental disease, body condition, heart rate,
femoral pulse quality and rhythm, SpO2, PCV, TP, pH, plasma lactate
concentration, or extracellular BE. The coefficients, OR, P-values, 95%
CI, pseudo-R2values, and number of dogs (n)withcontributingdatafor
significant associations of linear and ordinal logistic regressions for all
dogs are listed in Table 3.ACRTincreaseof1secondwascorrelated
with a decrease in rectal temperature of 0.32◦C (0.58
◦F; 95% CI, –0.53
to –0.10◦C [–0.95 to –0.18
◦F]), a decrease in systolic blood pressure of
8.5 mm Hg (95% CI, –16.1 to –1.0 mm Hg), and a decrease in weight
of 3.56 kg (95% CI, –6.78 to –0.33 kg). In addition, a CRT increase of
1secondwascorrelatedwitha1.82greateroddsofthedoghaving
more pronounced mucous membrane pallor (95% CI, 1.18–2.86), 1.77
greater odds of having delayed skin turgor (95% CI, 1.03–3.04), and
1.68 greater odds of having an increased (i.e., poorer) mentation score
(95% CI, 1.09–2.61).
When adjusted for hospital location (ER or ICU) via subgroup analy-
sis, CRT among the ER population of dogs (n=40) was associated with
body weight (coefficient =–4.99; 95% CI, –9.48 to –0.49; P=0.03), TPP
TAB L E 2 Physical examination and clinicopathologic parameters
of dogs in the emergency room (ER; n=40), ICU (n=71), and
combined ER and ICU (n=111) at the time of capillary refill time
measurement
ER ICU
ER and
ICU
Capillary refill time (s)
Median 1.2 1.1 1.1
Range 0.1–4.1 0–5.6 0–5.6
Not recorded 0 0 0
Rectal temperature (◦C)
Median 38.7 37.9 38.2
Range 34.6–40.8 33.9–40.4 33.9–40.8
Not recorded 6 8 14
Heart rate (per min)
Median 130 112 119
Range 68–180 45–260 45–260
Not recorded 3 2 5
Systolic blood pressure (mm Hg)
Median 144 141 144
Range 85–200 60–290 60–290
Not recorded 21 10 31
Left atrial enlargementa
Present 5 8 13
Absent 4 19 23
Not recorded 31 44 75
SpO2(%)
Median 96 97 96
Range 88–99 87–100 87–100
Not recorded 31 637
Mucous membrane color
Too pal e (%) 0(0) 0(0) 0(0)
Pale (%) 7 (18) 7 (10) 14 (13)
Normal (%) 27 (68) 47 (67) 74 (67)
Hyperemic (%) 6 (15) 16 (23) 22 (20)
Not recorded 0 1 1
Skin turgor
Normal (%) 21 (64) 62 (91) 83 (82)
Decreased (%) 12 (36) 6 (9) 18 (18)
Not recorded 7 3 10
Femoral pulse quality
Weak (%) 6 (18) 7 (12) 13 (14)
Fair (%) 6 (18) 10 (17) 16 (17)
Normal (%) 20 (61) 39 (66) 59 (64)
Bounding (%) 1 (3) 3 (5) 4 (4)
Not recorded 712 19
(Continues)

CHALIFOUX ET AL.589
TAB L E 2 (Continued)
ER ICU
ER and
ICU
Mucous membrane moistness
Dry (%) 14 (40) 24 (35) 38 (37)
Moist (%) 19 (54) 41 (59) 60 (58)
Ptyalism (%) 2(6) 4(6) 6(6)
Not recorded 5 2 7
Dental disease
None (%) 4 (12) 6 (9) 10 (10)
Mild (%) 10 (30) 24 (37) 34 (35)
Moderate (%) 10 (30) 20 (31) 30 (31)
Severe (%) 9 (27) 15 (23) 24 (25)
Not recorded 7 6 13
Body condition
Underweight (%) 6 (17) 5 (8) 11 (11)
Normal (%) 19 (54) 31 (47) 50 (50)
Overweight (%) 10 (29) 30 (46) 40 (40)
Not recorded 5 5 10
APPLE mentation score
0(%) 31 (82) 54 (77) 85 (79)
1(%) 3(8) 6(9) 9(8)
2(%) 1(3) 3(4) 4(4)
3(%) 2(5) 6(9) 8(7)
4(%) 1(3) 1(1) 2(2)
Not recorded 2 1 3
SIRS status
Does not meet SIRS criteria (%) 3 (13) 13 (22) 16 (20)
Meets SIRS criteria (%) 20 (87) 46 (78) 66 (81)
Not recorded 17 12 29
PCV (%)
Median 44 38 40
Range 25–72 21–56 21–56
Not recorded 12 23 35
Total plasma protein (g/L) (g/dL)
Median 71 (7.1) 58 (5.8) 62 (6.2)
Range 32–98
(3.2–
9.8)
36–86
(3.6–
8.6)
32–98
(3.2–
9.8)
Not recorded 12 23 35
pH
Median 7.4 7.4 7.4
Range 7.2–7.5 7.2–7.5 7.2–7.5
Decreased (%) 3 (13) 12 (35) 15 (26)
Normal (%) 19 (79) 19 (56) 38 (66)
Increased (%) 2 (8) 3 (9) 5 (9)
Not recorded 16 45 61
(Continues)
TAB L E 2 (Continued)
ER ICU
ER and
ICU
Plasma lactate concentration (mmol/L) (mg/dL)
Median 2.1 (18.9) 1.2(10.8) 1.5 (13.5)
Range 0.8–4.8
(7.2–
43.2)
0.25–8.0
(2.3–
72.1)
0.25–8.0
(2.3–
72.1)
Decreased (%) 0(0) 0(0) 0(0)
Normal (%) 12 (50) 31 (84) 43 (71)
Increased (%) 12 (50) 6 (16) 18 (30)
Not recorded 16 34 50
Base excess (mmol/L) (mEq/L)
Median –5.5 –2.2 –4.3
Range –15.3 to
6.0
–13.8 to
6.1
–15.3 to
6.1
Decreased (%) 15 (63) 15 (44) 30 (52)
Normal (%) 8 (33) 18 (53) 26 (45)
Increased (%) 1 (4) 1 (3) 2 (3)
Not recorded 16 37 53
Abbreviations: APPLE, acute patient physiologic and laboratory evalua-
tion; SIRS, systemic inflammatory response syndrome; SpO2, arterial blood
hemoglobin oxygen saturation by pulse oximetry.
aLeft atrial-to-aortic root ratio >1.5 on thoracic ultrasound,or definitive left
atrial enlargement present on thoracic radiographs.
(coefficient =0.71; 95% CI, 0.31–1.10; P=0.001), systolic blood pres-
sure (coefficient =–12.70; 95% CI, –24.3 to –1.08; P=0.033), fluid
therapy (OR =0.04; 95% CI, 0.01–0.22; P<0.001), LAE (OR =5.12;
95% CI, 1.30–20.06; P=0.019), skin turgor (OR =4.03; 95% CI, 1.69–
9.57; P=0.002), and body condition (OR =0.53; 95% CI, 0.28–
1.00; P=0.005) on binomial and ordinal logistic regression and linear
regression analyses. Comparatively, CRT among the ICU population
of dogs (n=71) was significantly associated with rectal temperature
(coefficient =–0.70; 95% CI, –1.07 to –0.33; P<0.001), mucous mem-
brane color (OR =0.54; 95% CI, 0.35–0.85; P=0.007), and APPLE
mentation score (OR =1.69; 95% CI, 1.08–2.65; P=0.023) on lin-
ear and ordinal logistic regression. The significant association between
CRT and TPP, LAE, and body condition was only present among the ER
subgroup, whereas all significant associations among the ICU subgroup
(rectal temperature, mucous membrane color, and APPLE mentation
score) were also identified in the total population, regardless of loca-
tion.
Finite mixture modeling was able to identify 2 latent groups within
the distribution of the CRT. The 95% CI for each group was 1.0–1.2
seconds and 1.7–3.4 seconds, representing 2 separate distributions of
canine CRTs. No additional latent groups were identified. The CRT was
then dichotomized into the variable of a CRT <or ≥1.7 seconds in order
to evaluate whether a cutoff value of 1.7 seconds may represent the
upper limit of a normal CRT in dogs. Spearman’s correlation analysis
determined that femoral pulse quality,LAE, body weight, and TPP were
potentially associated (i.e., with the criterion of alpha <0.2) with the

590 CHALIFOUX ET AL.
TAB L E 3 Linear and ordinal logistic regression correlation coefficients, odds ratios, 95% confidence intervals, R2values, pseudo-R2values,
number of observations, and P-values for significant associations identified between the capillary refill time and select variables of interest for all
dogs in the combined emergency room and ICU (n=111)
Linear regression Coefficient 95% CI R2nP-value
Rectal temperature (◦C) –0.32 –0.53 to 0.10 0.083 97 0.004
Systolic blood pressure –8.53 –16.09 to 0.97 0.061 80 0.028
Body weight –3.56 –6.78 to 0.33 0.042 110 0.031
Ordinal logistic regression OR 95% CI Pseudo-R2n P-value
Mucous membrane color 0.54 0.35–0.85 0.040 110 0.007
Skin turgor 1.77 1.03–3.04 0.046 101 0.039
APPLE mentation score 1.68 1.09–2.61 0.031 108 0.019
Abbreviations: APPLE, acute patient physiologic and laboratory evaluation; CI, confidence interval; n,numberofobservations;OR,oddsratio.
dichotomous variable of a CRT <or ≥1.7 seconds. However, subse-
quent logistic regression modeling failed to reveal any significant asso-
ciations between the highlighted variables and a dichotomous CRT cut-
off of 1.7 seconds.
Spearman’s correlation analysis determined that femoral pulse
quality, LAE, body weight, body condition, and TP were potentially
associated with the dichotomous variable of a CRT <or ≥1.3 seconds.
Logistic regression modeling revealed a significant though weak associ-
ation between increases in body weight and lower odds of a CRT ≥1.3
seconds (OR =0.97; 95% CI, 0.94–0.99; P=0.02; pseudo-R2=0.043).
No further variables were significantly associated with a dichotomous
CRT cutoff of 1.3 seconds.
4DISCUSSION
To the authors’ knowledge, this is the first veterinary study to quantita-
tively assess the relationship of various physical and clinicopathologic
parameters of known hemodynamic relevance to CRT using a stan-
dard method. Numerous studies in the human medical field have identi-
fied various confounders that have the potential to hinder the reliabil-
ity of CRT measurement. As CRT has been shown to have poor inter-
observer agreement11,12,17–22 and to minimize variation in determi-
nation of CRT, a single observer was designated for evaluation of the
CRT in this study. Strozik et al.5showed that CRT in newborns var-
ied significantly when pressing times less than 3 seconds were applied,
whereas no significant difference in CRT values was found for pressing
times of 3–7 seconds. A later study determined that CRT was signif-
icantly shorter when a brief cutaneous pressing time of 1–2 seconds
was applied compared to an extended pressing time of 3–4 seconds
in neonates.14 As the majority of prospective studies and guidelines in
human medicine use an extended pressing time for the assessment of
CRT,3,4,6–9,11,12,15,16,18,19,21,28,35,37,51,52 the authors chose 4 seconds in
this study to minimize error associated with minor fluctuations in pres-
sure application time and to maximize efficiency for clinical application.
Furthermore, CRT variability has been associated with different mea-
surement sites.46,9,11,15 The oral mucosa of the inner lip was selected
as the site of CRT assessment in this study as it is a common and
easily assessable site in dogs. Although the gingival mucosa has been
used in previous canine studies,45,53 the authors opted against its use
for standardization as inflammatory changes may accompany severe
gingivitis and alter focal CRT measurements. Lack of a stopwatch to
quantify CRT measurement has been shown to impair reliability,27 and
repeated measurements at the same site have been shown to result
in significantly shorter CRTs on repeat evaluations.3,9 The latter may
be attributed to capillary bed vasodilation secondary to warming of
the site from repeated contact,9or a persistent increase in hydrostatic
pressure among the precapillary blood vessels.
Despite its universal application, CRT measurement still lacks a
standardized method of assessment in veterinary medicine. Consid-
ering the findings of our study and the relevant human literature, the
method used to assess CRT in the current study (Table 1) may serve as
abaselineforfutureresearchinvestigatingthepotentialuseofCRTas
a diagnostic and prognostic tool in veterinary medicine. Furthermore,
the authors caution the validity of comparing a CRT obtained from dif-
ferent locations and by different observers. One should avoid immedi-
ately (within 2 min) repeating CRT assessment at the same site as refill
times may be falsely shortened on subsequent evaluations.3,9
CRT appears to provide reliable information in the assessment of
interstitial dehydration in children.7,13,23–27 Although this relationship
has not been recognized among adults,13,30,37 a prolonged CRT has
been highlighted as one of the most useful signs for predicting ≥5%
dehydration in human pediatrics.25 Although a recent study was unable
to identify the CRT as a significant predictor of mild dehydration (<5%)
in healthy exercising dogs,53 our study found that the CRT of dogs in
the ER and ICU was significantly associated with delayed skin turgor, a
possible indication of interstitial dehydration.42 A significant positive
association was also identified between CRT and TPP among the ER
population of dogs. TPPs commonly increase with hemoconcentration
secondary to body fluid deficits,1although other causes are possible.
The results of our study suggest that CRT may serve as a more reli-
able indicator of interstitial dehydration than traditionallybelieved, but
requires further investigation.1,41–43
Although the relationship between body weight and resting heart
rate remains controversial in veterinary medicine,54–59 dogs with a
lower body weight were noted to have significantly longer CRTs in

CHALIFOUX ET AL.591
this study. This finding may represent an impairment in the ability of
smaller dogs with a higher resting heart rate to manifest compensatory
tachycardia in order to maintain adequate cardiac output in the face of
shock. However, due to recent data contesting the existence of a clini-
cally relevant correlation between basal heart rate and body weight in
dogs,54,56,57 this association may alternatively reflect a state of greater
tendency toward dehydration in dogs of lower body weight, or an inde-
pendent physiological relationship. As various breeds, ages, and body
conditions of dogs were included in this study, the authors caution
interpretation of this association. Additionally, although finite mixture
modeling and subsequent logistic regression found a significant weak
association between increases in body weight and lower odds of a
CRT ≥1.3 seconds, the OR was very close to 1 (OR =0.97). Conse-
quently, the authors caution against extrapolation of this finding.
A significant negative correlation between patient temperature and
CRT has been previously shown in people of various ages,3,9,11,12,16
similar to the findings of our study. As a dog’s temperature decreased,
asignificantincreaseintheCRTwasobserved.Thiseffectisthought
to be mediated by vasodilatory and vasoconstrictive responses to an
increase60 or decrease61 in body temperature, respectively. Potential
confounders such as illness severity may also be a driving force of this
association, as critical dogs with longer CRTs may have concurrently
had lower body temperatures. Interestingly,Gorelick et al.52 found that
the presence of fever in children had no clinically relevant impact on
CRT. These authors discuss the consistency of their findings with phys-
iologic data demonstrating that baroreceptor-driven vasoconstriction
predominates over vasodilation mediated by temperature changes in
the face of shock.52,62 Although the incidence of shock in Gorelick’s
study population was not reported, 34% of patients were noted to have
a fluid deficit of at least 5%, and 4.7% had a fluid deficit of 10% or
more.52 If a patient with an elevated body temperature goes into shock,
peripheral vasoconstriction may result in a prolonged CRT despite
simultaneous pyrexia. Only 6% of dogs in our study had a rectal temper-
ature >39.4◦C, compared to 26% with a rectal temperature <37.8◦C.
The low incidence of pyrexia in our study likely limited the prevalence
of shock and hyperthermia occurring simultaneously, thus allowing an
association between elevations in body temperature and a shortened
CRT to be recognized. Based on these findings, the effect of body tem-
perature on a patient’s CRT should still be considered when making
clinical assessments in dogs, particularly with regard to hypothermic
patients.
Finally, subgroup analysis to account for differences between the
ER and ICU populations of dogs revealed that CRT was significantly
associated with multiple variables in the ER population that were not
identified in the ICU or total dog populations. Positive associations
were noted between the CRT and TPP, and the presence of LAE.
These additional associations identified in the ER population are
likely related to data retrieval from a subgroup of dogs with a greater
range of fluid deficits and hemodynamic derangements because CRT
measurement occurred at the time of triage in most of these cases.
Many ER patients had yet to be fully stabilized at the time of CRT
assessment, as evidenced by the lower incidence of fluid therapy in the
ER (8%) compared to the ICU (75%). A negative association was noted
between the CRT and body condition in that increases in CRT were
associated with greater odds of having a lower body condition (thinner
dogs tended to have longer CRT). Although the underlying mechanism
of this potential association is unknown, it may suggest that peripheral
vasoconstriction is more readily appreciated by observers in dogs with
less body fat. Alternatively, this finding may be attributed to a greater
volume deficit in dogs with lower body condition, as animals with less
fat have greater maintenance volume requirements per kilogram of
body weight. Although this subgroup may be more representative of
dogs presenting to an emergency facility, these findings are drawn
from a relatively small number of patients (n=41); thus, the authors
caution against extrapolation of these associations. Differences in
precision between the 2 blood gas analyzers in the ER and ICU were
also accounted for by evaluating the potential role of hospital location
(ER or ICU) on the statistical associations with CRT; however, no
differences were noted among the blood gas variables. Regardless,
results of the current study are limited by lack of a standardized
sampling site, collection method, and the use of multiple blood gas
analyzers.
Irrespective of the relationship between the CRT and the global
cardiovascular status, peripheral perfusion alterations have been
shown to be a significant prognostic indicator in various disease
states.24,27,30–32,35,63–85 Numerous studies have suggested that the
prognostic value of peripheral perfusion surpasses that of sys-
temic hemodynamics,35,64,77,81,83 with multivariate analysis frequently
highlighting the independent role of peripheral perfusion in out-
come prediction.67–69,75,77,83,85 The importance of CRT in gen-
eral prognostication appears the strongest among human pediatric
patients,8,24,64–68,74,78,79,86 though it has also been shown to play a cru-
cial role in the identification and management of septic shock in both
pediatric67,4 and adult30,51,63,73,76,77,80–83 populations. Although the
utility of assessing CRT to predict outcome in dogs was beyond the
scope of this study, the human literature is highly encouraging in cer-
tain disease states using cutaneous derived CRT. Future studies are
needed in veterinary medicine to evaluate the potential prognostic
value of standardized CRT.
This study has limitations. Although the majority of the data were
prospectively obtained at the time of CRT measurement, certain data
points were extracted from the medical record and treatment sheets
at the time point closest to CRT measurement. Despite careful review
of the medical records and consultation with clinicians and staff, it
is possible that certain data points may not have been an accurate
representation of the patient’s cardiovascular state at the time of CRT
measurement. Although this may have predisposed the study to type
II errors, the authors suspect that a type I error would be unlikely to
occur with this design limitation. As a result, the statistically significant
associations found in this study are likely clinically valid, although
additional associations may exist that were not identified. However,
the temporal gap between some data points and CRT measurement
remains a limitation. Furthermore, patients were not provided a
defined acclimation period following admission to the ER or ICU, nor
was sedation or anxiety level assessed at the time of CRT measure-
ment. Due to the observational nature of the study, the investigation

592 CHALIFOUX ET AL.
of certain variables was also limited by the low number of dogs with
available data.
As all dogs included in the study were located in the ER or ICU, no
healthy control group was used for comparison. Although finite mix-
ture modeling identified 2 latent groups of dogs within the distribu-
tion of the CRT, no clinically relevant or statistically significant asso-
ciations were found between the investigated cutoff values of either
1.3 or 1.7 seconds and any variable of interest. Therefore, the rele-
vance of a potential cutoff value existing between 1.2 and 1.7 seconds is
unknown and does not necessarily represent a clinical cutoff between
healthy and diseased dogs, but rather a distinction between 2 distri-
butions of CRTs among dogs with varied disease processes in the ER
and ICU. The lack of a normal control population may have limited the
study’s ability to identify a clinically useful cut-off value. Due to the
observational nature of the study, data collection was prohibited in
some critical cases due to patient instability. Failure to include a ran-
domized proportion of all cases at the veterinary hospital may have
resulted in a bias toward more stable dogs, and consequently shorter
CRTs. Additionally, the exclusion of aggressive dogs may have excluded
painful dogs, which may have been sicker. The observer performing the
CRT measurement was not blind to the data collection, which may have
introduced bias. Although the use of 1 single observer was chosen to
avoid interobserver variability in the CRT, this resulted in CRT assess-
ment occurring at various stages of presentation due to the logistics
of data collection. Because data were not all obtained upon triage in
the ER and admission in the ICU, the variability associated with these
different stages of presentation may have affected the study’s results.
Additionally, the clinical application of a single observer to assess and
trend CRT may not be feasible in all settings.
As continuous blood gas data were compiled from 2 separate ana-
lytic machines in the ER and ICU, there is an inherent discrepancy asso-
ciated with its analysis. However, no significant associations between
blood gas variables and the CRT were identified in the compiled data,
and subgroup analysis was used to confirm this finding within the sepa-
rate ER and ICU populations. One set of reference intervals from the
hospital was applied to all clinicopathologic data. Lack of individual
machine-derived reference intervals may have increased the margin of
error associated with the results. Additionally, as venous blood sam-
ples were obtained during placement of a peripheral IV catheter in the
ER and the majority of ICU patients had blood drawn from a centrally
placed catheter or sampling line, acid–base assessment may have been
limited by the compilation of data from both central and peripheral
sites.87
It is also important to note that although skin turgor is an estimate
of hydration status, it may be affected by any change in skin elasticity,
which may have confounded the results of this study. Finally, as pub-
lished body condition scales were not used, the reliability and statisti-
cal assessment of this parameter was also limited. Despite these limi-
tations, our study highlights the value of CRT assessment as part of the
physical examination in veterinary medicine and serves as a baseline
reference for the standardization of CRT in dogs.
5CONCLUSION
CRT assessment is widespread throughout veterinary medicine
despite lack of clear evidence regarding its use. A standard and reliable
approach to CRT assessment using a single observer, a single location,
apressingtimeof4seconds,andarecordingdevicewasusedinthis
study. The inner lip oral mucosa serves as an easily accessible loca-
tion for assessment in dogs. This study has identified an association
between the CRT and rectal temperature, systolic blood pressure,
body weight, mucous membrane color, skin turgor, and APPLE menta-
tion score in dogs. Based on these results, the CRT may provide insight
into the hydration status and hemodynamic stability of canine patients.
Nonetheless, it is important to consider potential confounders of the
CRT such as ambient and patient temperature. As the human literature
suggests, CRT may play a role in outcome prediction in veterinary
medicine. Further interventional research is needed to evaluate the
normal range of CRT in healthy dogs, to determine both the intra-
and interobserver variability associated with CRT measurement in
veterinary medicine, and to investigate the clinical use of CRT as a
prognostic indicator, particularly in the areas of critical illness and
septic shock.
CONFLICT OF INTEREST
The authors declare no conflict of interest.
ORCID
Nolan V. Chalifoux DVM https://orcid.org/0000-0002-8666-4443
Deborah C. Silverstein DVM, DACVECC https://orcid.org/0000-0001-
6948-4494
ENDNOTES
aOslo Silver 2.0 Twin Stopwatch and Countdown Timer, Marshall-
Browning International Corporation, Hilton Head Island, SC.
bUltrasonic Doppler Flow Detector, Parks Medical Electronics, Inc., Aloha,
OR.
cCardell 9402 Veterinary Monitor, Midmark, Tampa, FL.
dHERAEUS Pico 17 Centrifuge, ThermoFisher SCIENTIFIC, Langensel-
bold, Germany.
eJorVet J-0351 Refractometer, Jorgensen Labs, Loveland, CO.
fStat Profile pHOx Ultra, NOVA Biomedical, Waltham, MA.
gRAPIDPoint 500, Siemens, Munich, Germany.
hSTATA SE, version 14.2, StataCorp LLC,College Station, TX.
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SUPPORTING INFORMATION
Additional supporting information may be found online in the Support-
ing Information section at the end of the article.
How to cite this article: Chalifoux NV, Spielvogel CF,
Stefanovski D, Silverstein DC. Standardized capillary refill time
and relation to clinical parameters in hospitalized dogs. JVet
Emerg Crit Care. 2021;31:585–594.
https://doi.org/10.1111/vec.13088