Capillary refill time: is it still a useful clinical sign?
- PubMed: 21519051
Abstract
Capillary refill time (CRT) is widely used by health care workers as part of the rapid, structured cardiopulmonary assessment of critically ill patients. Measurement involves the visual inspection of blood returning to distal capillaries after they have been emptied by pressure. It is hypothesized that CRT is a simple measure of alterations in peripheral perfusion. Evidence for the use of CRT in anesthesia is lacking and further research is required, but understanding may be gained from evidence in other fields. In this report, we examine this evidence and factors affecting CRT measurement. Novel approaches to the assessment of CRT are under investigation. In the future, CRT measurement may be achieved using new technologies such as digital videography or modified oxygen saturation probes; these new methods would remove the limitations associated with clinical CRT measurement and may even be able to provide an automated CRT measurement.
Capillary refill time: is it still a useful clinical sign?
Capillary Refill Time: Is It Still a Useful Clinical Sign?
Amelia Pickard, MbChB, FRCA,*‡ Walter Karlen, PhD, MSc,†
and J. Mark Ansermino, MBBCh, MSc (INF), FRCPC*‡
Capillary refill time (CRT) is widely used by health care workers as part of the rapid,
structured cardiopulmonary assessment of critically ill patients. Measurement involves the
visual inspection of blood returning to distal capillaries after they have been emptied by
pressure. It is hypothesized that CRT is a simple measure of alterations in peripheral
perfusion. Evidence for the use of CRT in anesthesia is lacking and further research is
required, but understanding may be gained from evidence in other fields. In this report, we
examine this evidence and factors affecting CRT measurement. Novel approaches to the
assessment of CRT are under investigation. In the future, CRT measurement may be achieved
using new technologies such as digital videography or modified oxygen saturation probes;
these new methods would remove the limitations associated with clinical CRT measurement
and may even be able to provide an automated CRT measurement. (Anesth Analg 2011;113:
120–3)
Capillary refill time (CRT) is defined as the timetaken for a distal capillary bed to regain its colorafter pressure has been applied to cause blanching.
It was first introduced by Beecher et al.1 in 1947 using the
categories normal, definite slowing, and very sluggish.
These were correlated with the presence and severity of
shock. In 1980, Champion included CRT measurement in
his trauma score2 and it was subsequently endorsed by
the American College of Surgeons. CRT has become
widely used in adults and children and has been incor-
porated into advanced life support guidelines as part of
the rapid, structured cardiopulmonary assessment of
critically ill patients.3
The upper limit of normal for CRT was defined as 2
seconds, based on the observations of a member of the
clinical staff working with Dr. Champion.4 Over the past 30
years, this definition, the factors affecting CRT, and the
validity of CRT measurements have been debated in the
literature.
Measurement of CRT involves the visual inspection of
blood returning to distal capillaries after they have been
emptied by pressure application. The physiological prin-
ciples of peripheral perfusion are complex. How well a
distal capillary bed is perfused depends on a number of
factors; the main determinants are capillary blood flow (a
product of the driving pressure, arteriolar tone, and
hemorheology) and capillary patency (reflected by the
functional capillary density, the number of capillaries in a
given area that are filled with flowing red blood cells).
Arteriolar tone depends on a fine balance between vaso-
constrictive (norepinephrine, angiotensin II, vasopressin,
endothelin I, and thromboxane A2) and vasodilatory (pros-
tacyclin, nitric oxide, and products of local metabolism
such as adenosine) influences, which together regulate
capillary perfusion depending on the metabolic require-
ments of the tissue cells.5 It is hypothesized that alterations
in distal capillary bed perfusion will affect the measure-
ment of CRT by altering the time for the distal capillaries to
become refilled with blood. It is important to note that there
are no current publications directly supporting this theory.
In this article, we focus on the potential use of CRT
measurement in anesthesia although evidence for this
specifically is lacking. A number of published studies have
determined the factors that affect CRT measurement and
these are summarized. Furthermore, we examine some of
the methods for automated measurement of CRT.
FACTORS AFFECTING CRT MEASUREMENT
The nature of the clinical CRT measurement makes it
susceptible to errors. Various factors may have a significant
impact on the results obtained and are rarely considered by
health care workers.6
Age
Age affects CRT measurement. The upper limit of normal
for CRT in neonates was found to be 3 seconds irrespective
of sex, gestation, weight, size for gestational age, nursery
containers, or phototherapy.7 In children, an upper limit of
normal of 2 seconds has been reported.8–10 Studies in
adults have found a wider variation,11 with an average
increase of 3.3% per decade of age.12 One study found a
median CRT for the pediatric population (up to 12 years
old) of 0.8 second; for adult men, 1.0 second; adult women,
1.2 seconds; and in those older than 62 years, 1.5 seconds.9
This study concluded that if 95% of all normal patients are
to be contained within the normal range then the upper
limit of normal for adult women should be increased to 2.9
seconds and for the elderly to 4.5 seconds.
Temperature
Ambient, skin, and core temperature affect CRT measure-
ment. The CRT of healthy children in a warm environment
(mean 25.7°C) was 2 seconds but only 31% had a similar
measurement in a cold environment (mean 19.4°C).10 The
From the Departments of *Anesthesiology, Pharmacology and Therapeutics,
and †Electrical and Computer Engineering, University of British Columbia,
and ‡Department of Anesthesia, BC Children’s Hospital, Vancouver, British
Columbia, Canada.
Accepted for publication February 4, 2011.
The authors declare no conflicts of interest.
Reprints will not be available from the authors.
Address correspondence to Amelia Pickard, MbChB, FRCA, Department of
Anesthesia, BC Children’s Hospital, 1L7 4480 Oak St., Vancouver, BC
Canada V6H 3V4. Address e-mail to ameliapickard@googlemail.com.
Copyright © 2011 International Anesthesia Research Society
DOI: 10.1213/ANE.0b013e31821569f9
120 www.anesthesia-analgesia.org July 2011 • Volume 113 • Number 1
under radiant heaters.7 Similar findings have been seen in
adults; CRT decreased by 1.2% per degree Celsius increase
in ambient temperature.12 Local skin temperature affects
CRT in both adults and children. In adults, the immersion
of a hand into cold water at 14°C prolonged CRT.9 Finger-
tip skin temperature varied with the ambient temperature
and each 1°C reduction in skin temperature was accompa-
nied by a 0.21 second increase in CRT.10 Furthermore, a
statistically significant relationship was found between
CRT and core temperature; CRT was on average 5% shorter
for each 1°C increase in tympanic temperature.12 These
relationships also exist for newborns whose CRT decreased
as ambient, skin, and axillary temperature increased.13
Ambient Light
Poor light conditions make it difficult to assess CRT. In
daylight conditions (partly cloudy day, approximately 4000
lux), CRT was reported as normal in 94.2% of healthy
participants compared with only 31.7% of the same partici-
pants in dark conditions (moonlight or street lamp, ap-
proximately 3 lux).14
Pressure Application
There is no universal agreement on the optimal duration
and amount of pressure or site used when assessing CRT.
Applying moderate pressure for 3 seconds,15 5 sec-
onds,9,10,13,14 or until the capillary bed blanches16 has been
suggested. Pressure applied for 3 seconds gives a shorter
CRT; no difference was found with pressure applied for 3
to 7 seconds.17 Application of light pressure (the minimal
pressure to cause blanching) resulted in shorter CRT than
moderate pressure and with less variability.8 CRT measure-
ment at different sites of the body will produce different
results. CRT measurements in newborns from the midpoint
of the forehead and chest are more consistent than mea-
surements from the heel or palm.7 CRT measured at the
heel can be significantly longer than in the finger.8,10 In
newborns, especially premature babies, testing the pulp of
the finger is more difficult compared with using the fore-
head or chest where movement is less likely to interfere
with the testing. The World Health Organization advocates
using the nail of the thumb or big toe15; other studies
suggest using the soft tissue at the kneecap or forearm
level.18 A survey of pediatric health care workers found
that approximately two-thirds perform CRT on the chest
with only one-third using the pulp of the distal phalanx of
the finger.6 This finding is at odds with studies, which
mainly use the distal phalanx.8,10,12,19
Intra- and Interobserver Reliability
Poor interobserver reliability is a major limitation to the use
of the test. The interobserver reliability of CRT measure-
ment (using a standardized method to assess the CRT,
without a timing device, to a resolution of half a second) on
clinically stable adult patients in the emergency depart-
ment showed a mean difference in CRT measurements
among clinicians of 0 seconds; however, the 95% limits of
agreement were1.7 to1.9 seconds. More importantly, in
only 70% of subjects being studied was there agreement as
to CRT being normal or abnormal (using a 2-second upper
limit of normal).20 In another study, 5 experienced physi-
cians measured the CRT on each of 5 patients’ halluces.11
Evaluating intraobserver reliability, they found an overall
intraclass coefficient (ICC) of 0.72; however, the overall
standard error of the measurement was1.94 seconds. The
ICC for interobserver reliability was worse. Two studies
standardized the method of measuring CRT and used a
stopwatch to measure time. The first found that the ICC for
interobserver reliability was 0.7, and for intraobserver
reliability, 0.96.10 The second, a study of neonates, found
that the correlation coefficient for CRT measurement on the
foot among 3 observers ranged from 0.47 to 0.68 and for
the hand, 0.55 to 0.71.13 The latter 2 results might not be
representative of usual clinical practice given the strict
method applied for assessment of CRT. A study of children
admitted to a district hospital in Kenya evaluated 4 clini-
cians’ assessments of CRT on 100 patients. A low-moderate
agreement was found ( 0.42); however, better agree-
ment was found for CRT 1 second and 4 seconds.21
In addition to the variations that can occur because of
differences in amount and duration of pressure applied to
the finger, the clinician must also decide on the end point of
capillary refilling. Initial rapid partial refilling of the capil-
laries may be followed by a slower complete filling. Defin-
ing the end point is subjective and introduces further error
in the assessment of CRT.
THE CLINICAL APPLICATION OF
CRT MEASUREMENT
As mentioned above, there are no publications relating
specifically to the use of CRT measurement in anesthesia.
Its potential use in this field must be inferred from the
currently available evidence.
Pediatrics
There is a good correlation between CRT measurement and
degree of dehydration in children admitted to the hospital
with diarrhea. A CRT of 1.5 to 3 seconds is associated with
a fluid deficit of 50 to 100 mL/kg (measured as difference
in weight from time of admission to that after rehydra-
tion in infants with diarrhea) and a CRT of 3 seconds
suggests a deficit of 100 mL/kg.8 A prolonged CRT was
a major predictor of children who proved to have 5%
dehydration as judged by subsequent weight recovery in
the hospital.22 Children with dehydration (5% body
weight deficit) had a statistically significant longer mean
CRT (2.0 1.0 seconds vs 1.3 0.5 seconds) compared
with well-hydrated children. The presence of fever in
these children did not have a clinically important effect
on the estimate of CRT.23 A more recent review investi-
gating clinical measurements to assess dehydration in
children found that CRT was the best individual sign for
diagnosing children with 5% dehydration.16
In children with septic shock in the pediatric intensive
care unit, CRT was compared with hemodynamic vari-
ables. The best correlation was between CRT and stroke
volume index (r 0.46; 95% confidence interval,0.67 to
0.18) and lactate (0.47; 0.21 to 0.66), but this was still
modest. CRT showed best predictive ability to identify a
low stroke volume index when it was 6 seconds.19 Of
note, most patients were receiving inotropic support for
Capillary Refill Time: Is It Still a Useful Clinical Sign?
July 2011 • Volume 113 • Number 1 www.anesthesia-analgesia.org 121
CRT but is representative of the pediatric intensive care
unit population. No correlation between CRT and other
hemodynamic variables was found in children after cardiac
surgery.19
Prolonged CRT was found to be independently associ-
ated with death in children with severe and complicated
malaria in Sub-Saharan Africa (a disease that results in 2
million deaths annually). For children with severe anemia
associated with malaria, the risk of dying was 2-fold higher
if they had a prolonged CRT.24 Prolonged CRT (3 sec-
onds) is also a component of a prognostic scoring scale
developed for African meningococcal epidemics.25
A delayed CRT was identified as one of the strongest
warnings for serious infection in developed countries in a
recent high-profile review of clinical features used to con-
firm or exclude the possibility of serious infection in
children presenting to ambulatory care settings.26 This
accords with results published by the World Health Orga-
nization for resource-poor countries.27
Adults
The presence of a CRT of 2 seconds is, however, not
predictive of mild-to-moderate hypovolemia in adults. The
CRT was inconsistent when measured before and after
rehydration in 32 adult emergency patients with a history
suggestive of hypovolemia and hypotension or abnormal
orthostatic signs (increase in heart rate of 20 beats per
minute, or diastolic blood pressure decrease by 15 mm
Hg when the patient changed from a supine to standing
position), and in 47 blood donors before and after a 450-mL
blood donation. Using the 2-second upper limit of normal
gave a sensitivity of 11% for the blood donors, 47% for
patients with abnormal orthostatic signs, and 77% for those
with hypotension.28 CRT measurement with subjective
assessment of peripheral perfusion, in resuscitated criti-
cally ill adult patients assessed in the first 24 hours of
admission and once they were hemodynamically stable,
was able to identify those with a more severe organ
dysfunction and higher lactate levels.29
From the available evidence, it seems that CRT measure-
ment is most useful in the assessment of patients with
shock states. In these situations, there may be an alteration
in the balance of vasoconstrictor and vasodilator substances
and in the cross-talk between endothelial cells so that
regulation of the microvascular blood flow is impaired.
Abnormalities also include arteriovenous shunting, “stop-
flow” capillaries (flow is intermittent), “no-flow” capillaries
(capillaries are obstructed), failure of capillary recruitment,
and increased capillary permeability with interstitial
edema. Capillaries may become obstructed because of
swollen endothelial cells, reduced deformability of circulat-
ing erythrocytes, leukocyte-platelet-fibrin thrombi, or com-
pression by edema fluid, the end result being a reduction in
the functional capillary density. This suggests that CRT
may indeed be measuring alterations in perfusion of the
distal capillary bed. The link between systemic hemody-
namics and this peripheral perfusion is relatively loose, so
that these alterations can be observed even when systemic
hemodynamics are within satisfactory goals. However, if
cardiac output and arterial pressure are critically altered,
then they can affect peripheral perfusion.30 If CRT is indeed
a simple measure of the state of distal capillary bed
perfusion, then it is not surprising that Tibby et al.19 did not
find an important correlation between systemic hemody-
namic variables and CRT measurement. The findings from
other studies that CRT is a good predictor of significant
dehydration, serious infection, severe organ dysfunction,
and higher lactate levels relate to CRT as a measure of distal
perfusion as a whole rather than being equivalent to any
one single hemodynamic variable.
This evidence may be extrapolated to the use of CRT
during the preoperative assessment of patients and in
patients undergoing general anesthesia, particularly emer-
gency procedures and those involving significant blood
loss and large fluid shifts.
Attention has focused more recently on automated
methods of measuring CRT. These include digital videog-
raphy (digitally measured capillary-refill time [DCRT])31
and the use of a photoplethysmographic (PPG) sensor
based on a blue-light emitter.32
DCRT replaces visual observation by substituting an
electronic image sensor array for the human eye. In a study
of 83 children with acute gastroenteritis who were assessed
by clinicians to have at least mild dehydration, DCRT was
found to be more accurate at determining the presence of
significant dehydration (5%) than overall clinical assess-
ment. The range of DCRT measurements in well-hydrated
children (0.2–0.4 seconds) was substantially less than that
of the standard CRT measurement.
The low wavelength light of the blue-light PPG sensor
only penetrates as far as the upper skin capillaries. To
detect the occlusion of skin capillaries and track the refill
process, pressure was applied to the probe until the signal
from the PPG sensor disappeared with subsequent release
after 4 to 5 seconds. Three variables have been suggested
for estimating refill time: time for the signal to reach the
original baseline level after pressure release; time for the
signal to reach its maximum; and time for the signal to
return from maximum to its initial level.
Methods other than CRT are being used to digitally
assess peripheral perfusion. Body temperature gradient
measurements, orthogonal polarization spectral imaging,
peripheral perfusion index derivation from pulse oximetry,
near-infrared spectroscopy, and laser Doppler flowmetry
are examples of semiautomated methods. Each of these
methods offers advantages and limitations that have been
previously discussed.33
Digitalized techniques for measuring CRT are not avail-
able to the practicing clinician, and current designs requir-
ing a computer for processing results, specially rebuilt
pulse oximeter probes, or a video camera render them
impractical for routine use in the clinical setting. Before
automatically measured CRT can replace the standard
manual test, the techniques must be validated in a broad
range of subjects, including studies to evaluate their robust-
ness in different lighting and temperature conditions. Digi-
talized CRT measurement offers new techniques for the
quantification of CRT and the opportunity to define a new
“gold standard” for noninvasive CRT measurement. For
example, a temperature sensor measuring ambient or skin
MEDICAL INTELLIGENCE ARTICLE
122 www.anesthesia-analgesia.org ANESTHESIA & ANALGESIA
ing the CRT to provide a temperature-corrected value, and
a sensor used to measure CRT could be used in combina-
tion with other clinical variables such as heart rate, pulse
oximeter saturation, and respiratory rate to produce a
diagnostic tool for clinical triage.
In summary, CRT measurement is affected by multiple
external factors but has predictive value in the assessment
of dehydration and serious infection in children. There are
few outcomes data to support its use in adults. In an
intensive care unit with good light and in a warm room, a
CRT of 2 seconds might be reassuring but, as with all
tests, clinical decisions should not be based on CRT mea-
surement in isolation but rather as one aspect of the clinical
picture as a whole. There is no evidence to justify its use in
anesthetized patients. Operating rooms are cold, patients
are often draped, which limits access, and because most
anesthetics are potent vasodilators, the use of CRT to guide
practice is not justified. The possibility of a false-positive or
false-negative assessment is simply too great. Digitalized
and perhaps automated CRT measurements have the po-
tential to overcome some of these limitations. The use of
innovative technology in the assessment of CRT would be
an opportunity to apply more robust and reliable noninva-
sive methods to assess the peripheral circulation.
DISCLOSURES
Name: Amelia Pickard, MbChB, FRCA.
Contribution: This author helped write the manuscript.
Attestation: Amelia Pickard approved the final manuscript.
Name: Walter Karlen, PhD, MSc.
Contribution: This author helped write the manuscript.
Attestation: Walter Karlen approved the final manuscript.
Name: J. Mark Ansermino, MBBCh, MSc (INF), FRCPC.
Contribution: This author helped write the manuscript.
Attestation: J. Mark Ansermino approved the final manuscript.
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