Intraobserver and interobserver reliability of standardized capillary refill time in dogs is high following observer training

Aina Claret Department of Clinical Sciences, College of Veterinary Medicine, Auburn University, Auburn, AL

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Stefania Gelendi Department of Clinical Sciences, College of Veterinary Medicine, Auburn University, Auburn, AL

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Kendon Kuo Department of Clinical Sciences, College of Veterinary Medicine, Auburn University, Auburn, AL

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Maureen McMichael Department of Clinical Sciences, College of Veterinary Medicine, Auburn University, Auburn, AL

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Katherine Gerken Department of Clinical Sciences, College of Veterinary Medicine, Auburn University, Auburn, AL

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Pen-Ting Liao Department of Clinical Sciences, College of Veterinary Medicine, Auburn University, Auburn, AL

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Abstract

OBJECTIVE

To assess intraobserver and interobserver reliability of capillary refill time (CRT) measurement in dogs using a standardized technique after training.

ANIMALS

20 dogs presented to the emergency room.

METHODS

Dogs presented to the emergency room were prospectively recruited. Using a timing device and standardized technique, CRT was measured at the oral mucosa of the inner lip. Measurements were performed by 2 emergency and critical care residents (observer 1 [Ob1] and observer 2 [Ob2]) and repeated 3 times by each observer for each dog. CRT values and signalment were recorded. Intraobserver and interobserver reliability were analyzed by calculation of the coefficient of variation (CV%), intraclass correlation coefficient (ICC), and minimal detectable difference. Reliability was considered high if CV% was lower than 10% and ICC was between 0.9 and 1.

RESULTS

Median CRT for Ob1 was 1.22 seconds and for Ob2 was 1.19 seconds. Intraobserver reliability was high, evidenced by a median CV% of 6.2% (range, 1.0% to 18.6%) and 9.5% (range, 1.3% to 22.6%) and an ICC of 0.97 (95% CI, 0.94 to 0.99) and 0.95 (95% CI, 0.90 to 0.98) for Ob1 and Ob2, respectively. Between observers, the CV% was 4.4% (range, 0.8% to 17.5%) and the ICC was 0.98 (95% CI, 0.94 to 0.99), indicating high interobserver reliability. The minimal detectable differences for intraobserver and interobserver were 0.30 and 0.34 seconds, respectively.

CLINICAL RELEVANCE

The reported high reliability of CRT despite its subjective nature enhances its usefulness in daily practice. However, further research on the validity of CRT is warranted.

Abstract

OBJECTIVE

To assess intraobserver and interobserver reliability of capillary refill time (CRT) measurement in dogs using a standardized technique after training.

ANIMALS

20 dogs presented to the emergency room.

METHODS

Dogs presented to the emergency room were prospectively recruited. Using a timing device and standardized technique, CRT was measured at the oral mucosa of the inner lip. Measurements were performed by 2 emergency and critical care residents (observer 1 [Ob1] and observer 2 [Ob2]) and repeated 3 times by each observer for each dog. CRT values and signalment were recorded. Intraobserver and interobserver reliability were analyzed by calculation of the coefficient of variation (CV%), intraclass correlation coefficient (ICC), and minimal detectable difference. Reliability was considered high if CV% was lower than 10% and ICC was between 0.9 and 1.

RESULTS

Median CRT for Ob1 was 1.22 seconds and for Ob2 was 1.19 seconds. Intraobserver reliability was high, evidenced by a median CV% of 6.2% (range, 1.0% to 18.6%) and 9.5% (range, 1.3% to 22.6%) and an ICC of 0.97 (95% CI, 0.94 to 0.99) and 0.95 (95% CI, 0.90 to 0.98) for Ob1 and Ob2, respectively. Between observers, the CV% was 4.4% (range, 0.8% to 17.5%) and the ICC was 0.98 (95% CI, 0.94 to 0.99), indicating high interobserver reliability. The minimal detectable differences for intraobserver and interobserver were 0.30 and 0.34 seconds, respectively.

CLINICAL RELEVANCE

The reported high reliability of CRT despite its subjective nature enhances its usefulness in daily practice. However, further research on the validity of CRT is warranted.

Introduction

Capillary refill time (CRT) is defined as the time needed for a distal capillary bed to return to its baseline color after applying enough pressure to cause blanching.1 CRT is a noninvasive, easy-to-use clinical test used to evaluate peripheral perfusion and circulatory status.2 In cats and dogs, CRT is commonly measured at the gingival or buccal mucous membranes, and anecdotally, a CRT longer than 2 seconds is associated with impaired perfusion.1 In people, a prolonged CRT after initial resuscitation has been associated with organ failure and a higher risk for mortality in patients with septic shock.35 Among other markers of peripheral perfusion, such as skin temperature gradient or peripheral perfusion index, CRT showed the highest accuracy in predicting complications in people undergoing major abdominal surgery.6 Furthermore, a recent study7 reported that CRT improved significantly after fluid administration in septic patients, suggesting its potential role in guiding treatment and resuscitation in critically ill patients. In dogs, CRT was significantly correlated with systolic blood pressure, suggesting its potential use as an indicator of hemodynamic stability.8 However, CRT also significantly correlated with rectal temperature and mucous membrane color in the above study, indicating that it still requires further evaluation and validation despite its widespread use in clinical settings.

Reliability is an essential quality of a clinical test, and it is defined as “the degree to which the measurement is free from measurement error.”9 Therefore, when repeated, a reliable test will allow users to get the same results with the same patient conditions.9 Although CRT requires subjective interpretation of color changes, this does not automatically disqualify it from being a reliable test.10

Reliability can be assessed in several different ways, such as within the same observer (intraobserver reliability), between different observers (interobserver reliability), and over time (test-retest reliability).11 Intraobserver and interobserver reliability of CRT measurement has been studied in people, with conflicting results. Overall, agreement between observers was poor in nontrained physicians and nurses1215 but can become excellent with standardized protocols and training.3,6 Similarly, intraobserver reliability was high in experienced and trained medical staff.7 Chalifoux et al8 described a standardized technique for measuring CRT in dogs using a stopwatch; however, studies assessing observer reliability of CRT in veterinary medicine are lacking.

The objective of this study was to assess both intraobserver and interobserver reliability in CRT measurement in dogs presented to the emergency room (ER) when performed by 2 veterinarians with similar experience and using a standardized technique after training. We hypothesized that intraobserver and interobserver reliability would be high when training and standardized technique were applied.

Methods

Animals

This prospective nonrandomized study was conducted at the Bailey Small Animal Teaching Hospital at Auburn University. The study was approved by the Auburn University IACUC (2023-5219), and informed owner consent was obtained. Dogs that were presented to the ER were eligible for inclusion. No restrictions were applied for breed, weight, gender, reproductive status, underlying disease, or presenting complaint. Exclusion criteria included heavily pigmented mucous membranes or those that were too pale to blanch, aggressiveness, and patients that did not tolerate manipulation of the head, muzzle, gums, or lips.

Measurements and data collection

CRT was measured at the oral mucosa of the inner lip as described by Chalifoux et al.8 After everting the upper lip with the left hand, pressure was applied to the oral mucosa of the inner lip with the pad of the index finger of the right hand for 4 seconds. Enough pressure was applied to cause blanching. Before starting data collection, both observers applied pressure with their index fingers on each other’s hands to ensure that a similar amount of force was used throughout the study. The right hand held a stopwatch device (Oslo Silver 2.0 Twin Stopwatch and Countdown Timer; Marshall-Browning International Corp) with a countdown of 4 seconds that ended with an audible alarm, followed by an automatic timer to measure CRT. The timer was manually stopped as soon as the observer recognized that the blanched area had returned to its original color. CRT was measured and recorded to the hundredth of a second.

Measurements were performed by 1 first-year and 1 second-year emergency and critical care resident and were repeated 3 times consecutively by each observer for each dog. All measurements were performed in the same area of the inner lip in each individual dog, but the site could differ between dogs depending on mucosal pigmentation and patient position. Between observers, measurements were taken within approximately 5 minutes of each other, although the exact time was not recorded. Ambient temperature and light were unchanged, and no treatments were administered between each dog’s measurements. Patient positioning was not recorded, and no particular efforts were made to maintain the same position in each dog. The order of the observers was the same throughout the study, and observer 2 (Ob2) was blinded to the measurements obtained by observer 1 (Ob1). Before starting data collection for the present study, both observers practiced the same protocol in at least 20 dogs (data not reported) to become proficient with the technique.

Statistical analysis

Preliminary data from serial CRT measurements performed by one of the observers showed an intraclass correlation coefficient (ICC) of 0.9. Based on this result, together with a precision of 10% for the 95% CI and 3 repetitions/subject, 2 observers, the desired sample size was 14 dogs.16 Six dogs were added to the calculated sample size to account for attrition. Therefore, 20 dogs were expected to be enrolled in the study.

Data was assessed for normality using the Shapiro-Wilk test. Descriptive statistics of continuous data were reported as median and range for nonnormally distributed variables or as mean ± SD (SD) for normally distributed variables. Categorical data were described as frequency and percentage. Due to the small sample size of all subgroups and since it was not an objective of this study, the correlation between observer reliability and signalment, underlying disease, or presenting complaint was not analyzed.

The coefficient of variation (CV%) was calculated as the ratio between the SD and mean of repeated measurements, expressed as a percentage (CV% = [SD/mean] X 100).17 The CV% is used to assess the measurement error of the data as a part of the reliability of the measurements.9 The higher the CV%, the greater the variability and the lower the reliability. Generally, a CV% < 10% suggests low variability and high reliability, whereas a CV% > 20% is indicative of high variability and low reliability.18 For intraobserver reliability, the CV% was calculated for each observer using all 3 measurements performed in each dog. For interobserver variability, the CV% was calculated by comparing the average of the 3 measurements from each patient between observers. The average was used to decrease measurement errors.11

The ICC was calculated by the ratio of the between-patients or between-groups variance to the total variance. The ICC provides valuable contextual information for interpreting the magnitude of measurement error in relation to the variability between patients or groups. Greater differences between patients or groups would tolerate a higher measurement error. A higher ICC indicates that the test is more effective in distinguishing between the patients or groups being tested. An ICC > 0.90 suggests excellent reliability, between 0.75 and 0.90 good reliability, between 0.50 and 0.75 moderate reliability, and < 0.4 poor reliability.19 The ICC and their 95% CIs were calculated using the SPSS statistical package (version 23; SPSS Inc) based on an absolute-agreement, 2-way mixed-effects model.19 Both single and repeated measures were reported for intraobserver ICC, and only single measures were reported for interobserver ICC to mimic the clinical practice. For intraobserver reliability, the ICC was calculated using all 3 measurements obtained from each patient. For interobserver reliability, the ICC was calculated by comparing the average of the 3 measurements from each patient between observers.

The SEM was calculated on the basis of Eliasziw et al.20 The minimum detectable difference (MDD) was calculated by 2.77 times the SEM.20,21 The MDD is a statistical estimate that represents the smallest amount of change that can be detected by a measurement method, taking measurement errors into account.

Results

A total of 20 dogs were enrolled in the study. The mean age was 8.3 years (SD, 3.8 years), and the mean weight was 24.6 kg (SD, 15.1 kg). Six (30%) dogs were neutered males, 3 (15%) were intact males, and 11 (55%) were neutered females. Fourteen (70%) dogs were classified as purebred, and 6 (30%) were classified as mixed-breed dogs.

The raw data is presented (Figure 1). The median CRT for Ob1 was 1.22 seconds (range, 0.59 to 2.59 seconds) and for Ob2 was 1.19 seconds (range, 0.6 to 2.69 seconds). The CV% obtained for Ob1 and Ob2 in all 20 dogs is shown (Figure 2). The CV% between Ob1 and Ob2 is shown (Figure 3). The median CV% for Ob1 was 6.2% (range, 1.0% to 18.6%) and 9.5% for Ob2 (range, 1.3% to 22.6%). The median CV% between Ob1 and Ob2 using the average CRT measurement from each dog was 4.4% (range, 0.8% to 17.5%).

Figure 1
Figure 1

Capillary refill time measurements from both observers for all 20 dogs. The solid (black) and empty (white) triangles represent measurements from observer 1 (Ob1) and observer 2 (Ob2), respectively. The first, second, and third measurements are arranged from left to right for each observer and each dog.

Citation: Journal of the American Veterinary Medical Association 262, 1; 10.2460/javma.23.07.0417

Figure 2
Figure 2

Coefficients of variation (CV%) for Ob1 and Ob2. The black and white columns represent the CV% for each dog from Ob1 and Ob2, respectively.

Citation: Journal of the American Veterinary Medical Association 262, 1; 10.2460/javma.23.07.0417

Figure 3
Figure 3

Coefficients of variation for comparison of Ob1 and Ob2. Each column represents the CV% for each dog.

Citation: Journal of the American Veterinary Medical Association 262, 1; 10.2460/javma.23.07.0417

The ICCs for Ob1 were 0.973 (95% CI, 0.943 to 0.988) and 0.991 (95% CI, 0.980 to 0.996) for single and average measures, respectively. The ICCs for Ob2 were 0.951 (95% CI, 0.901 to 0.979) and 0.983 (95% CI, 0.965 to 0.993) for single and average measures, respectively. The ICC between Ob1 and Ob2 was 0.979 (95% CI, 0.947 to 0.991).

The SEM was 0.11 seconds and 0.122 seconds for intraobserver and interobserver, respectively. The MDD was 0.30 seconds and 0.34 seconds for intraobserver and interobserver, respectively.

Discussion

The main finding of this study was that CRT measurement was reliable in dogs when performed by veterinarians using a standardized technique after training, based on ICC higher than 0.9 and CV% lower than 10% for each observer individually (intraobserver) and for the comparison between the 2 observers (interobserver).

The role of CRT as a tool to guide treatment and assess the cardiovascular status of critically ill patients is an emerging area of research in people.37 In patients with sepsis and septic shock, an abnormal CRT after initial stabilization was found to be correlated with a higher risk for mortality.3,4 Similarly, Van Genderen et al6 suggested that CRT could be used for the early identification of complications in postoperative patients undergoing major abdominal surgery. However, due to the subjective nature of CRT assessment and lack of technique standardization, some authors have questioned the clinical usefulness of measuring CRT.2,22 For any clinical tool to be useful in daily practice, the interpretation of the measurements should be reliable both within and among observers. In this context, reliability refers to how consistently 1 or multiple observers produce similar results when they are exposed to the same conditions, regardless of the time at which the observations are made. Factors such as differences in technique (how much and how long the pressure is applied, use of a chronologic device, and location of the capillary bed), personnel (experience, training, and visual reaction time), patients (signalment, underlying conditions, and compliance), and circumstances and environments in which CRT is taken (emergency vs appointment, lighting conditions, and room temperature) could contribute to measurement variability.2,23 Several studies have analyzed observer variability of CRT measurement in people,3,7,1215,2427 with results ranging from poor to excellent agreement. It is important to note that the techniques, measurement sites, observers’ experience, and studied population differed among these studies; thus, these results should be interpreted cautiously. Some examples of the different techniques used included measurement of CRT with a standardized pressure device,26 estimation of CRT from a video recording,1214 or blind assessment of CRT without a timing device.15,25 Overall, intraobserver and interobserver reliability were higher when CRT was performed with a standardized technique and training was applied.3,6 Therefore, in the present study, the fact that CRT measurements were standardized, together with both observers having practiced the technique prior to data collection, could explain the high intraobserver and interobserver reliability reported in the results.

CRT can be significantly affected by several factors.2,23 Both ambient and core temperatures have been shown to impact CRT in people. In adults23 and newborns,27 CRT decreased as ambient and body temperature increased. Lighting can also significantly impact CRT estimation, with poor lighting resulting in a more difficult assessment.28 In the current study, environmental temperature and light were not standardized but remained constant between measurements for each dog to minimize bias. CRT measurements may also be affected by the amount and duration of pressure applied, with a shorter duration and lighter pressure resulting in a lower CRT value.29 Furthermore, variations in the visual reaction time to stop the timer when measuring CRT may impact the results. Visual reaction time, defined as the time between the onset of a stimulus and an individual’s response, is influenced by the individual’s duration of practice.30 Studies have shown that visual reaction times become more consistent with training.30 Applying this finding to the present study, improved performance and decreased variability may have occurred as the observers performed more CRT measurements with the timing device. However, there was no apparent trend in CV% over time (Figure 2). This may be attributed to the training applied before data collection. CRT may decrease when performed consecutively within < 1 minute.23,27 This phenomenon is thought to be secondary to applying pressure repetitively, leading to vasodilation and a more rapid refill.27 In the present study, there was no consistent trend of shortening CRT between the 3 measurements within or between observers despite all measurements being performed within approximately 5 minutes. Therefore, performing consecutive CRT measurements within a short window of time had minimal impact on measuring CRT. Patient positioning can also affect CRT measurements.31,32 In people, CRT measured at the index finger was significantly prolonged in the supine position compared to the sitting position.31 Furthermore, hand elevation from the heart level also resulted in a higher CRT potentially due to decreased arterial pressure at the measurement site, resulting in a more prolonged CRT.31,32 A similar phenomenon could occur in dogs when CRT is measured at the inner lip, with potentially higher CRT values obtained when the head is above the heart level. Further studies are needed to assess the effect of head and body position on CRT measurement in dogs. In the current study, differences in the dogs’ posture could have impacted CRT measurements. However, the potential changes would affect the absolute CRT values rather than observer reliability. Since patient positioning was very similar between consecutive measurements and observers to the best of the author’s recollection, it is deemed unlikely that position changes had a significant influence on the results of this study.

Although the results of this study showed an overall high intraobserver reliability, some dogs had a particularly low intraobserver and/or interobserver reliability in their CRT measurements. For instance, dogs 1 and 19 had a low intraobserver reliability for Ob1, and dogs 1, 2, 4, 6, and 19 had a low intraobserver reliability for Ob2, based on a CV% higher than 10%. The reason for these discrepancies is unknown, as no common factors among these patients were appreciated. It is possible that the first 2 dogs had a lower intraobserver reliability due to insufficient training, but this hypothesis would not explain the high CV% and unreliable readings observed in dog 19. Differences in the CRT value also cannot explain the high CV% observed in these patients since dogs 1, 4, and 19 had a CRT < 1 second, while the CRT for dogs 2 and 6 was between 1 and 2 seconds.

In people, interobserver reliability was reported to be higher in patients with a more prolonged CRT and lower for values < 1 second.25 Based on these findings, the high interobserver CV% observed in dogs 3 and 4 could be explained by a lower CRT value, since both dogs had a CRT < 1 second. However, 4 other dogs (1, 13, 15, and 19) had a CRT < 1 second but their interobserver reliability was high, with some of them (1, 13, and 15) even having a CV% < 5%. Therefore, it is considered unlikely that a shorter CRT had a major impact on interobserver reliability in the current study. Future studies are warranted to explore the factors that affect reliability of CRT measurements in dogs.

Technique standardization improves the external validity of the results by minimizing variance in measurements caused by differences in technique. For example, in people, measurements can vary depending on where CRT is assessed.24,27 In studies evaluating the use of CRT as a prognostic indicator or as a tool to assist in treatment guidance, high observer variability could mask the genuine cause-and-effect relationship that is being studied due to unreliable measurements. The results of this study showed that a standardized CRT technique after training is reliable in dogs; therefore, the role of CRT in treatment guidance and outcome prediction in veterinary medicine should be further explored.

Subjective assessment of CRT without a timing device, also known as “naked-eye” estimation, is considered the most commonly used technique in small animal medicine.1 However, based on previous studies of people, this technique showed poor reproducibility between observers and some authors discourage its use as a tool to assess perfusion disturbances.13,15,25 Considering the widespread use of the “naked-eye” estimation of CRT in dogs and cats, further studies analyzing observer variability would help determine whether this technique is adequate to assess peripheral perfusion in daily practice.

One major limitation of CRT is the lack of a gold standard. Therefore, proving that measurements are accurate is challenging, if not impossible. In the effort to objectively quantify CRT, several automatized CRT measurement devices have been explored.3335 A recently developed device (DiCART II; DicarTech) showed promising results, reporting good correlation with human-measured CRT and adequate precision and reliability.35 A similar device has been adapted for automated CRT measurement in dogs.36 Nevertheless, these devices seemed to be highly affected by variations in environmental light and patient size and conformation, limiting their use in clinical practice. These devices have also only been compared to subjective CRT measurements performed by people. Therefore, even if they might provide more objectivity, their use might not be superior to a properly standardized technique, and more studies are needed to establish the proper gold standard.

The CV%, ICC, and MDD provide objective and distinct information about the reliability of the measurements.17 CV% quantifies the dispersion of repeated measurements, normalized to the mean. This normalization is particularly valuable when the dispersion is correlated with the mean (eg, higher dispersion with higher mean and lower dispersion with lower mean). The CV% can indicate absolute precision in that a lower CV% reflects similar repeated measurements and therefore a higher precision.37 However, to determine how precise is “precise enough,” the user must consider the magnitude of differences the measurement method is required to detect. The ICC is an index of the variance among the different subjects or groups in relation to the total variance and thus could be considered as precision relative to the magnitude of differences.37 A higher ICC suggests that the differences observed between patients or groups are relatively greater than the measurement error occurring within patients or groups, indicating a higher level of relative precision. In other words, CV% can be used to determine the precision of a particular method, but analysis of ICC can provide confidence that the method is precise enough to differentiate between patients or groups in the sample population. The MDD represents the smallest differences or changes in a measurement that is considered statistically significant. When changes are lower than the MDD, it is important to consider the possibility of measurement error rather than attributing it to actual changes.17 The MDD calculated from SEM is not specific to the sample population being assessed and can be generalized to a broader population using the same methodology.21 In the same context, a higher MDD suggests that the method can only detect larger differences and may miss clinically significant changes; therefore, it is less reliable.17 In this study, the MDD for intraobserver was 0.30 seconds, indicating that when the technique used in the present study is applied, any changes above 0.30 seconds measured by the same person can be considered actual changes. Whether 0.30 second changes are clinically meaningful requires future research and was beyond the scope of this study.

Limitations included that dogs presenting to the ER were enrolled regardless of their signalment, presenting complaint, or underlying disease, as the goal was to get a wide range of CRT values. However, only 2 dogs within the studied population had a CRT > 2 seconds. One study showed that interobserver agreement was greatest for significantly prolonged CRT25; however, further studies including a larger population with more profound perfusion derangements are needed to prove this finding in dogs.

Second, despite efforts to standardize the amount of pressure applied, this was done subjectively, and the pressure applied likely differed between observers. Standardization of the pressure using more objective measures, such as a standardized pressure syringe device,26 was considered impractical and would not mimic daily practice.

Another limitation was that variations in the positioning of the study subjects between measurements cannot be entirely ruled out and could have had an impact on the results as previously discussed.

Moreover, the fact that Ob1 was not blinded to the measurements from Ob2 could also be considered a limitation. However, the order of the observers was the same throughout the study and Ob1 always performed and recorded the CRT before Ob2; thus, Ob2 had minimal to no effect on the performance of Ob1. Another limitation was that observers were not blinded to their own measurements, which could have led to observer bias. Whether blinding the operator to their own measurements provides better or worse intraobserver reliability warrants further research. Furthermore, observers were not blinded to the patients’ conditions or physical exam findings, which could have influenced the observers’ notion of an expected CRT value. Finally, measurements were performed by 2 veterinarians with prior training; therefore, the results from this study might not apply to nontrained observers.

CRT measurements had high interobserver and intraobserver reliability. The results suggest that CRT can be highly reliable in dogs when performed by trained veterinarians using a standardized technique. Further studies are required to assess observer variability in a wider range of CRT values and among people with different levels of experience and training. Since the standardization of CRT can be cumbersome in daily practice, evaluation of observer variability using the “naked-eye” estimation of CRT would also be of interest.

Acknowledgments

None reported.

Disclosures

The authors declare that ChatGPT-3.5 was used for grammar assistance, but no content was created by ChatGPT-3.5.

Funding

The authors have nothing to disclose.

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