Interstitial glucose monitoring has acceptable clinical accuracy in juvenile dogs

Zsofia Vigh Department of Veterinary Clinical Sciences, College of Veterinary Medicine, Purdue University, West Lafayette, IN

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Paula A. Johnson Department of Veterinary Clinical Sciences, College of Veterinary Medicine, Purdue University, West Lafayette, IN

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Hsin-Yi Weng Department of Comparative Pathobiology, College of Veterinary Medicine, Purdue University, West Lafayette, IN

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Elizabeth J. Thomovsky Department of Veterinary Clinical Sciences, College of Veterinary Medicine, Purdue University, West Lafayette, IN

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Aimee C. Brooks Department of Veterinary Clinical Sciences, College of Veterinary Medicine, Purdue University, West Lafayette, IN

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Abstract

OBJECTIVE

To compare the performance of an interstitial glucose monitor (IGM) versus a portable blood glucose monitor (PBGM) in sick juvenile dogs in a veterinary ICU.

ANIMALS

16 client-owned dogs admitted to the university teaching hospital under 1 year of age with systemic illness.

PROCEDURES

Paired interstitial and blood glucose samples were collected. A third glucose measurement with a reference method was obtained when IGM and PBGM values were clinically disparate. Analytical accuracy was measured by Pearson correlation and agreement statistics, including mean absolute relative difference (MARD), bias, and 95% limits of agreement. The Parkes consensus error grid analysis was performed to assess clinical accuracy.

RESULTS

159 paired glucose measurements were available for analysis. Comparison of IGM readings to PBGM measurements resulted in an MARD of 15.4% and bias of –2.6%, with the 95% limits of agreement ranging from –42.5% to 37.4%. Positive correlation between IGM and PBGM (Pearson r = 0.65) was found. On consensus error grid analysis, 100% of the pairs fell into clinically acceptable zones (74.2% in zone A, and 25.8% in zone B). When disparate IGM and PBGM readings were compared to a laboratory reference standard (n = 13), both methods resulted in high MARD and wide limits of agreement.

CLINICAL RELEVANCE

The IGM provides clinically acceptable glucose measurements compared to PBGM to monitor glucose levels in juvenile dogs in a clinical setting. Further clinical studies with a larger sample size, particularly in the hypoglycemic range, are needed to assess IGM performance in the lower glucose range.

Abstract

OBJECTIVE

To compare the performance of an interstitial glucose monitor (IGM) versus a portable blood glucose monitor (PBGM) in sick juvenile dogs in a veterinary ICU.

ANIMALS

16 client-owned dogs admitted to the university teaching hospital under 1 year of age with systemic illness.

PROCEDURES

Paired interstitial and blood glucose samples were collected. A third glucose measurement with a reference method was obtained when IGM and PBGM values were clinically disparate. Analytical accuracy was measured by Pearson correlation and agreement statistics, including mean absolute relative difference (MARD), bias, and 95% limits of agreement. The Parkes consensus error grid analysis was performed to assess clinical accuracy.

RESULTS

159 paired glucose measurements were available for analysis. Comparison of IGM readings to PBGM measurements resulted in an MARD of 15.4% and bias of –2.6%, with the 95% limits of agreement ranging from –42.5% to 37.4%. Positive correlation between IGM and PBGM (Pearson r = 0.65) was found. On consensus error grid analysis, 100% of the pairs fell into clinically acceptable zones (74.2% in zone A, and 25.8% in zone B). When disparate IGM and PBGM readings were compared to a laboratory reference standard (n = 13), both methods resulted in high MARD and wide limits of agreement.

CLINICAL RELEVANCE

The IGM provides clinically acceptable glucose measurements compared to PBGM to monitor glucose levels in juvenile dogs in a clinical setting. Further clinical studies with a larger sample size, particularly in the hypoglycemic range, are needed to assess IGM performance in the lower glucose range.

Introduction

Glucose abnormalities (dysglycemia) are reported in dogs and cats with a variety of illnesses.1 While either high or low blood glucose can cause serious complications, hypoglycemia is more life-threatening in the short term. Prompt correction of severe hypoglycemia is necessary to avoid serious complications such as altered mentation, seizures, blindness, and ultimately irreversible brain damage and death.2,3 Clinical trials evaluating the effect of dysglycemia on survival in veterinary patients are lacking, but a recent retrospective study found a higher mortality rate in dogs with dysglycemia when compared to normoglycemic patients.1

Puppies and kittens are more prone to developing hypoglycemia than adult animals due to their relatively low levels of stored glycogen and immature hepatic enzyme systems.2,4,5 A variety of conditions can cause low blood glucose levels in young animals, including neonatal and juvenile hypoglycemia, portosystemic shunts, toxicities, and severe infections including parvovirus and coronavirus.2,3,68 In this patient population, frequent blood glucose sampling is often limited by patient size, stress, nursing staff workload, and potential iatrogenic anemia. Intermittent assessments may result in under-recognition of dysglycemia or recognition only when clinical signs develop.

Portable blood glucose monitors (PBGMs) are commonly used in veterinary settings to measure blood glucose. Several monitors are available to use in dogs and cats; each analyzes venous or capillary glucose from a small sample within seconds, and each has been found to be clinically accurate in a stable patient population.9,10 However, each only provides glucose readings intermittently and requires a blood draw for each reading.

To combat these limitations, continuous glucose measuring systems are gaining interest in both human and veterinary critical care settings. Interstitial glucose monitors (IGMs) measure the glucose content of the interstitial fluid without blood sampling. They typically consist of a small sensor and a reader. The sensor is applied to the skin and measures the glucose in the interstitial fluid. Since glucose moves freely between the plasma and interstitial compartment down its concentration gradient, interstitial glucose values correlate with plasma values, but lag behind by about 5 to 15 minutes.11,12 The sensor measures interstitial glucose every few minutes and transmits the data wirelessly to a monitor or a smart phone to display continuous real-time glucose measurements. Newer-generation IGMs do not need blood sampling for calibration and can stay in place for several weeks. The IGM provides continuous readings and identifies changes in glucose levels that would have been missed by intermittent sampling.

Studies with IGMs in adult diabetic cats and dogs, including patients with diabetic ketoacidosis, have shown them to be safe and well tolerated with acceptable clinical accuracy.1318 The use of IGM in a heterogenous human ICU population requiring continuous insulin infusion reduced blood sampling for point-of-care glucose testing by 60%.19 As many pediatric veterinary patients may have limited vascular access and small blood volumes, reduction of blood sampling would be advantageous in this population. Thus, interstitial monitors would be ideal for a pediatric veterinary patient population, as they do not entail any blood sampling, require only a short period of restraint to place the sensor, and can provide readings as frequently as required by the animal’s condition rather than being limited by the animal’s size, ability to be handled, or available blood volume.

The aim of this study was to compare IGM (FreeStyle Libre; Abbott) readings against PBGM (AlphaTrack2 glucometer; Zoetis) measurements in nondiabetic dogs under 1 year of age in the veterinary ICU. We hypothesized that IGM performance in this population would allow acceptable clinical decision-making compared to PBGM measurements based on correlation, agreement measures, and the consensus error grid (CEG) analysis.

Materials and Methods

Animals

Client-owned dogs < 1 year of age admitted to the University Veterinary Hospital with an expected length of hospitalization of at least 48 hours were prospectively enrolled. The study protocol was approved by Purdue University’s Animal Care and Use Committee, and owners’ consent was obtained before enrollment (IACUC protocol No. 2103002117).

Patient data, including age, sex, breed, body weight, presenting complaint, baseline physical exam parameters, initial blood glucose measurement, working diagnosis, and use of dextrose supplementation, were recorded. All diagnostic and treatment decisions about each patient were at the discretion of the attending clinician.

Patients with scheduled CT or MRI scans were excluded since the IGM sensor has to be removed before such diagnostics. Patients with skin conditions affecting the dorsal cervical area or having a known allergy to any of the materials in the sensor were excluded. Any patient with a body weight < 300 g were excluded, and situations in which the attending clinician decided that enrollment was not in the best interest of the patient were also excluded. The 300 g weight limit was set to ensure that the planned total volume of blood sampling would not exceed 1% of the animal’s body weight. If blood sampling could not be obtained within 10 minutes of restraint, the sampling was aborted and the animal was excluded from the study.

Glucose measurement

Routine point-of-care blood glucose measurement at our institution is performed with the PBGM (AlphaTrack2 glucometer; Zoetis), which requires 0.3 µL of blood/measurement with a detection range of 20 to 750 mg/dL. The PBGM was used as described in the user manual.20 The measurements were obtained from a capillary or venous sample by a licensed veterinary technician as per the patient’s routine care; the site of sampling and the type of sample were not standardized.

The IGM sensor (FreeStyle Libre; Abbott) was applied to each patient in the dorsal cervical region lateral to the spinous process. A 3 X 3-cm area of the skin was clipped and prepped with isopropyl alcohol wipes provided with the IGM. The sensor was applied and secured with a few drops of tissue glue (Vetbond; 3M Animal Care Products) as needed. The IGM automatically measures the interstitial glucose with a detection range of 40 to 500 mg/dL. It is factory calibrated and can stay in place up to 14 days. It stores readings every 15 minutes for 8 hours of data and displays the real-time measurement when scanned. A digital reader (FreeStyle Libre Reader; Abbott) was used to obtain glucose readings from the unit. The reader displays the glucose reading at the time of scan, a trend arrow, and a graph displaying 8 hours of glucose history.

Each glucose reading was classified into 1 of 3 different clinical ranges: low (≤ 70 mg/dL), acceptable (71 to 180 mg/dL), or high (≥ 181 mg/dL). These glucose ranges in our study were taken from the CEG analysis, which assumes the target glucose range to be between 70 and 180 mg/dL,21 consistent with previous veterinary studies.13,16,18

When the glucose measurements from the IGM and PBGM fell in different ranges, it was considered a clinically significant difference. On these occasions, a third measurement using venous whole blood was determined with a commercial blood glucose analyzer (Catalyst One analyzer; IDEXX Laboratories Inc) as a reference value.

Data collection

At the time of admission to the ICU, the IGM sensor was applied to the skin. After the 1-hour wetting period (the time required for the sensor to activate and begin recording data), continuous interstitial glucose measurements were obtained and recorded. The sensor was scanned at the first, second, and third hour after placement, then at least every 6 hours for 48 hours.

At the same time, blood glucose levels were measured from capillary or venous whole blood with the PBGM at the same intervals as interstitial glucose (the first, second, and third hour after the sensor was placed, then at least every 6 hours for 48 hours) resulting in at least 10 paired readings/enrolled patient. More frequent blood glucose readings (paired IGM:PBGM readings) were obtained if desired by the clinician on the case. The PBGM glucose was measured prior to scanning the IGM sensor.

Statistical analysis

For glucose measures, mean ± SD and median (range) were reported. Pearson correlation and agreement statistics, including mean absolute relative difference (MARD), bias, and 95% limits of agreement, were reported to assess analytical accuracy. All statistical analyses were performed with a commercially available software program (Excel version 16.69.1; Microsoft Corp; and MedCalc version 12.7; MedCalc Software Ltd).

The Parkes CEG analysis for human type 1 diabetes was performed to assess clinical accuracy as previously described.21 Briefly, in people with type 1 diabetes, the risk of incorrect treatment decisions (failure to treat, overcorrection, and anticorrection) were judged on the basis of differences between the measured glucose values. Each pair of glucose readings was classified into 1 of the 5 risk zones to evaluate the clinical consequences of a discordant value. The risk zones ranged from no effect on clinical outcome (A) to dangerous consequences (E) on the basis of the assumption that the target blood glucose values were within 70 and 180 mg/dL.21

Results

Sixteen dogs were enrolled in the study; 11 intact females, 4 intact males, and 1 spayed female. The median age was 3 months (range, 2 to 6 months), and the median body weight was 3.7 kg (range, 0.9 to 15.9 kg). There were 6 mixed-breed dogs, 2 American Pit Bull Terriers, 2 Yorkshire Terriers, 2 Golden Retrievers, and 1 each of the following: French Bulldog, Australian Shepherd, Labrador Retriever, Chihuahua, and German Shepherd Dog. Five dogs were hospitalized for parvoviral enteritis, 4 for congenital cardiac anomalies, 3 for trauma, 2 for unspecified gastroenteritis, 1 for juvenile hypoglycemia, and 1 for a peritoneal-pericardial diaphragmatic hernia. Six patients received dextrose IV (Dextrose 50% injection) supplementation, 4 with parvoviral enteritis, 1 with other unspecified gastroenteritis, and 1 with juvenile hypoglycemia. Dextrose supplementation ranged from 1.25% to 5% concentration in IV fluids.

The IGM sensor was placed within 3 hours following patient admission to the hospital. The placement was well tolerated in all dogs. No premature detachment of the sensors was observed. On 4 occasions, the sensor failed to work; in 2 out of the 4 sensor failures, it failed immediately after placement and was replaced. On the third occasion, the sensor failed to work after 7 measurements and this sensor was not replaced. In 1 dog, the sensor failed to give a reading for the sixth data point but worked for all of the other time points. This happened in the operating room while the patient was under general anesthesia. There was no problem reported with the sensor before or after the patient was in the operating room. One dog died after 6 measurements. There were no adverse reactions, apart from mild erythema on the skin after sensor removal that resolved in each patient on its own.

Excluding the 1 failed reading, a total of 159 paired IGM and PBGM readings were obtained from 16 dogs. The median number of paired measurements was 10 (range, 6 to 14) per patient.

The majority (62.9%) of the IGM readings were lower than the PBGM readings, resulting in a lower mean and median interstitial glucose concentration of 133.2 ± 34.2 mg/dL and 132.0 (56.0 to 321.0) compared to 138.4 ± 28.6 mg/dL and 138.0 (64.0 to 236.0) for the PBGM.

When comparing the IGM readings to PBGM measurements (159 data pairs), the MARD was 15.4% and the bias was –2.6% with the 95% limits of agreement ranging from –42.5% to 37.4% (Table 1). Positive correlation was found between IGM and PBGM (Pearson r = 0.65).

Table 1

Agreement between glucose concentrations reported by the interstitial glucose monitor (IGM), portable blood glucose monitor (PBGM), and reference blood analyzer.

Glucose comparisons MARD BIAS 95% limits of agreement
IGM to PBGM (n = 159) 15.4% –2.6% –42.5% to 37.4%
IGM to reference test (n = 13) 26.5% 13.7% –41.7% to 69.1%
PBGM to reference test (n = 14) 32.5% 25.2% –29.2% to 79.6%

Bias = Mean relative difference. MARD = Mean absolute relative difference.

95% limits of agreement = bias ± 1.96 X SD.

A total of 88.7% (141/159) of the paired IGM and PBGM readings fell into the same glycemic range. The majority of the paired readings that were in the same glycemic range were between 71 and 180 mg/dL (136/141 [96.5%]). A total of 5/141 (3.5%) of the paired readings were higher than 181 mg/dL, and none were in the low glucose range (Table 2).

Table 2

Classification of clinical glycemic ranges on the basis of portable blood glucose monitor (PBGM) and interstitial glucose monitor (IGM) readings. Data are expressed as frequency counts (%).

PBGM glucose range ≤ 70 mg/dL PBGM glucose range 71–180 mg/dL PBGM glucose range ≥ 181 mg/dL
IGM glucose range ≤ 70 mg/dL 0 (0) 3 (1.9) 0 (0)
IGM glucose range 71–180 mg/dL 1 (0.6) 136 (85.5) 6 (3.8)
IGM glucose range ≥ 181 mg/dL 0 (0) 8 (5.0) 5 (3.1)

On 18 of 159 (11.3%) occasions, the IGM and PBGM reading fell in different glucose ranges. Of the 18 discordant pairs, a third blood glucose measurement on a laboratory analyzer was available for comparison on 13 occasions. The remaining 5 discordant data points did not have a reference value obtained in a timely enough fashion for accurate comparison (> 1 hour). Both the PBGM and IGM data points showed high variability when compared to a laboratory reference method with an MARD of 26.5% for the IGM and 32.5% for the PBGM, respectively, and a wide range of limits of agreement (Table 1).

All of the paired PBGM (x-axis) and IGM (y-axis) readings were plotted on the CEG to evaluate clinical accuracy (Figure 1). Of the 159 pairs, 118 (74.2%) fell into zone A and 41 (25.8%) were in zone B. No pairs fell into the zones C, D, or E.

Figure 1
Figure 1

Parkes consensus error grid analysis of the 159 paired (interstitial glucose monitor and portable blood glucose monitor) data points; 74.2% (118/159) of the pairs fell into zone A (no effect on clinical action), and 25.8% (41/159) fell into zone B (altered clinical action—little or no effect on clinical outcome). No pairs fell into the other zones.

Citation: Journal of the American Veterinary Medical Association 261, 10; 10.2460/javma.23.02.0103

When IGM values were compared to a laboratory reference test, all pairs (n = 13) fell into zone A+B (Figure 2).

Figure 2
Figure 2

Parkes consensus error grid analysis of the 13 interstitial glucose monitor data points compared to laboratory reference value. All of the 13 pairs fell into zone A (no effect on clinical action) and zone B (altered clinical action—little or no effect on clinical outcome). No pairs fell into the other zones.

Citation: Journal of the American Veterinary Medical Association 261, 10; 10.2460/javma.23.02.0103

Discussion

To the authors’ knowledge, this was the first study to evaluate an IGM in a sick, juvenile patient population in a clinical setting. Our results indicate that the IGM can be safely used in the target population to monitor glucose levels with acceptable clinical accuracy compared to the PBGM.

In our study, more than half of the IGM readings were lower than the simultaneously obtained PBGM measurements, meaning that the IGM tended to underestimate the PBGM values. This was also indicated by the small negative bias between the IGM when compared to the PBGM. In the clinical settings, this negative bias might be desirable, as it would decrease the risk of missing true hypoglycemia.

When IGM readings were compared to PBGMs, the MARD was 15.4% with wide limits of agreement. The MARD measures the average difference between paired values, and it is commonly used to assess analytical accuracy in IGMs. Higher MARD (25%) with limited agreement was reported in a previous veterinary study, in which the IGM performance was assessed against PBGM readings in diabetic dogs.18 Also, MARD values between 8.8% to 32.1% were reported with a variety of IGM devices used in people.22 In human studies, MARDs < 14% are typically considered acceptable.23 Although single numerical MARD values are often reported to compare results across varying devices, it has limitations as a statistical tool. It does not reflect nonlinear performance of the device throughout the glucose range and is influenced by several factors, including the number of paired measurements and the accuracy of the test used as a reference. This likely explains the wide differences of MARDs seen across various studies.2224

The correlation in our study between the interstitial and blood glucose values (Pearson r = 0.65) was lower than reported in previous veterinary studies comparing IGM to PBGM in diabetic dogs (Pearson r ranged from 0.89 to 0.94).13,16,18 Given the free movement of glucose between the blood and interstitial compartment, a strong correlation between the 2 compartments was expected. The relatively lower correlation in our study might be explained by the nondiabetic patient population and use of dextrose supplementation, which may result in a limited range of glucose levels, as most of our results were in the euglycemic range. This reduced data variation may lead to reduction of the correlation coefficient.25 Weaker correlations due to restricted data ranges were also evident in a study18 of diabetic dogs in which only weak to moderate correlations were found when dividing the glucose readings into the hypoglycemic (r = 0.33), euglycemic (r = 0.49), and hyperglycemic ranges (r = 0.74).

Despite only observing limited analytical accuracy between the IGM and PBGM, the IGM showed acceptable clinical accuracy compared to both the PBGM and reference test on the basis of CEG analysis. The CEG analysis was originally designed based on the consensus opinion of human endocrinologists evaluating the clinical impact of inaccuracies in blood glucose measurements in people with diabetes using point-of-care self-monitoring devices.21 While the target blood glucose range of 70 to 180 mg/dL was optimized for humans, the CEG has been used to evaluate glucose monitors in veterinary studies.13,16,18,26 The risk of incorrect treatment decisions (failure to treat, overcorrection, and anticorrection) were classified into 1 of the 5 risk zones based on the differences between the measured glucose values, as follows: A, no effect on clinical action; B, altered clinical action—little or no effect on clinical outcome; C, altered clinical action—likely to affect clinical outcome; D, altered clinical action—could have significant medical risk; and E, altered clinical action—could have dangerous consequences.21 All of the paired glucose measurements in the present study fell into zones A and B, indicating that clinical decision-making is acceptable based on the IGM results and will not likely compromise patient outcome when compared to results of the PBGM and reference test. Previous studies of stable diabetic canine patients and patients with diabetic ketoacidosis reported ≥ 99% and ≥ 95% of the glucose readings into zones A and B when comparing IGM to PBGM.13,16,18 When assessing the hypoglycemic range alone (glucose < 70 mg/dL), 93% of the readings fell into zones A and B.13 In a recent observational study of healthy research dogs with induced hypoglycemia, 80.1% of the readings fell into zones A and B and 19.9% into zone C (altered clinical action likely to affect clinical outcome) when IGM readings were compared to a laboratory reference test.26 This study was conducted on healthy animals, with rapid changes in blood glucose caused by injections of regular insulin to mimic an insulin overdose. As rapid changes may not allow as much time for interstitial equilibration with blood glucose, this may explain the higher numbers of zone C readings found in this study.

In our study, when discordant IGM and PBGM readings were compared to a reference analyzer, we found high MARD and a wide range of limits of agreement, suggesting poor agreements between both point-of-care readings and the reference test. Generally, PBGMs are considered to have acceptable accuracy for clinical decision-making, although they are not considered to be the gold standard due to the variable analytical accuracy with wide limits of agreement when compared to the reference standard.9,2729 Therefore, it is not surprising that there was poor agreement between the methodologies assessed here. Moreover, as a general rule, a glucose measurement with a laboratory reference analyzer is recommended when clinical signs do not agree with a point-of-care analyzer value.16,18,30 Similarly, wide variability was also reported in previous studies comparing IGM to a laboratory reference test or an arterial blood gas analyzer.18,31,32 In our study, when the IGM was evaluated in the CEG analysis against the reference values, all pairs fell into zones A and B, indicating good clinical accuracy. However, only a small number of pairs (n = 13) were available for analysis in this study.

Of the sensors that failed to read, most failed immediately on placement, allowing for quick replacement for continued monitoring. One sensor failed to give a reading while the patient was in the operating room under general anesthesia. This sensor was not replaced and spontaneously recovered functionality once the patient recovered from anesthesia. IGMs have been used in human surgical patients, and intermittent signal loss during surgery, likely due to interference with electrocautery, has been reported.33 The manufacturer also describes possible failure due to sensor overheating. The exact cause of failure was not investigated in our study; however, electrocautery and heat support were in use during the procedure.

The main limitation of this study was that only a few readings fell into the hypoglycemic range (1 PBGM reading and 3 IGM readings), which precluded this study from making inference about IGM performance during hypoglycemic events. Explanations for the lack of hypoglycemic events could be the small sample size, patient selection, and active clinical management to prevent hypoglycemia. As the IGM was placed at ICU admission, many patients had already received initial treatment for hypoglycemia at presentation in the emergency room. A total of 6 of the 16 animals received dextrose during their hospitalization; all received supplementation without documented clinical hypoglycemic events occurring in the ICU. Another limitation of this study was that clinicians were not blinded to IGM results; thus, use of the IGM may have enhanced clinical glucose monitoring and prompted clinicians to start dextrose supplementation earlier than they would have otherwise on the basis of trends reported by the IGM. Larger sample size and blinding the attending clinicians to the IGM results might have overcome these limitations. Finally, other patient factors, including skin thickness and hydration status, may have an influence on IGM performance16,18,30; these factors were not assessed in our study.

In conclusion, our study found acceptable clinical accuracy with the IGM compared to PBGM on the basis of error grid analysis in a nondiabetic juvenile canine patient population. Additional blood glucose measurement, ideally with a laboratory reference method, is indicated for situations in which the obtained glucose value does not fit the clinical picture, as neither the PBGM nor the IGM is considered gold standard. Further clinical trials with a larger sample size and blinding to IGM results are needed to assess IGM performance during hypo- or hyperglycemic events.

Acknowledgments

This study was funded by the Purdue Veterinary Hospital Emergency and Critical Care Department. No third-party funding or support was received in connection with this study or the writing or publication of the manuscript.

The authors declare that there were no conflicts of interest.

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