Real-Time Continuous Glucose Monitoring Shows High Accuracy within 6 Hours after Sensor Calibration: A Prospective Study
Zhou J-X (2013) Real-Time Continuous Glucose Monitoring Shows High Accuracy within 6 Hours after Sensor
Calibration: A Prospective Study. PLoS ONE 8(3): e60070. doi:10.1371/journal.pone.0060070
Real-Time Continuous Glucose Monitoring Shows High Accuracy within 6 Hours after Sensor Calibration: A Prospective Study
Xiao-Yan Yue. 0
Yi Zheng. 0
Ye-Hua Cai 0
Ning-Ning Yin 0
Jian-Xin Zhou 0
Richard C. Willson, University of Houston, United States of America
0 Department of Critical Care Medicine, Beijing Tiantan Hospital, Capital Medical University , Beijing , China
Accurate and timely glucose monitoring is essential in intensive care units. Real-time continuous glucose monitoring system (CGMS) has been advocated for many years to improve glycemic management in critically ill patients. In order to determine the effect of calibration time on the accuracy of CGMS, real-time subcutaneous CGMS was used in 18 critically ill patients. CGMS sensor was calibrated with blood glucose measurements by blood gas/glucose analyzer every 12 hours. Venous blood was sampled every 2 to 4 hours, and glucose concentration was measured by standard central laboratory device (CLD) and by blood gas/glucose analyzer. With CLD measurement as reference, relative absolute difference (mean6SD) in CGMS and blood gas/glucose analyzer were 14.4%612.2% and 6.5%66.2%, respectively. The percentage of matched points in Clarke error grid zone A was 74.8% in CGMS, and 98.4% in blood gas/glucose analyzer. The relative absolute difference of CGMS obtained within 6 hours after sensor calibration (8.8%67.2%) was significantly less than that between 6 to 12 hours after calibration (20.1%613.5%, p,0.0001). The percentage of matched points in Clarke error grid zone A was also significantly higher in data sets within 6 hours after calibration (92.4% versus 57.1%, p,0.0001). In conclusion, real-time subcutaneous CGMS is accurate in glucose monitoring in critically ill patients. CGMS sensor should be calibrated less than 6 hours, no matter what time interval recommended by manufacturer.
Funding: The study was funded by Beijing Municipal Health Bureau (Grant Number: 2009-3-28. Website: http://english.bjhb.gov.cn). The funders had no role in
study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
. These authors contributed equally to this work.
Epidemiologic data have shown that there is a high incidence of
hyperglycemia in critically ill patients, and its occurrence is
associated with adverse clinical outcome [1,2]. On the other hand,
intensive glucose control may carry the risk of inducing
hypoglycemia [3,4]. Recent study by The NICE-SUGAR Study
Investigators suggested that both of moderate and severe
hypoglycemia induced by intensive glucose control were associated
with an increased risk of death in critically ill patients .
Although the appropriate target range of blood glucose in critically
ill patients is inconclusive at present time, it has been widely
accepted that accurate and timely measurement of blood glucose is
essential in intensive care unit (ICU) setting, even in patients
receiving a conventional glucose control protocol [6,7].
There are currently two options for clinical glucose
measurement in hospitalized patients: central laboratory devices (CLD)
and point-of-care (POC) devices. Although CLD provides the
most accurate results , it is not suitable for bedside glucose
monitoring in ICU because of its slow turn-around time. POC
devices are more commonly used for glucose monitoring in ICU
patients . POC handheld glucose analyzer with capillary blood
sampling is originally designed for patients home use as
selfmonitoring of blood glucose. Although handheld glucose analyzer
can provide a fast bedside result, its accuracy in critically ill
patients has been questioned [9,10]. Another type of POC
instrument commonly used in glucose monitoring in ICU is blood
gas analyzer with function of glucose measurement . It has been
found that glucose measurements by blood gas/glucose analyzers
located in ICU are more accurate than those by handheld glucose
analyzers [11,12]. The main disadvantage of glucose measurement
by a blood gas/glucose analyzer is its intermittent and invasive
nature. The limitation of glucose monitoring method in critical
care settings may contribute to the discrepancy of results in glucose
control studies, which may hamper the further investigation .
These issues have urged the need for real-time continuous glucose
monitoring system (CGMS) devices .
For the past few years, several CGMS devices have been applied
in critically ill patients [11,1426]. However, preliminary results of
CGMS accuracy in ICU patients have been mixed, and seldom
studies employed CLD serum glucose measurement as reference in
accuracy investigation. Most CGMS devices measure
subcutaneous interstitial glucose concentration by enzymatic glucose oxidase
electrode, thus timed calibration of CGMS sensor by blood
glucose measurement is required . Up to now, there has been
no study carried out to evaluate the influence of calibration
method on CGMS accuracy. In present study, a real-time
subcutaneous CGMS was used in adult critically ill patients to
evaluate CGMS accuracy with standard CLD serum glucose
measurement as reference. The purpose of this study was to
determine the accuracy of CGMS, especially for the influence of
calibration time on accuracy.
Materials and Methods
The study was performed in accordance with the Declaration of
Helsinki, and study protocol was reviewed and approved by
Research Ethic Committee in Beijing Tiantan Hospital, Capital
Medical University (Beijing, China). Written informed consent was
obtained from patients or their relatives.
Study population and routine practice for glucose
We carried out this prospective study in a 12-bed neurosurgical
ICU in a 1000-bed university hospital, from January to April in
2012. Consecutive patients were screened and enrolled if they had
hyperglycemia (blood glucose concentration greater than
10.0 mmol/L measured by ICU-based blood gas/glucose
analyzer) at admission, and their expected lengths of stay in ICU were
more than 48 hours. Exclusion criteria were patients younger than
18 years old, patients with hemoglobin concentration less than
100 g/L, patients admitted only for overnight postoperative
monitoring, or patients in moribund and not likely to survive
more than 24 hours. The demographic characteristics of enrolled
patients were collected prospectively, including reasons for ICU
admission, age, sex, history of diabetes mellitus, blood glucose
concentration at admission, Acute Physiology And Chronic Health
Evaluation (APACHE) II score on ICU admission, and use of
insulin infusion during study period.
We employed a conventional glucose control protocol in our
ICU [28,29]. Continuous insulin infusion was initiated if the blood
glucose concentration measured by ICU-based blood gas/glucose
analyzer exceeded 11.1 mmol/L. The blood glucose target was set
between 7.8 and 11.1 mmol/L. When the blood glucose
concentration fell below 10.0 mmol/L, the insulin infusion was
decreased. When the blood glucose fell below 7.8 mmol/L, the
insulin infusion was stopped.
Glucose levels of enrolled patients were monitored by a
realtime subcutaneous CGMS, the San MediTechs Dynamic Glucose
Monitoring System (DGMSH, San Meditech Medical Technology
Co., Ltd, Huzhou, Zhejiang, China). This system is composed of
three parts: a disposable subcutaneous glucose sensor, a
pagersized monitor, and dynamic glucose analysis software for
downloading stored data to a computer. The subcutaneous sensor
contains an enzymatic glucose oxidase electrode connecting to the
monitor by a cable. The values are displayed on the monitor as
means of 16 glucose measurements over the last 3 minutes,
allowing real-time continuous glucose monitoring. The range of
glucose measurement by this CGMS is 1.7 to 25.0 mmol/L.
After patient recruitment, CGMS sensor was placed in the
subcutaneous tissue on the left or right upper arm, and transparent
tape was used to secure the sensor to the skin. After 3 hours
warmup period for CGMS, whole blood was sampled from a deep
venous catheter, and blood glucose concentration was measured
by a GEM Premier 3000 blood gas/glucose analyzer
(Instrumentation Laboratory, Lexington, MA, USA) with the glucose-oxidase
methods. This blood glucose value was used as the initial CGMS
calibration. Subsequent calibrations were performed every
12 hours by using the same method. The GEM Premier 3000
blood gas/glucose analyzer was located in ICU. Sensor site was
inspected by one of the investigators at least twice daily for signs of
local irritation, infection, or bleeding. According to manufacturers
instruction manual, a CGMS sensor can be used up to 72 hours.
Sensors were removed if the patients glucose concentration had
been stayed within target range for 24 hours, or in other cases the
patient was transferred to another unit or died. The monitor can
automatically detect sensor malfunction, which occurs because of
low sensor current. If a sensor failed longer than 1 hour, the sensor
was removed and a new sensor was inserted.
Blood samples were obtained every 2 to 4 hours during study
period. Approximately 2 ml of blood was withdrawn in a
heparinized syringe (BD PresetTM, LOT: 1263532, Becton
Dickinson and Company, Plymouth, UK) from a deep venous
catheter after 3 ml of blood was discarded. Additional samples
were also collected at ICU physicians own discretion for clinical
need by using the same method. All blood samples were collected
by one of the investigators.
The blood sample was divided into two parts. In one part, blood
glucose concentration was immediately measured by a GEM
Premier 3000 blood gas/glucose analyzer. During the study
period, maintenance, calibration, and quality control of this blood
gas/glucose analyzer was performed on a regular basis by the
central hospital laboratory. The other part of blood sample was
immediately sent to the central laboratory in a serum-separating
tube (BD VacutainerH SSTTM II Advance, LOT: 1266616,
Becton Dickinson and Company, Plymouth, UK). After
centrifugation, the serum glucose concentration was measured by a
HITACHI 7600-020 biochemical analyzer (Hitachi
High-Technologies, Tokyo, Japan) with an oxygen electrode oxidation
method. At the same time of blood sampling, glucose value on
CGMS monitor was also documented by one of the investigators.
For glucose measurement, each data set at one time point
contained three simultaneous glucose measurements: serum
glucose concentration measured by CLD, whole venous blood
glucose concentration measured by GEM Premier 3000 blood
gas/glucose analyzer, and subcutaneous interstitial glucose
concentration monitored by CGMS.
The alarm of CGMS was turned off to avoid interruption to
bedside physicians and nurses clinical decision. Although bedside
nursing and physician teams were aware of patients enrolment,
they did not assess CGMS readings and change the patient
management according to values from the CGMS.
Statistical analyses were carried out by using MS Excel for
MAC (Microsoft Corporation, Beijing, China) and SPSS statistical
software (version 10.0, SPSS, Chicago, IL). Categorical variables
were expressed as percentages. Continuous data were checked for
normal distribution by Kolmogorov-Smirnov test, and were shown
as mean and standard deviation (SD) or median with the 25th and
75th percentiles, when applicable.
By using the standard serum glucose concentration measured by
CLD as reference, the accuracy of glucose measurement by
CGMS or GEM Premier 3000 blood gas/glucose analyzer was
analyzed. The numerical accuracy of measurements was evaluated
by calculating relative absolute difference (RAD: absolute
difference between time-matched measurement and reference divided
by reference value, multiplied by 100), and by Bland and Altmans
limits of agreement analysis . Bias was defined as the mean of
the difference between measurement and reference (measurement
minus reference). Upper and lower limit of agreement were
defined as bias61.96 SD of the mean bias.
Clinical accuracy was evaluated by Clarke error grid analysis
(Matlab R2011a, The Mathworks, Beijing, China) . Results
were divided into five zones: A, B, C, D, and E. Comparison
points within zone A represent tested values that differ from the
reference value by no more than 20%. Zone B includes
comparison points that differ by more than 20%, but do not
result in an alteration in treatment. Points in zone C would result
in an overcorrection of acceptable glucose values. Points in zone D
would result in failure to detect and treat errors. Comparisons in
zone E would result in opposite treatment decisions. Values in
zones A and B represent clinically accurate or acceptable results.
In order to clarify the influence of calibration time on the
accuracy of CGMS, data sets were divided into those within
6 hours and those between 6 and 12 hours after CGMS sensor
calibration. In order to determine the accuracy of CGMS at
various glucose concentrations, data sets were evaluated over three
different ranges for CLD serum glucose concentration: less than
3.9 mmol/L (hypoglycemia), 3.9 to 10.0 mmol/L (euglycemia),
and greater than 10.0 mmol/L (hyperglycemia).
Categorical variables were analyzed by x2 test. Comparisons of
continuous data were performed by using unpaired t-test for
normally distributed variables, and the Mann-Whitney U test for
non-normally distributed variables. A p-value of less than 0.05 was
considered statistically significant.
During study period, 684 patients were assessed for eligibility
and 666 patients were excluded. The reasons for exclusion were
admission only for overnight postoperative monitoring in 602
patients, blood glucose concentration less than 10.0 mmol/L at
admission in 33 patients, younger than 18 years old in 19 patients,
hemoglobin concentration less than 100 g/L in 9 patients, and in
moribund and not likely to survive more than 24 hours in 3
patients. Finally, 18 patients were enrolled and 35 CGMS sensors
were used during study period. Four sensors displayed malfunction
and all occurred within the first 3 hours after sensor placement.
Sensors were well tolerated in all patients. No serious adverse skin
reactions, infections, or bleeding occurred during study period. All
enrolled patients received insulin infusion during the study period,
and no patient died. Demographic data of patients are shown in
Table 1. In total, 314 glucose measurement data sets were
obtained for analysis.
Accuracy of real-time CGMS
With serum glucose concentration measured by CLD as
reference, the RAD (mean6SD) between CGMS and CLD
measurements was 14.4%612.2%. Bland and Altman plot is
shown in Figure 1. Bias and upper and lower limits of agreement
between CGMS and CLD values were 0.10, 3.46, and
23.25 mmol/L, respectively (Figure 1). In Clarke error grid
analysis, there were 74.8% matched points in zone A and 25.2%
in zone B, and no values in zone C, D or E (Figure 2).
Accuracy of real-time CGMS at different time after sensor
The RAD between CGMS and CLD measurements in data sets
obtained within 6 hours after sensor calibration (8.8%67.2%) was
significantly lower than those obtained between 6 to 12 hours after
calibration (20.1%613.5%, p,0.0001, Table 2). Bias and limits of
agreement are also shown in Table 2. There was no significant
difference in bias (p = 0.199). The percentage of matched points in
History of diabetes mellitus
Blood glucose concentration at admission (mmol/L)
Time of CGMS monitoring per patient (hours)
Reason for ICU admission
Severe traumatic brain injury
Acute lung injury after craniotomy
Acute lung injury after chest trauma
Data are mean 6 SD, or n (%) unless otherwise stated.
zone A of error grid analysis was significantly higher in data sets
within 6 hours after calibration than that between 6 to 12 hours
after calibration (92.4% versus 57.1%, p,0.0001, Table 2).
Accuracy of real-time CGMS at different serum glucose
In total of 314 data sets, only one had CLD serum glucose value
less than 3.9 mmol/L (3.5 mmol/L). In this data set,
corresponding CGMS value was 3.9 mmol/L. Data of RAD and limits of
agreement in euglycemic (3.9 to 10.0 mmol/L) and hyperglycemic
levels (greater than 10.0 mmol/L) are shown in Table 2. There
was no significant difference in RAD between the two different
serum glucose levels (15.4%613.8% in euglycemia and
13.2%69.8% in hyperglycemia, p = 0.228). However, Bias in
hyperglycemic levels was significantly more negative than that in
euglycemic levels (p,0.0001). The percentage of matched points
in zone A of Clarke error grid analysis was significantly higher in
data sets in hyperglycemic levels than that in euglycemic levels
(81.0% versus 69.9%, p = 0.026, Table 2). When analysis was
performed only in data sets obtained within 6 hours after sensor
calibration, no significant differences were found either in RAD
(8.8%67.2% versus 8.7%67.3%, p = 0.950) or percentage of
matched points in Clarke error grid zone A (90.6% versus 95.1%,
p = 0.370) between different glucose levels. Bias in hyperglycemic
levels was also significantly more negative than that in euglycemic
levels (0.16 versus 20.32 mmol/L, p = 0.006).
Accuracy of ICU-based GEM Premier 3000 blood gas/
glucose analyzer (GEM)
With serum glucose concentration measured by CLD as
reference, the RAD between GEM and CLD measurements was
6.5%66.2%. Bias and upper and lower limits of agreement
between GEM and CLD values were 20.26, 1.35, and
21.87 mmol/L, respectively. In Clarke error grid analysis, there
were 98.4% matched points in zone A and 1.6% in zone B, and no
values in zone C, D or E.
Real-time glucose monitoring has been advocated for many
years to improve glycemic management in critical care settings
[6,27]. In present study, the accuracy of a real-time subcutaneous
CGMS was assessed in glucose monitoring in critically ill patients.
Figure 1. Bland and Altman plot between CGMS and CLD values. Differences between individual time matched CGMS and CLD values (y-axis)
are plotted against means of time matched values (x-axis). Bias (solid line) and upper and lower limits of agreement (dashed line) are also displayed.
CGMS = continuous glucose monitoring system. CLD = central laboratory device.
An acceptable accuracy was found, either numerically or clinically,
for subcutaneous CGMS in real-time glucose monitoring. Most
importantly, CGMS showed highly accurate within 6 hours after
sensor calibration. Different methods and time intervals for
CGMS sensor calibration have been employed by studies in
ICU settings, and this may contribute to the disparity in results in
accuracy evaluation. Sensors were calibrated against capillary,
arterial, and venous blood glucose measurement by POC
handheld glucose analyzers [14,17,18,2023,25,26], or against
arterial blood glucose values by ICU based blood gas/glucose
analyzers [11,15,16,19,24]. Sensor calibration was performed
every 6 hours in majority of studies [11,1416,19,23,24], whereas
12-hour time interval [18,20,21] and before each meal  were
chosen in other studies. Up to now, no study has been carried out
to investigate the influence of calibration time on accuracy of
CGMS. According to recommendation by the manufacturer, we
calibrated sensors in 12-hour interval. Although CLD value is
considered the gold standard for blood glucose measurement, it
is not suitable for simultaneous CGMS sensor calibration because
of its slow turn-around time. Because glucose measurement by
ICU-based blood gas/glucose analyzer has been proven to be
more accurate than that by POC handheld glucose analyzers
[11,12], we finally chose venous glucose concentration measured
blood gas/glucose analyzer as GCMS calibration method. With
CLD measurement as reference, our results for numerical
agreement and Clarke error grid analysis are comparable to those
studies with 12-hour calibration interval [18,20,21]. Furthermore,
the results from data sets within 6 hours after calibration showed a
higher accuracy, with 8.8%67.2% of RAD and 92.4% of matched
points in Clarke error grid zone A (Table 2). These results are
similar to those studies in critically ill patients by Corstjens et al
 and Brunner et al . Both of the studies employed blood
gas/glucose analyzer and 6-hour interval for CGMS sensor
calibration. Our study indicates that, no matter what time interval
for sensor calibration recommended by manufacturer, CGMS
should be calibrated shorter than 6 hours. However, although
over 300 paired samples were analyzed in present study, we only
enrolled 18 patients in a single ICU. So the results of our study
may not be generalizable to other critically ill populations. Further
studies are needed in the field of real-time glucose monitoring.
There was only one CLD glucose measurement below
3.9 mmol/L during the study period. This may be contributed
to the fact that we only enrolled patients with hyperglycemia at
admission and we employ a conventional glucose control protocol
in our routine clinical practice. For comparison between
euglycemia and hyperglycemia, although RAD was not
significantly different in this two glucose levels, limits of agreement
between CGMS to CLD measurements was significantly more
negative in hyperglycemia (bias = 20.60 mmol/L, upper and
lower limits of agreement = 3.11 to 24.31 mmol/L) than that in
euglycemia (bias = 0.65 mmol/L, upper and lower limits of
agreement = 3.26 to 24.31 mmol/L), even in data sets within
6 hours after sensor calibration. This might be explained by the
lag of change for interstitial glucose concentration to serum
glucose concentration . Although this bias was clinical
acceptable, danger of underestimation of hyperglycemia by
CGMS also existed. To avoid this bias, reference measurement,
such as ICU-based blood gas/glucose analysis, should be
performed when CGMS monitoring exhibits abrupt change.
Blood gas analyzer with function of glucose measurement is one
of the most frequently used glycemic monitoring methods in ICU
settings [3,28,33]. Most of ICUs in China have been equipped
with this kind of instrument, and measurement of blood glucose
has become routine care in these ICUs . Several studies have
been carried out to determine the accuracy of blood gas/glucose
analyzers in blood glucose measurement [11,12]. In present study,
we used deep venous blood in glucose measuring by an ICU-based
gas/glucose analyzer. With serum glucose concentration measured
by CLD as reference, blood gas/glucose analyzer measurements
show a pretty good numerical and clinical accuracy, with
6.5%66.2% of RAD and 98.4% of points in Clarke error grid
zone A. This result indicates that the ICU-based blood gas/
glucose analyzer is an accurate alternative for CLD glucose
measurement, which can serve as a standard method for glucose
monitoring and CGMS sensor calibrating.
The major limitation in our study is that there were too few
glucose data below 3.9 mmol/L to investigate the accuracy of
CGMS monitoring in hypoglycemic state. After publication of
NICE-SUGAR study , many physicians in our ICU are
concerned about hypoglycemia during tight glucose control, and
therefore to employ a conventional glucose control protocol in
clinical practice. For further study, more patients are needed to
increase the chance of hypoglycemia for CGMS accuracy
investigation. In order to prevent the interruption of CGMS
reading on routine clinical care, we turned off alarm of CGMS
during the study. The main theoretical usefulness of CGMS is its
ability to detect glucose concentration variation and give alert.
Further study is needed to investigate the accuracy of CGMS
during change of glucose indicated by preset alarms.
Real-time subcutaneous CGMS is an accurate glucose
monitoring method in critically ill patients. CGMS sensor should be
calibrated less than 6 hours, no matter what time interval
recommended by manufacturer.
We would like to thank dear nurses in our ICU. This study would not have
been possible without their assistances. We also want to thank Ms. Rong
for her advices on English writing.
Number of data sets
Upper and lower limits of agreement (mmol/L)
Percentage of matched points in Clarke error grid
Table 2. RAD, limits of agreement analysis, and Clarke error grid analysis between CGMS and CLD values in data sets at different
time after CGMS sensor calibration and in different glycemic ranges.
Comparisons of RAD and bias were performed by unpaired t-test. Difference in percentage of matched points in Clarke error grid zone A was analyzed by x2 test. RAD
was calculated as absolute difference between time-matched CGMS and CLD value divided by CLD value, multiplied by 100. Bias was defined as the mean of the
difference between time-matched CGMS and CLD values (CGMS minus CLD). Euglycemic level was defined as CLD serum glucose concentration of 3.9 to 10.0 mmol/L,
and hyperglycemic level was defined as CLD serum glucose concentration greater than 10.0 mmol/L. Upper and lower limit of agreement were defined as bias61.96 SD
of the mean bias. CGMS = continuous glucose monitoring system. CLD = central laboratory device. RAD = relative absolute difference.
Data sets in different glycemic ranges
Conceived and designed the experiments: XYY YZ JXZ. Performed the
experiments: XYY YZ NNY JXZ. Analyzed the data: XYY YZ YHC JXZ.
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