633485

research-article2016
DSTXXX10.1177/1932296816633485Journal of Diabetes Science and TechnologyPratumvinit et al

Original Article

Journal of Diabetes Science and Technology

The Effects of Temperature and Relative

1­–7
© 2016 Diabetes Technology Society
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DOI: 10.1177/1932296816633485

Measurements in Hospital Practice in a dst.sagepub.com

Tropical Clinical Setting

Busadee Pratumvinit, MD1, Nattakom Charoenkoop, MD1,

Soamsiri Niwattisaiwong, MD1, Gerald J. Kost, MD, PhD, MS, FACB2,
and Panutsaya Tientadakul, MD1

Abstract
Background: Hospitals in tropical countries experience conditions that exceed manufacturer temperature and humidity
limits for point-of-care (POC) glucose reagents. Our goal was to assess the effects of out-of-limits storage temperature,
operating temperature, and operating humidity on POC glucose measurement reliability.

Methods: Quality control measurements were performed monthly using glucose test strips stored under controlled
conditions and in inpatient wards under ambient conditions. Glucose test strips were evaluated in groups organized by
operating temperatures of 24-25 (group 1), 28-29 (group 2), and 33-34°C (group 3), and relative humidity (RH) of ≤70 (group
A), ~80 (group B), and ~90% (group C).

Results: Glucose results for different storage conditions were inconsistent. Measurements at higher operating temperatures
had lower values with mean differences of –2.4 (P < .001) and –36.5 (P < .001) mg/dL (28-29 vs 24-25°C), and –3.6 (P < .001)
and –37.4 (P < .001) mg/dL (33-34 vs 24-25°C) for low and high control levels, respectively. Measurements at higher RH had
lower values with mean differences of –4.0 (P < .001) and –13.2 (P < .001) mg/dL (~80 vs ≤70% RH), and –5.8 (P < .001) and
–16.6 (P < .001) mg/dL (~90 vs ≤70% RH) for low and high levels, respectively.

Conclusions: High temperature and high RH decreased glucose concentrations for the POC oxidase-based system we
evaluated. We recommend that individual hospitals perform stress testing, then determine if maximum absolute differences,
which represent highest risk for patients, are clinically significant for decision making by using error grid analysis.

Keywords
environmental stress, glucose, glucose meter, humidity, point of care, and temperature

Inaccuracy of glucose monitoring may derive from test strip, Methods

patient, pharmacological, environmental, and other factors.1
Incorrect results may cause serious harm and change clinical Glucose Meters and Test Strips
decisions.2,3 To ensure reliable results, POC devices and test We evaluated the photometric SureStep®Flexx meter,
strips should be stored and operated according to manufac- SureStep™ Hospital glucose test strips, and control solutions
turer specifications. In tropical settings, temperature and
relative humidity may exceed specified ranges. 1
Department of Clinical Pathology, Faculty of Medicine Siriraj hospital,
Our goal was to assess the effects of storage tempera- Mahidol University, Bangkok, Thailand
2
Point-of-Care Testing Center for Teaching and Research, School of
ture, operating temperature, and operating relative humid-
Medicine, University of California and Knowledge Optimization®, Davis, CA,
ity (RH) when ambient conditions in patient ward areas USA
naturally exceeded manufacturer limits because of the
Corresponding Author:
tropical setting of Siriraj Hospital. During ISO 228704,5
Busadee Pratumvinit, Department of Clinical Pathology, Faculty of
certification inspection, we discovered out-of-limit tem- Medicine Siriraj Hospital, Mahidol University, 2 Wang Lang Rd, Bangkok
perature and RH discrepancies that had to be investigated noi, Bangkok 10700, Thailand.
and corrected. Email: busadee.pra@mahidol.ac.th

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2 Journal of Diabetes Science and Technology 
(LifeScan, Milpitas, CA), which use glucose oxidase enzyme
specific for D-glucose to report a plasma glucose-calibrated
result. Glucose in blood interacts with glucose oxidase to
produce gluconic acid and hydrogen peroxide. Peroxidase on
the test strip causes the hydrogen peroxide to react with dyes
and produce a blue color, the intensity of which is correlated
with the concentration of plasma glucose. Test strips expired
4 months after opening. According to manufacturer specifi-
cations, test strips and control solutions should be stored out-
side a refrigerator in a cool and dry location below 30°C
(86°F) and used at an operating temperature of 18-30°C
(64.4-86°F) and RH of 30-70%.
The study was performed at Siriraj Hospital, a tertiary
care teaching and public hospital in Bangkok during
November 2007-March 2008, February-March 2012, and
June-July 2011, for storage temperature, operating tempera-
ture, and operating humidity experiments, respectively.
Siriraj Hospital, the largest university hospital of Thailand,
has 2200 beds, 15 critical care units, 1800 physicians includ-
ing residents, and 3000 registered nurses.
Approximately 500 000 POC glucose tests are performed
per year in 147 sites. Personnel performing POC glucose
tests comprise 2200 nurses, 230 residents, 660 medical stu-
dents, 15 clinical pathologists, and 60 laboratory technicians,
all trained to competency levels specified in ISO 22870.
Storage Temperature Experiment
Experiments were performed in actual ambient conditions
over 2 consecutive 4-month periods, from November to
February, considered winter in Thailand, and during summer
and the early rainy season, March to June. In each period,
test strips and low and high control solutions with the same
lot number were used.
To assess the effects of ambient temperature on test stabil-
ity, half of the strips were stored in the medical storage unit
(controlled condition) of Siriraj Hospital, while the other half
were kept in different non-air-conditioned inpatient wards: 5
wards (wards A-E) during November to February, and 6
wards (wards A-F) during March to June. The temperature of
the storage room was controlled at 25°C (77°F).
Ambient temperatures in the medical storage unit and
inpatient wards were measured every hour with 24-hour con-
tinuous temperature monitors (ESCORT Intelligent MINI
data loggers, Cryopak, Edison, NJ). Because control solu-
tions can be used for 3 months after opening, new bottles of
control solutions (the same lot) were used at the end of the
third month in each study period.
We performed glucose measurements using quality con-
trol solutions stored in the storage unit and inpatient wards
by the same operator monthly to avoid introducing operator
bias. The same lots of 2 levels of control solutions, and a
single glucose meter were used for all sites. Glucose concen-
trations were measured by using 1 test strip for each control
level from each vial stored in each storage site. Glucose con-
centrations obtained from unopened strip and control
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solution bottles at each site at the beginning of each study
period were used as baseline.
Operating Temperature Experiment
Two levels of control solutions were used to obtain glucose
measurements at 3 ambient temperature ranges: 24-25 (group
1), 28-29 (group 2), and 33-34°C (group 3) (75.2-77, 82.4-
84.2, and 91.4-93.2°F), 1 day per temperature range (n = 20
per group). The same glucose meter and the same lot of QC
reagents stored under controlled condition were used in this
experiment. The first 2 temperature ranges were observed in
air-conditioned settings and were within manufacturer speci-
fications, while group 3 was in a setting that lacked air-
conditioning and was out-of-limit. All test results were
obtained by a single operator.
Operating Relative Humidity Experiment
Glucose concentrations in 2 levels of control solution
reagents were measured at ambient RH ≤70% (control group
or group A, n = 20). In the experimental groups, out-of-limit
glucose concentrations were measured at ambient RH of
approximately 80 (group B, n = 18) and 90% (group C,
n = 20). The experiment was performed in 1 day per each RH
range with 1 glucose meter and the same test strip lots stored
under controlled condition by a single operator.
Statistical Analysis
Data for comparisons were normally distributed without out-
liers. Statistical analysis was performed using 1-way ANOVA
Dunnett’s test for comparisons of glucose results in storage
temperatures among different months and baseline, and dif-
ferent operating temperatures and operating humidity.
Unpaired t-test for the means was used to compare mean glu-
cose concentrations between the medical storage unit and
inpatient wards each month. A P value < .05 was considered
statistically significant. We used PASW version 18.0 for
Windows (SPSS Inc, Chicago, IL).
Results
Storage Temperature Experiment
During November to January, no temperatures exceeded
30°C in the medical storage unit. Temperatures were elevated
in up to 29.0% (481/1658 recordings) of the inpatient wards
(Table 1). Wards had 1657-1658 records available for analy-
sis during November to January except ward A, which had
only 168 records due to the technical omissions. The tem-
perature in the medical storage unit was monitored and veri-
fied to be within acceptable range during November to
January, so we did not record it during March to June.
Temperatures exceeding 30°C (86°F) were 0.8-71.6% of
inpatient wards during this period (Table 1).
Pratumvinit et al 3

Table 1.  Storage Temperatures in the Medical Storage Unit and Inpatient Wards During 2 Periods: November to January (Winter) and
March to June (Summer and Early Rainy Season).

Medical
storage unit Ward A Ward B Ward C Ward D Ward E Ward F
Nov-Jan
N 1658 168 1658 1658 1657 1658 NA
Mean ± SD (°C) 22.1 ± 0.8 27.9 ± 1.1 29.4 ± 1.4 28.6 ± 1.7 29.1 ± 1.6 27.2 ± 1.2 NA
Mean ± SD (°F) 71.8 ± 1.5 82.2 ± 1.9 85.0 ± 2.5 83.5 ± 3.0 84.3 ± 2.9 80.9 ± 2.1 NA
Min-Max (°C) 20-28.5 26-29.5 25-32.5 24-32 24-32.5 24-31 NA
Min-Max (°F) 68-83.3 78.8-85.1 77-90.5 75.2-89.6 75.2-90.5 75.2-87.8 NA
% T>30°C (86°F) 0 0 29.0 17.1 22.6 0.2 NA
Mar-Jun
N NA 2771 2771 2771 2771 2771 2771
Mean ± SD (°C) NA 28.5 ± 1.3 30.5 ± 1.0 30.6 ± 0.9 30.1 ± 1.3 27.3 ± 1.0 30.2 ± 0.9
Mean ± SD (°F) NA 83.3 ± 2.4 86.9 ± 1.8 87.1 ± 1.6 86.1 ± 2.3 81.2 ± 1.8 86.3 ± 1.6
Min-Max (°C) NA 24-32 24.5-34 24-32.5 24.5-33.5 24.5-31.5 25-33
Min-Max (°F) NA 75.2-89.6 76.1-93.2 75.2-90.5 76.1-92.3 76.1-88.7 77-91.4
% T>30°C (86°F) NA 11.3 58.7 71.6 46.6 0.8 46.4

N, number of data points for temperature record, which was done every hour; NA, not available; T, temperature.

Figure 1 shows glucose measurement results using low
and high level control solutions for strips stored in the medi-
cal storage unit and inpatient wards. Glucose concentrations
differed significantly in November, December, and February
(P = .019, .026, <.001 for low level; P = .027, .025, .019 for
high level). Only the low level was significantly different at
baseline, in March, April, and May (P = .039, .043, .024, and
.027, respectively).
By ANOVA and Dunnett’s multiple comparison testing,
glucose concentrations tested with strips stored in the medi-
cal storage unit from the following months were not different
from baseline except for low level control solutions between
March and baseline (P = .012), as well as April and baseline
(P = .002). For glucose strips stored in inpatient wards, glu-
cose concentrations were different in the low level control
between February and baseline (P < .001). The range of glu-
cose concentration in low level control tested by strips stored
in inpatient wards was highest in April (10 mg/dL), the hot-
test month of the year. In addition, the range in high level
control of strips in inpatient wards was highest during March
and April (55 mg/dL) (Figure 1).
Operating Temperature Experiment
Table 2A shows actual temperature and RH. Operating tem-
perature was divided into 3 groups: 24-25 (group 1), 28-29
(group 2), and 33-34°C (group 3); RH was within acceptable
range for all temperature groupings. When the temperature
was low, RH also was low. Mean differences in low control
and high control solutions between group 2 and group 1 were
–2.4 (95% CI –1.0, –3.8, P < .001) and –6.5 (95% CI –26.7,
–46.3, P < .001) mg/dL, respectively. Mean difference between
group 3 and group 1 were –3.6 mg/dL (95% CI –2.1, –5.1,
P < .001) for low level and –37.4 mg/dL (95% CI –27.6, –47.1,
P < .001) for high level control solution (Figure 2).
Operating Humidity Experiment
Table 2B shows the actual temperature and RH at RH ≤70
(group A), ~80 (group B), and ~90% (group C). The operat-
ing temperature was within acceptable limits for all RH
groupings. Mean difference between groups B and A was
–4.0 mg/dL (95% CI –2.8, –5.1, P < .001), and between
groups C and A, –5.8 mg/dL (95% CI –4.7, –6.9, P < .001) for
low level control solution. For the high level control solution,
mean difference between groups B and A was –13.2 mg/dL
(95% CI –5.9, –20.5, P < .001), and between groups C and A,
–16.6 mg/dL (95% CI –9.5, –23.7, P < .001) (Figure 3).
Clinical Impact
We assessed the clinical impact of the glucose measurement
by using the surveillance error grid.6 We used the maximum
value of glucose concentration in each experimental group as
the reference blood glucose (BG) and the minimum value of
glucose concentration in each group as the measured BG in
the software by Kovatchev et al.7 We found that paired com-
parisons of maximum and minimum values of glucose con-
centrations in each experiment were within zone A, which
was the allowable total error region usually associated with
no harm.6
Discussion
The most impactful results in this research were higher oper-
ating temperature resulted in lower glucose concentrations,
and higher operating RH also resulted in lower glucose con-
centrations. Not all inpatient wards maintained storage tem-
perature below 30°C. Glucose concentration differences
between the medical storage unit and inpatient wards were
inconsistent with respect to time and levels of the control

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4 Journal of Diabetes Science and Technology 

Figure 1.  Comparison of glucose measurements from storage temperature experiments between 2 periods in the medical storage unit
and inpatient wards. Results were obtained with glucose test strips stored in the medical storage unit (black solid lines) for 4 months
and in inpatient wards (gray solid lines) for 4 months during 2 periods: November to February (A, C) and March to June (B, D). Frames
A and B show glucose measurements obtained with the low control reagent, C and D with the high control reagent. Means are shown
with 95% confidence interval (CI) cross bars. The dashed lines show the span of the minimum and maximum glucose concentrations.
Note that in some cases, the range was quite high. In the first period, the number of replicates was 10, 10; 10, 8; 8, 8; 8, 8; and 8, 8 for
baseline, November, December, and February, respectively. In the second period, the number of replicates was 12 for baseline and all 4
months (March to June). *P < .05. ***P < .001.

solution when assessed with respect to baseline. Storage
temperature, operating temperature, or RH might be the
cause of these differences.
When the operating temperature increased, glucose con-
centration decreased, as shown in Figure 2. Glucose concen-
trations measured at 28-29 and 33-34°C were statistically
significantly lower than those measured at 24-25°C.
However, glucose concentration measured at 28-29°C, as
specified by the manufacturer, was not different from that
measured at 33-34°C using the high level control. For the
low level control, glucose concentration measured at
28-29°C was different statistically from that measured at
33-34°C, but the mean difference of 1.2 mg/dL was not clin-
ically significant.
Increased RH generated lower glucose values as shown in
Figure 3. Previous studies have demonstrated that high tem-
perature and high RH affected glucose values from different
manufacturers differently. For example, high operating

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Pratumvinit et al 5

Table 2.  Actual Temperature and Relative Humidity in Different Groups of Operating Temperature (A) and Operating Humidity (B).
A.

Operating temperature Group 1, 24-25°C Group 2, 28-29°C Group 3, 33-34°C

experiment (75.2-77°F) (82.4-84.2°F) (91.4-93.2°F)
Actual temperature
Range (°C) 23.6-26.4 28.2-29 32.9-34.2
Range (°F) 74.5-79.5 82.8-84.2 91.2-93.6
Actual humidity (%)
Range 40-55 57-64 62-69

B.

Operating humidity experiment Group A, ≤70% Group B, ~80% Group C, ~90%

Actual temperature
Range (°C) 26.4-27.9 27.8-28.5 27.3-28.5
Range (°F) 79.5-82.2 82.0-83.3 81.1-83.3
Actual relative humidity (%)
Range 49-70 79-83 89-90

Figure 2.  Glucose concentrations (mean, 95% CI) observed with low level (A) and high level (B) control solutions. Data were obtained
at the operating temperatures of 24-25°C (75.2-77°F), 28-29°C (82.4-84.2°F), and 33-34°C (91.4-93.2°F); n = 20 for each group. The
dashed lines represent the minimum and maximum glucose concentrations. Operating temperature specified by the manufacturer is 18-
30°C (64.4-86°F). *P < .05. ***P < .001.

temperature results in overestimates by some glucose
meters,8,9 while others underestimate.10 Lam et al showed that
short-term exposure (15 minutes) of glucose test strips and
meters to high temperature and high humidity resulted in ele-
vated glucose results as high as 33 mg/dL, and that the com-
bined effects of stressing both meters and test strips at the
same time were synergistic.11
Degradation of enzyme may explain the changes in test
performance. With simulated disaster climates, such as
Hurricane Katrina (set point range 20-45°C [68-113°F];
humidity, 31-96%), glucose values were lower with
glucose-oxidase based test strips results, and higher with
glucose-dehydrogenase based test strips.12 Studies have
examined the instability of glucose oxidase enzyme.13-15
High temperature dissociates flavin adenine dinucleotide
cofactors and destroys the secondary and tertiary structure of
glucose oxidase.
Cembrowski et al performed BG measurements using
SureStep®Flexx and found that the glucose concentrations
for the quality control solutions and patient samples were
consistently higher in the winter months. This finding is
probably due to the very low indoor humidity associated

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6 Journal of Diabetes Science and Technology 

Figure 3.  Glucose concentrations (mean, 95% CI) measured using low level (A) and high level (B) control solutions at ≤70% (n = 20),
~80% (n = 18), and ~90% (n = 20) relative humidity. The dashed lines represent the minimum and maximum glucose concentrations.
Operating humidity specified by manufacturer is 30-70%. ***P < .001.

with external subzero temperatures. Low humidity will be
accompanied by rapid evaporation of blood samples. The
average weekly temperatures in that study varied from –25°C
in the winter to +20°C in the summer.16 Our study was per-
formed in a clinical tropical setting where we found that
higher operating temperature and RH decreased glucose val-
ues. In general, environmental factors can affect several POC
tests and quality control reagents as well.16-20
To our knowledge, this is the first article to use error grids6
for the assessment of environmental effects on bedside glu-
cose meter performance in a tropical country. Using the maxi-
mum value in each group as the reference BG and the
minimum value in each group as the measured BG in the soft-
ware by Kovatchev et al,7 found that paired data of maximum
and minimum values of glucose concentrations in all 3 exper-
iments were within zone A, an allowable total error region
usually causing no harm.6 Siriraj Hospital POC Committee,21
composed of physicians from several departments, agreed
that while the effects of temperature and RH thus far did not
appear to have affected medical decision making, maximally
discrepant results had potential to do so. Hence, precaution-
ary measures will be implemented to preserve the quality of
bedside testing on clinical wards in the future.
Siriraj Hospital critical care areas are air-conditioned. We
confirmed that temperature and RH are maintained within
manufacturer specifications, so there was no need to study
environmental stress effects in critical care units. One limita-
tion of our study was that higher temperatures were accompa-
nied by higher RH. Therefore, effects of temperature on test
strip enzyme may be confounded by simultaneous alteration
of RH. The use of QC reagents was a logical first step, since
each glucose meter must perform within manufacturer speci-
fications, but at the same time, represents a limitation of the
study. Cembrowski et al observed that glucose concentrations
for QC solutions were higher in the winter months and found
the same results in human blood.16
Conclusions
High temperature and RH decreased the glucose values
obtained with glucose oxidase-based meters. Therefore, we
recommend performing quality control if out of range of
operating temperature or RH occurs. Glucose test strips
should be used only if quality control results are within
acceptable ranges. Proper monitoring of temperature and RH
during storage and test performance is necessary to ensure
reliability. In tropical countries, risk management principles,
for example, individualized quality control plans,22 can be
implemented to ensure the quality of test results, which may
be affected by environmental stresses. These precautions
should facilitate ISO certification and long-term quality of
patient care.
Abbreviations
BG, blood glucose; CI, confidence interval; POC, point of care;
QC, quality control; RH, relative humidity.
Acknowledgments
We thank Suthipol Udompunturak, MSc, and Julaporn Pooliam,
MSc, for their help in the statistical analysis.
Declaration of Conflicting Interests
The author(s) declared no potential conflicts of interest with respect
to the research, authorship, and/or publication of this article.
Funding
The author(s) disclosed receipt of the following financial support
for the research, authorship, and/or publication of this article: BP

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Pratumvinit et al 7
and PT were supported by Chalermprakiat grants from the Faculty
of Medicine Siriraj Hospital, Mahidol University.
13. Zoldak G, Zubrik A, Musatov A, Stupak M, Sedlak E.
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