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Glucose Measurement in the Operating Room: More Complicated than It Seems

Rice, Mark J. MD*; Pitkin, Andrew D. MBBS, MRCP, FRCA*; Coursin, Douglas B. MD

doi: 10.1213/ANE.0b013e3181cc07de
Patient Safety: Review Article
Chinese Language Editions

Abnormalities of blood glucose are common in patients undergoing surgery, and in recent years there has been considerable interest in tight control of glucose in the perioperative period. Implementation of any regime of close glycemic control requires more frequent measurement of blood glucose, a function for which small, inexpensive, and rapidly responding point-of-care devices might seem highly suitable. However, what is not well understood by many anesthesiologists and other staff caring for patients in the perioperative period is the lack of accuracy of home glucose meters that were designed for self-monitoring of blood glucose by patients. These devices have been remarketed to hospitals without appropriate additional testing and without an appropriate regulatory framework. Clinicians who are accustomed to the high level of accuracy of glucose measurement by a central laboratory device or by an automated blood gas analyzer may be unaware of the potential for harmful clinical errors that are caused by the inaccuracy exhibited by many self-monitoring of blood glucose devices, especially in the hypoglycemic range. Knowledge of the limitations of these meters is essential for the perioperative physician to minimize the possibility of a harmful measurement error. In this article, we will highlight these areas of interest and review the indications, technology, accuracy, and regulation of glucose measurement devices used in the perioperative setting.

Published ahead of print February 8, 2010 Supplemental Digital Content is available in the text.

From the *Department of Anesthesiology, University of Florida College of Medicine, Gainesville, Florida; and Department of Anesthesiology and Medicine, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin.

Supported by institutional funds from the University of Florida and the University of Wisconsin.

Disclosure: The authors report no conflict of interest.

Address correspondence and reprint requests to Mark J. Rice, MD, University of Florida College of Medicine, PO Box 100254, Gainesville, FL 32610-0254. Address e-mail to mrice@anest.ufl.edu.

Accepted November 11, 2009

Published ahead of print February 8, 2010

Dysglycemia, defined as diabetes-induced hyperglycemia in patients with undiagnosed diabetes, impaired glucose tolerance, impaired fasting glucose, stress-induced hyperglycemia, or hypoglycemia with or without exogenous insulin, is present in many perioperative patients. Current estimates place the prevalence of Type 2 diabetes in the American population older than 20 years at 12.9%. An estimated 40% of those individuals or 5% of the adult population in the United States remain undiagnosed and untreated.1 Stress-induced hyperglycemia develops in patients without diabetes and is attributed to insulin resistance caused by endogenous and exogenous catecholamines and glucocorticoids, excessive glycogenolysis and gluconeogenesis, and cytokine release secondary to inflammation.2,3 Therefore, blood glucose is measured routinely in the perioperative environment.

Intraoperative hyperglycemia has been shown to be detrimental during a variety of surgical procedures including general surgery,4,5 liver transplantation,6 and vascular7 and cardiac surgery.811 With evidence that tight control of blood glucose in the intensive care unit (ICU) may reduce mortality,12 the American Diabetes Association (ADA) published guidelines suggesting blood glucose in critically ill patients be kept as close to 110 mg/dL as possible and generally <140 mg/dL13; the Surviving Sepsis Campaign and the American Association of Clinical Endocrinologists made similar recommendations.14,15 The initial outcome benefit first observed in the ICU has not been replicated for intraoperative glucose control,16,17 and a subsequent meta-analysis of 34 randomized trials of intensive glucose control in the ICU found no effect on hospital mortality but did confirm an increased risk of hypoglycemia.18 The most recent large study of intensive glucose control (the “NICE-SUGAR” trial) showed that it increased the incidence of hypoglycemia and mortality among adults in the ICU.19 There is growing evidence that intense glucose control as currently practiced might not provide benefit in a heterogeneous critically ill patient population and the resulting increase in hypoglycemia is certainly concerning.20,21

Although a recent meta-analysis stated that tighter glucose control may be associated with improved outcome for surgical ICU patients, this remains open to investigation and should not be extrapolated to the dynamic intraoperative surgical setting.20*

It is evident that intraoperative or critical care control of blood glucose necessitates frequent monitoring of blood glucose to avoid hypoglycemia, but it is less well understood that there is a wide variation in accuracy of different glucose measuring instruments frequently used in hospitals today. There are currently 2 options for clinical glucose measurement. The first is a central laboratory device (CLD), and the second is a point-of-care (POC) device used in the clinical setting, producing a rapid and convenient blood glucose reading. In this article, the technology, accuracy, and regulation of blood glucose measurement systems in use today in the perioperative and critical care environment will be reviewed, with particular emphasis on the need for accurate results within the hypoglycemic range.

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POC GLUCOSE MEASUREMENT DEVICES

Efforts to improve glucose control for patients with diabetes led to the development of self-monitoring of blood glucose (SMBG) devices in the 1970s, designed to allow quick and easy blood glucose measurement at home using a small sample of capillary blood. Ease of use and speed led to these same devices being marketed in the hospital environment either unchanged from the home product or repackaged as a hospital-specific product using the same measurement technology. Two other devices not intended for SMBG use are marketed for clinical POC use: the iStat system (Abbot Point-of-Care, Princeton, NJ) and the HemoCue® analyzer (HemoCue, Lake Forest, CA). POC devices have 3 main advantages over CLDs: first, they are considerably less expensive; second, they give almost immediate results compared with the time taken to label, package, and send a sample to the laboratory and await the result to be reported; and third, the sample volume needed is minimal (<10 μL).22 The main disadvantage of POC devices is their lack of accuracy compared with CLDs.

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GLUCOSE MEASUREMENT TECHNIQUES

Because the glucose molecule is small and colorless, and thus very difficult to directly measure, all current clinical glucose measurement devices use an indirect enzymatic technique.23,24 Three enzyme systems are used. In CLD systems, hexokinase phosphorylates glucose to glucose-6-phosphate, which is subsequently oxidized by glucose-6-phosphate dehydrogenase using nicotinamide adenine dinucleotide (NAD) as a cofactor, forming NADH, which is measured optically. SMBG uses 2 basic technologies as shown in Figure 1:

  • Glucose oxidase catalyzes the oxidation of glucose to gluconic acid and hydrogen peroxide, the concentration of which is proportional to the concentration of glucose in the sample. The hydrogen peroxide causes a color change in a specific indicator dye that has been impregnated in the test strip. The extent of the color change is measured by an optical method (reflectometric technique). This method is most frequently used in older SMBG devices. Newer glucose oxidase devices use ferrocyanide instead of hydrogen peroxide and measure the current that is produced by the reaction, converting it into a glucose reading (amperometric method).
  • Glucose-1-dehydrogenase catalyzes the conversion of glucose to gluconolactone with concomitant conversion by a coenzyme of NAD to NADH. The NADH concentration is then proportional to the glucose concentration and can be measured by optical absorption at a wavelength of 340 nm or by the amperometric method. This reaction is also used in SMBG devices and the HemoCue analyzer.
Figure 1

Figure 1

Newer SMBG devices use glucose dehydrogenase (GDH) with the coenzyme pyrroloquinoline quinone (PQQ), which has the advantage of being insensitive to ambient oxygen and less subject to electrochemical interference. However, whereas glucose oxidase is extremely specific for glucose, GDH-PQQ may react with other sugars such as maltose, galactose, mannose, xylose, and ribose, and its specificity for glucose varies depending on its method of manufacture (microbially from Bacillus spp. or using recombinant DNA techniques). Patients receiving peritoneal dialysis using the osmotic agent icodextrin 7.5% may absorb and metabolize icodextrin to shorter polysaccharides, mainly maltose, causing erroneously high readings.2528 The GDH enzyme can also be denatured by high levels of urea,29 and falsely high readings may be produced by this system in the presence of high levels of uric acid, a reducing agent whose concentration is typically increased in renal failure.30 The results from some POC devices are also significantly affected by medications administered to patients in the perioperative and critical care environment such as acetaminophen, dopamine, L-dopa, and mannitol.31,32 Patient and environmental factors affecting accuracy are summarized in Table 1.24

Table 1

Table 1

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FACTORS AFFECTING GLUCOSE MEASUREMENT

Glucose concentration is typically reported as a plasma value rather than a whole blood concentration. The glucose concentration in plasma is approximately 11% higher than whole blood because of the higher water content in plasma (93%) compared with erythrocytes (73%). Therefore, a multiplier of 1.11 for the conversion of glucose in blood to plasma has been recommended.33 Plasma glucose concentration has traditionally been used because physiologic activity of glucose corresponds more closely with plasma concentration; therefore, CLDs always report glucose as a plasma value and most POC devices, although they measure whole blood glucose, are calibrated to report plasma glucose.34 Anemia decreases and polycythemia increases the difference between whole blood and plasma glucose not only for the above reasons but also through impedance of plasma diffusion into the test strip by the higher viscosity caused by increased hematocrit (Fig. 2).24,3537 A notable exception is the HemoCue, which gives reliable results over a wide range of hematocrit values.38 A number of newer meters have some compensation for varying level of hematocrit, be it anemia or polycythemia. Currently, there is limited information available for all commercially available devices and their various test strips in determining the presence of a potential error associated with an abnormally high or low hematocrit. Caution should be used by the clinician while interpreting a meter-measured glucose concentration in an anemic patient because there is the potential for the reading to be falsely elevated with some meters using certain test strips. A formula for compensation of the measured glucose value for this hematocrit effect has been proposed,39 but because newer devices may be unaffected by or already internally compensate for varying hematocrit (Fig. 3),40 any correction should only be applied if it is known to be appropriate for the specific meter in use.

Figure 2

Figure 2

Figure 3

Figure 3

Blood glucose sampling in the operating room can be taken from anywhere that blood is available including venous sites, arterial catheters, and fingertips. Fingertip sampling, most frequently used by patients with diabetes in the home environment, is similar physiologically to capillary blood. The ADA recommends using venous blood samples for measurement and reporting, because the use of capillary blood sampling (Table 2, No. 1) may lead to measurement error.41 In general, arterial blood has higher glucose levels than capillary blood, which in most circumstances is slightly higher than venous blood, although this sometimes depends on the rate of change of the concentration. The difference between capillary and venous glucose is typically not significant in nonhypotensive fasting subjects, but can be up to 8% higher in capillary blood with changing glucose concentrations.42,43 Circulatory shock results in increased tissue glucose extraction and a lower glucose value in capillary than venous blood. The arterial and central venous blood glucose are more likely to be underestimated when measuring capillary blood glucose specimens from severely hypotensive patients, resulting in an incorrect diagnosis of systemic hypoglycemia, compared with normotensive patients.44 Arterial blood glucose has been shown to be significantly higher than both capillary and venous blood glucose.45,46

Table 2

Table 2

A number of POC devices using glucose oxidase reactions in their testing media are susceptible to errors caused by high or low oxygen concentrations. Tang et al.47 showed that errors of ≥15% could occur in patients with a PaO2 >100 mm Hg. Conversely, these devices have been shown to underestimate blood glucose at altitude by 1% to 2% per 1000 feet of elevation,48,49 and errors of >15% have been shown when analyzing hypoxic blood (PO2 <44 mm Hg).50 The severity of the errors at low PaO2 is highly dependent on the type of test strip (electrochemical versus photometric) and the particular enzyme used.

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ACCURACY OF GLUCOSE MEASUREMENT DEVICES

Accuracy of blood glucose measurement devices is typically assessed using Clarke error grid analysis (EGA) whereby device results are plotted against those obtained from a reference device (Fig. 3). The graph is divided into zones representing the clinical significance of a result occurring within that area. In the Clarke EGA, zone A represents <20% deviation from reference, zone B consists of results with >20% deviation that would result in no or benign treatment, zone C represents overcorrection of acceptable blood glucose levels, zone D represents clinically dangerous failure to detect errors, and zone E results in erroneous treatment (contradictory decisions).51 Results in zones A and B are usually regarded as clinically acceptable. The EGA is illustrated by Stork et al.52 (Fig. 4) who compared the results obtained from the HemoCue, a POC device that uses photometric measurement of a GDH reaction, with those from a Yellow Springs Instrument (YSI), a CLD with very high accuracy. The samples were taken from volunteers with a wide range of blood glucose values obtained by insulin clamping,52 a research technique that uses a carefully controlled insulin infusion to test the range of a glucose measurement device. It is readily apparent that at low blood glucose levels, a clinically hazardous error may still occur within zone A, which has been expanded in the lower left corner of the graph. Evaluation of glucose measurement devices using Clarke EGA has been assigned considerable weight by the Food and Drug Administration (FDA), yet a potentially fatal measurement error in the hypoglycemic range could be found acceptable by using it.

Figure 4

Figure 4

Whereas the HemoCue exhibits good Clarke grid agreement with the reference instrument at hypoglycemic levels, the same is not true for all POC devices, especially those originally intended for SMBG use. Table 3 shows the percentage bias of 7 glucose meters from 4 different manufacturers compared with a reference CLD (also the YSI) over a range of blood glucose levels.22 A difference of >10% was observed >61% of the time for all blood glucose levels, and in the hypoglycemic range, a difference of >20% occurred 57% of the time. This disturbing lack of accuracy with low blood glucose values was echoed by Kanji et al.53 who found clinical agreement between a POC device (the Accu-Chek Inform®, Roche, Basel, Switzerland) and a CLD in 69.9% of arterial samples and 56.8% of capillary samples. During hypoglycemia, defined as <4.5 mmol/L (81 mg/dL), clinical agreement occurred in 55.6% of arterial samples and only 26.3% of capillary samples. Finkielman et al.54 retrospectively compared bedside glucose measurements (“bGlu”) using an SMBG device (SureStepFlexx®, LifeScan, New Brunswick, NJ) and 1 of 2 hospital CLDs (“pGlu”). On 18 occasions (of 816 simultaneous measurements) when the bGlu was reported as being <50 mg/dL, the simultaneous CLD results had a mean of 66.9 mg/dL, but with a range of 13 to 198 mg/dL. This is illustrated in Figure 5, which shows a second method to display glucose measurement device accuracy, the Bland-Altman difference plot.55 The authors concluded that “for the individual patient, bGlu gives an unreliable estimate for pGlu. All of those taking care of critically ill patients should be aware of the limitations of bedside glucometry.”

Table 3

Table 3

Figure 5

Figure 5

Slater-Maclean et al.56 investigated the accuracy of 3 SMBG devices (LifeScan SureStepFlexx, Roche Accu-Chek Inform, and Abbott FreeStyle® [Abbott Laboratories, Abbott Park, IL]) and a POC blood gas analyzer (Bayer Chiron 865®) compared with a CLD (the YSI) in critical care patients. Good agreement was found for one of the SMBG devices (the Abbott FreeStyle, Abbot Diabetes Care, Alameda, CA) and the blood gas analyzer compared with the reference measurement for arterial samples, although considerable inaccuracy occurred with capillary sampling. However, there were very few measurements <70 mg/dL and none <40 mg/dL, illustrating the difficulty of assessing accuracy in the hypoglycemic range. Hoedemaekers et al.57 compared 3 POC devices (Accu-Chek Sensor®, HemoCue, and Abbott Precision®) with a POC blood gas analyzer using glucose oxidase (RapidLab®, Siemens Diagnostics, Deerfield, IL) validated by a reference CLD, which uses the hexokinase method (Aeroset, Abbott Diagnostics, Basel, Switzerland). The paired samples were obtained from ICU and non-ICU patients whose blood glucose was managed according to the Van den Berghe et al. protocol.12 The results were compared with International Organization for Standardization standards (glucose values >4.1 mmol/L [74 mg/dL] need to be within 20% of reference values and <4.1 mmol/L [74 mg/dL] need to be within 0.8 mmol/L [14.4 mg/dL] of reference values, 95% of the time),58 which showed that “… glucose results from three POC testing devices were inaccurate in both the ICU and non-ICU patients. Among ICU patients, inaccurate glucose readings were most frequently falsely elevated, resulting in misinterpretation of high glucose values with subsequent inappropriate insulin administration or masking true hypoglycemia” (Fig. 6). They concluded that although “these POC devices seem attractive because of simple handling and rapid results, they should not be used in ICU patients.”57 Given the poor performance of POC devices in the hypoglycemic range, it is our opinion that they should not be used in conjunction with perioperative insulin therapy, and we appeal to investigators not to use them as diagnostic tools during investigator-initiated clinical trials.

Figure 6

Figure 6

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REGULATION OF GLUCOSE MEASUREMENT DEVICES

Glucose measurement devices for clinical use in the United States today are regulated by the FDA and are governed by the Clinical Laboratory Improvement Amendments Act.59 Manufacturers are required to demonstrate both accuracy of the device and supply evidence of testing for confounding factors (such as variations in hematocrit) that may lead to an inaccurate result. SMBG devices must also show satisfactory human factors performance before their introduction (Table 2, No. 2). This is important because results obtained from SMBG devices may vary considerably depending on the person operating the device. Manufacturers typically publish accuracy data obtained from testing under ideal conditions using trained technicians or highly selected patients; greater inaccuracy is seen with less-skilled users (Fig. 7).60 Where the results obtained in the operating room environment would be in this spectrum of results is unknown, but would clearly depend on the training of the particular operator. Clinical laboratory devices typically exhibit accuracy of 2.2% to 2.8% coefficient of variation (CV: the ratio of the SD to the mean),23 but as discussed earlier, POC devices have significantly greater imprecision. Blood gas analyzers have been shown to have accuracy similar to CLDs.61 The need to improve diabetes care by establishing widespread home glucose monitoring has resulted in a covert compromise between accuracy and convenience for SMBG devices. A panel assembled in 1996 by the FDA including representation from the ADA, National Institutes of Health, and Centers for Disease Control reviewed accuracy standards for home glucose meters and produced a consensus document calling for results from SMBG devices to be within 10% total error (bias plus imprecision) and for future meters to achieve <5% total error.62 Very few, if any, of the SMBG devices introduced since then have achieved this level of accuracy.56,60,63,64 Current guidance in draft form from the FDA has not changed significantly from 1996; the FDA target for accuracy (using ISO 15197:2003) for SMBG meters is 95% of readings within 20% of reference for glucose values of ≥75 mg/dL and within 15 mg/dL of reference in the hypoglycemic range. Specific guidance to manufacturers advises that they must “… clarify that critically ill patients (e.g., those with severe hypotension or shock, hyperglycemic-hyperosmolar state, hypoxia, severe dehydration, diabetic ketoacidosis) should not be tested with blood glucose meters because inaccurate results may occur” (Table 2, No. 3). Despite this advice, the perioperative environment has seen SMBG devices migrate into routine clinical practice in recent years where their lack of accuracy compared with CLD devices is not well publicized and thus allows the potential for serious clinical error to result, particularly in relation to recognition of hypoglycemic events.

Figure 7

Figure 7

In August 2009, the FDA issued an alert to warn health care practitioners of the potential for serious clinical errors with SMBG devices using GDH-PQQ enzyme systems in patients receiving icodextrin peritoneal dialysis solution and other therapeutic products containing nonglucose sugars such as immunoglobulins. Devices that use GDH-PQQ are listed in the FDA Web site referred to in Table 2, No. 4. The alert also reminded practitioners that CLDs do not use GDH-PQQ enzyme systems (hexokinase is typical for CLDs). This warning is a timely reminder of the limitations of current technology used in POC glucose measurement devices and the potential for serious clinical error that can result.

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SUMMARY

The recent upsurge of interest in improving glycemic control during the perioperative period has brought the subject of glucose measurement into sharp focus. Close glucose control, whatever the debate over its usefulness, demands frequent measurement of blood glucose, which makes the rapid results and bedside convenience of POC devices highly attractive to the clinician. This increased emphasis on monitoring blood glucose has been a significant factor in propelling the proliferation of SMBG devices into the hospital environment without an appropriate regulatory framework. Despite the FDA's guidance, SMBG devices are now frequently used in the perioperative and critical care settings where many users simply do not appreciate their lack of accuracy compared with laboratory glucose results. In addition, few SMBG devices currently marketed to hospitals have been assessed objectively in an appropriate patient population in the open literature; the lag between product release and evaluation means that their replacements, which often have a similar or identical trade name, may have very different performance characteristics. Whether the inaccuracy of SMBG devices (particularly in the hypoglycemic range) has contributed to the lack of clinical benefit of tight glycemic control seen in recent studies is unclear, but because many health care professionals do not appreciate that SMBG results cannot simply be substituted for CLD glucose results, there is the potential for significant harm. At present, we recommend avoiding use of SMBG devices for glucose measurement during perioperative clinical trials. Furthermore, the routine use of these instruments in the perioperative period should be on an individualized basis related to patient characteristics, medications, and intra- and postoperative events. Abnormal glucose levels should be corroborated using CLD technology. It is our responsibility as anesthesiologists, perioperative physicians, and intensivists caring for patients with a wide range of blood glucose values to understand the limitations of all glucose measurement devices used in the perioperative setting.

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AUTHOR CONTRIBUTIONS

All authors helped in manuscript preparation and literature search. All authors approved the final manuscript.

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ACKNOWLEDGMENTS

The authors thank John L. Smith, PhD, and Nikolaus Gravenstein, MD, for their helpful contributions to this review.

* Prielipp R, Coursin D. Perioperative glucose management in the operating room. Intensive insulin therapy for tight glycemic control. Proceedings from the Seventh Conference of the Cardinal Health Center for Safety and Clinical Excellence. San Diego, CA, 2007:24–6.
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