Relationship between Near Infrared Spectroscopy and Intra-compartmental Pressures

The Journal of Emergency Medicine, Vol. 44, No. 2, pp. 292–298, 2013 Copyright Ó 2013 Elsevier Inc. Printed in the USA. All rights reserved 0736-4679/$ - see front matter

http://dx.doi.org/10.1016/j.jemermed.2012.06.018

Original Contributions

RELATIONSHIP BETWEEN NEAR INFRARED SPECTROSCOPY AND INTRA-COMPARTMENTAL PRESSURES William M. Reisman, MD,* Michael S. Shuler, MD,† Tracy L. Kinsey, MSPH,† Ashley L. Cole, MPH,‡ Thomas E. Whitesides Jr., MD,* Maria G. Davila, MD,* Emily K. Smith, MPH,† and Thomas J. Moore, MD* *Emory University, Atlanta, Georgia, †Athens Orthopedic Clinic, Athens, Georgia, and ‡J and M Shuler Inc., Athens, Georgia Reprint Address: Michael S. Shuler, MD, Athens Orthopedic Clinic, 1765 Old West Broad St., Bldg #2 - Suite 200, Athens, GA 30606

, Abstract—Background: Near infrared spectroscopy (NIRS) has been suggested as a possible means for detecting perfusion deficits in patients with acute compartment syndrome (ACS). Study Objectives: To longitudinally examine NIRS in an ACS model to determine its responsiveness to decreasing perfusion pressure. Methods: A NIRS sensor pad was placed under a tourniquet over the anterior compartment in the mid-tibia region on 20 volunteers. Initial perfusion pressures and NIRS values were recorded. The tourniquet pressure was sequentially raised by 10 mm Hg in 10-min intervals until systolic pressure was surpassed. NIRS values and perfusion pressure were determined at the end of each 10-min interval. Results: There was no change in mean NIRS values from the initial baseline until 30 mm Hg of perfusion pressure was reached. Additionally, a statistically significant drop in mean NIRS values was observed as perfusion pressures dropped from 10 mm Hg to 0 mm Hg, and again with subsequent decreases of 10 mm Hg perfusion pressure until systolic pressure was surpassed. Conclusions: These results coincide with previously published studies using alternative methods of measuring blood flow or perfusion. NIRS values were responsive to decreasing perfusion pressures over a longitudinal period of time in an ACS model. These results suggest that NIRS may be useful for continuous, non-invasive monitoring of patients for whom ACS is a concern. Additional studies on traumatized patients are required. Ó 2013 Elsevier Inc.

INTRODUCTION Acute compartment syndrome (ACS) can have catastrophic sequelae if not diagnosed and treated appropriately. Clinical suspicion confirmed with physical examination and intra-compartmental measurements are the mainstay for diagnosis (1,2). The pressure gradient between the diastolic blood pressure and the intracompartmental pressure (ICP), known as the perfusion pressure (PP), is the critical variable in determining tissue perfusion (3–7). Although intramuscular measurements are invasive and can vary greatly if not performed correctly, pressure measurements are the only objective tool currently available to clinicians (8–13). Near infrared spectroscopy (NIRS) has been used to measure the tissue oxygenation in multiple clinical areas. NIRS has received the most attention to date in cerebral perfusion and has been validated in multiple studies (14–18). Similar to a pulse oximeter, NIRS utilizes visible light to determine the proportion of oxygenated and deoxygenated hemoglobin approximately 2–3 cm below the skin surface (16,19–21). Several studies have examined NIRS in the setting of ACS (22–26). Giannotti et al. and Shuler et al. both examined NIRS in the setting of established ACS (25,26). However, in both these studies, a single NIRS reading was obtained at a single point in time. One of the potential benefits of NIRS is its ability to provide

, Keywords—compartment syndrome; near infrared spectroscopy; perfusion pressure

RECEIVED: 19 August 2011; FINAL SUBMISSION RECEIVED: 28 February 2012; ACCEPTED: 28 June 2012 292

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continuous and responsive readings of muscle oxygenation. The purpose of this prospective study was to evaluate a clinically available NIRS device and determine its responsiveness with respect to increasing ICPs and a decreasing perfusion gradient. To correlate NIRS values with perfusion pressure, an established model for ACS was implemented using a tourniquet around the lower leg. This model has been validated in previous studies (27–34). MATERIALS AND METHODS Institutional review board approval and consent from each volunteer was obtained for the study. Twenty volunteers were recruited and enrolled for evaluation from hospital house staff and faculty. Inclusion criteria for this study included male and female subjects between the ages of 16 and 75 years who were willing to participate in the study. Exclusion criteria included volunteers with previous injury to the lower extremity, vascular disease or insufficiency, or pulmonary disease. For each subject, age, sex, race, body mass index (BMI), and calf circumference were recorded. NIRS measurements were determined using an INVOS cerebral oximeter (Somanetics, Troy, MI), a continuous dual-wavelength near infrared spectrometer. Based on the differential absorption characteristics of deoxyhemoglobin and oxyhemoglobin, muscle oxygenation can be determined (14–16,18,35). Each volunteer was supine with the heel on a rolled sheet to maintain the leg at the height of the heart (Figure 1). A NIRS sensor was positioned on the surface of the skin at the mid-diaphyseal region, over the anterior compartment. A 10-cm-wide lower leg tourniquet (Zimmer ATS 2000, Zimmer Inc., Warsaw, IN) was placed on the ipsilateral leg over the NIRS sensor, to manipulate perfusion under the sensor. Dahn et al. showed that tourniquet pressure was within 1–2 mm Hg of the ICP under the tourniquet (31). A sphygmomanometer (Dinamap Pro 400 V2, GE, Fairfield, CT) placed on the brachium of the volunteer was used to obtain blood pressure measurements. After NIRS pad and tourniquet placement, an initial 2-min period was used to obtain a sustained baseline. The NIRS device cycled every 6 s to display a new value, which is stored in its internal memory. The tourniquet was then inflated to 10 mm Hg. At the end of a 10-min interval, NIRS values and blood pressure were recorded. The tourniquet was then raised by 10 mm Hg for another 10-min interval. Repeat measurements were performed at the end of each 10-min interval for blood pressure and muscle oxygenation. This process was repeated until the systolic blood pressure was surpassed; once it was surpassed, the cuff was deflated to minimize volunteer

Figure 1. A photograph of the near infrared spectroscopy (NIRS) pad placed under a tourniquet with the heel on a rolled towel with the patient lying supine.

discomfort and risk of complication. As per protocol, the cuff would be deflated if not tolerated. Statistical Analysis NIRS values were normalized to each patient’s baseline value and reported as the NIRS difference (NIRS value minus baseline NIRS value before any cuff inflation). Perfusion pressure (mm Hg) was calculated as diastolic blood pressure minus tourniquet pressure. NIRS differences were plotted across decreasing perfusion pressures. Mean values for NIRS difference were calculated within 10-mm Hg intervals of perfusion pressure to characterize the average change during each interval. The signed rank test was used to test whether mean NIRS values of each perfusion pressure interval were significantly different from baseline. The Mann-Whitney test was used to test for differences of mean values between adjacent intervals. RESULTS Twenty adult volunteers were recruited to participate. The average age was 30 (range: 25–37) years. There were 14 male and 6 female subjects. The mean BMI was 26 (range: 19–30) kg/m2. Calf circumference averaged 39 (range: 34–47) cm. There were no trends found based on BMI or calf circumference and NIRS values. There were 14 white, three black, two Asian, and one Hispanic subject. All subjects tolerated the full protocol; no volunteer required the study be stopped early secondary to pain. Figure 2 shows the individual and mean patterns of longitudinal change in NIRS values from baseline as PP decreases. No significant changes were observed in mean NIRS values from the start of cuff inflation until 30 mm Hg of PP was reached (mean NIRS difference at interval of 25 to 34 mm Hg = 2.5 percentage points, p < 0.001;

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Figure 2. Line graph illustrates the individual patterns (n = 20 subjects) of change of near infrared spectroscopy (NIRS) value from baseline as perfusion pressure decreased during the experiment. For each subject, pressure of the cuff was raised by 10 mm Hg every 10 min, with NIRS value and blood pressure measurements obtained at the end of each time interval immediately before the next increase of cuff pressure. At each point of measurement, NIRS value change from baseline was calculated as preexperiment baseline value minus the current value, and diastolic perfusion pressure was calculated as diastolic blood pressure minus cuff pressure. Red circles indicate the mean value of NIRS difference from baseline across subjects within each 10-mm Hg range of perfusion pressure (range = y-axis value minus 5 mm Hg to plus 4 mm Hg).

Table 1). Increasingly rapid declines were observed with decreasing PP (Figure 2). A statistically significant drop in mean NIRS values was observed as PP dropped from 10 mm Hg to 0 mm Hg, and again with subsequent intervals, until 20 mm Hg was reached (3.6, 5.6, and 18.3 percentage point decline in average change in NIRS values between 10 and 0, 0 and 10, and 10 and 20 mm Hg perfusion pressure intervals, respectively; p = 0.001, p = 0.023, and p = 0.001, respectively; Table 1). Figure 3 shows the NIRS values for one patient over time. DISCUSSION ACS is defined by poor perfusion, culminating in muscle and nervous tissue necrosis. NIRS provides an opportunity for continuous monitoring of tissue oxygenation, the critical factor in ACS. Previous studies have demonstrated an inverse correlation between NIRS and compartment pressures, as well as the ability of NIRS to detect diminished muscle oxygenation in established ACS patients (25,26). This study examines the responsiveness of NIRS to increasing compartment pressures over time in an ACS model. The results of this study demonstrate the responsiveness of NIRS to increasing compartment pressures (and decreasing perfusion pressure) over time. In particular, the changes observed in NIRS values in the presence of gradually increasing pressure corresponded remarkably well with the most important clinical thresholds in perfu-

sion pressure. The earliest significant change in NIRS from baseline was seen at approximately 30 mm Hg of perfusion pressure (Table 1; p = 0.001), consistent with the observed onset of muscle injury and necrosis and the suggested threshold for decompression (4,5,7). As perfusion pressure dropped to approximately 10 mm Hg (a known point of ischemia), the average NIRS difference of subsequent 10 mm Hg intervals were significantly decreased from their adjacent preceding interval. This suggests a trend of rapid decline beginning at approximately 10 mm Hg perfusion pressure, on average (Figure 2). Blood flow or muscle oxygenation measured by NIRS showed minimal changes until tourniquet pressures approached diastolic pressure. Once diastolic pressure was surpassed, the NIRS readings dropped off precipitously. Muscle oxygenation continued to fall as pressures surpassed mean arterial pressure and approached systolic pressure. NIRS values declined dramatically after perfusion pressure dropped below 10 mm Hg. Perfusion pressure of +10 to 0 mm Hg was associated with NIRS values of approximately 5–8 average percentage points below baseline (Table 1), suggesting that a possible threshold for detection of decreased compartment pressure might exist at some magnitude of NIRS difference larger than 8 percentage points below baseline. Further studies, including sensitivity and specificity analyses and large samples of injured subjects, are needed to properly determine a viable diagnostic cut point.

0.215 <0.001§ 0.023§ NIRS = near infrared spectroscopy. * Perfusion pressure (mm Hg) = diastolic blood pressure tourniquet pressure; Interval range = value minus 5 to value plus 4. † Signed rank test for whether mean NIRS values changed significantly from baseline. ‡ Mann-Whitney test for whether mean NIRS value changed significantly from the preceding interval. § Statistically significant changes.

0.295 0.972 0.513

0.386

0.570

0.294

0.299

0.009§

<0.001§ 4.4 <0.001§ 18.3§ <0.001§ 5.6§ <0.001§ 1.2 0.897 0.1 1.00 0.3

1.00 0.2

0.220 0.3

0.084 1.5

0.001§ 0.9

<0.001§ 0.9

<0.001§ 3.6§

36.5§ 32.1§ 13.8§ 4.6§ 3.4§

Mean NIRS (%) change (from patient’s baseline) p Value† Mean NIRS (%) change (from preceding interval) p Value‡

0.0

+0.3

+0.1

+0.2

0.1

1.6

2.5§

10

8.2§

295

20 30 40 50 60 70 80 90 Perfusion Pressure Interval* (interval range = 5 to value +4)

Table 1. Change of NIRS (%) from Patients’ Baseline Measurements with Decreasing Perfusion Pressure

0

10

20

30

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Previous studies evaluating a threshold for cerebral hypoxia using NIRS technology are consistent with the results observed in this study. Kurth et al., who monitored brain lactate, adenosine triphosphate levels, electroencephalograms (EEGs), cerebral blood flow, and sagittal sinus oxygen levels on piglets, observed a mean decrease of 24 percentage points from baseline when signs of hypoxia were detected (36). Cho et al. used somatosensoryevoked potentials and EEGs to determine brain ischemia among patients undergoing carotid endarterectomy (37). Using the INVOS, they observed an average drop in tissue oxygenation of 11 percentage points among patients who showed ischemic changes, compared to a 3-percentagepoint drop in those with well-perfused brains. Although the metabolic characteristics of skeletal muscle and cerebral tissue are not identical, these studies offer support for the percentage point change threshold observed in this study. Limitations There are some limitations to this study. Although compartment syndrome can only be simulated using circumferential compression and elevation in humans, there are several inherent weaknesses with a tourniquet model for simulation of a compartment syndrome. Heppenstall et al. described the effects of tourniquet application when compared to intra-compartmental infusion, using the Starling model (33). Blood flow decreases as cuff pressure approaches diastolic pressure, but limited flow does continue due to systolic pressures and venous congestion until systolic pressure is surpassed by the cuff. However, this phenomenon of continued flow above diastolic pressures was detectable using NIRS. Although perfusion did decline precipitously once tourniquet pressure rose above diastolic, there was still some indication of flow, because values continued to decline as compression was increased over diastolic. Pressure measurements were obtained using standard tourniquets and sphygmomanometers. These measurements were obtained in this manner to limit the invasiveness of the study, which was performed on human subjects. A 10-cm-wide tourniquet was utilized in this study, which does not distribute the pressure as well as a wider tourniquet. The authors approximate that there is roughly a 4–5-mm Hg inherent error in the system. Due to this fact, the intra-compartmental pressure was assumed to be equal to tourniquet pressure, as shown by Dahn et al. (31). Only the anterior compartment was monitored during the study. The anterior compartment was chosen for ease of access and superficial location for pressure transmission and NIRS readings. Lastly, as described by multiple sources, including Shuler et al., there is a hyperemic effect associated with

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Hypereremia Baseline: rSO2 = 71

80 70 60 rSO2

Recovery

50 PP=28 mmHg rSO2 = 62 Decrease from baseline = 13

40

PP=12 mmHg rSO2 = 61

PP= -1 mmHg rSO2 = 58

30 20

Deflation

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Figure 3. A plot of near infrared spectroscopy (NIRS) values vs. times showing changes in NIRS values in response to increasing tourniquet pressures in a sample patient. Arrows indicate the points where tourniquet pressure was increased, as well as diastolic and mean arterial pressures. PP = perfusion pressure.

trauma (26,38–44). This response is detectable by NIRS (26,44). This phenomenon was not accounted for in this model. As in previous studies using this model as well as the infusion technique, an experimental source of trauma was not incorporated (44). The use of human study subjects prohibited the use of experimentally induced trauma. To obtain more accurate information on the transition to ischemic conditions, patients with extremity injuries will need to be examined in a longitudinal fashion. CONCLUSION NIRS has been shown to be responsive and inversely correlated to increasing intra-compartmental pressures (26). This study shows that muscle oxygenation is responsive to perfusion pressure changes over a continually monitored period of time. NIRS demonstrates minimal changes in perfusion until perfusion pressure drops below 10 mm Hg. As perfusion is compromised, oxy-hemoglobin concentration within the muscle also declines. Additionally, a change of roughly 8 percentage points of NIRS using this device correlated with diminished perfusion. Combined with previous research, this study suggests the potential value that NIRS possesses as an objective, non-invasive, and continuous monitor in the traumatic patient with signs of compartment syndrome. Acknowledgment—Funding was provided by Somanetics, Inc in the form of equipment donation only.

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ARTICLE SUMMARY 1. Why is this topic important? Near infrared spectroscopy (NIRS) has potential as a diagnostic method for acute compartment syndrome (ACS). 2. What does this study attempt to show? This study utilized a tourniquet model to simulate acute compartment syndrome in 20 volunteers to evaluate the responsiveness of NIRS as perfusion pressure decreases. 3. What are the key findings? NIRS values dropped significantly from baseline at approximately 30 mm Hg perfusion pressure, an established clinically recommended threshold in ACS diagnosis. NIRS values began to drop significantly from the preceding interval, beginning at 0 mm Hg perfusion pressure (when tourniquet pressure exceeded diastolic blood pressure) until systolic pressure was surpassed. 4. How is patient care impacted? Current diagnosis of ACS relies heavily on physician judgment. Available objective diagnostic methods are painful and unreliable. The use of NIRS to diagnose ACS presents an important opportunity to improve patient care by decreasing the number of missed cases of ACS and unnecessary fasciotomies.