Association of the Bedside Shivering Assessment Scale and derived EMG power during therapeutic hypothermia in survivors of cardiac arrest

Resuscitation 82 (2011) 1100–1103

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Short communication

Association of the Bedside Shivering Assessment Scale and derived EMG power during therapeutic hypothermia in survivors of cardiac arrest夽,夽夽 Teresa May a,∗ , David B. Seder a , Gilles L. Fraser a , Chunhao Tu b , Barbara McCrum a , Lee Lucas c , Richard R. Riker a a

Maine Medical Center Neuroscience Institute and Department of Critical Care Services, United States University of New England School of Pharmacy, United States c Maine Medical Center for Outcomes Research and Evaluation, United States b

a r t i c l e

i n f o

Article history: Received 7 December 2010 Received in revised form 4 February 2011 Accepted 7 March 2011

Keywords: Therapeutic hypothermia Cardiac arrest Shiver Bedside Shivering Assessment Scale Derived EMG

a b s t r a c t Introduction: Shivering during therapeutic hypothermia (TH) after cardiac arrest (CA) is common, but the optimal means of detection and appropriate threshold for treatment are not established. In an effort to develop a quantitative, continuous tool to measure shivering, we hypothesized that continuous derived electromyography (dEMG) power detected by the Aspect A2000 or VISTA monitor would correlate with the intermittent Bedside Shivering Assessment Scale (BSAS) performed by nurses. Methods: Among 38 patients treated with TH after CA, 853 hourly BSAS measurements were compared to dEMG power measured every minute by a frontal surface electrode. Patients received intermittent vecuronium by protocol to treat clinically recognized shivering (BSAS > 0). Mean dEMG power in decibels (dB) was determined for the hour preceding each BSAS measurement. dEMG and BSAS were compared using ANOVA. Results: The median dEMG power for a BSAS score of 0 (no shivering) was 27 dB (IQR 26–31 dB), BSAS 1 was 30.5 dB (IQR 28–35 dB), BSAS 2 was 34 dB (IQR 30–38 dB), and BSAS 3 was 34.5 dB (IQR 32–44.25). The dEMG for BSAS ≥ 1 (shivering) was statistically different from BSAS 0 (p < 0.0001). dEMG and BSAS correlated moderately (r = 0.66, p < 0.001). Conclusion: dEMG power measured from the forehead with the Aspect A2000 or VISTA monitor during therapeutic hypothermia correlated with the Bedside Shivering Assessment Scale. Given its continuous trending of dEMG power, the A2000 or VISTA may be a useful research and clinical tool for objectively monitoring shivering. © 2011 Elsevier Ireland Ltd. All rights reserved.

1. Introduction Therapeutic hypothermia (TH) improves the neurological outcome of selected adults surviving cardiac arrest and newborns with asphyxial encephalopathy.1–4 Shivering is an important barrier to cooling, and is associated with increases in metabolism, oxygen consumption, resting energy expenditure, carbon dioxide production and lower brain tissue oxygen levels.5–7 The approach to measurement and treatment of shivering during TH varies greatly between institutions with inconsistent recommendations regarding best care.8,9 The Bedside Shivering Assessment Scale (BSAS) is a simple ordinal tool that rates

夽 A Spanish translated version of the summary of this article appears as Appendix in the final online version at doi:10.1016/j.resuscitation.2011.03.037. 夽夽 Disclaimer: None. ∗ Corresponding author at: DO, 22 Bramhall St, Portland, ME 04102, United States. E-mail address: [email protected] (T. May). 0300-9572/$ – see front matter © 2011 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.resuscitation.2011.03.037

shivering from zero (no shivering), to one (mild shivering localized to neck or thorax), two (moderate shivering extending to upper extremities) or three (severe shivering of trunk, upper, and lower extremities).6 The BSAS has proven interrater reliability and construct validity with increasing BSAS scores associated with increasing hypermetabolic index and oxygen consumption.6 Though reliable, the BSAS remains an intermittent, subjective, observer-dependent assessment, requiring clinicians to periodically examine the patient. A quantitative, objective, continuous monitor may improve recognition of shivering and help guide specific anti-shivering therapy, including neuromuscular blockade (NMB).3–5,10,11 Our TH clinical program routinely monitors patients with the bispectral index (BIS) A2000 or VISTA monitor (Aspect Medical Systems, Inc., Norwood, MA) which also displays derived electromyographic power (dEMG) in decibels (dB).12,13 We observed that the dEMG power appeared to correlate with shivering activity, and hypothesized that the dEMG signal from the Aspect A2000 or VISTA monitors might correlate with the BSAS.

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Fig. 1. Front panel of the Aspect A-2000TM BIS Monitor. dEMG is displayed as a quantitative bar (each tick mark represents 2.5 dB from 30 to 55 dB) and as a secondary trend variable (range from 30 to 80 dB displayed on the right-sided Y axis). Adapted with permission from the A-2000TM Bispectral IndexTM (BISTM ) Monitoring System Operating Manual.13

2. Methods This study was approved by the Maine Medical Center Institutional Review Board with a waiver of informed consent. From March 2009 to April 2010, we prospectively collected data from all patients receiving TH after cardiac arrest, including demographics, medications administered, and the discharge Cerebral Performance Category (CPC) with good outcome defined as a CPC of 1 or 2. Our protocol involves hypothermia induction with cold intravenous fluids and the Arctic Sun Therapeutic Temperature Management System (Medivance Co, Louisville, CO), continuous analgosedation with propofol and fentanyl infusions, and intermittent NMB with vecuronium (typical dosing 0.1 mg/kg) to treat detectable shivering (BSAS > 1). The BIS is routinely monitored with the Aspect A2000 or VISTA monitors from a frontal (Fp1 or Fp2 – Fz) montage, and “BIS1” represents the BIS baseline value after the first dose of NMB.12 In addition to reporting the BIS, these monitors display dEMG power in decibels (calculated from total power in the 70–110 Hz range) as a horizontal EMG power bar near the top of the screen and as a secondary trend variable (Fig. 1).12,13 2.1. dEMG and BSAS Our nurses record hourly bladder or esophageal temperature, shivering activity using BSAS, and medication doses. Data from the Aspect monitors were downloaded and timing of NMB doses retrospectively confirmed by the characteristic sharp drop in dEMG (Fig. 2). The dEMG values were compared before and after NMB administration for the first shivering event. For comparison with BSAS values, dEMG power was calculated as the mean value for the hour prior to each BSAS measurement. 2.2. Data analysis Continuous data are presented as means (±standard deviation) or, if not normally distributed, as median (interquartile range).

Fig. 2. Derived EMG power in decibels (line) during 24 h of TH from a single patient. Triangles represent hourly Bedside Shivering Assessment Scale recorded by bedside nurses. The 4 stars represent administration of intermittent neuromuscular blockade in response to clinically recognized shivering (note increasing dEMG in each case).

Nominal and categorical data are presented as count and percentage for each category. To control for multiple measurements per subject, paired dEMG and BSAS measurements were compared using ANOVA. As a sensitivity analysis, correlation was assessed between the mean dEMG for the hour preceding the first values of BSAS 1, 2, 3, and 0 for each patient using Spearmans correlation. Pre- and post NMB dEMG data were compared using the paired t-test. A p value < 0.05 was considered statistically significant. 3. Results Of 72 consecutive cardiac arrest survivors treated with TH, 19 patients were excluded for incomplete BSAS data, 12 for incomplete dEMG data, 2 died prior to completion of TH, and 1 received continuous NMB. This cohort included 38 patients (30 [79%] were male) with a mean age of 59 (18) years, a body mass index of 29.6 (6.7), time to recovery of spontaneous circulation of 22 (13) min, and an

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Fig. 3. Boxplot for the Bedside Shivering Assessment Score and mean hourly dEMG power. The horizontal bar within the box is the median, base of box = 1st quartile, top = 3rd quartile, and whiskers represent the range of values for hourly dEMG values at each BSAS Score. The dEMG values for hours with shivering (BSAS 1–3) were greater than for hours with no shivering (BSAS 0, 27 dB (IQR 26–31 dB) p < 0.0001), but BSAS 1, 2, and 3 were not different from one another. Note that BSAS 1-3 (n = 140) includes the next three individual plots for BSAS 1, 2, and 3.

initial cardiac rhythm of VT/VF in 21/38 (55%). The mean BIS1 was 22 (17) and the CPC score was 1 or 2 in 16/38 (42%). 853 hourly BSAS measurements were compared to the corresponding preceding hour’s dEMG power, with 713 h of no shivering (BSAS score of 0, 84% of hypothermia time), and 140 h (16%) with detectable shivering: 88 BSAS scores of 1 (10%), 42 scores of 2 (5%), and 10 scores of 3 (1%). Patients received a mean of 4.8 doses of NMB during the 24 h of TH induction and maintenance. The mean dEMG at the time of treating the first clinically recognized shivering episode was 37.4 dB which decreased to 26.6 dB (1.7, p < 0.001) after NMB. The lowest and highest mean dEMG values were 23 dB and 68 dB. 3.1. BSAS and EMG The mean EMG power corresponding to a BSAS of zero was 27 dB (IQR 26–31 dB), 30.5 dB for BSAS 1 (IQR 28–35 dB), 34 dB for BSAS 2 (IQR 30–38 dB) and 34.5 dB for BSAS 3 (IQR 32–44). The dEMG values for hours with shivering (BSAS 1, 2, or 3) were greater than for hours with no shivering (BSAS 0, p < 0.0001), but not different from one another (Fig. 3). When just the first values for BSAS 1, 2, 3, and 0 for each patient were evaluated (n = 95), a moderate correlation was noted with dEMG (r = 0.66, 95% CI 0.53–0.76, p < 0.001). 4. Discussion In cardiac arrest survivors treated with therapeutic hypothermia, continuous derived EMG power from frontal sensors with the Aspect A2000 or VISTA monitors is greater when shivering is detected using the Bedside Shivering Assessment Scale. This is the first study we are aware of that has used continuous objective monitoring to quantify shivering during therapeutic hypothermia after cardiac arrest. Shivering in comatose patients is not easily detected in its early stages.14 Available objective techniques for measuring shivering such as EMG monitoring with needle electrodes, skin temperature gradients, or indirect calorimetry are impractical for routine clinical use and are often unavailable.6,15 A reliable and available objective method to measure shivering may be beneficial for both clinical and research purposes. The dEMG continuous monitoring provided by the Aspect monitors may be such a tool. A predictable pattern of shivering progression is recognized, from early activation of facial and neck muscles, advancing to chest, trunk, and extremity shivering.14 The forehead location for dEMG recording by the Aspect monitors may allow shiver to be detected at a lower intensity and an earlier timepoint, including fine shivering difficult to detect without instruments. It is unknown whether “subclinical shivering” has an important impact on metabolism,

heat generation, or brain perfusion, or whether use of objective tools would improve patient outcomes. Incorporating this information into treatment protocols will be complex, since treatment of shivering varies greatly between institutions, and many protocols have been proposed, utilizing 5-HT agents, magnesium, alpha 2-agonists, opioids, buspirone, dantrolene, propofol, and doxapram alone and in combination.16,17 Several important limitations of this research warrant explanation. Our protocol requires BSAS to be recorded hourly which does not necessarily coincide with the timing of shivering episodes. Additionally, using a clinical record increases the chance of documentation errors; we noted instances when BSAS was recorded as zero even though nurses had documented clinical shivering and administered treatment for this. Although a strong statistical difference was present between shivering and non-shivering hours, we did not show a difference between BSAS scores of 1, 2, and 3. We believe this may represent a Type II error related to the relatively small percent of hours scored as BSAS 2 or 3. In addition, dEMG was displayed as a small horizontal line on the Aspect monitor and was potentially visible to nurses measuring BSAS. It is possible that nurse knowledge of dEMG values may have altered routine care or influenced BSAS assessment. Future blinded studies would better address this issue. Although brain electrical activity, such as seizures, or non-biological electrical signals could confound dEMG values, the correlation we found with BSAS and impact of neuromuscular blockade on this measurement suggests these artifacts are minimal. This report describes the first application of dEMG data from Aspect monitors as possible continuous shivering monitors. This novel approach may provide several advantages when compared to intermittent clinician assessment, including earlier recognition of shivering and more reliable objective measurement, but this remains unproven. A reliable tool to quantify shivering is an important first step to defining treatment thresholds for shivering, including how sedation and analgesic medications affect shivering, and how varying intensity of shivering may affect or be affected by the severity of brain injury. Additional study and validation is needed before this approach can be recommended as a standard clinical or research tool. 5. Conclusions Derived EMG power measured in decibels from the Aspect A2000 and VISTA monitors correlates with the Bedside Shivering Assessment Scale in patients undergoing therapeutic hypothermia after cardiac arrest. The dEMG may facilitate more precise measurement of shivering at the bedside, with potential clinical and research utility. Conflict of interest statement We report no conflict of interests in regard to this submission. Funding None. References 1. Jacobs S, Hunt R, Tarnow-Mordi W, Inder T, Davis P. Cooling for newborns with hypoxic ischaemic encephalopathy. Cochrane Database Syst Rev 2007;4:CD003311. 2. Hypothermia after Cardiac Arrest Study G. Mild therapeutic hypothermia to improve the neurologic outcome after cardiac arrest. N Engl J Med 2002;346:549–56. 3. Brooks SC, Morrison LJ. Implementation of therapeutic hypothermia guidelines for post-cardiac arrest syndrome at a glacial pace: seeking guidance from the knowledge translation literature. Resuscitation 2008;77:286–92.

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