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ABSTRACT |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Many critically ill patients develop significant skeletal muscle weakness in the Intensive Care Unit (ICU), which ultimately may cause difficulties in weaning from mechanical ventilation and a protracted, expensive ICU stay. Reliable monitoring of muscle strength in this environment is difficult. The purpose of this study was to develop a reproducible, nonvolitional method of measuring adductor pollicis (AP) muscle function by magnetic stimulation of the ulnar nerve (MSUN) that could be applied to patients in the ICU and operating theater (OT). Fifty subjects (32 healthy control subjects [12 of whom were elderly], 12 ICU patients with critical illness [mean APACHE II score 20], and six otherwise healthy patients requiring minor surgery in the OT) received MSUN. In 12 of the normal subjects electrical stimulation of the ulnar nerve (ESUN) and MSUN were compared and AP twitch tension (Tw AP) and surface electromyogram (EMG) were measured. Close agreement was found between supramaximal Tw AP (median [95% CI] for MSUN 6.3 N [5-7.2 N] and ESUN 6.9 N [5.2-7.8 N] [p = NS]). Median (95% CI) values with MSUN for the 20 young and 12 elderly control subjects were 6.9 N (5.3-7.4 N) and 7.1 N (4.4-9.8 N). Median (95% CI) Tw AP for the ICU group was 4.2 (2.2-6.7 N) and for the OT group was 5.8 (4-9.1 N). Tw AP was significantly reduced in ICU patients compared with age-matched controls (p = 0.01). MSUN can be used to measure neuromuscular function in both the laboratory and clinical settings including the ICU.
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Critical care neuromyopathy is increasingly recognized in critically ill patients but there is no method to assess the strength of small peripheral muscles that can be easily applied in clinically challenging environments. Measurement of adductor pollicis muscle (AP) tension elicited by electrical stimulation of the ulnar nerve (ESUN) is an established technique in human muscle physiology (1, 2). The test is attractive because the muscle itself is easily accessible and has sole innervation from the ulnar nerve, thereby enabling complete assessment of neuromuscular function (3). However, few data have been generated by the use of ESUN in the Intensive Care Unit (ICU), reflecting the difficulty of applying the technique in the critically ill (4). For routine strength measurement maximum voluntary contractile force (MVC) is often preferred because of the discomfort of supramaximal electrical nerve stimulation, especially with repeated measurements and high stimulation frequencies (5). However, effort dependent maneuvers for measuring strength are not always suitable for patients in the ICU and operating theater (OT). This is mainly because the ability to perform true MVC relies on subject motivation and cooperation, which is not possible in unconscious or sedated patients; nonvolitional techniques are therefore required.
Based on the previous success of applications of magnetic stimulation (MS) both in the laboratory (6, 7), and in the clinical setting (8, 9), we hypothesized that the use of MS of the ulnar nerve (MSUN) for measurement of adductor pollicis twitch tension (Tw AP) and compound muscle action potential (CMAP) might be both physiologically valid and feasible in critically ill patients. In this report we have provided a detailed evaluation to compare the technique of MSUN with traditional ESUN in normal subjects, establish the reproducibility of MSUN, and demonstrate the utility of MSUN in normal subjects (young and elderly) and in patients in the ICU and the OT.
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METHODS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Subjects
We studied a total of 50 subjects who were divided into three groups (Table 1). In addition, to compare young normal subjects with healthy elderly subjects we divided Group 1 into subgroups 1a (20 young control subjects) and 1b (12 elderly control subjects).
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The severity of illness in the ICU patients (Group 2) was assessed within 24 h of admission to ICU using the Acute Physiology and Chronic Health Evaluation (APACHE) II score (10). The patients in Group 3 were undergoing elective varicose vein surgery and were free from neurological disease. None of the subjects had metallic prostheses or had sustained an injury to the arm necessitating immobilization for more than 1 wk within the preceding yr. The protocol was approved by the Kings College Hospital Ethics Committee, and all subjects gave written informed consent.
Recording of AP Tension and EMG
AP muscle function was studied using the technique described by Merton (1) with a modified handboard. The board was extensively revised to ensure hand and forearm immobilization during stimulation without risk of ischemia (Figure 1). After preparing the skin with alcohol, silver/silver chloride surface electromyogram (EMG) electrodes (Arbo Medical, CT) were positioned longitudinally over AP with the reference electrode placed on the tip of the index finger. The EMG signal was then carried to a Neurosign 100 amplifier (Magstim Co. Ltd., Whitland, Dyfed, Wales).
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The skin was marked with a pen to outline the flexor carpi ulnaris tendon along its length and the site of the ulnar styloid. The supinated hand and forearm were then placed in a rigid perforated plastic arm splint (North Coast Medical, San Jose, CA) that covered the anterior, lateral, and medial aspect of the forearm (Figure 1) and was secured with velcro tapes to the board to avoid rotation of the wrist. The fingers were comfortably flexed over a padded adjustable metal bar situated over the palm of the hand. The thumb was abducted and its metacarpophalangeal and interphalangeal joints fully extended. A strain gauge (range 0-20) kg) (Strainstall, Cowes, Isle of Wight, UK) mounted on the board was connected to a metal loop around the proximal phalanx of the thumb by an inextensible metal chain. The strain gauge was securely positioned parallel to the thumb ensuring that the metal chain was perpendicular to both. Both force and EMG (when measured) were simultaneously recorded and amplified and the signals were passed via a 12-bit NB-MIO-16 analog-digital input-output board (National Instruments, Austin, TX) to a Macintosh Quadra Centris 650 computer (Apple Computer, Inc., Cupertino, CA) running LabView software sampling at 10 kHz. The arm splint was designed so that a window in the plastic was positioned over the ulnar nerve at the wrist allowing access for stimulation. The point of stimulation was between the flexor carpi ulnaris tendon and the ulnar artery 2.5 cm distal to the intersection of the two previously marked lines.
Stimulation Technique
Electrical stimulation (ES). The ulnar nerve was stimulated with square-wave impulses of 0.1 ms duration from a bipolar surface stimulating electrode powered by an electrical stimulator (Medelec Ltd., Old Woking, Surrey, UK). The cathode position was standardized and placed distal to the anode at the intersection of the two marked lines marking the flexor carpi ulnaris tendon and the ulnar styloid (Figure 2A). With this position maintained the active EMG recording electrode over the thenar eminence was at least 5 cm from the stimulating electrode.
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Magentic stimulation (MS). A 43-mm figure of eight coil (P/N 8459) powered by a Magstim 200 stimulator (Magstim Co. Ltd., Whitland, Dyfed, Wales) was used. The coil was positioned firmly against the skin with the focus of the output of the magnetic field over the ulnar nerve at the same point as for electrical stimulation (Figure 2B). Optimum position and orientation of the coil head were examined.
Maximum voluntary contraction (MVC). Subjects were asked to perform a maximum voluntary contraction without flexing their thumb and the ratio between MVC and Tw AP was calculated. During the MVC a superimposed supramaximal stimulation (interpolated twitch) was delivered to the ulnar nerve when force reached a plateau, to assess the level of voluntary activation (Figure 3). This maneuver was repeated three time and the MVC was accepted for comparison with resting twitch tension if the interpolated twitch was less than 5% of the potentiated Tw AP.
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Protocols
MSUN was performed on all subjects.
Group 1a (20 young control subjects): A comparison was made between ESUN and MSUN in 12 of the control subjects and in six of these control subjects the comparison was repeated on three to five occasions. Measurement of MVC was made in 10 control subjects. In five control subjects the spread of the MSUN was compared to ESUN (see CROSSOVER STUDY following).
Group 1b (12 elderly control subjects): Twitch force and CMAP amplitude was recorded in all subjects. Six subjects performed an MVC.
Group 2 (12 ICU patients): Twitch force was measured in all patients and CMAP amplitude was measured in seven patients. Only two patients were able to attempt an MVC.
Group 3 (six OT patients): MSUN was performed and the twitch force was measured in these patients prior to the induction of anesthesia.
Temperature regulation. The AP is a small peripheral muscle that has little insulation from subcutaneous fat. It is therefore essential to take steps to standardize the temperature of the muscle during testing as the mechanical properties of muscle are influenced by changes in temperature, specifically there is slowing of the relaxation rate on cooling and acceleration on warming. Studies were preceded by immersion of the hand and forearm in a water bath at 44° C for 10 min to enable muscle temperature to reach 35° C (11) and kept warm by radiant heat provided by a lamp during studies. Potentiation. To minimize twitch potentiation (12) the subjects were required to rest quietly for 20 min without moving their hand before measurements were made. Twitch-on-twitch potentiation was avoided by a standardized stimulation protocol with 30 s between each single twitch.
Ensurance of supramaximal stimulation. On each occasion preliminary studies were performed to confirm that both the force and CMAP when measured were maximal. First (when using MS) the orientation of the coil head was changed by 180° relative to the ulnar nerve to maximize Tw AP. Second the resting tension was adjusted by increasing and decreasing the distance between the loop on the thumb and the strain gauge, until maximum twitch force was produced with 100% stimulator output. Finally, stimuli were delivered at a range of intensities (60-100%) to confirm that supramaximal stimulation was achieved at 100% stimulator output. Reproducibility. To address the issue of reproducibility MSUN was performed on two separate occasions on all control subjects from Group 1a and on six of the subjects on three to five occasions.Additional Study
Crossover study. A substudy was performed to investigate whether MSUN also depolarizes the median nerve. The ulnar nerve was stimulated supramaximally with ES and MS while simultaneously recording the CMAP over AP and abductor pollicis brevis (APB), which is innervated by the median nerve.
Data Analysis
Force measurements were made from baseline to peak twitch tension (Figure 6). Time to peak tension (TTPT) was from the start of the stimulus marker to the peak of the twitch response. EMG amplitude was measured from peak to peak and conduction time was measured from the stimulus marker on the onset of the CMAP. The precision of the technique was determined by calculating the coefficient of variance for repeat measurements of supramaximal twitch tension. The agreement between Tw AP electrical and Tw AP magnetic stimulation was assessed by the method of Bland and Altman (13). Values for supramaximal Tw AP between the different groups were analyzed by one-way analysis of variance (ANOVA), and significance was determined with the Tukey multiple comparison test.
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RESULTS |
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Supramaximality
Tw AP was supramaximal, judged by force, in 48 of 50 subjects. In Group 1a, 19 of the 20 control subjects were supramaximal for Tw AP and CMAP amplitude. The remaining control subject was not quite supramaximal on either occasion, although absolute values for Tw AP elicited by MSUN were of the same order of magnitude as those elicited by ESUN (mean 588 N versus 648 N). In the 12 control subjects that received MSUN and ESUN supramaximality for force was achieved with MSUN at a mean (range) stimulator output of 92% (90-95%) of maximum (Figure 4) and CMAP at a mean (range) stimulator output of 85% (80-95%) of maximum. Supramaximality for force was achieved with ESUN at a mean (range) stimulator output of 170 V (120-200 V) and CMAP at a mean (range) stimulator output of 140 V (80-180 V). In one patient in Group 2 who had severe edema, no plateau of force or EMG was achieved, suggesting submaximal stimulation. Electrical stimulation was also attempted but a high voltage was required to produce a twitch response and, being uncomfortable for the patient, was discontinued. In Groups 1b and 3 all subjects and patients were supramaximally stimulated.
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Comparison of Tw AP with MSUN and ESUN
The median (95% confidence interval) Tw AP in Group 1a with MSUN was 6.3 N (5-7.2 N) and with ESUN was 6.9 N (5.2-7.8 N) (p = NS). A Bland and Altman plot (Figure 5) demonstrated no relationship between the difference between tests and their mean value with a mean difference of 0.1 N (SD ± 0.73) between the techniques.
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Comparison of Tw AP with MSUN among Group 1, 2, and 3
The mean (95% CI) value with MSUN was for Group 1a 6.9 (5.3-7.4 N), Group 1b 7.1 N (4.4-9.8 N), Group 2 4.2 N (2.2-6.7 N) (Table 2), and Group 3 5.8 N (4-9.1 N). There was a significant difference only between Group 1 and Group 2 (p < 0.05).
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Reproducibility of the Tw AP
The mean (range) within-occasion coefficient of variance for supramaximal Tw AP in Group 1a was 6.9% (0.8-9%) with ESUN and 6.4% (4.2-9.9%) with MSUN. In Group 1b the within-occasion coefficient of variance (range) for MSUN was 5.2 (2.6-8.1), in Group 2 it was 7.8% (3-9%), and in Group 3 it was 3.5% (1.4-5.3%). The mean between occasion coefficient of variance for Group 1a was 6.4%.
CMAP
The median (95% CI) CMAP in Group 1a was 5.8 mV (3.9-9.2 mV) measured in 10 control subjects, in Group 1b it was 5.7 mV (3.8-7.4 mV) measured in 12 control subjects, and in Group 2, in which 7 of the 12 patients had CMAP measured, it was 2.5 mV (1.4-4.7 mV). There was no significant difference between the values in Group 1a and Group 1b, however, there was a significant difference between Group 1 and 2 (p = 0.01).
Conduction Time
The mean (range) conduction time measured in 10 control subjects in Group 1a was 3.3 ms (3-3.6 ms), in Group 1b, measured in 12 control subjects, it was 3.6 ms (3.2-4.1 ms), and in Group 2, measured in 10 patients, it was 3.95 ms (3.3-4.5 ms). CT was not measured in Group 3. There was no significant difference between the values in Group 1a and Group 1b, however, there was a significant difference between Group 1 and Group 2 (p < 0.05).
Tw AP/MVC Ratio
Some subjects did not fully activate AP during voluntary contractions. We therefore defined a true MVC as > 95% occlusion of the potentiated interpolated Tw AP. MVC data were available in 10 control subjects from Group 1a in whom the mean MVC was 76.1 N with a mean Tw AP/MVC ratio of 0.09. In Group 1b the mean MVC from six control subjects was 72.9 N with a mean Tw AP/MVC ratio of 0.10. Only two patients in Group 2 were able to attempt a voluntary maneuver, neither of whom managed a true MVC.
Effect of Coil Orientation
In all subjects coil orientation had an effect on Tw AP and CMAP. The optimal position for stimulation was when the short axis of the magnetic coil was positioned parallel to the long axis of the ulnar nerve (Figure 2B).
Crossover Study
With ESUN the mean CMAP recorded over AP in six subjects was 7.4 mV and 6.96 mV with MSUN; simultaneous recordings over the APB recorded a CMAP of 1.9 mV with ESUN and 2.1 mV with MSUN (Figure 7).
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Acceptability of the Technique in the Patients
MSUN was tolerated by patients and normal subjects; in ICU patients no obvious signs of discomfort (e.g., facial expression or physiological change in vital signs) were seen.
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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The main finding of this study is that it is possible to achieve supramaximal activation of the AP muscle by MSUN. The twitch response elicited is reproducible and the technique can be successfully employed in the ICU and OT.
Practical Aspects of Hand Board Design
The majority of data concerning AP contractility have been obtained using tetanic ES and minimal data exist on the single twitch (14, 15). We believe that our modifications to the design of the handboard have improved reproducibility compared with previous studies of AP by immobilizing the forearm during MSUN and MVC and by avoiding rotation of the wrist and lifting of the hand.
Selectivity of Stimulation with MSUN
The amplitude of the CMAP measured from AP and APB was similar with both electrical and magnetic stimulation of the ulnar nerve, demonstrating that with correct positioning of the coil, the magnetic field is likely to maximally excite the ulnar nerve without activation of the median nerve or at least to no greater extent than ESUN. The small CMAPs from APB are therefore likely to be the result of volume conduction (16) rather than propagation along an alternative neural pathway such as the median nerve.
Can Ulnar Nerve Latency be Measured with MSUN?
Previous investigators (17, 18) have considered that the measurement of conduction velocity is difficult when using MS to stimulate at the wrist. This was due to the imprecision in defining the site of nerve depolarization and an unacceptably large shock artifact obscuring the start of the stimulation. This conclusion was reached from studies using circular coils that do not always achieve supramaximal stimulation. If stimulation is submaximal an unknown proportion of nerve fibers is depolarized and latency can vary. More recently a figure of eight coil has been used (19), as in this study, which gives more focal depolarization and, furthermore, supramaximal stimulation is usually achieved; in particular the point of nerve depolarization is reliably determined by using anatomical reference sites and the problem of shock artifact has been overcome with a stimulus marker. This technique may therefore be useful for measurement of latency in patients if strict standardization of the technique is applied. A large series of normal values would be desirable for the purposes of comparison.
Tw AP as a Measure of Strength
The use of isometric twitch tension as a measure of strength assumes a constant relationship between the force produced by the single twitch and the force produced by tetanic stimulation (or a truly maximal MVC). This relationship is known for a wide variety of animal and human skeletal muscles (20). The range of Tw AP/MVC ratios in normal subjects in this study was narrow (0.08-0.12), suggesting that this relationship is valid. None of 12 patients with critical illness was able to generate a true MVC, and under these circumstances the Tw AP may be a useful method of assessing AP strength.
The Utility of the Technique
Tw AP technique causes minimal disruption to position or treatment, and is well tolerated even by the sickest of patients. Magnetic stimulation does not require precise positioning, so the presence of vascular catheters does not prevent measurements. Tw AP, like twitch transdiaphagmatic pressure (Tw Pdi) and twitch quadriceps tension (Tw Q), could be a robust technique for the assessment of skeletal muscle function. Used in combination these tests would allow investigators to quantify both the distribution and progression of skeletal muscle function in the critically ill. Sequential measurements may provide an important tool for the assessment of interventions such as physiotherapy, new drug or hormone treatments, and supplementary nutrition.
ESUN, when supramaximal, is uncomfortable because of high current densities under the electrodes, which may cause sensory fibers to be activated. The firing threshold for motor fibers is much lower than for sensory fibers with MS (21), and this may explain the acceptability of MSUN. In this study maximal stimulation of the ulnar nerve was achieved with a stimulus intensity of 90-95% of maximum stimulator output with close skin contact. Since supramaximal stimulation was achieved near maximal stimulator output we recommend that with this technique skin contact is assured to avoid submaximal stimulation.
The 12 patients we studied in the ICU had a range of diagnoses, as listed in Table 2, and none had neuromuscular disease prior to ICU admission. The mean Tw AP and CMAP were significantly lower and the CT prolonged in patients compared to healthy controls. Although the main aim of studying this group of patients was to test the feasibility of the technique in the ICU environment, the data support the view that muscle weakness is relatively common in the ICU.
We conclude that muscle strength in terms of Tw AP can be accurately measured with magnetic stimulation of the ulnar nerve. The technique is acceptable to patients and feasible in clinically demanding environments. The evaluation of interventions that are aimed at avoiding or reversing weakness could be facilitated by the technique of MSUN.
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Footnotes |
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Support provided for M. L. Harris by NHS Executive Grant RDF 028.
(Received in original form February 16, 1999 and in revised form December 21, 1999).
Correspondence and requests for reprints should be addressed to M. L. Harris, Respiratory Muscle Physiology Laboratory, Guy's King's and St. Thomas' School of Medicine, Kings College Hospital, Bessemer Rd., London SE5 9PJ, UK. E-mail: lou.harris{at}kcl.ac.uk| |
References |
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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