Avaliação da ativação do músculo respiratório em indivíduos lesão medular Inglês

Respiratory Physiology & Neurobiology 173 (2010) 171\u2013178 Contents lists available at ScienceDirect R espirat ory Ph y siology & Neur obiology journal homepage: www.elsevier.com/locate/resphysiol Evaluation of respiratory muscle activation in individuals with chronic spinal cord injury Alexander Ovechkin a , b , \u2217 , Todd Vitaz c , Daniela Terson de Paleville b , Sevda Aslan a , William McKay c a Department of Neurological Surgery, University of Louisville, Louisville, KY, USA b Department of Physiology and Biophysics, University of Louisville, Louisville, KY, USA c Norton Neuroscience Institute, Louisville, KY, USA article info Article history: Accepted 30 July 2010 Keywords: Respiratory muscles Spinal cord injury Motor control Surface electromyography abstract This study was undertaken to physiologically characterize respiratory muscle control in eighteen indi- viduals with spinal cord injury (SCI) through comparison with 14 matched non-injured (NI) subjects. Standard pulmonary function measures (FVC, FEV 1 ,P I max and PE max ) were obtained along with surface electromyographic (sEMG) recording from respiratory muscles. A vector analysis of sEMG was used to calculate Similarity Index (SI) values relating SCI subject sEMG patterns to those produced by NI subjects. SI values for inspiratory and expiratory tasks were very consistent within the NI group, 0.92 ± 0.03 and 0.93 ± 0.04 (mean ± SD), respectively. Altered multi-muscle patterns in the SCI group produced SI values that trended lower 0.84 ± 0.11 for inspiratory tasks and were signi\ufb01cantly lower, 0.59 ± 0.22 for expira- tory tasks. SI values for expiratory tasks were also signi\ufb01cantly correlated with SCI levels and pulmonary function measures. These results suggest that pulmonary function after SCI is dependent upon the degree to which multi-muscle activation patterns are disrupted. © 2010 Elsevier B.V. All rights reserved. 1. Introduction Following spinal cord injury (SCI), control of limb muscles inner- vated from within and below the injury zone is altered leading to paresis ( Wirth et al., 2008 ), paralysis ( McKay et al., 2004 ) and spasticity ( Adams and Hicks, 2005 ). Although not as well-studied, the same is true for muscles of the trunk that are used in breath- ing ( Anderson et al., 2008; Laffont et al., 2003 ). When SCI alters the control of trunk muscles, respiratory function is compromised ( Schilero et al., 2009; Winslow and Rozovsky, 2003 ), leading to sec- ondary debilitating effects that impact recovery ( Linn et al., 2000 ) and quality of life ( Walter et al., 2002 ). In fact, respiratory complica- tions are among the leading causes of death in acute ( De Vivo et al., 1999 ) and chronic SCI ( Garshick et al., 2005 ). Progress is being made in the treatment of respiratory dysfunction brought by SCI ( Brown et al., 2006 ), but the evaluation of any new intervention requires the use of appropriate physiological evaluation ( Alexander et al., 2009; American Thoracic Society/European Respiratory Society, 2002; Lim and Tow, 2007 ). Current assessment tools are not designed for quantitative evaluation of the trunk and respiratory motor con- trol after SCI. Traditionally, parameters that quantify respiratory \u2217 Corresponding author at: Frazier Rehab Institute, 220 Abraham Flexner Way, Suite 1506, Louisville, KY 40202, USA. Tel.: +1 502 581 8675; fax: +1 502 582 7605. E-mail addresses: avovec02@gwise.louisville.edu , alexander.ovechkin@jhhs.org (A. Ovechkin). motor function such as Forced Vital Capacity (FVC), Forced Expi- ratory Volume in 1 s (FEV 1 ), Maximal Expiratory Pressure (PE max ) and Maximal Inspiratory Pressure (PI max ) have been used in clinical and research testing to measure the strength of respiratory muscles ( Jain et al., 2006; Stolzmann et al., 2008 ). However, such assessment does not examine the quality of the multi-muscle motor control being provided by the central nervous system. Although surface electromyography (sEMG) recorded from respiratory muscles can be used to detect and diagnose neuromuscular pathology, ampli- tude variability has inhibited efforts to develop objective measures of respiratory motor control ( American Thoracic Society/European Respiratory Society, 2002 ). SCI-altered motor control of limb muscles has been extensively characterized using neurophysiological methods ( Dimitrijevic, 1988 ). The recording of multiple-muscle sEMG during volitional and re\ufb02ex motor tasks within the Brain Motor Control Assessment protocol (BMCA) ( Sherwood et al., 1996 ) was used to demon- strate that more than 60% of people, clinically paralyzed by SCI, retained some degree of translesional conduction ( McKay et al., 2004; Sherwood et al., 1992 ). Lee et al. (2004) developed a vector- based analytic tool that calculates an index value from sEMG data recorded from multiple lower-limb muscles during the voluntary movement tasks within the BMCA. This analysis quanti\ufb01es the amount of sEMG activity separately from the degree to which the distribution of sEMG output to the set of muscles recorded from a test subject resembles that of a group of neurologically intact control subjects. This index calculation has been shown to have 1569-9048/$ \u2013 see front matter © 2010 Elsevier B.V. All rights reserved. doi: 10.1016/j.resp.2010.07.013 172 A. Ovechkin et al. / Respiratory Physiology & Neurobiology 173 (2010) 171\u2013178 Table 1 Characteristics of non-injured (NI) and spinal cord injured (SCI) participants. Subjects Age (years) Sex Height (cm) Weight (kg) Level of SCI AIS category Time after SCI (mo) SCI ( n = 18) A33 (C3A) 51 M 188 82 C3 AIS-A 24 A35 (T3A) 50 M 185 91 T3 AIS-A 396 A38 (C4A) 37 F 175 51 C4 AIS-A 252 A37 (T4A) 24 M 188 70 T4 AIS-A 24 A39 (T5A) 35 M 178 79 T5 AIS-A 192 A43 (T3A) 30 M 188 95 T3 AIS-A 24 B06 (C4B) 37 F 170 56 C4 AIS-B 24 B07 (T2B) 23 M 185 79 T2 AIS-B 12 C09 (C7C) 26 M 183 99 C7 AIS-C 24 D16 (C3D) 45 M 155 91 C3 AIS-D 108 C16 (T4C) 35 M 183 84 T4 AIS-C 72 D18 (T5D) 20 M 183 80 T5 AIS-D 48 C11 (L2C) 31 M 170 77 L2 AIS-C 24 C14 (C4C) 41 M 193 59 C4 AIS-C 12 D20 (C5C) 63 M 183 73 C5 AIS-C 12 C17 (T3C) 53 M 183 79 T3 AIS-C 264 D21 (C5D) 22 F 157 57 C5 AIS-D 72 D22 (T3D) 44 M 173 59 T3 AIS-D 144 Mean ± SD 37 ± 12 N/A 179 ± 10 76 ± 14 N/A N/A 96 ± 111 NI ( n = 14) Mean ± SD 40 ± 10 N/A 171 ± 97 2 ± 13 N/A N/A N/A ID codes include the AIS level and category of each SCI subject. high face validity, sensitivity and speci\ufb01city ( Lim et al., 2005 ) and good test\u2013retest reliability for lower-limb motor tasks ( Lim and Sherwood, 2005 ). Motor control of the trunk, especially as it relates to respiration, has not been fully investigated neurophysiologically. Therefore, this study was undertaken to neurophysiologically eval- uate respiratory motor control after SCI in relation to standard pulmonary function outcomes. 2. Methods All assessments were carried out in the Neuroscience Collabo- rative Center at the Frazier Rehab Institute after informed consent was obtained as approved by the Institutional Review Board for human research of the University of Louisville. Eighteen persons with chronic SCI, three females and \ufb01fteen males, were assessed. In addition, 14 non-injured (NI) subjects, \ufb01ve females and nine males, with no history of respiratory dysfunction or smoking were recorded to calculate the normative sEMG-based index values described below. Physical characteristics of sex, height, and weight were matched for the two groups ( Table 1 ). 2.1. Clinical assessment The American Spinal Injury Association Impairment Scale (AIS) was used to determine the neurological level and clinical motor completeness (severity) of the spinal cord lesion ( American Spinal Injury Association and International Spinal Cord Society, 2006; Marino et al., 2003 ). The AIS categorizes spinal cord injury severity and motor level based on the subjective estimation of voluntary contraction strength for \ufb01ve upper-limb (C 5 to T 1 ) and \ufb01ve lower- limb (L 2 to S 1 ) muscles on each side. It also determines a sensory level from the perception of light touch and pin prick for C 2 through S 5 dermatomes. The AIS has been shown to be a reliable estimate for use in clinical assessment of SCI ( Marino et al., 2008 ). For this study, eight SCI participants were classi\ufb01ed as clinically motor-complete (AIS-A or AIS-B) and ten were motor-incomplete (AIS-C or AIS-D), with neurological levels of SCI ranging from C 3 to L 2 ( Table 1 ). 2.2. Pulmonary function test (PFT) Standard spirometry ( Kelley et al., 2003 ) was performed in the sitting position by using BreezeSuite System (MedGraphics, St. Paul, MN). FVC and FEV 1 were obtained and expressed as the per- cent of a predicted value for each subject based on a database of neurologically intact individuals with no known pulmonary complaints that was derived based on gender, age, and height ( Hart et al., 2005 ). Three acceptable spirograms were obtained and the result of the best attempt was used ( American Thoracic Society/European Respiratory Society, 2002 ). A Differential Pres- sure Transducer (MP45-36-871-350) with UPC 2100 PC card and software from Validyne Engineering (Northridge, CA) was used to measure PI max and PE max in sitting position. The PI max was measured during maximal inspiratory effort beginning at near residual volume and PE max was measured during maximal expira- tory effort starting from near total lung capacity ( American Thoracic Society/European Respiratory Society, 2002 ). Subjects were asked to use a three-way valve system with rubber tube as mouthpiece (Airlife 001504). The pressure meter incorporated a 1.5 mm diam- eter leak to prevent glottic closure and to reduce buccal muscle contribution during measurements ( Grif\ufb01ths and McConnell, 2007; Smyth et al., 1984 ). The assessment required that a sharp, forceful effort be maintained for a minimum of 2 s. The maximum pres- sure was taken as the highest value that is sustained for 1 s ( Black and Hyatt, 1969 ). The maximum value from three maneuvers that varied by less than 20% were averaged. 2.3. Respiratory Motor Control Assessment (RMCA) The RMCA is a multi-muscle sEMG-based measure of motor output from the central nervous system recorded during volun- tary motor tasks attempted in the supine position under strictly controlled conditions that was based on the BMCA principles ( Sherwood et al., 1996 ). The RMCA protocol consists of the fol- lowing voluntary maneuvers followed by 5 min of quiet breathing: full unloaded expiration or inspiration immediately followed by, maximum inspiratory pressure task (MIPT) or maximum expira- tory pressure task (MEPT), respectively. Each maneuver was cued by an audible tone and repeated three times. Unloaded efforts were maintained for a minimum of 3 s and MIP/MEP efforts were maintained for a minimum of 5 s. Airway pressure was recorded during MEPT and MIPT using a three-way valve system with a pres- sure transducer as described above. Surface EMG recordings were recorded during these tasks using an Eclipse Neurological Worksta- tion (Axon Systems Inc., Hauppauge, NY) with pairs of recessed, FE9 silver\u2013silver chloride cap surface electrodes (Grass Instruments, W Warwick, RI) centered over the muscle belly and placed 3 cm A. Ovechkin et al. / Respiratory Physiology & Neurobiology 173 (2010) 171\u2013178 173 Table 2 Summary of pulmonary function testing (PFT) values obtained during spirometry and Respiratory Motor Control Assessment in SCI and NI individuals. Subjects PFT FVC (% predicted) FEV 1 (% predicted) PI max (cm H 2 O) PE max (cm H2O) PI max MIPT (cm H 2 O) PE max MEPT (cm H 2 O) SCI ( n = 18) A33 (C3A) 45 37 \u2212 65 27 \u2212 49 26 A35 (T3A) 64 66 \u2212 105 67 \u2212 49 40 A38 (C4A) 51 47 \u2212 20 23 \u2212 22 21 A37 (T4A) 54 75 \u2212 58 73 \u2212 47 74 A39 (T5A) 53 44 \u2212 103 57 \u2212 32 55 A43 (T3A) 68 58 \u2212 109 53 \u2212 90 50 B06 (C4B) 53 36 \u2212 28 42 \u2212 27 36 B07 (T2B) 85 82 \u2212 73 81 \u2212 70 69 C09 (C7C) 68 60 \u2212 75 82 \u2212 78 71 D16 (C3D) 98 99 \u2212 47 60 \u2212 48 58 C16 (T4C) 67 55 \u2212 76 43 \u2212 40 41 D18 (T5D) 90 80 \u2212 66 84 \u2212 64 77 C11 (L2C) 119 112 \u2212 91 84 \u2212 74 72 C14 (C4C) 32 26 \u2212 38 23 \u2212 35 22 D20 (C5C) 97 101 \u2212 70 75 \u2212 72 59 C17 (T3C) 104 102 \u2212 114 80 \u2212 80 110 D21 (C5D) 81 61 \u2212 49 31 \u2212 54 27 D22 (T3D) 85 69 \u2212 59 59 \u2212 32 54 Mean ± SD 73 ± 23 * 67 ± 25 * \u2212 69 ± 27 58 ± 22 * \u2212 54 ± 20 53 ± 23 * NI ( n = 14) Mean ± SD 116 ± 13 * 106 ± 10 * \u2212 77 ± 26 109 ± 27 * \u2212 68 ± 23 101 ± 17 * * Note that FVC, FEV 1 ,P E max , and PE max MEPT were signi\ufb01cantly reduced in the SCI group compared to NI group ( p apart for each muscle recorded. Skin was prepared to reduce intra- electrode impedance. Right (R) and left (L) upper trapezius (UT) and upper portion of pectoralis (PEC) on midclavicular line; 6th Inter- costals on anterior axillary line (IC 6 ); rectus abdominus at umbilical level (RA); and oblique abdominus on the midaxillary line at the umbilical level (OBL) muscles were recorded ( American Thoracic Society/European Respiratory Society, 2002 ). The ground electrode was placed over the acromion process. The incoming sEMG sig- nals were ampli\ufb01ed with a gain of 500, \ufb01ltered at 30\u20131000 Hz and sampled at 2000 Hz. 2.4. sEMG data analysis Analysis windows of 3 s each for unloaded inspiration and expi- ration and 5 s each for MIPT or MEPT were determined from the event marker recorded with the cuing tone that signaled the sub- ject when to begin and end the task ( Fig. 3 ). To eliminate noise and ECG artifact, this value was corrected by subtracting the aver- aged activity computed from the same time window duration during quiescent recording immediately preceding the maneuver. The envelope of sEMG activity for each muscle was calculated using a root mean square (RMS) algorithm ( American Thoracic Society/European Respiratory Society, 2002; Sherwood et al., 2000 ) that produced a mean value in \u242e V. Three repeated trials for each task were averaged ( McKay et al., 2004 ). An ensemble average of those three repeated trials was obtained for each muscle (channel). The multi-muscle activation patterns were evaluated by adapt- ing a vector-based analysis method developed for the voluntary movement segment of the lower-limb BMCA protocol termed, the voluntary response index (VRI) ( Lee et al., 2004 ). The VRI calculation produces two values: Magnitude (Mag) and the Similarity Index (SI) for each phase of each maneuver. The Mag represents the length of the Response Vector (RV) which is the resultant vector calculated from the RMS values for all muscles that expresses the total amount of sEMG activity recorded during the time window analyzed. The SI provides a value between 0 and 1.0 that quanti\ufb01es how closely the multi-muscle distribution of activation in a test subject pat- tern matches the Prototype Response Vector (PRV) developed from Fig. 1. Surface electromyography (sEMG) recorded during quiet breathing in the supine position in (A) a non-injured individual (NI) and (B) a person with a C 3 , AIS-A SCI (C3A). Muscles shown are right and left upper trapezius (RUT/LUT), pectoralis (RPEC/LPEC), 6th intercostals (RIC 6 /LIC 6 ), rectus abdominus (RRA/LRA), and oblique abdominus (ROBL/LOBL). The inspiration phase is marked by bars at the bottom. The amplitude scale for RUT and LUT is 200 \u242e V (*) while all others are 20 \u242e V. Note that the symmetrical low-amplitude activation seen in A is lost in B and that there is increased background with inappropriate bursting in the both UT, LPEC, and LIC 6 (marked with circles). 174 A. Ovechkin et al. / Respiratory Physiology & Neurobiology 173 (2010) 171\u2013178 Fig. 2. sEMG recorded during a maximum inspiratory pressure task in (A) a non-injured individual (NI) and (B) a person with C 3 , AIS-A SCI (C3A). Note that an additional burst can be seen in the intercostal (RIC 6 and LIC 6 ), rectus abdomihus (RRA and LRA), and oblique abdominus (ROBL and LOBL) muscles (B) (marked with ellipses) superimposed in one trial only over the pattern of volitional activation to perform the requested task that was highly repeatable across three trials. Also note the exaggerated compensatory use of the upper trapezius (RUT and LUT) muscles during inspiration in comparison to the pattern in the SCI subject. *Amplitude scale was 2 mV for the RUT and LUT muscles. Fig. 3. (A and B) Maximum expiratory pressure task and (C and D) maximum inspiratory pressure task in a non-injured individual (NI) and a person with C 3 , AIS-A SCI (C3A). Pressure developed is shown on top and simultaneously recorded sEMG activity on the bottom. Maximum expiratory (PE max ) and inspiratory (PI max ) pressure during MEPT and MIPT marked with horizontal dashed line. Initiation of the task is marked by an arrow. Vertical dashed lines represent the 3-s and 5-s analysis windows for index calculations for unloaded and loaded tasks. Note the absence and decreased activity in expiratory muscles (B): internal intercostal (IC 6 ), rectus abdominus (RA), oblique abdominus (OBL) during MEPT and decreased activity of external intercostal (IC 6 ) muscles during MIPT which subsequently decreased the Similarity Index (SI) and PE max and PI max in the SCI subject. The amplitude scale for upper trapezius (RUT and LUT) muscles for SCI individual is 2 mV (*) while all others are 400 \u242e V. Note the subsequent increase in Magnitude (Mag) values. A. Ovechkin et al. / Respiratory Physiology & Neurobiology 173 (2010) 171\u2013178 175 non-injured subjects for the same volitional task. The PRV for each maneuver was generated by averaging the RVs from the 14 NI con- trol subjects. The SI value was computed for each task as the inner product, or cosine of the angle between the test-subject RV and PRV obtained from NI subjects. An SI value of 1.0 represents the best match for compared vectors. 2.5. Statistical analysis A two-sided t -test to detect a difference for each independent variable was used. Pearson correlation coef\ufb01cient ( r p ) or Spear- man\u2019s rank correlation coef\ufb01cient ( r s ) calculation was used to determine the strength of the relationship between parametric or non-parametric data sets, respectively. A level of signi\ufb01cant dif- ference was reached when p value was equal to or less than 0.05. Statistical analysis was conducted in NCSS/PASS Software (v. 2002, Kaysville, UT). 3. Results 3.1. Pulmonary function test Spirometric measures (FVC and FEV 1 ) and expiratory mus- cle strength parameters (PE max and P max MEPT) were signi\ufb01cantly reduced in the SCI group compared to those in NI group. Although mean values were lower in the SCI group, the differences between the two groups for PI max and PI max MIPT were not statistically sig- ni\ufb01cant ( Table 2 ). 3.2. Respiratory muscle activation patterns In the SCI group, sEMG recordings showed increased activity of the upper trapezius and pectoralis muscles, marked side-to-side amplitude asymmetries in other muscles during quiet breath- ing and respiratory tasks ( Figs. 1\u20134 ), and a loss or reduction of expiratory muscle activation during the loaded expiratory tasks ( Figs. 2\u20134 ). Quiet breathing in NI subjects was marked by low- amplitude symmetrical activity in the intercostal muscles during inspiration ( Fig. 1 A). Within the SCI group, resting inspiration was accompanied by different degrees of intercostal muscle activation depending on the level and completeness of the spinal cord lesion ( Fig. 1 B). One subject with a C3, clinically motor-complete lesion, had nearly regularly repeating involuntary bursting, recorded from the left pectoralis and intercostal muscles, that was not syn- chronized with the respiratory cycle ( Fig. 1 B). In this patient, such bursting appeared without provocation during quiet breath- ing and with greater amplitude when triggered during the MIPT ( Fig. 2 B). In both groups, the Mag values for all tasks showed consider- able variability across the subjects ( Table 3 ) and failed to show any correlation to spirometrical values or to the AIS-based clas- si\ufb01cation in the SCI group. SI values which are dependent on how similar the multi-muscle distribution of sEMG activity is to that of NI group were very consistent across the NI group showing very low standard deviation from the mean values for both inspira- tory and expiratory tasks, 0.92 ± 0.03 and 0.93 ± 0.04 (mean ± SD), respectively, when averaged for both unloaded and loaded tasks). In contrast, in SCI group, SI values for unloaded and loaded expi- ratory tasks were altered showing reduced SI values of 0.84 ± 0.11 and 0.59 ± 0.22, respectively, when averaged for both unloaded and loaded tasks) and were signi\ufb01cantly reduced compared to those of the NI group ( Table 3 ). During MEPT, NI subjects exhibited appropriate activation of expiratory muscles (intercostal, rectus abdominus and oblique) which was associated with high PE max and SI values ( Fig. 3 A). In contrast, muscle activation patterns during MEPT in the SCI group were altered, showing compensatory activation of upper trapezius and pectoralis muscles coupled with decreased or absent activation of rectus abdominus and oblique muscles, bringing a reduction in PE max and calculated SI values ( Figs. 3B and 4 ). Inspiratory sEMG patterns in those SCI subjects were less altered showing differ- ent levels of intercostal muscle activity producing PI max and SI values close to those recorded in the NI group ( Fig. 3 C and D; Tables 2 and 3 ). Fig. 4. sEMG activity during the maximum expiratory pressure task in individuals with SCI shown in order of AIS-determined injury level, top row were AIS motor-complete. Initiation and completion of the task is marked by arrows. Note that the increasingly appropriate activation of the expiratory muscles [internal intercostal (RIC 6 and LIC 6 ), rectus abdominus (RRA and LRA), oblique abdominus (ROBL and LOBL)] and decreasing activation of compensatory muscles [pectoralis (RPEC and LPEC)] across the range of injury levels and AIS scale categories is associated with increasing the Similarity Index (SI) values. Note the presence of activity in muscles innervated from below the injury level in the tope three, AIS motor-complete subjects. *Indicates an amplitude scale of 2 mV. 176 A. Ovechkin et al. / Respiratory Physiology & Neurobiology 173 (2010) 171\u2013178 Table 3 Summary of Magnitude (Mag) and Similarity Index (SI) values obtained during Respiratory Motor Control Assessment in SCI and NI individuals. Subjects Mag ( \u242e V) SI Unloaded Loaded Unloaded Loaded Inspiration Expiration MIPT MEPT Inspiration Expiration MIPT MEPT SCI ( n = 18) A33 (C3A) 99 2 329 273 0.68 0.21 0.77 0.23 A35 (T3A) 12 5 15 4 0.95 0.56 0.94 0.56 A38 (C4A) 63 39 89 118 0.69 0.24 0.72 0.43 A37 (T4A) 14 25 94 179 0.85 0.60 0.58 0.83 A39 (T5A) 46 23 27 52 0.73 0.69 0.79 0.73 A43 (T3A) 56 38 134 129 0.92 0.35 0.95 0.52 B06 (C4B) 34 9 33 58 0.80 0.35 0.91 0.68 B07 (T2B) 50 41 96 141 0.90 0.53 0.79 0.77 C09 (C7C) 19 15 50 54 0.92 0.75 0.91 0.72 D16 (C3D) 57 9 27 36 0.88 0.83 0.99 0.77 C16 (T4C) 48 43 62 156 0.80 0.39 0.94 0.49 D18 (T5D) 29 39 99 114 0.99 0.75 0.81 0.91 C11 (L2C) 15 20 11 47 0.70 0.87 0.92 0.82 C14 (C4C) 140 67 196 105 0.79 0.57 0.94 0.54 D20 (C5C) 178 23 152 79 0.83 0.44 0.90 0.76 C17 (T3C) 19 6 36 83 0.81 0.83 0.75 0.95 D21 (C5D) 22 34 60 71 0.93 0.20 0.97 0.43 D22 (T3D) 20 24 24 25 0.82 0.32 0.65 0.76 Mean ± SD 51 ± 46 26 ± 17 80 ± 85 96 ± 65 0.83 ± 0.09 0.53 ± 0.22 * 0.85 ± 0.12 0.66 ± 0.19 * NI ( n = 14) Mean ± SD 33 ± 17 15 ± 11 35 ± 19 66 ± 46 0.94 ± 0.04 0.91 ± 0.07 * 0.91 ± 0.05 0.94 ± 0.03 * * Note signi\ufb01cant difference in SI values between NI and SCI groups for unloaded expiration and MEPT ( p 0.05). Note also high variability of the Mag values in both groups. In the SCI group, multi-muscle activation patterns for the MEPT were positively correlated with the neurological injury level ( r s = 0.62, p = 0.006, Fig. 4 A). SI values for unloaded expiration were also signi\ufb01cantly, but less correlated with injury level ( r s = 0.56, p = 0.02). Further, PE max values recorded during PFT and MEPT ( Table 2 ) were highly correlated with SI values for MEPT ( Fig. 4 B). SI values for the MIPT were not correlated with injury level ( r s = \u2212 0.12, p = 0.63). Also, PI max values recorded during PFT and MIPT did not correlate with SI values ( r s = \u2212 0.07, p = 0.79 and r s = \u2212 0.23, p = 0.35, respectively) ( Fig. 5 ). Similar \ufb01ndings were obtained from the examination of unloaded efforts as measured prior to each MIPT and MEPT task performance ( Fig. 3 and Table 3 ). Mag values were highly vari- able across subjects in both groups for all tasks. Like the results from loaded tasks, SI values for unloaded inspiration were higher and more consistent in the NI group than the SCI group but the differences failed to reach signi\ufb01cance. For expiration, unloaded SI values were signi\ufb01cantly lower in the SCI group than the NI group. Further, SI values for unloaded expiration correlated less well but signi\ufb01cantly with FEV 1 ( r p = 0.57, p = 0.001). SI values for unloaded expiration correlated well with those from loaded expi- ration ( r p = 0.77, p = 0.0002). 4. Discussion In the data presented and as might be expected, better pul- monary function was found in subjects with lower injury levels and motor-incomplete lesions. As previously reported by others ( Baydur et al., 2001; Jain et al., 2006; Mateus et al., 2007 ), expiratory function as presented by FVC, FEV 1 ,P E max , and PE max MEPT val- ues obtained during this study, were signi\ufb01cantly impaired in the group with SCI and were related to the clinically determined level and severity of injury ( Table 2 ). In contrast, the inspiration-related parameters, PI max and PI max MIPT, were not statistically different from those of the NI group ( Table 2 ). This was likely due to the fact that all SCI subjects in this study retained functional diaphragm innervation. Underlying these functional changes brought by SCI is altered control of the muscles of respiration that results from damage to the spinal cord ( Schilero et al., 2009 ). The loss or demyelina- Fig. 5. (A) Scatter diagram and linear regression of Similarity Index (SI) values during maximum expiratory pressure task (MEPT) vs. the neurological level of SCI. (B) SI values compared to the maximum expiratory pressure (PE max ) recorded during PFT (opened circles and dashed correlation line) and MEPT (black circles and solid correlation line). A. Ovechkin et al. / Respiratory Physiology & Neurobiology 173 (2010) 171\u2013178 177 tion of long-tract axons as they transit the lesion zone, the loss of interneuronal circuitry that integrates supraspinal and spinal activity with peripheral input within the injury zone, and the dis- ruption of synaptic interaction within surviving circuitry alter, to varying degrees, the multi-muscle activation patterns needed to perform motor tasks ( Kern et al., 2005 ). In humans, this disrupted circuitry can only be examined two ways. First, through post- mortem neuropathological examination, it has been shown that structural disruption is highly individualized, with differing sever- ity spatial distribution within and along the cord ( Kakulas, 2004 ). The other approach is to examine spinal motor output in the form of multi-muscle activation as performed here. According to the Amer- ican Thoracic Society and European Respiratory Society Statement, the sEMG amplitude variability and complexity of EMG analy- sis has inhibited efforts to develop objective measures of motor control ( American Thoracic Society/European Respiratory Society, 2002 ). Our results show that the sEMG vector analysis-based algo- rithm used here has good face validity as regards the impact of SCI on control of respiratory muscles. Further, this analysis method can be used to quantitatively characterize respiratory motor con- trol despite the subject-to-subject EMG amplitude variability. One would still expect that the vectors could be affected by skin thick- ness, subcutaneous fat, muscle mass, and electrode positions. VRI calculation separates the Magnitude (the length of resultant vector which represents the overall amplitude of sEMG during a particular task) from the distribution of EMG activity across multiple muscles (resultant vector direction). From methodological standpoint, the most important advantage of this vector-based analysis is the fact that SI represents distribution of the sEMG activity independently from the overall amplitude. In other words, the overall amount of EMG can be different from subject to subject; however, if the dis- tribution of this activity across the muscles is similar to the normal pattern, the SI will be close to 1.0 indicating their high similar- ity. In addition, we dealt with it through the use of a non-injured subject group that was matched for age, weight, and height to the patient group. This study was a \ufb01rst attempt to apply quantitative evaluation of multi-muscle sEMG to the assessment of respiratory motor control with the goal of providing objective outcome mea- sures that can be analyzed statistically. With the use of this analytic tool, it should be possible to objectively evaluate the effects of exist- ing and new intervention strategies on impaired respiratory motor control in persons with SCI and other disorders. As with limb movements for which the multi-muscle distribu- tion patterns were highly consistent within each subject and across all non-injured subjects ( Lim and Sherwood, 2005 ), unloaded and loaded inspiration and expiration tasks were performed here with quite similar patterns across NI subjects ( Table 3 ). Thus, the cal- culated prototypes provided reliable references against which to calculate SI values and quantify the degree of difference in the multi-muscle distribution patterns produced by those with chronic SCI for the respiratory tasks examined. As a result, the activation of compensatory muscles combined with the reduction or loss of activity in appropriate muscles in SCI subjects for a task was charac- terized by the lower SI values reported here. Within each category of the AIS, multi-muscle activation patterns varied considerably. In some subjects with motor-complete cervical lesions, trunk muscles could be activated as part of the expiratory pattern in some sub- jects. This \ufb01nding was clearly not described by the AIS severity and spinal level assessment because the AIS does not incorporate the testing of trunk muscles, many of which are innervated from multi- ple cervical and thoracic spinal cord segments, into its calculation. Further, incomplete lesions characteristically contain highly indi- vidualized degrees of slowed and lost long-tract conduction across the injury. This increases the variability of function observed across any group of people with SCI ( Mateus et al., 2007 ). Finally, the obser- vation that spasticity could modify respiratory performance in one subject in this study ( Figs. 1 and 2 ) suggests that the ability to rec- ognize and quantify the effects of motor events unrelated to the respiratory task may have some value when selecting intervention strategies. In contrast to the SI, Mag values, representing the overall sEMG amplitude, were highly variable in both study groups as was reported for lower-limb motor control ( Lee et al., 2004 ). In addition, Mag values in the SCI group were often higher due to large increases in upper trapezius amplitude and activation of other compensatory muscles ( Fig. 4 ). All subjects with SCI showed signi\ufb01cantly altered multi-muscle activation patterns for expiration tasks when compared to the non- injured group ( Table 3 ) as quanti\ufb01ed by the SI calculation. The lack of difference between SCI and NI groups for PFT and SI values for inspiration was possibly the result of increased variance within the PFT data brought by mechanical attributes of the method ( Schilero et al., 2009 ) and impaired contractile characteristics of the respi- ratory muscles ( Kowalski et al., 2007 ). Our data also show that, as with limb muscles ( Lee et al., 2004 ), higher SI values, are related to greater similarity between test-subject patterns and those within the normal prototype for respiratory tasks ( Figs. 3 and 4 ). The results presented here show that central nervous system control of trunk muscles used to perform respiratory motor tasks after neuro- logical disease or injury can be objectively measured and validated through comparison with accepted standard measures of pul- monary function. Although the SI, as used here, does not describe in which way the pattern may be different, it does provide a uni\ufb01ed index value with which the severity of disruption can be compared across individuals and change over time or due to intervention can be tracked. However, further study needs to be undertaken to examine additional information that can be obtained from the sEMG signals. For example, sEMG as recorded here can be used to quantitatively describe: speci\ufb01c agonist\u2013antagonist relationship ratios; measures of asymmetry; the transition between inspiratory to expiratory phases and the spasticity seen in some of the record- ings described here can be used to further differentiate and register change. Whether interventions to improve respiratory control are based on structural, pharmacological, activity-dependent, or com- bined modalities, the goal will always be to modify, at a basic level, the way in which the central nervous system accomplishes control of the muscles of respiration. Therefore, sensitive measurement of muscle activation, such as applied here, will be needed. Acknowledgements The authors would like to express their appreciation to Matthew Nitzken, and Manpreet Chopra for their contributions to this work. This work was supported by grants from Paralyzed Veterans of America Research Foundation (PVA RFG 2613) and Christopher and Dana Reeves Foundation (CDRF OA2-0802-2). References Adams, M.M., Hicks, A.L., 2005. Spasticity after spinal cord injury. Spinal Cord 43, 577\u2013586. Alexander, M.S., Anderson, K.D., Biering-Sorensen, F., Blight, A.R., Brannon, R., Bryce, T.N., Creasey, G., Catz, A., Curt, A., Donovan, W., Ditunno, J., Ellaway, P., Finnerup, N.B., Graves, D.E., Haynes, B.A., Heinemann, A.W., Jackson, A.B., Johnston, M.V., Kalpakjian, C.Z., Kleitman, N., Krassioukov, A., Krogh, K., Lammertse, D., Magasi, S., Mulcahey, M.J., Schurch, B., Sherwood, A., Steeves, J.D., Stiens, S., Tulsky, D.S., Van Hedel, H.J., Whiteneck, G., 2009. Outcome measures in spinal cord injury: recent assessments and recommendations for future directions. Spinal Cord 47, 582\u2013591. American Spinal Injury Association and International Spinal Cord Society, 2006. International Standards for Neurological Classi\ufb01cation of Spinal cord Injury. ASIA and ISCS, Chicago. American Thoracic Society/European Respiratory Society, 2002. ATS/ERS Statement on respiratory muscle testing. Am. J. Respir. Crit. Care Med. 166, 518\u2013624. Anderson, K., Aito, S., Atkins, M., Biering-Sorensen, F., Charlifue, S., Curt, A., Ditunno, J., Glass, C., Marino, R., Marshall, R., Mulcahey, M.J., Post, M., Savic, G., Scivo- letto, G., Catz, A., 2008. Functional recovery measures for spinal cord injury: an 178 A. Ovechkin et al. / Respiratory Physiology & Neurobiology 173 (2010) 171\u2013178 evidence-based review for clinical practice and research. J. Spinal Cord Med. 31, 133\u2013144. Baydur, A., Adkins, R.H., Milic-Emili, J., 2001. Lung mechanics in individuals with spinal cord injury: effects of injury level and posture. J. Appl. Physiol. 90, 405\u2013411. Black, L.F., Hyatt, R.E., 1969. Maximal respiratory pressures: normal values and rela- tionship to age and sex. Am. Rev. Respir. Dis. 99, 696\u2013702. Brown, R., DiMarco, A.F., Hoit, J.D., Garshick, E., 2006. Respiratory dysfunction and management in spinal cord injury. Respir. Care 51, 853\u2013868. De Vivo, M.J., Krause, J.S., Lammertse, D.P., 1999. Recent trends in mortality and causes of death among persons with spinal cord injury. Arch. Phys. Med. Rehabil. 80, 1411\u20131419. Dimitrijevic, M.R., 1988. Residual motor functions in spinal cord injury. Adv. Neurol. 47, 138\u2013155. Garshick, E., Kelley, A., Cohen, S.A., Garrison, A., Tun, C.G., Gagnon, D., Brown, R., 2005. A prospective assessment of mortality in chronic spinal cord injury. Spinal Cord 43, 408\u2013416. Grif\ufb01ths, L.A., McConnell, A.K., 2007. The in\ufb02uence of inspiratory and expiratory muscle training upon rowing performance. Eur. J. Appl. Physiol. 99, 457\u2013466. Hart, N., Laffont, I., de la Sota, A.P., Lejaille, M., Macadou, G., Polkey, M.I., Denys, P., Lofaso, F., 2005. Respiratory effects of combined truncal and abdominal support in patients with spinal cord injury. Arch. Phys. Med. Rehabil. 86, 1447\u20131451. Jain, N.B., Brown, R., Tun, C.G., Gagnon, D., Garshick, E., 2006. Determinants of forced expiratory volume in 1 second (FEV1), forced vital capacity (FVC), and FEV1/FVC in chronic spinal cord injury. Arch. Phys. Med. Rehabil. 87, 1327\u20131333. Kakulas, B.A., 2004. Neuropathology: the foundation for new treatments in spinal cord injury. Spinal Cord 42, 549\u2013563. Kelley, A., Garshick, E., Gross, E.R., Lieberman, S.L., Tun, C.G., Brown, R., 2003. Spirom- etry testing standards in spinal cord injury. Chest 123, 725\u2013730. Kern, H., McKay, W.B., Dimitrijevic, M.M., Dimitrijevic, M.R., 2005. Motor control in the human spinal cord and the repair of cord function. Curr. Pharm. Des. 11, 1429\u20131439. Kowalski, K.E., Romaniuk, J.R., DiMarco, A.F., 2007. Changes in expiratory muscle function following spinal cord section. J. Appl. Physiol. 102, 1422\u20131428. Laffont, I., Durand, M.C., Rech, C., De La Sotta, A.P., Hart, N., Dizien, O., Lofaso, F., 2003. Breathlessness associated with abdominal spastic contraction in a patient with C4 tetraplegia: a case report. Arch. Phys. Med. Rehabil. 84, 906\u2013908. Lee, D.C., Lim, H.K., McKay, W.B., Priebe, M.M., Holmes, S.A., Sherwood, A.M., 2004. Toward an objective interpretation of surface EMG patterns: a voluntary response index (VRI). J. Electromyogr. Kinesiol. 14, 379\u2013388. Lim, H.K., Lee, D.C., McKay, W.B., Priebe, M.M., Holmes, S.A., Sherwood, A.M., 2005. Neurophysiological assessment of lower-limb voluntary control in incomplete spinal cord injury. Spinal Cord 43, 283\u2013290. Lim, H.K., Sherwood, A.M., 2005. Reliability of surface electromyographic measure- ments from subjects with spinal cord injury during voluntary motor tasks. J. Rehabil. Res. Dev. 42, 413\u2013422. Lim, P.A., Tow, A.M., 2007. Recovery and regeneration after spinal cord injury: a review and summary of recent literature. Ann. Acad. Med. Singapore 36, 49\u201357. Linn, W.S., Adkins, R.H., Gong Jr., H., Waters, R.L., 2000. Pulmonary function in chronic spinal cord injury: a cross-sectional survey of 222 southern California adult outpatients. Arch. Phys. Med. Rehabil. 81, 757\u2013763. Marino, R.J., Barros, T., Biering-Sorensen, F., Burns, S.P., Donovan, W.H., Graves, D.E., Haak, M., Hudson, L.M., Priebe, M.M., 2003. International standards for neu- rological classi\ufb01cation of spinal cord injury. J. Spinal Cord Med. 26 (Suppl. 1), S50\u2013S56. Marino, R.J., Jones, L., Kirshblum, S., Tal, J., Dasgupta, A., 2008. Reliability and repeata- bility of the motor and sensory examination of the international standards for neurological classi\ufb01cation of spinal cord injury. J. Spinal Cord Med. 31, 166\u2013170. Mateus, S.R., Beraldo, P.S., Horan, T.A., 2007. Maximal static mouth respiratory pres- sure in spinal cord injured patients: correlation with motor level. Spinal Cord 45, 569\u2013575. McKay, W.B., Lim, H.K., Priebe, M.M., Stokic, D.S., Sherwood, A.M., 2004. Clinical neurophysiological assessment of residual motor control in post-spinal cord injury paralysis. Neurorehabil. Neural Repair 18, 144\u2013153. Schilero, G.J., Spungen, A.M., Bauman, W.A., Radulovic, M., Lesser, M., 2009. Pulmonary function and spinal cord injury. Respir. Physiol. Neurobiol. 166, 129\u2013141. Sherwood, A.M., Dimitrijevic, M.R., McKay, W.B., 1992. Evidence of subclinical brain in\ufb02uence in clinically complete spinal cord injury: discomplete SCI. J. Neurol. Sci. 110, 90\u201398. Sherwood, A.M., Graves, D.E., Priebe, M.M., 2000. Altered motor control and spastic- ity after spinal cord injury: subjective and objective assessment. J. Rehabil. Res. Dev. 37, 41\u201352. Sherwood, A.M., McKay, W.B., Dimitrijevic, M.R., 1996. Motor control after spinal cord injury: assessment using surface EMG. Muscle Nerve 19, 966\u2013979. Smyth, R.J., Chapman, K.R., Rebuck, A.S., 1984. Maximal inspiratory and expiratory pressures in adolescents. Normal values. Chest 86, 568\u2013572. Stolzmann, K.L., Gagnon, D.R., Brown, R., Tun, C.G., Garshick, E., 2008. Longitudinal change in FEV1 and FVC in chronic spinal cord injury. Am. J. Respir. Crit. Care Med. 177, 781\u2013786. Walter, J.S., Sacks, J., Othman, R., Rankin, A.Z., Nemchausky, B., Chintam, R., Wheeler, J.S., 2002. A database of self-reported secondary medical problems among VA spinal cord injury patients: its role in clinical care and management. J. Rehabil. Res. Dev. 39, 53\u201361. Winslow, C., Rozovsky, J., 2003. Effect of spinal cord injury on the respiratory system. Am. J. Phys. Med. Rehabil. 82, 803\u2013814. Wirth, B., van, H.H., Curt, A., 2008. Foot control in incomplete SCI: distinction between paresis and dexterity. Neurol. Res. 30, 52\u201360.

Avaliação da ativação do músculo respiratório em indivíduos lesão medular Inglês

UNIC

Fisiologia Humana I

Continue navegando

Materiais relacionados

Perguntas relacionadas

Sobre Lesão Medular, assinale a alternativa CORRETA. A) O quadro clinico geral se traduz em paresia e distonia muscular, principalmente dos músculo...

Observe as seguintes afirmativas sobre o choque neurogênico e sobre o choque medular. Quais estão corretas? I — O choque medular é causado pela des...

Observe as seguintes afirmativas sobre o choque neurogênico e sobre o choque medular. Quais estão corretas? I — O choque medular é causado pela des...

Durante a avaliação neuromuscular de um paciente com lesão medular cervical, é o teste frequentemente utilizado para avaliar a função dos músculos ...

Outros materiais