Respiratory Physiology & Neurobiology 217 (2015) 54–62

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Compensatory muscle activation during forced respiratory tasks in individuals with chronic spinal cord injury Daniela Terson de Paleville a,b,∗ , Douglas Lorenz c a b c

University of Louisville, Health and Sport Sciences, United States University of Louisville, Neurosciences Collaborative Center, Frazier Rehab Institute, Louisville, KY, United States University of Louisville, Department of Bioinformatics and Biostatistics, United States

a r t i c l e

i n f o

Article history: Received 18 March 2015 Received in revised form 2 July 2015 Accepted 3 July 2015 Available online 11 July 2015 Keywords: Spinal cord injury Respiratory function Electromyography

a b s t r a c t When lesions in the spinal cord occur, the neural activation of respiratory muscles is compromised (De Troyer and Heilporn, 1980; De Troyer et al., 1986, 1990; Estenne et al., 2000a) resulting in significant respiratory dysfunction (De Troyer and Heilporn, 1980; Linn et al., 2000, 2001; Yokoba et al., 2003). However the underlying mechanisms that contribute to this dysfunction remain unclear. The aims of this study were: (1) to investigate whether a correlation exists between pulmonary function and the International Standards for the Neurological Classification of Spinal Cord Injury (ISNCSCI) examination scores for sensory and motor function; (2) to evaluate whether compensatory muscle activation plays a role in pulmonary function after spinal cord injury (SCI). We recorded Forced Vital Capacity (FVC); Forced Expiratory Volume in 1 s (FEV1 ); and electromyography (EMG) of respiratory muscles during maximum respiratory tasks in 36 with SCI and 15 neurologically intact participants. Results indicate that pulmonary function (FVC, FEV1 ) was strongly correlated with motor and sensory scores from the ISNCSCI exam and maximal expiratory pressure (MEP) was also significantly related to ISNCSCI sensory scores ( = 0.73, p < .001) and moderately, but significantly correlated to motor scores ( = 0.41, p = .04). After SCI, there is a compensatory recruitment of accessory muscles upper trapezius during maximal inspiratory pressure (MIP) and pectoralis and latissimus dorsi during MEP that is significantly higher than in non-injured (p < .001). © 2015 Elsevier B.V. All rights reserved.

1. Introduction When lesions in the cervical or thoracic segments of the spinal cord occur, the neural activation of respiratory muscles can be compromised (De Troyer and Heilporn, 1980; Baydur et al., 2001; Branco et al., 2007; De Troyer et al., 1986, 1990; De Troyer and Estenne, 1990; Estenne et al., 2000b) resulting in significant respiratory dysfunction (Linn et al., 2000, 2001; Cotton et al., 2005; DeVivo, 2012; DeVivo et al., 1999a,b). A clinical relevant aspect of impaired respiration in individuals with spinal cord injury (SCI) is the inability to cough adequately. Although cough reflex is preserved even after SCI (Dicpinigaitis et al., 1999), these individuals suffer from ineffective coughing due to paralyzed or weak respiratory muscles, resulting in accumulation of secretions that

∗ Corresponding author at: University of Louisville, Crawford gym 111, Louisville, KY 40292, United States. E-mail address: [email protected] (D. Terson de Paleville). http://dx.doi.org/10.1016/j.resp.2015.07.001 1569-9048/© 2015 Elsevier B.V. All rights reserved.

can cause airway obstruction and provide growth media for the development of pneumonia (Cotton et al., 2005). In fact, this is a common secondary complication after injury and is among the leading causes of death in acute (DeVivo et al., 1999a) and chronic (Garshick et al., 2005) SCI. Previous reports indicate that pulmonary function parameters, including forced vital capacity (FVC), forced expiratory volume in 1 s (FEV1 ), and maximal inspiratory and expiratory pressures (MIP and MEP, respectively) are negatively correlated with the injury level (Linn et al., 2001; Baydur et al., 2001; Estenne et al., 2000b; Garshick et al., 2005; Kelley et al., 2003). However, the effects of the severity of injury determined by the International Standards for the Neurological Classification of Spinal Cord Injury (ISNCSCI) examination (Waring et al., 2010) on these parameters remain unclear. A number of investigations have suggested that there is a correlation between pulmonary function and the neural activation of muscles involved in respiration (Linn et al., 2000; De Troyer et al., 1986). Peak expiratory flow rate is correlated with the EMG activity of pectoralis major and latissimus dorsi (De Troyer et al., 1986; Estenne and De Troyer, 1990; Fujiwara et al., 1999). EMG amplitude

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of intercostal muscles show significant increases with incremental respiratory loads in inspiratory muscle endurance tests in healthy individuals (Yokoba et al., 2003). However, the literature is limited in addressing the compensatory action of accessory muscles when primer movers for inspiration or expiration are weak or paralyzed as in SCI. We hypothesize that FVC, FEV1 , MEP and MIP show a positive correlation to the ISNCSCI sensory and motor scores for the spinal cord injury. Additionally, we suggest that lower pulmonary function values are associated to higher EMG amplitude of the respiratory muscles above the level of the injury (i.e. accessory muscles).

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shock is concluded determined by presence of muscle tone, deep tendon reflexes or muscle spasms; had a non-progressive SCI above T6; were classified as International Standards for the Neurological classification of Spinal Cord Injury (ISNCSCI) A,B,C or D; were not ventilator dependent for respiration; had a sustained SCI at least 6 months prior to entering the study and were at least 18 years of age. Persons with clinically recognizable concomitant head injury were not enrolled in this study. Six of the SCI participants were undergoing locomotor training, and the rest either have standard physical therapy or not therapy at the time of the recordings. Participants’ characteristics are shown in Table 1. 2.2. Neurological assessment

2. Materials and methods 2.1. Demographic and clinical characteristics This study was approved by the University of Louisville’s Institutional Review Boards in compliance with all the institutional and federal regulations concerning the ethical use of human volunteers for research studies. Fifty-one volunteers, including 36 participants with chronic traumatic SCI and 15 neurologically intact individuals, participated in this study (Table 1). SCI participants were classified using the American Spinal Injury Association impairment scale (AIS) as follows: 12 were cervical motor complete (AIS grade A–B), 11 were cervical motor incomplete SCI (AIS grade C–D), 8 cervical motor incomplete, 8 thoracic motor complete, 5 as thoracic motor incomplete and 15 participants were neurologically intact participants. Evaluations were performed within 7 days of an ISNCSCI examination. All the 36 SCI subjects participated on the pulmonary function portion of the study. However, only 25 of the SCI (6 cervical motor complete AIS grade A–B, 7 cervical motor incomplete AIS grade C–D, 7 thoracic motor complete AIS grade A–B and 5 thoracic motor incomplete AIS grade C–D) participated on the EMG assessment during MEP and MIP. Eight of the SCI and 5 of the neurologically intact participants were female, and all were between 20 and 54 years of age (37.1 ± 13.5). One SCI participant was diagnosed as central cord syndrome. Non-injured participants had no history of neuromuscular disease, back or join pain, were in stable medical condition without cardiopulmonary disease and were non-smokers. SCI participants were in stable medical condition without cardiopulmonary disease, had no painful musculoskeletal dysfunction, unhealed fracture, contracture, pressure sore or urinary tract infection; had no clinically significant depression, psychiatric disorders or ongoing drug abuse; showed clear indications that the period of spinal

The AIS based on the ISNCSCI was used to determine the neurological level and clinical motor completeness severity of the spinal cord lesion (Waring et al., 2010; Marino et al., 2003). The ISNCSCI categorizes SCI severity and motor level based on the evaluation of voluntary contraction strength for five upper limb (C5 to T1 ) and five lower limb (L2 to S1 ) muscles bilaterally. The AIS also determines a sensory level from the perception of light touch and pin prick for C2 through S5 dermatomes. The ISNCSCI has been shown to be a reliable estimate for use in clinical assessment of SCI (Waring et al., 2010; Marino et al., 2003; Marino and Graves, 2004). 2.3. Pulmonary function test FVC and FEV1 were obtained and expressed as the percent of predicted value for each subject based on a large database of healthy, neurologically intact individuals with no known pulmonary complaints that was derived based on gender, age, and height (Kelley et al., 2003; ATS/ERS, 2002). Three acceptable spirograms were obtained and the result of the best attempt was used. A Differential Pressure Transducer (MP45-36-871-350) with UPC 2100 PC card and software from Validyne Engineering (Northridge, CA) was used to measure MIP and MEP. MIP was measured during maximal inspiratory effort beginning at near residual volume and MEP was measured during maximal expiratory effort starting from near total lung capacity (Black and Hyatt, 1969). 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 diameter leak to prevent glottic closure and to reduce buccal muscle contribution during measurements. The assessment required that a sharp, forceful effort be maintained for a minimum of 2 s. The maximum pressure was taken as the highest value that is sustained for 1 s (Black and Hyatt, 1969). The maximum

Table 1 Clinical characteristics of participants by neurological level and injury severity; values are counts or mean ± SD. Group

Gender

Age (years)

Cervical motor complete (n = 12) Cervical motor incomplete (n = 11) Thoracic motor complete (n = 8) Thoracic motor incomplete (n = 5) Non-injured (n = 15)

4F; 8M 2F; 9M 1F; 7M 1F; 4M 7F; 8M

37 30 37 40 39

± ± ± ± ±

13 8 17 13 10

Weight (Lb.) 169 184 175 160 165

± ± ± ± ±

47 33 53 26 34

Height (in) 70 71 69 70 68

± ± ± ± ±

3 3 5 4 3

Time since SCI (months) 52 ± 35 22 ± 11 102 ± 75 92 ± 50 N/A

Table 2 Summary statistics (mean ± SD) for pulmonary function (FEV1 , FVC, MEP, MIP) by neurological level and injury severity. SCI Level

Severity

Cervical

Complete Incomplete

FVC (% predicted) 52 ± 17 73 ± 17

FEV1 (% predicted) 50 ± 19 69 ± 16

MEP (cm H20) 43 ± 20 63 ± 16

62 ± 27 93 ± 19

MIP (cm H20)

Thoracic

Complete Incomplete

79 ± 26 94 ± 7

72 ± 25 85 ± 13

52 ± 22 65 ± 30

54 ± 20 79 ± 31

Non-injured

N/A

109 ± 14

100 ± 10

100 ± 29

78 ± 25

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Fig. 1. Scatterplots of FVC, FEV1 , MEP, and MIP against AIS motor, light touch, and pin prick scores by neurological level and injury severity. The panel for motor preservation scores show that every subject with thoracic motor complete received the same score, however the values for maximal respiratory tasks range from very low to normal values for MEP, MIP, FEV1 and FVC. Values in the bottom right corner reflect group sample sizes, as Cervical complete/Cervical incomplete/Thoracic complete/Thoracic incomplete.

Table 3 Spearman rank correlation coefficients and p-values between pulmonary function variables (FVC, FEV1 , MEP, and MIP) and AIS scores for motor, light touch, and pin prick evaluation.

value from three maneuvers that varied by less than 20% were averaged.

over the muscle belly and with a distance between electrodes of 3 cm for each muscle recorded. After standard skin preparation to reduce intra-electrode impedance, pairs of surface EMG electrodes spaced 2 cm apart were placed over the muscle bellies of the right and left upper portion of pectoralis on midclavicular line; 6th intercostals on anterior axillary line; rectus abdominus at umbilical level; external obliques on the midaxillary line at the umbilical level and diaphragm region (ATS/ERS, 2002). The ground electrode was placed over the acromion process. The incoming EMG signals were amplified with a gain of 500, filtered at 30–1000 Hz and sampled at 2000 Hz and mean rectified; burst duration and integrated values were calculated.

2.4. Electromyography (EMG)

2.5. Statistical analyses

Surface EMG was recorded during the pulmonary function neurophysiologic assessment using an Eclipse Neurological Workstation (Axon Systems Inc., Hauppauge, NY) and RMA100 (MicroDirect, Lewiston, ME) with pair of FE9 silver–silver chloride surface electrodes (Grass Instruments, W Warwick, RI) centered

All measured outcomes (FVC, FEV1 , MEP, MIP, and integrated EMG) were summarized with means and standard deviations, medians, minima, and maxima. Summary statistics were calculated by study group: cervical complete, cervical incomplete, thoracic complete, thoracic incomplete. For each outcome variable, we fit

Variable

Motor

Light Touch

Pin Prick

FVC FEV1 MEP MIP

0.61 (p < .001) 0.62 (p < .001) 0.41 (p = 0.04) 0.23 (p = 0.25)

0.68 (p < .001) 0.70 (p < .001) 0.52 (p = 0.01) 0.05 (p = 0.81)

0.60 (p < .001) 0.67 (p < .001) 0.73 (p < .001) 0.42 (p = 0.06)

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Table 4 Median values of integrated EMG activity [IQR] for expiratory muscles by neurological level and severity and for injured and non-injured subjects. Group

Rectus abdominus

Obliques

Latissimus dorsi

Pectoralis

Cervical motor complete Cervical motor incomplete Thoracic motor complete Thoracic motor incomplete All SCI Non-injured

0 [0,0] 35 [17,269] 16 [6,38] 41 [0,72] 15 [0,44] 53 [29,83]

0 [0,0] 38 [16,248] 43 [0,143] 88 [25,97] 31 [0,95] 78 [59,160]

210 [132,232] 235 [211,306] 168 [104,292] 106 [46,141] 196 [103,273] 28 [18,91]

191 [61,417] 213 [93,399] 190 [101,247] 84 [62,225] 158 [83,288] 57 [35,104]

Fig. 2. Scatterplots of MEP against integrated EMG (log scaled) for expiratory muscles (rectus abdominus and obliques) in SCI and NI subjects. EMG activity in the rectus abdominus in NI was significant related to MEP, as MEP increased 7.1 mmHg for every one log-unit increase in EMG (p = .05). For SCI subjects, the relationship between rectus abdominus activity and MEP was reduced (slope = 3.5) but statistically significant. Plots are based on repeated observations from 6 complete cervical patients, 7 incomplete cervical patients, 7 complete thoracic patients, 4 incomplete thoracic patients, and 15 non-injured individuals.

linear models with two-level factors for neurological level (cervical, thoracic), injury severity (complete, incomplete), and an interaction term between level and severity. We conducted targeted comparisons of subgroups – cervical complete vs. cervical incomplete, thoracic complete vs. incomplete, cervical complete vs. thoracic complete, cervical incomplete vs. thoracic incomplete – through F tests from linear contrasts applied to the fitted linear models. Relationships between pulmonary function and ISNCSCI motor and sensory scores were examined through calculation of Spearman rank correlation coefficients. Integrated EMG was compared among the SCI groups using a non-parametric rank sum tests for clustered data introduced by Datta and Satten (2005). Relationships between MEP/MIP and EMG for SCI and non-injured individuals were examined through the fitting of linear mixed effects models, with log-EMG and injury status (SCI or non-injured) as fixed effects. F-tests of the mixed effects model coefficients evaluated the linear relationship between log-integrated EMG and MEP/MIP. Integrated EMG was log-transformed in fitting the models to reduce heavy right-skewness in these variables.

We calculated correlation coefficients between motor, light touch, and pin prick scores from the ISNCSCI exam and MEP using a marginal correlation coefficient for clustered data (Lorenz et al., 2011). All hypothesis tests were conducted at the 0.05 level, and all analyses were conducted with pairwise deletion of cases with missing values. All analyses were conducted using the open-source R software environment (R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Vienna, Austria, v. 2.12.2).

3. Results Thirty-six individuals with SCI and 15 non-injured individuals were included in the study. The SCI group was largely male (77%) and was diverse with respect to neurological level of injury (cervical or thoracic), severity of injury (complete or incomplete), age, weight, height, and time since injury at enrollment (Table 1). The non-injured group was nearly balanced with respect to

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Fig. 3. Scatterplots of MEP against integrated EMG (log scaled) for accessory muscles for expiration (latissimus dorsi and pectoralis) in SCI and NI subjects. EMG amplitude of the latissimus dorsi (p < .001) and pectoralis (p < .001), was significantly higher for SCI subjects than non-injured subjects. EMG activity in the latissimus dorsi and the pectoralis was not significantly related to MEP in SCI (p > .09) and NI subjects (p > .50). Plots of the latissimus dorsi are based on repeated observations from 4 complete cervical patients, 5 incomplete cervical patients, 5 complete thoracic patients, 3 incomplete thoracic patients, and 9 non-injured individuals. Plots of the pectoralis are based on repeated observations from 6 complete cervical patients, 7 incomplete cervical patients, 7 complete thoracic patients, 4 incomplete thoracic patients, and 15 non-injured individuals. Table 5 Median values of integrated EMG activity [IQR] for inspiratory muscles by neurological level and severity, and for injured and non-injured subjects. Group

Diaphragm

Intercostals

Upper trapezius

Scalenes

Sternocleidomastoid

Cervical complete Cervical incomplete Thoracic complete Thoracic incomplete All spinal cord injured Non-injured

59 [41,67] 72 [51,93] 68 [55,208] 92 [51,197] 66 [50,132] 48 [27,119]

55 [27,146] 75 [57,181] 75 [48,139] 64 [56,95] 70 [50,148] 43 [30,125]

177 [127,597] 133 [92,288] 266 [198,646] 117 [68,194] 187 [117,426] 116 [59,183]

403 [150,682] 367 [158,588] 393 [257,499] 281 [247,289] 289 [181,549] 178 [110,222]

421 [158,486] 289 [168,628] 419 [388,600] 366 [303,432] 399 [197,529] 289 [192,373]

gender (53% male) and was diverse with respect to age, weight, and height. 3.1. Pulmonary function Pulmonary function (FEV1 , FVC) varied by the neurological level and severity of SCI (Table 2). Subjects with thoracic SCI exhibited significantly higher FEV1 than those with cervical SCI (F1,31 = 4.24, p = .05) and subjects with incomplete injuries had higher FEV1 than subjects with complete injuries (F1,31 = 8.31, p = .007). There was no significant interaction between level and severity (F1,31 = 0.14, p = .71). Analysis of subgroups showed that subjects with incomplete injury had significantly higher FEV1 than subjects with complete injury in the cervical subgroup (F1,31 = 6.59, p = .02), but not the thoracic subgroup (F1,31 = 1.86, p = .18). Subjects with cervical and thoracic injury level did not significantly differ in the complete (F1,31 = 3.69, p = .06) and incomplete subgroups (F1,31 = 1.41, p = .24) on FEV1 . Similar results were observed for FVC.

Overall, higher FVC was observed for thoracic subjects (F1,31 = 5.43, p = .03) and incomplete subjects (F1,31 = 14.07, p < .001), but there was no interaction of level and severity (F1,31 = 0.20, p = .66). Subjects with incomplete SCI had higher FVC than those with complete SCI in the cervical subgroup (F1,31 = 10.98, p = .002) but not the thoracic subgroup (F1,31 = 3.29, p = .08). Thoracic subjects had higher FVC than cervical subjects in the complete subgroup (F1,31 = 4.86, p = .04), but not in the incomplete subgroup (F1,31 = 1.82, p = .19). FEV1 and FVC were also measured in the 15 non-injured individuals included in the study. Mean FEV1 among non-injured individuals was significantly higher than mean FEV1 among individuals with cervical complete, cervical incomplete, and thoracic complete injuries (F1,45 > 14.97, p < .001), but not individuals with thoracic incomplete injuries (F1,45 = 2.78, p = .10). Mean FVC among non-injured individuals was significantly higher than mean FVC among individuals with cervical complete, cervical incomplete, and thoracic complete injuries (F1,45 > 17.21, p < .001), but not individuals with thoracic incomplete injuries (F1,45 = 2.78, p = .10).

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Fig. 4. Scatterplots of MIP against integrated EMG (log scaled) for inspiratory muscles (diaphragm region and intercostals) in SCI and NI subjects. In the diaphragm, MIP was significantly positively related to EMG activity in both SCI subjects (slope = 10.6, p = .003) and non-injured subjects (slope = 4.8, p = .02). Higher intercostal activity was significantly related to higher MIP in the SCI group (slope = 8.8, p = .03) but not in non-injured subjects (slope = 3.0, p = .10). Plots are based on repeated observations from 6 complete cervical patients, 7 incomplete cervical patients, 7 complete thoracic patients, 4 incomplete thoracic patients, and 15 non-injured individuals.

Neurological level (F1,31 = 3.96, p = .06) and severity (F1,31 = 0.56, p = .46) were not significant determinants of MEP. Thoracic subjects had significantly higher MIP than cervical patients (F1,31 = 11.01, p = .003), while MIP did not significantly differ by severity (F1,31 = 1.18, p = .29). Pulmonary function (FVC, FEV1 ) was strongly correlated with motor and sensory AIS scores (Fig. 1 and Table 3). MEP was also significantly related to AIS scores, being most strongly correlated with pin prick scores (Spearman’s  = 0.73, p < .001) and moderately, but significantly correlated to motor scores ( = 0.41, p = .04). MIP was not significantly associated with any motor or sensory score, although the correlation between MIP and pinprick scores exhibited a moderate correlation of marginal significance ( = 0.42, p = .06). We noted that five individuals – all having incomplete SCI – exhibited motor scores of 78 and greater. These scores were outlying with respect to other observed motor scores in our sample (60 was next largest) and outlying with respect to the apparent linear relationships with pulmonary function. Spearman correlation coefficients for motor scores without these 5 observations were 0.60 for FVC, 0.65 for FEV1 , 0.64 for MEP, and 0.68 for MIP. 3.2. Muscle activity during forced expiration and inspiration During MEP, subjects with SCI exhibited significantly lower EMG activity than non-injured subjects in the expiratory muscles, the rectus abdominus (Datta–Satten rank sum test, 21 = 10.47, p = .001) and the obliques (21 = 11.21, p < .001, Table 4). Conversely, EMG amplitude of the latissimus dorsi (21 = 12.35, p < .001) and pectoralis (21 = 13.00, p < .001), was significantly

higher for SCI subjects than non-injured subjects. Integrated EMG for the rectus abdominus (23 = 17.27, p = .001) and obliques (23 = 16.35, p = .001) significantly differed among the four SCI subgroups defined by neurological level and severity, but no definitive pattern was evident among the 4 level/severity subgroups. The four SCI subgroups did not significantly differ in EMG activity for the latissimus dorsi (23 = 5.19, p = .16) and pectoralis (23 = 2.47, p = .48). For the expiratory muscles (rectus abdominus and obliques), EMG activity and MEP were positively related (Fig. 2). Among non-injured subjects, EMG activity in the rectus abdominus had a significant impact on MEP, as MEP increased 7.1 mmHg for every log-unit increase in EMG (F1,78 = 3.97, p = .05). Among SCI subjects, the impact of rectus abdominus activity was reduced (slope = 3.5) but statistically significant (F1,78 = 6.66, p = .01). Although the slopes of the lines of best fit were larger in non-injured subjects, indicating higher efficiency of the abdominal muscle in promoting expiration, the difference in slopes between groups was non-significant (F1,78 = 0.83, p = .36). Similar results were seen for the oblique muscles. Non-injured subjects improved MEP by 11.7 mmHg for every log-unit increase in EMG in the oblique muscles, and SCI subjects improved MEP by 8.1, both reflect significant impact (F1,74 > 8.18; p < .006). The difference in slopes between non-injured and SCI subjects was non-significant (F1,74 = 0.59, p = .44). Accessory muscles for expiration were not significantly related to MEP (Fig. 3). EMG activity in the latissimus dorsi and the pectoralis did not significantly influenced MEP in SCI (F1,52 = 2.96, F1,76 = 0.01; p > .09) and non-injured subjects (F1,52 = 0.46, F1,76 = 0.26; p > .50). Subjects with SCI exhibited significantly higher EMG activity than non-injured subjects in the inspiratory muscles, the diaphragm region (Datta–Satten rank sum test, 21 = 4.91, p = .03)

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Fig. 5. Scatterplots of MIP against integrated EMG (log scaled) for accessory muscles for inspiration (upper trapezius, scalenes, and sternocleidomastoid) in SCI and NI subjects. Only the upper trapezius activity was significantly positively related to MIP (slope = 11.1, p = .003) in SCI subjects; activity in the scalenes (slope = 8.6, p = .15) and sternocleidomastoid (slope = 6.2, p = .29) were not significantly related to MIP. Plots of the upper trapezius are based on repeated observations from 6 complete cervical patients, 7 incomplete cervical patients, 7 complete thoracic patients, 4 incomplete thoracic patients, and 15 non-injured individuals. Plots of the scalenes and sternocleidomastoid are based on repeated observations from 4 complete cervical patients, 6 incomplete cervical patients, 4 complete thoracic patients, 3 incomplete thoracic patients, and 9 non-injured individuals.

and the intercostals (21 = 7.52, p = .006), as well as in the accessory muscles for inspiration, the upper trapezius (21 = 6.83, p = .009), the scalenes (21 = 8.13, p = .004), and the sternocleidomastoid (21 = 6.45, p = .01, Table 5) during maximal forced inspiration. The four SCI subgroups defined by neurological level and severity did not significantly differ with in EMG activity in any of the 5 muscles (213 = 3.96, p > .27). Figs. 4 and 5 show the neural activation of inspiratory muscles during MIP. MIP was significantly and positively related to

EMG activity in both SCI subjects (slope = 10.6, F1,78 = 9.26, p = .003) and non-injured subjects (slope = 4.8, F1,78 = 6.04 p = .02) for the diaphragm region. Although diaphragm activity had a larger impact on MIP for SCI when compared with non-injured subjects (Fig. 4), the difference was not significant (F1,78 = 2.14, p = .15). Increased intercostal activity significantly improved MIP in the SCI group (slope = 8.8, F1,77 = 4.65, p = .03) (Fig. 4) but not in non-injured subjects (slope = 3.0, F1,77 = 2.82, p = .10). The difference in slopes between groups was non-significant (F1,77 = 1.74, p = .19). Among

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the accessory muscles for inspiration (Fig. 5), only the upper trapezius significantly improved MIP (slope = 11.1, F1,77 = 9.56, p = .003) in SCI subjects; activity in the scalenes (slope = 8.6, F1,53 = 2.17, p = .15) and sternocleidomastoid (slope = 6.2, F1,53 = 1.16, p = .29) were not significantly related to MIP. In non-injured subjects, both increased upper trapezius activity (slope = 11.3, F1,77 = 9.11, p = .003) and increased scalene activity (slope = 14.0, F1,53 = 5.38, p = .02) significantly improved MIP; activity in the sternocleidomastoid was unrelated (slope = 12.5, F1,53 = 2.59, p = .11). There were no differences in MIP impact between SCI and noninjured subjects for any muscles of these three muscles (F < 0.43; p > .51). In Section 2.1 we noted that MEP was significantly associated with motor, light touch, and pin prick scores from the ISNCSCI examination. In order to address potential confounding of the MEP–EMG relationships noted above, we calculated correlation coefficients between EMG for each muscle and ISNCSCI exam scores. We noted three significant correlations – EMG from the rectus abdominus muscles was significantly associated with light touch scores (coefficient = 0.36, p = 0.04) and pin prick scores (coefficient = 0.47, p = .001), and EMG from the oblique muscles was significantly associated with pin prick scores (coefficient = 0.45, p = .003). There were no other significant ISCNSCI score–EMG correlations (p > .16).

Warren et al., 2014), suggesting a compensatory action of the unaffected hemidiaphragm or accessory muscles. In the present study, we found that upper trapezius is being recruited and contributes to higher inspiratory pressures in SCI participants. During MIP, SCI individuals showed higher integrated EMG activity of the diaphragm and intercostals as well as the accessory muscles for inspiration than non-injured. EMG activity of the diaphragm was positively correlated for both SCI and non-injured. Increased neural activation of the intercostals has an impact in MIP in SCI, in other words, when SCI individuals showed higher EMG activity in the intercostals, MIP was improved. Higher neural activation of accessory muscles for inspiration were related to higher MIP in non-injured. However, only upper trapezius was significantly related to higher MIP in the SCI group. Compensatory activity was also observed for expiratory tasks in humans (De Troyer and Heilporn, 1980; De Troyer et al., 1986; De Troyer and Estenne, 1990; Estenne et al., 1989, 2000b; Estenne and De Troyer, 1987, 1990; Fujiwara et al., 1999; Morgan and De Troyer, 1984). Strengthening of accessory muscles have been related with a better cough production and with an increased expiratory reserve volume (De Troyer et al., 1986; Estenne and De Troyer, 1990; Estenne et al., 1989). However we observed that higher EMG activation of pectoralis was not related with higher forced expiratory function in this population.

4. Discussion

5. Conclusions

The respiratory system is under sophisticated neural control. When the dorsal respiratory group fires it signals the phrenic nerve to contract the diaphragm and intercostal nerves to contract external intercostals. The diaphragm and the external intercostals are the prime movers for quiet inspiration. As ventilatory demands increase, for example during exercise, other accessory muscles for inspiration are recruited. Expiration is usually passive and occurs due to the elastic recoil of the lungs. However, if it is necessary, expiration occurs by the active involvement of the intracostal portion of the internal intercostal and abdominal musculature (i.e. forced expiration). These muscles are also actively involved during coughing and sneezing. When respiratory muscles are affected like after lesions of the cervical or upper thoracic segments of the spinal cord, reflex and voluntary activity of the respiratory muscles is dramatically affected impairing pulmonary function (National Spinal Cord Injury Statistic Center, 2012). Injuries to the cervical segments of the spinal cord often result in paralysis of the respiratory muscles (De Troyer and Heilporn, 1980; Fugl-Meyer, 1971). Animal studies have demonstrated the plasticity of the respiratory system after injuries of the central nervous system. C2 hemisections and phrenicotomy in rats decreased tidal volume and increased respiratory rate (Golder et al., 2003). However no changes were observed in the C2 hemisection shamoperated rats, suggesting a greater recruitment of other muscles at the level of the spinal lesion to compensate with the respiratory demands. Similar findings were observed in hemisection models in dogs (Katagiri et al., 1994). These animal models have been meaningful to understand the neurophysiological mechanisms of pulmonary dysfunction associated with SCI. However, transections and hemisections do not commonly occur in humans with SCI. Even in persons characterized as clinically motor complete SCI, sparing descending fibers are evident (Kakulas, 1984, 1999). This has been also demonstrated with sensitive neurophysiological assessments (McKay et al., 2004, 2011a,b; Sherwood et al., 1992, 2000). Thus, evaluation of respiratory function after contusive injuries models is more clinically relevant. Studies using contusion models suggest that acutely, hemi diaphragmatic activity is compromised, but rapidly recovered (Nicaise et al., 2012a,b, 2013; Awad et al., 2013;

The purpose of this study was to investigate the neural role of spinal cord injury on pulmonary dysfunction in individuals with cervical and upper thoracic spinal cord injury. First, we compared pulmonary function among groups with different levels and severity of spinal cord injury. This finding is in agreement with previous investigations (Linn et al., 2000, 2001; Claxton et al., 1998; Schilero et al., 2009). Individuals with thoracic motor complete SCI received the same motor preservation score, however the values for maximal respiratory tasks range from very low to normal values for MEP, MIP, FEV1 and FVC. These forced voluntary respiratory tasks, especially MEP and FEV1 require activation of expiratory muscles, which are innervated by thoracic spinal segments (at or below the level of the injury for participants in this study). The findings of this study have several clinical implications that need to be emphasized. First, even though that a statistical correlation between AIS scores and respiratory parameters exist; pulmonary function after SCI cannot be predicted using the current validated scales for motor or sensory preservation. The majority of the muscles involved in forced expiration and coughing are innervated by thoracic spinal nerve segments that are not evaluated in the AIS scale. Therefore, caution should be used in predicting pulmonary function outcomes based solely on the level and severity of injury based on this grading system. Efforts are being made to develop a SCI pulmonary function basic data set in order to facilitate consistent collection and reporting findings about pulmonary function in the SCI population (Biering-Sorensen et al., 2012). This and similar studies will provide more insight on ways to characterize people at risk to develop pneumonia and other pulmonary complications secondary to SCI. Second, after a neurological lesion, there is plasticity in the nervous system involving new compensatory strategies to counteract the lack of neural activation of the prime mover muscles for inspiration and expiration. For instance, latissimus dorsi is an accessory muscle for forced expiration in individuals with paralyzed rectus. As predicted, EMG activity of the rectus abdominus and external obliques muscles were significantly higher in non-injured than in SCI individuals. Neural activity of accessory muscles for expiration was higher in SCI than in non-injured individuals as integrated EMG

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