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Journal of Motor Behavior Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/vjmb20
Local Muscle Fatigue and 3D Kinematics of the Cervical Spine in Healthy Subjects a
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Daniel Niederer , Lutz Vogt , Torsten Pippig , Rudolf Wall & Winfried Banzer a
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Department of Sports Medicine, Goethe-University Frankfurt/Main, Germany
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Department of Clinical Aviation Medicine, German Air Force Institute for Aviation Medicine, Fürstenfeldbruck, Germany Published online: 16 Jul 2015.
Click for updates To cite this article: Daniel Niederer, Lutz Vogt, Torsten Pippig, Rudolf Wall & Winfried Banzer (2015): Local Muscle Fatigue and 3D Kinematics of the Cervical Spine in Healthy Subjects, Journal of Motor Behavior, DOI: 10.1080/00222895.2015.1058241 To link to this article: http://dx.doi.org/10.1080/00222895.2015.1058241
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Journal of Motor Behavior, Vol. 0, No. 0, 2015 Copyright © Taylor and Francis Group, LLC
RESEARCH ARTICLE
Local Muscle Fatigue and 3D Kinematics of the Cervical Spine in Healthy Subjects Daniel Niederer1, Lutz Vogt1, Torsten Pippig2, Rudolf Wall1, Winfried Banzer1
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1 Department of Sports Medicine, Goethe-University Frankfurt/Main, Germany. 2Department of Clinical Aviation Medicine, €rstenfeldbruck, Germany. German Air Force Institute for Aviation Medicine, Fu
ABSTRACT. The authors aimed to further explore the effects of local muscle fatigue on cervical 3D kinematics and the interrelationship between these kinematic characteristics and local muscle endurance capacity in the unimpaired cervical spine. Twenty healthy subjects (38 § 10 years; 5 women) performed 2 £ 10 maximal cervical flexion–extension movements. Isometric muscle endurance tests (prone/supine lying) were applied between sets to induce local muscle fatigue quantified by Borg scale rates of perceived exertion (RPE) and slope in mean power frequency (MPF; surface electromyography; m. sternocleidomastoideus, m. splenius capitis). Cervical motion characteristics (maximal range of motion [ROM], coefficient of variation of the 10 repetitive movements, mean angular velocity, conjunct movements in transversal and frontal plane) were calculated from raw 3D ultrasonic movement data. Average isometric strength testing duration for flexion and extension correlated to the cervical ROM (r D .49/r D .48; p < .05). However, Student’s t test demonstrated no significant alterations in any kinematic parameter following local muscle fatigue (p > .05). Although subjects’ cervical muscle endurance capacity and motor output seems to be conjugated, no impact of local cervical muscle fatigue on motor function was shown. These findings underline the importance of complementary measures to address muscular performance and kinematic characteristics in outcome assessment and functional rehabilitation of the cervical spine.
activities of daily living (ADL; Takeuchi et al., 2007). Following the aim to reveal adequate measures for multimodal musculoskeletal interventions for CNPP, research considering patients’ movement alterations is warranted (Chiu et al., 2011; Hakkinen, Kautiainen, Hannonen, & Ylinen, 2008; Martel, Dugas, Dubois, & Descarreaux, 2011). Preliminary evidence points toward an interrelationship between musculoskeletal endurance and neuromuscular function in CNPP. For instance, cervical muscle fatigue is related to poor postural control in healthy adults (Gosselin, Rassoulian, & Brown, 2004; Schieppati, Nardone, & Schmid, 2003; Vuillerme, Pinsault, & Vaillant, 2005). Data on the transferability of this suggested relationship on motor performance of the neck is lacking so far. In unimpaired subjects and concerning different parts of the musculoskeletal system than the neck, previous research demonstrates inconsistent data on the possible association of muscle fatigue and kinematics. While local muscle fatigue was shown to negatively affect kinematic outcomes of the rotator cuff during arm elevation (Tsai, McClure, & Karduna, 2003) and of the lower limbs during side-step maneuvers (Cortes, Greska, Kollock, Ambegaonkar, & Onate, 2013), other studies on fatigued hip extensors and flexors suggest no influence on kinematics during jump landing movements (Hollman, Hohl, Kraft, Strauss, & Traver, 2012) or running (Abt et al., 2011). Concerning the cervical spine, slowly assessed neck ROM was shown to decrease following overhead work (Shin, An, Oh, & Yoo, 2012). The authors suggest that shoulder muscle fatigue has led to this phenomenon. The limited ability of muscles to shorten in fatigued conditions (Cheng, Davidson, & Rice, 2010), altered afferent feedback from muscles (Bilodeau, Henderson, Nolta, Pursley, & Sandfort, 2001), or increases in spontaneous discharges of mechanically sensitive nonspindle muscle afferents (Hayward, Wesselmann, & Rymer, 1991) are discussed as potential underlying physiologic mechanisms for the affection of muscle fatigue on ROM. Due to this conceivable but not yet investigated relation, in the present study we aimed to further explore the interrelationship of local muscle endurance capacity and cervical 3D kinematics and to investigate potential
Keywords: local muscle fatigue, cervical kinematics, muscle endurance, range of motion, movement variability
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n addition to musculoskeletal disorders (Alricsson, Harms-Ringdahl, Sch€ uldt, Ekholm, & Linder, 2001; Lee, Nicholson, & Adams, 2005; Peolsson, Almkvist, Dahlberg, Lindqvist, & Pettersson, 2007), current research demonstrates altered movement characteristics in chronic neck pain patients (CNPP) in comparison with unimpaired subjects. In particular, maximal cervical spine range of motion (ROM) is impaired in such patients (Chiu & Lo Sing, 2002; Strimpakos, 2011). Additionally, CNPP often show constricted movement consistencies (Sj€ olander, Michaelson, Jaric, & Djupsj€ obacka, 2008; Vogt, Segieth, Banzer, & Himmelreich, 2007). These constrictions occur by means of increased movement variability, angle reproducibility deficits, and larger nonintended conjunct movements while performing planar movements. Despite the pertinence of these alterations in movement characteristics, most rehabilitation programs primarily include measures to impact on muscular strength, stiffness, and endurance to improve muscle performance and functional stabilization in CNPP. Interventions targeting movement patterns are commonly neglected. Only low to moderate quality evidence supports the relevance of such exercise approaches for CNPP rehabilitation (Gross et al., 2008; Kay et al., 2012) also in terms of improvements in
Correspondence address: Daniel Niederer, Department of Sports Medicine, Goethe-University Frankfurt/Main, Ginnheimer Landstraße 39, Frankfurt am Main 60487, Germany. e-mail: [email protected] Color versions of one or more of the figures in the article can be found online at www.tandfonline.com/vjmb. 1
D. Niederer et al.
differences in means in cervical flexion–extension ROM and movement consistency prior to and following local muscle fatigue induction in the unimpaired cervical spine. We hypothesized that muscle fatigue would negatively affect kinematics and that muscle endurance capacity and kinematic characteristics are positively interrelated.
Methods Ethical Standards The study was approved by a local ethical review committee for medical research and conducted in accordance to the ethical standards set by the Declaration of Helsinki (1964) with its modifications (Fortaleza, 2013).
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Participants Twenty subjects (M age D 38 § 10 years; body mass index D 24.9 § 3.3 kg*m¡2; five women) were recruited in the German Air Force Institute for Aviation Medicine (F€ urstenfeldbruck, Germany). The subjects were physical active full-time employees and reported regular engagements in physical activity (e.g., running, cycling, swimming) at moderate to vigorous intensity. They were recruited through personal addressing. Each participant signed informed consent prior to study enrollment. Exclusion criteria included any previous surgery of the spine; known neck disorders or neck pain in the previous 12 months; persistent or passed cervical spine complaints based on space-occupying, inflammatory, traumatic, or systemic processes; the intake of painkilling drugs, analgesics, or muscle relaxants; radicular or pseudoradicular neurologic symptoms; inflammatory rheumatic diseases, osteoporosis, fracture, and/or surgery within the last six months; severe cardiovascular, pulmonary, neurological, cancerous, endocrinologic, and psychiatric diseases; fibromyalgia; hemophilia; pregnancy; and participation in other studies. Experimental Design Participants performed two sets (pre–post) of 10 repetitive maximal cervical flexion–extension movements (upright sitting position). Standardized isometric muscle endurance tests were applied between sets to induce local muscle fatigue, which was quantified by the slope in mean power frequency (MPF) of the EMG signal. Actual pain intensity were collected after cervical movements sets and following the isometric muscle endurance test and elicited by a single question and measured in millimeters (pain intensity) on a 100 mm visual analog scale (VAS; 0 D no pain, 100 D most severe pain). Following the assessments of pain intensity, Borg ratings of perceived exertion (RPE) in ratings of 6–20 on a Likert-type scale ranging from 6 (no exertion at all) to 20 (maximal exertion) was collected. 2
Cervical Spine Kinematics A noninvasive external three-dimensional ultrasonic movement analysis system (Zebris CMS 70, Isny, Germany; error of measurement 0 D flexion; < 0 D extension.
Ljungquist, Fransson, Harms-Ringdahl, Bj€ ornham, & Nygren, 1999; Olson, Millar, Dunker, Hicks, & Glanz, 2006; Peolsson et al., 2007; Peolsson & Kjellman, 2007). For that purpose, subjects positioned themselves in a standardized prone (extension) followed by supine (flexion) lying position with their arms close to the body and stretched legs. Participants’ head and neck were positioned in a comfortable neutral position. Neutral position was self-determined and investigator controlled. During these validated flexion– extension tests, the head had to be held static by submaximal isometric contraction in accordance to the direction of muscles’ eccentric function. For the extension test, an additional standardized weight (men D 4 kg, women D 2 kg) was hold by a belt and positioned on the sutura lambdoidea. Participants had to maintain the goniometer-controlled position until subjective exhaustion, until the position could not be maintained (evasion > 5 ) or until the occurrence of severe cervical pain. The second kinematic assessment followed less than 1 min after local muscle fatigue induction termination. Bipolar surface electromyography (EMG; BIOVISION, Wehrheim, Germany, differential instrumentation amplifier; input impedance 10 GV, CMMR 130 db, RTI noise 8 nVxHz, gain 2,500, filter 10 Hz low cutoff, 700 Hz high cutoff) was applied during flexion–extension endurance tests. For signal detection, Ag/AgCI electrodes (rectangular 4 £ 5 mm embedded in circular 10 mm diameter gel pad, blue sensor N-00-S [ Medicotest GmbH, Andernach, Germany] 2 cm interelectrode distance) were used. To assess muscle activity on m. sternocleidomastoideus (flexion) and 2015, Vol. 0, No. 0
m. splenius capitis (extension; Falla, Jull, & Hodges, 2004; Harrison et al., 2009) EMG was applied on one body side only (left or right). Body side was chosen randomized by a computer-generated randomization list. Electrodes were attached on the muscle belly (m. sternocleidomastoideus: 1 cm under the mandibula, m. splenius capitis: height of C4). Reference electrode was fixed on a muscle-free area on the skin cranial to the acromion. To quantify local myoelectric manifestations of muscle fatigue, the initial and ending 5 s of the EMG signal (at any one time for extension and flexion) were selected. For data analysis (Watscope software, Northern Digital Inc., Waterloo, Ontario, Canada), MPF was calculated for each time segment using a fast Fourier transformation. Slopes in MPF over time were used to estimate muscular endurance. Compared to the initial MPF, a slope of > 10% in average indicates local muscle fatigue (Harrison et al., 2009). Statistical Analysis Statistical procedures were executed using SPSS 19.0 (SPSS Inc., Chicago, IL) or BiAS for Windows (version 10 [2012], Goethe-University of Frankfurt, Frankfurt am Main, Germany) after the examination of underlying assumptions for parametric group and parametric correlation analyses testing. Dependent Student’s t tests were calculated for pre–post differences of means regarding CV, maximum oscillation angles (ROM, ROT, LAT), and V. To detect possible interrelationships, initial movement analysis outcomes were compared to muscle endurance testing 3
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duration using bivariate correlation analysis. Furthermore, partial correlations using age as covariate were calculated. A two-sided p-value of less than .05 was considered as statistically significant.
Although subjects’ cervical muscle endurance capacity and motor output seems to be conjugated, no impact of local cervical muscle fatigue on motor function, in detail on ROM, CV, ROT, and LAT was shown.
Results
Discussion
No participant had to be excluded, neither during screening nor after study enrollment. Descriptive results for both 3D kinematics and local muscle fatigue induction are shown in Table 1. Analysis of VAS revealed that only one (extension 12 mm) to two subjects (flexion 10–12 mm) displayed mild neck pain intensity following muscle fatigue induction (all other subjects’ VAS was 0 mm). Student’s t tests for comparisons of means revealed no significant alterations in kinematic parameters following local muscle fatigue (p > .05; coefficient of variation: .03 § .016 vs. .029 § .018; maximal ROM 128 § 23 vs. 125 § 19 ; mean angular movement velocity: 63 § 26 /s vs. 64 § 25 /s; conjunct movements in transversal: 16 § 7 vs. 14 § 4 and frontal plane: 11 § 4 vs. 11 § 3 ). Correlation analysis revealed significant correlations between both average isometric strength testing duration for flexion (162 § 88 s; RPE: 16 § 2; MPF: –16 § 8%; r D .48) and extension (542 § 367 s; RPE: 15 § 2; MPF: ¡13 § 10%; r D .49) to cervical ROM (p < .01; Figure 2) but not between testing duration and any other kinematic outcome (p > .05). Partial correlation analysis and correlation coefficients comparisons revealed no systematic influence of age on the correlation coefficient (r D .47, N D .038 for flexion; r D .55, N D .25 for extension; p > .05). Derived from the MPF-slope and according to the cutoffs (Harrison et al., 2009), each subject was fatigued on—at least—one of the tested sides: flexion (slope > 10%: n D 17; slope 0–10%: n D 3; no slope: n D 0) or extension (slope > 10%: n D 12; slope 0–10%: n D 8; no slope: n D 0).
The present study on cervical spine 3D kinematics and local muscle fatigue revealed a moderate association of isometric muscle endurance testing duration and maximal ROM in healthy adults’ cervical spine as hypothesized. Nevertheless and in contrary to the hypothesis, no systematic influence of local muscle fatigue on cervical movement patterns was observed. Present studies’ findings of a mean MPF slope of 13% (extension) and 15% (flexion) correspond to previously published findings reporting slopes of approximately 15% for flexion and 11.2% for extension in asymptomatic subjects (Harrison et al., 2009). Overall, the increase in RPE and the decrease in EMG frequency found in the present study are symptomatic for muscle fatigue (Madeleine, 2010). The duration of the local muscle endurance testing (extension M D 542 s; flexion M D 162 s) are somewhat higher than reference values in healthy adults (Domenech, Sizer, Dedrick, McGalliard, & Brismee, 2011; Edmondston et al., 2011). This disagreement may partially be explicable by the comparably lower age and higher proportion of males in our sample. Nevertheless, our subjects’ mean slope > 10% and its comparability to recent findings indicate sufficient objective local muscle fatigue values to discuss the present results as valid. According to the cutoff value, a minority of subjects were not fatigued following the extension task (slope of < 10%). Nevertheless, no subject showed an increase in MPF after isometric muscle endurance testing. Thus, subjects are discussed as fatigued. A negative impact of cervical muscle fatigue on postural control in healthy adults was shown in previous research (Gosselin et al., 2004; Schieppati et al., 2003; Vuillerme et al.,
TABLE 1. Characteristics for Cervical 3D Kinematics and Local Muscle Fatigue Induction Tests
Duration (s)
Local Muscular Fatigue Induction (M § SD and 95% CI) RPE (pts.)
Extension 542 § 367 [370, 714]
Flexion 162 § 88 [120, 203]
Pre (M § SD) [95% CI] Post (M § SD) [95% CI]
CV (%) 3.0 § 1.6 [2.3, 3.8] 2.9 § 1.8 [2.1, 3.8]
Extension Flexion 15 § 2 16 § 2 [13, 16] [15, 17] Cervical Spine 3D Kinematics ROM ( ) V ( *s¡1) 128 § 23 62 § 26 [117, 139] [50, 75] 125 § 19 64 § 25 [116, 134] [52, 75]
MPF-Slope (%) Extension 13 § 10 [9, 16]
Flexion 16 § 8 [13, 19]
ROT (%) 12.5 § 6 [9.5, 15.6] 11.1 § 3.4 [9.3, 12.8]
LAT (%) 8.1 § 2.6 [6.8, 9.4] 8.4 § 2.5 [7.1, 9.6]
Note. RPE D rates of perceived exertion; MPF D mean power frequency; CV D movement variability; ROM D range of motion; V D angular movement velocity; ROT conjunct movements in rotation; LAT D conjunct movements in lateral flexion.
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Cervical Kinematics and Muscle Fatigue
FIGURE 2. Individual data and correlation curves for initial range of motion (ROM) with the independent variable duration of the standardized isometric neck muscle endurance test (seconds) and the dependent variable ROM including corresponding two-sided 95% CI.
2005). In the present study, this relationship could not be transferred to cervical motor function itself. This finding may be explicable by the fact that the endpoint accuracy (i.e., motor goal) of a multijoint movement seems to be reachable despite fatigue-induced muscle performance deficits by using compensatory motion strategies (Emery & C^ ote, 2012). In particular, complex multimuscle movements may be performed unrestricted irrespective of local muscle fatigue using nonfatigued synergists or agonist muscles (Cote, Feldman, Mathieu, & Levin, 2008). By using this strategy, the motor goal itself 2015, Vol. 0, No. 0
may still be achievable as long as the adapted movement satisfies the tasks’ aim (Fuller, Fung, & C^ote, 2011; Fuller, Lomond, Fung, & C^ote, 2009). The potentially impaired joint position sense and delayed neuromuscular responses (Rozzi, Lephart, & Fu, 1999) following the local muscle fatigue may not impact kinematics of multijoint movements’ kinematics. A transfer of that strategy into cervical movement behavior characteristics is supposable. Nevertheless, our findings indicate that nonintended conjunct movements (ROT, LAT) not necessarily belong to this strategy nor are they influenced by 5
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local muscle fatigue. Thus, not only the motor goal is still achievable but as well the motion sequence itself remains unaffected by fatigue. In addition to the conjunct movements, CV remained unaffected by neck muscle fatigue. Position sense acuity and neck muscles coactivation are suggested to be involved in conjunct movements as well as higher movement variability (Sj€ olander et al., 2008) and do not seem to be affected by muscle fatigue in the cervical region in asymptomatic subjects. Several studies describe a decrease in cervical muscle endurance capacity (Lee et al., 2005; Peolsson & Kjellman, 2007) and impaired kinematic patterns (Chiu & Lo Sing, 2002; Strimpakos, 2011) in CNPP compared with healthy controls. In combination with our findings of a linear association between muscle endurance and ROM, a positive relationship between muscle and joint status is suggested. This finding corresponds well with Santos et al. (2010) and Carpes, Reinehr, and Mota (2008), who demonstrated that joint ROM and muscular capacity seem to be associated. An explanation for this association could be that sufficient endurance-trained muscles may support optimal cervical joints positioning followed by an increase in ROM. Recent study has shown a negative linear association of cervical kinematic characteristics and age (Niederer, Vogt, Rickert, Wilke, & Banzer, 2015) but not between age and cervical muscle endurance capacity (Domenech et al., 2011). The present study’s results, derived from the partial correlations and correlation coefficients comparisons do not support the association of age and kinematics. The associations of ROM and muscular endurance capacity are therefore relevant. Previous research demonstrates inconsistent data on the possible association of muscle fatigue and kinematics (Abt et al., 2011; Cortes et al., 2013; Hollman et al., 2012; Tsai et al., 2003). Concerning the neck region, unilateral cervical muscle fatigue is even suggested to improve repositioning accuracy in asymptomatic subjects (Malmstr€om et al., 2010). This finding is in contrast to the one we found in the present study. In the study of Malmstr€ om et al., local muscle fatigue was, in contrast to the present study, induced unilateral and the main outcome was based on repositioning accuracy. Following all these inconsistencies, the assignability of these approaches for bilateral neck muscle fatigue and its interdependence with motion characteristics may be limited. From a more practical point of view, the present findings may provide implications for the assignment of impaired or pathologically altered motion characteristics and the selection as well as rating of asymptomatic subjects attending for high-load tasks. The relevance of kinematics on the performance of ADL is not finally delineated. Although the value of ADL is linearly accompanied with impairments in cervical kinematics (Takeuchi et al., 2007) the impact of particular kinematic measures on ADL is not systematically evaluated but may not be a limiting factor (Bible, Biswas, Miller, Whang, & Grauer, 2010; Cobian, Daehn, Anderson, 6
& Heiderscheit, 2013). During the performance of 16 simple ADLs, even though maximal or even nearly maximal ROM did not occur (Bible et al., 2010), 64–68% of individual ROM was reached during picking an object up from the floor and washing oneself (Cobian et al., 2013). A greater ROM of almost 100% was shown during the performance of certain higher intensity activities such as athletics (Cobian, Sterling, Anderson, & Heiderscheit, 2009). Therefore, the potential to accurately perform cervical movements (not only end ROM) despite fatigued neck muscles may is of importance in performing high-load tasks. In such tasks, performing adequate movement patterns under complicated terms like muscle fatigue may be of importance to prevent dysfunctional motion characteristics and thus musculoskeletal disorders (Takala, 2002). This suggested association is nevertheless under ambiguous discussion for the neck region. In a recently published study, the results suggest that neither isometric neck muscle strength nor (passive) cervical ROM has a predictive value for the later occurrences of neck pain in asymptomatic women (Salo, Ylinen, Kautiainen, H€akkinen, & H€akkinen, 2012). In contrary and with a hazard ratio of .44 (95% CI [0.19, 1.05]) an increased cervical ROM was protective against the later occurrence of neck pain (Hush, Michaleff, Maher, & Refshauge, 2009). Likewise, subjects with low isometric neck endurance capacity were shown to have an increased risk for neck pain development (Relative Risk D 1.22; 95% CI [1.00, 1.49]; Hamberg-van Reenen et al., 2006). Although not finally delineated, persons with higher abilities to handle muscle fatigue in terms of neuromuscular control may be selected using present studies’ approach to assess sensorimotor function under local muscle fatigue. Along with the potential relevance for asymptomatic subjects, the relevance for CNP rehabilitation can be discussed. Following that, the findings underline the importance of complementary measures to address both muscular performance and kinematic characteristics in outcome assessments and functional rehabilitation of the cervical spine. Notwithstanding our findings of a moderate correlation of muscle endurance capacity and motor output in healthy subjects, no systematic interrelationship among muscle fatigue, performance, and motion characteristics was shown. Although speculative, one therefore can suggest that muscular stiffness and endurance programs neglecting neuromuscular control may be insufficient to influence neck kinematics. Thus, improvements in kinematics may be reached providing immediate feedback on movement performance in addition to the muscular stiffness and endurance training. Another reason for the possible relevance to address and assess muscle performance and motor capacity simultaneously in the rehabilitation of idiopathic neck pain is the suggested association of both muscle strength and ROM with the level of pain in CNPP (Hagen, Harms-Ringdahl, Enger, Hedenstad, & Morten, 1997; Takala, 2002). This as well is of importance due to the impaired isometric cervical muscle endurance described in Journal of Motor Behavior
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Cervical Kinematics and Muscle Fatigue
CNPP (Armijo-Olivo et al., 2010; Lee et al., 2005; Peolsson & Kjellman, 2007). However, due to the suggested altered muscle fiber properties in CNPP, which may be induced by pain (Falla, Farina, Kanstrup Dahl, & Graven-Nielsen, 2008), our results’ assignability for CNPP may be limited. Thus, further research is warranted to elucidate potential interrelationships of motor function and muscular capacity with changes in pain perception in CNPP, likewise, to ensure an optimal treatment approach for CNPP. In addition, extending the measures to other planes (horizontal and transversal plane) as well as to multiplane movements or even 3D acceleration might have revealed further information on the topic and should be considered by future researchers, likewise. Although a potential influence of occupancy and the physical activity behavior on motion characteristics and cervical muscle endurance in unimpaired subjects is supposable, these relations have not been proven yet (Carroll et al., 2008; Domenech et al., 2011). Nevertheless, further research on this suggested relation is warranted and may influence or expand our findings. CONCLUSIONS While a linear association between strength testing duration and end ROM might be suggested, no systematic influence of local muscle fatigue on cervical movement patterns was observed. These findings may be of importance for outcome assessments in unimpaired subjects attending for high-load tasks and underline the importance of complementary measures to address both muscular performance and kinematic characteristics in outcome assessment of the cervical spine. FUNDING The present study was initiated and funded by the German Federal Institute of Sport Science and realized within MiSpEx—the National Research Network for Medicine in Spine Exercise. REFERENCES Abt, J. P., Sell, T. C., Chu, Y., Lovalekar, M., Burdett, R. G., & Lephart, S. M. (2011). Running kinematics and shock absorption do not change after brief exhaustive running. Journal of Strength and Conditioning Research, 25, 1479–1485. Allison, G. T., & Fukushima, S. (2003). Estimating three-dimensional spinal repositioning error: The impact of range, posture, and number of trials. Spine, 28, 2510–2516. Alricsson, M., Harms-Ringdahl, K., Sch€uldt, K., Ekholm, J., & Linder, J. (2001). Mobility, muscular strength and endurance in the cervical spine in Swedish Air Force pilots. Aviation, Space, and Environmental Medicine, 72, 336–342. Armijo-Olivo, S., Fuentes, J. P., da Costa, B. R., Major, P. W., Warren, S., Thie, N. M., & Magee, D. J. (2010). Reduced endurance of the cervical flexor muscles in patients with concurrent temporomandibular disorders and neck disability. Manual Therapy, 15, 586–592.
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assessing back and neck dysfunction—discriminative ability for patients versus healthy control subjects. Physiotherapy Research International, 4, 123–140. Madeleine, P. (2010). On functional motor adaptations: From the quantification of motor strategies to the prevention of musculoskeletal disorders in the neck-shoulder region. Acta Physiologica (Oxford), 199 (Suppl 679), 1–46. Malmstr€ om, E.-M., Karlberg, M., Holmstr€ om, E., Fransson, P.-A., Hansson, G.-A., & Magnusson, M. (2010). Influence of prolonged unilateral cervical muscle contraction on head repositioning—decreased overshoot after a 5-min static muscle contraction task. Manual Therapy, 15, 229–234. Martel, J., Dugas, C., Dubois, J.-D., & Descarreaux, M. (2011). A randomised controlled trial of preventive spinal manipulation with and without a home exercise program for patients with chronic neck pain. BMC Musculoskeletal Disorders, 12, 41. Niederer, D., Vogt, L., Rickert, M., Wilke, J., & Banzer, W. (2015). Age-related Cut-Offs for cervical movement behaviour to distinguish chronic idiopathic neck pain patients from unimpaired subjects. European Spine Journal, 24, 493–502. Olson, L. E., Millar, A. L., Dunker, J., Hicks, J., & Glanz, D. (2006). Reliability of a clinical test for deep cervical flexor endurance. Journal of Manipulative and Physiological Therapeutics, 29, 134–138. Peolsson, A., Almkvist, C., Dahlberg, C., Lindqvist, S., & Pettersson, S. (2007). Age- and Sex-Specific reference values of a test of neck muscle endurance. Journal of Manipulative and Physiological Therapeutics, 30, 171–177. Peolsson, A., & Kjellman, G. (2007). Neck muscle endurance in nonspecific patients with neck pain and in patients after anterior cervical decompression and fusion. Journal of Manipulative and Physiological Therapeutics, 30, 343–350. Rozzi, S. L., Lephart, S. M., & Fu, F. H. (1999). Effects of muscular fatigue on knee joint laxity and neuromuscular characteristics of male and female athletes. Journal of Athletic Training, 34, 106–114. Salo, P., Ylinen, J., Kautiainen, H., H€akkinen, K., & H€akkinen, A. (2012). Neck muscle strength and mobility of the cervical spine as predictors of neck pain: A prospective 6-year study. Spine, 37, 1036–1040. Santos, E., Rhea, M. R., Sim~ao, R., Dias, I., de Salles, B. F., Novaes, J., . . . Bunker, D. J. (2010). Influence of moderately intense strength training on flexibility in sedentary young women. Journal of Strength and Conditioning Research, 24, 3144–3149. Schieppati, M., Nardone, A., & Schmid, M. (2003). Neck muscle fatigue affects postural control in man. Neuroscience, 121, 277–285. Shin, S.-J., An, D.-H., Oh, J.-S., & Yoo, W.-G. (2012). Changes in pressure pain in the upper trapezius muscle, cervical range of motion, and the cervical flexion-relaxation ratio after overhead work. Industrial Health, 50, 509–515. Sj€ olander, P., Michaelson, P., Jaric, S., & Djupsj€ obacka, M. (2008). Sensorimotor disturbances in chronic neck pain—range of motion, peak velocity, smoothness of movement, and repositioning acuity. Manual Therapy, 13, 122–131. Strimpakos, N. (2011). The assessment of the cervical spine. Part 1: Range of motion and proprioception. Journal of Bodywork and Movement Therapies, 15, 114–124. Takala, E.-P. (2002). Static muscular load, an increasing hazard in modern information technology. Scandinavian Journal of Work, Environment, and Health, 28, 211–213. Takeuchi, K., Yokoyama, T., Ono, A., Numasawa, T., Wada, K., Kumagai, G., & Toh, S. (2007). Limitations of activities of daily living accompanying reduced neck mobility after cervical
Journal of Motor Behavior
Cervical Kinematics and Muscle Fatigue Vuillerme, N., Pinsault, N., & Vaillant, J. (2005). Postural control during quiet standing following cervical muscular fatigue: Effects of changes in sensory inputs. Neuroscience Letters, 378, 135–139. Youdas, J. W., Carey, J. R., & Garrett, T. R. (1991). Reliability of measurements of cervical spine range of motion—comparison of three methods. Physical Therapy, 71, 98–104, discussion 105–106. Received November 16, 2014 Revised May 24, 2015 Accepted June 1, 2015
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laminoplasty. Archives of Orthopaedic and Trauma Surgery, 127, 475–480. Tsai, N.-T., McClure, P. W., & Karduna, A. R. (2003). Effects of muscle fatigue on 3-dimensional scapular kinematics. Archives of Physical Medicine and Rehabilitation, 84, 1000–1005. Vogt, L., Portscher, M., Brettmann, K., Pfeifer, K., & Banzer, W. (2003). Cross-validation of marker configurations to measure pelvic kinematics in gait. Gait and Posture, 18, 178–184. Vogt, L., Segieth, C., Banzer, W., & Himmelreich, H. (2007). Movement behaviour in patients with chronic neck pain. Physiotherapy Research International, 12, 206–212.
2015, Vol. 0, No. 0
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Journal of Motor Behavior Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/vjmb20
Local Muscle Fatigue and 3D Kinematics of the Cervical Spine in Healthy Subjects a
a
b
a
Daniel Niederer , Lutz Vogt , Torsten Pippig , Rudolf Wall & Winfried Banzer a
a
Department of Sports Medicine, Goethe-University Frankfurt/Main, Germany
b
Department of Clinical Aviation Medicine, German Air Force Institute for Aviation Medicine, Fürstenfeldbruck, Germany Published online: 16 Jul 2015.
Click for updates To cite this article: Daniel Niederer, Lutz Vogt, Torsten Pippig, Rudolf Wall & Winfried Banzer (2015): Local Muscle Fatigue and 3D Kinematics of the Cervical Spine in Healthy Subjects, Journal of Motor Behavior, DOI: 10.1080/00222895.2015.1058241 To link to this article: http://dx.doi.org/10.1080/00222895.2015.1058241
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Journal of Motor Behavior, Vol. 0, No. 0, 2015 Copyright © Taylor and Francis Group, LLC
RESEARCH ARTICLE
Local Muscle Fatigue and 3D Kinematics of the Cervical Spine in Healthy Subjects Daniel Niederer1, Lutz Vogt1, Torsten Pippig2, Rudolf Wall1, Winfried Banzer1
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1 Department of Sports Medicine, Goethe-University Frankfurt/Main, Germany. 2Department of Clinical Aviation Medicine, €rstenfeldbruck, Germany. German Air Force Institute for Aviation Medicine, Fu
ABSTRACT. The authors aimed to further explore the effects of local muscle fatigue on cervical 3D kinematics and the interrelationship between these kinematic characteristics and local muscle endurance capacity in the unimpaired cervical spine. Twenty healthy subjects (38 § 10 years; 5 women) performed 2 £ 10 maximal cervical flexion–extension movements. Isometric muscle endurance tests (prone/supine lying) were applied between sets to induce local muscle fatigue quantified by Borg scale rates of perceived exertion (RPE) and slope in mean power frequency (MPF; surface electromyography; m. sternocleidomastoideus, m. splenius capitis). Cervical motion characteristics (maximal range of motion [ROM], coefficient of variation of the 10 repetitive movements, mean angular velocity, conjunct movements in transversal and frontal plane) were calculated from raw 3D ultrasonic movement data. Average isometric strength testing duration for flexion and extension correlated to the cervical ROM (r D .49/r D .48; p < .05). However, Student’s t test demonstrated no significant alterations in any kinematic parameter following local muscle fatigue (p > .05). Although subjects’ cervical muscle endurance capacity and motor output seems to be conjugated, no impact of local cervical muscle fatigue on motor function was shown. These findings underline the importance of complementary measures to address muscular performance and kinematic characteristics in outcome assessment and functional rehabilitation of the cervical spine.
activities of daily living (ADL; Takeuchi et al., 2007). Following the aim to reveal adequate measures for multimodal musculoskeletal interventions for CNPP, research considering patients’ movement alterations is warranted (Chiu et al., 2011; Hakkinen, Kautiainen, Hannonen, & Ylinen, 2008; Martel, Dugas, Dubois, & Descarreaux, 2011). Preliminary evidence points toward an interrelationship between musculoskeletal endurance and neuromuscular function in CNPP. For instance, cervical muscle fatigue is related to poor postural control in healthy adults (Gosselin, Rassoulian, & Brown, 2004; Schieppati, Nardone, & Schmid, 2003; Vuillerme, Pinsault, & Vaillant, 2005). Data on the transferability of this suggested relationship on motor performance of the neck is lacking so far. In unimpaired subjects and concerning different parts of the musculoskeletal system than the neck, previous research demonstrates inconsistent data on the possible association of muscle fatigue and kinematics. While local muscle fatigue was shown to negatively affect kinematic outcomes of the rotator cuff during arm elevation (Tsai, McClure, & Karduna, 2003) and of the lower limbs during side-step maneuvers (Cortes, Greska, Kollock, Ambegaonkar, & Onate, 2013), other studies on fatigued hip extensors and flexors suggest no influence on kinematics during jump landing movements (Hollman, Hohl, Kraft, Strauss, & Traver, 2012) or running (Abt et al., 2011). Concerning the cervical spine, slowly assessed neck ROM was shown to decrease following overhead work (Shin, An, Oh, & Yoo, 2012). The authors suggest that shoulder muscle fatigue has led to this phenomenon. The limited ability of muscles to shorten in fatigued conditions (Cheng, Davidson, & Rice, 2010), altered afferent feedback from muscles (Bilodeau, Henderson, Nolta, Pursley, & Sandfort, 2001), or increases in spontaneous discharges of mechanically sensitive nonspindle muscle afferents (Hayward, Wesselmann, & Rymer, 1991) are discussed as potential underlying physiologic mechanisms for the affection of muscle fatigue on ROM. Due to this conceivable but not yet investigated relation, in the present study we aimed to further explore the interrelationship of local muscle endurance capacity and cervical 3D kinematics and to investigate potential
Keywords: local muscle fatigue, cervical kinematics, muscle endurance, range of motion, movement variability
I
n addition to musculoskeletal disorders (Alricsson, Harms-Ringdahl, Sch€ uldt, Ekholm, & Linder, 2001; Lee, Nicholson, & Adams, 2005; Peolsson, Almkvist, Dahlberg, Lindqvist, & Pettersson, 2007), current research demonstrates altered movement characteristics in chronic neck pain patients (CNPP) in comparison with unimpaired subjects. In particular, maximal cervical spine range of motion (ROM) is impaired in such patients (Chiu & Lo Sing, 2002; Strimpakos, 2011). Additionally, CNPP often show constricted movement consistencies (Sj€ olander, Michaelson, Jaric, & Djupsj€ obacka, 2008; Vogt, Segieth, Banzer, & Himmelreich, 2007). These constrictions occur by means of increased movement variability, angle reproducibility deficits, and larger nonintended conjunct movements while performing planar movements. Despite the pertinence of these alterations in movement characteristics, most rehabilitation programs primarily include measures to impact on muscular strength, stiffness, and endurance to improve muscle performance and functional stabilization in CNPP. Interventions targeting movement patterns are commonly neglected. Only low to moderate quality evidence supports the relevance of such exercise approaches for CNPP rehabilitation (Gross et al., 2008; Kay et al., 2012) also in terms of improvements in
Correspondence address: Daniel Niederer, Department of Sports Medicine, Goethe-University Frankfurt/Main, Ginnheimer Landstraße 39, Frankfurt am Main 60487, Germany. e-mail: [email protected] Color versions of one or more of the figures in the article can be found online at www.tandfonline.com/vjmb. 1
D. Niederer et al.
differences in means in cervical flexion–extension ROM and movement consistency prior to and following local muscle fatigue induction in the unimpaired cervical spine. We hypothesized that muscle fatigue would negatively affect kinematics and that muscle endurance capacity and kinematic characteristics are positively interrelated.
Methods Ethical Standards The study was approved by a local ethical review committee for medical research and conducted in accordance to the ethical standards set by the Declaration of Helsinki (1964) with its modifications (Fortaleza, 2013).
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Participants Twenty subjects (M age D 38 § 10 years; body mass index D 24.9 § 3.3 kg*m¡2; five women) were recruited in the German Air Force Institute for Aviation Medicine (F€ urstenfeldbruck, Germany). The subjects were physical active full-time employees and reported regular engagements in physical activity (e.g., running, cycling, swimming) at moderate to vigorous intensity. They were recruited through personal addressing. Each participant signed informed consent prior to study enrollment. Exclusion criteria included any previous surgery of the spine; known neck disorders or neck pain in the previous 12 months; persistent or passed cervical spine complaints based on space-occupying, inflammatory, traumatic, or systemic processes; the intake of painkilling drugs, analgesics, or muscle relaxants; radicular or pseudoradicular neurologic symptoms; inflammatory rheumatic diseases, osteoporosis, fracture, and/or surgery within the last six months; severe cardiovascular, pulmonary, neurological, cancerous, endocrinologic, and psychiatric diseases; fibromyalgia; hemophilia; pregnancy; and participation in other studies. Experimental Design Participants performed two sets (pre–post) of 10 repetitive maximal cervical flexion–extension movements (upright sitting position). Standardized isometric muscle endurance tests were applied between sets to induce local muscle fatigue, which was quantified by the slope in mean power frequency (MPF) of the EMG signal. Actual pain intensity were collected after cervical movements sets and following the isometric muscle endurance test and elicited by a single question and measured in millimeters (pain intensity) on a 100 mm visual analog scale (VAS; 0 D no pain, 100 D most severe pain). Following the assessments of pain intensity, Borg ratings of perceived exertion (RPE) in ratings of 6–20 on a Likert-type scale ranging from 6 (no exertion at all) to 20 (maximal exertion) was collected. 2
Cervical Spine Kinematics A noninvasive external three-dimensional ultrasonic movement analysis system (Zebris CMS 70, Isny, Germany; error of measurement 0 D flexion; < 0 D extension.
Ljungquist, Fransson, Harms-Ringdahl, Bj€ ornham, & Nygren, 1999; Olson, Millar, Dunker, Hicks, & Glanz, 2006; Peolsson et al., 2007; Peolsson & Kjellman, 2007). For that purpose, subjects positioned themselves in a standardized prone (extension) followed by supine (flexion) lying position with their arms close to the body and stretched legs. Participants’ head and neck were positioned in a comfortable neutral position. Neutral position was self-determined and investigator controlled. During these validated flexion– extension tests, the head had to be held static by submaximal isometric contraction in accordance to the direction of muscles’ eccentric function. For the extension test, an additional standardized weight (men D 4 kg, women D 2 kg) was hold by a belt and positioned on the sutura lambdoidea. Participants had to maintain the goniometer-controlled position until subjective exhaustion, until the position could not be maintained (evasion > 5 ) or until the occurrence of severe cervical pain. The second kinematic assessment followed less than 1 min after local muscle fatigue induction termination. Bipolar surface electromyography (EMG; BIOVISION, Wehrheim, Germany, differential instrumentation amplifier; input impedance 10 GV, CMMR 130 db, RTI noise 8 nVxHz, gain 2,500, filter 10 Hz low cutoff, 700 Hz high cutoff) was applied during flexion–extension endurance tests. For signal detection, Ag/AgCI electrodes (rectangular 4 £ 5 mm embedded in circular 10 mm diameter gel pad, blue sensor N-00-S [ Medicotest GmbH, Andernach, Germany] 2 cm interelectrode distance) were used. To assess muscle activity on m. sternocleidomastoideus (flexion) and 2015, Vol. 0, No. 0
m. splenius capitis (extension; Falla, Jull, & Hodges, 2004; Harrison et al., 2009) EMG was applied on one body side only (left or right). Body side was chosen randomized by a computer-generated randomization list. Electrodes were attached on the muscle belly (m. sternocleidomastoideus: 1 cm under the mandibula, m. splenius capitis: height of C4). Reference electrode was fixed on a muscle-free area on the skin cranial to the acromion. To quantify local myoelectric manifestations of muscle fatigue, the initial and ending 5 s of the EMG signal (at any one time for extension and flexion) were selected. For data analysis (Watscope software, Northern Digital Inc., Waterloo, Ontario, Canada), MPF was calculated for each time segment using a fast Fourier transformation. Slopes in MPF over time were used to estimate muscular endurance. Compared to the initial MPF, a slope of > 10% in average indicates local muscle fatigue (Harrison et al., 2009). Statistical Analysis Statistical procedures were executed using SPSS 19.0 (SPSS Inc., Chicago, IL) or BiAS for Windows (version 10 [2012], Goethe-University of Frankfurt, Frankfurt am Main, Germany) after the examination of underlying assumptions for parametric group and parametric correlation analyses testing. Dependent Student’s t tests were calculated for pre–post differences of means regarding CV, maximum oscillation angles (ROM, ROT, LAT), and V. To detect possible interrelationships, initial movement analysis outcomes were compared to muscle endurance testing 3
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duration using bivariate correlation analysis. Furthermore, partial correlations using age as covariate were calculated. A two-sided p-value of less than .05 was considered as statistically significant.
Although subjects’ cervical muscle endurance capacity and motor output seems to be conjugated, no impact of local cervical muscle fatigue on motor function, in detail on ROM, CV, ROT, and LAT was shown.
Results
Discussion
No participant had to be excluded, neither during screening nor after study enrollment. Descriptive results for both 3D kinematics and local muscle fatigue induction are shown in Table 1. Analysis of VAS revealed that only one (extension 12 mm) to two subjects (flexion 10–12 mm) displayed mild neck pain intensity following muscle fatigue induction (all other subjects’ VAS was 0 mm). Student’s t tests for comparisons of means revealed no significant alterations in kinematic parameters following local muscle fatigue (p > .05; coefficient of variation: .03 § .016 vs. .029 § .018; maximal ROM 128 § 23 vs. 125 § 19 ; mean angular movement velocity: 63 § 26 /s vs. 64 § 25 /s; conjunct movements in transversal: 16 § 7 vs. 14 § 4 and frontal plane: 11 § 4 vs. 11 § 3 ). Correlation analysis revealed significant correlations between both average isometric strength testing duration for flexion (162 § 88 s; RPE: 16 § 2; MPF: –16 § 8%; r D .48) and extension (542 § 367 s; RPE: 15 § 2; MPF: ¡13 § 10%; r D .49) to cervical ROM (p < .01; Figure 2) but not between testing duration and any other kinematic outcome (p > .05). Partial correlation analysis and correlation coefficients comparisons revealed no systematic influence of age on the correlation coefficient (r D .47, N D .038 for flexion; r D .55, N D .25 for extension; p > .05). Derived from the MPF-slope and according to the cutoffs (Harrison et al., 2009), each subject was fatigued on—at least—one of the tested sides: flexion (slope > 10%: n D 17; slope 0–10%: n D 3; no slope: n D 0) or extension (slope > 10%: n D 12; slope 0–10%: n D 8; no slope: n D 0).
The present study on cervical spine 3D kinematics and local muscle fatigue revealed a moderate association of isometric muscle endurance testing duration and maximal ROM in healthy adults’ cervical spine as hypothesized. Nevertheless and in contrary to the hypothesis, no systematic influence of local muscle fatigue on cervical movement patterns was observed. Present studies’ findings of a mean MPF slope of 13% (extension) and 15% (flexion) correspond to previously published findings reporting slopes of approximately 15% for flexion and 11.2% for extension in asymptomatic subjects (Harrison et al., 2009). Overall, the increase in RPE and the decrease in EMG frequency found in the present study are symptomatic for muscle fatigue (Madeleine, 2010). The duration of the local muscle endurance testing (extension M D 542 s; flexion M D 162 s) are somewhat higher than reference values in healthy adults (Domenech, Sizer, Dedrick, McGalliard, & Brismee, 2011; Edmondston et al., 2011). This disagreement may partially be explicable by the comparably lower age and higher proportion of males in our sample. Nevertheless, our subjects’ mean slope > 10% and its comparability to recent findings indicate sufficient objective local muscle fatigue values to discuss the present results as valid. According to the cutoff value, a minority of subjects were not fatigued following the extension task (slope of < 10%). Nevertheless, no subject showed an increase in MPF after isometric muscle endurance testing. Thus, subjects are discussed as fatigued. A negative impact of cervical muscle fatigue on postural control in healthy adults was shown in previous research (Gosselin et al., 2004; Schieppati et al., 2003; Vuillerme et al.,
TABLE 1. Characteristics for Cervical 3D Kinematics and Local Muscle Fatigue Induction Tests
Duration (s)
Local Muscular Fatigue Induction (M § SD and 95% CI) RPE (pts.)
Extension 542 § 367 [370, 714]
Flexion 162 § 88 [120, 203]
Pre (M § SD) [95% CI] Post (M § SD) [95% CI]
CV (%) 3.0 § 1.6 [2.3, 3.8] 2.9 § 1.8 [2.1, 3.8]
Extension Flexion 15 § 2 16 § 2 [13, 16] [15, 17] Cervical Spine 3D Kinematics ROM ( ) V ( *s¡1) 128 § 23 62 § 26 [117, 139] [50, 75] 125 § 19 64 § 25 [116, 134] [52, 75]
MPF-Slope (%) Extension 13 § 10 [9, 16]
Flexion 16 § 8 [13, 19]
ROT (%) 12.5 § 6 [9.5, 15.6] 11.1 § 3.4 [9.3, 12.8]
LAT (%) 8.1 § 2.6 [6.8, 9.4] 8.4 § 2.5 [7.1, 9.6]
Note. RPE D rates of perceived exertion; MPF D mean power frequency; CV D movement variability; ROM D range of motion; V D angular movement velocity; ROT conjunct movements in rotation; LAT D conjunct movements in lateral flexion.
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Journal of Motor Behavior
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Cervical Kinematics and Muscle Fatigue
FIGURE 2. Individual data and correlation curves for initial range of motion (ROM) with the independent variable duration of the standardized isometric neck muscle endurance test (seconds) and the dependent variable ROM including corresponding two-sided 95% CI.
2005). In the present study, this relationship could not be transferred to cervical motor function itself. This finding may be explicable by the fact that the endpoint accuracy (i.e., motor goal) of a multijoint movement seems to be reachable despite fatigue-induced muscle performance deficits by using compensatory motion strategies (Emery & C^ ote, 2012). In particular, complex multimuscle movements may be performed unrestricted irrespective of local muscle fatigue using nonfatigued synergists or agonist muscles (Cote, Feldman, Mathieu, & Levin, 2008). By using this strategy, the motor goal itself 2015, Vol. 0, No. 0
may still be achievable as long as the adapted movement satisfies the tasks’ aim (Fuller, Fung, & C^ote, 2011; Fuller, Lomond, Fung, & C^ote, 2009). The potentially impaired joint position sense and delayed neuromuscular responses (Rozzi, Lephart, & Fu, 1999) following the local muscle fatigue may not impact kinematics of multijoint movements’ kinematics. A transfer of that strategy into cervical movement behavior characteristics is supposable. Nevertheless, our findings indicate that nonintended conjunct movements (ROT, LAT) not necessarily belong to this strategy nor are they influenced by 5
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local muscle fatigue. Thus, not only the motor goal is still achievable but as well the motion sequence itself remains unaffected by fatigue. In addition to the conjunct movements, CV remained unaffected by neck muscle fatigue. Position sense acuity and neck muscles coactivation are suggested to be involved in conjunct movements as well as higher movement variability (Sj€ olander et al., 2008) and do not seem to be affected by muscle fatigue in the cervical region in asymptomatic subjects. Several studies describe a decrease in cervical muscle endurance capacity (Lee et al., 2005; Peolsson & Kjellman, 2007) and impaired kinematic patterns (Chiu & Lo Sing, 2002; Strimpakos, 2011) in CNPP compared with healthy controls. In combination with our findings of a linear association between muscle endurance and ROM, a positive relationship between muscle and joint status is suggested. This finding corresponds well with Santos et al. (2010) and Carpes, Reinehr, and Mota (2008), who demonstrated that joint ROM and muscular capacity seem to be associated. An explanation for this association could be that sufficient endurance-trained muscles may support optimal cervical joints positioning followed by an increase in ROM. Recent study has shown a negative linear association of cervical kinematic characteristics and age (Niederer, Vogt, Rickert, Wilke, & Banzer, 2015) but not between age and cervical muscle endurance capacity (Domenech et al., 2011). The present study’s results, derived from the partial correlations and correlation coefficients comparisons do not support the association of age and kinematics. The associations of ROM and muscular endurance capacity are therefore relevant. Previous research demonstrates inconsistent data on the possible association of muscle fatigue and kinematics (Abt et al., 2011; Cortes et al., 2013; Hollman et al., 2012; Tsai et al., 2003). Concerning the neck region, unilateral cervical muscle fatigue is even suggested to improve repositioning accuracy in asymptomatic subjects (Malmstr€om et al., 2010). This finding is in contrast to the one we found in the present study. In the study of Malmstr€ om et al., local muscle fatigue was, in contrast to the present study, induced unilateral and the main outcome was based on repositioning accuracy. Following all these inconsistencies, the assignability of these approaches for bilateral neck muscle fatigue and its interdependence with motion characteristics may be limited. From a more practical point of view, the present findings may provide implications for the assignment of impaired or pathologically altered motion characteristics and the selection as well as rating of asymptomatic subjects attending for high-load tasks. The relevance of kinematics on the performance of ADL is not finally delineated. Although the value of ADL is linearly accompanied with impairments in cervical kinematics (Takeuchi et al., 2007) the impact of particular kinematic measures on ADL is not systematically evaluated but may not be a limiting factor (Bible, Biswas, Miller, Whang, & Grauer, 2010; Cobian, Daehn, Anderson, 6
& Heiderscheit, 2013). During the performance of 16 simple ADLs, even though maximal or even nearly maximal ROM did not occur (Bible et al., 2010), 64–68% of individual ROM was reached during picking an object up from the floor and washing oneself (Cobian et al., 2013). A greater ROM of almost 100% was shown during the performance of certain higher intensity activities such as athletics (Cobian, Sterling, Anderson, & Heiderscheit, 2009). Therefore, the potential to accurately perform cervical movements (not only end ROM) despite fatigued neck muscles may is of importance in performing high-load tasks. In such tasks, performing adequate movement patterns under complicated terms like muscle fatigue may be of importance to prevent dysfunctional motion characteristics and thus musculoskeletal disorders (Takala, 2002). This suggested association is nevertheless under ambiguous discussion for the neck region. In a recently published study, the results suggest that neither isometric neck muscle strength nor (passive) cervical ROM has a predictive value for the later occurrences of neck pain in asymptomatic women (Salo, Ylinen, Kautiainen, H€akkinen, & H€akkinen, 2012). In contrary and with a hazard ratio of .44 (95% CI [0.19, 1.05]) an increased cervical ROM was protective against the later occurrence of neck pain (Hush, Michaleff, Maher, & Refshauge, 2009). Likewise, subjects with low isometric neck endurance capacity were shown to have an increased risk for neck pain development (Relative Risk D 1.22; 95% CI [1.00, 1.49]; Hamberg-van Reenen et al., 2006). Although not finally delineated, persons with higher abilities to handle muscle fatigue in terms of neuromuscular control may be selected using present studies’ approach to assess sensorimotor function under local muscle fatigue. Along with the potential relevance for asymptomatic subjects, the relevance for CNP rehabilitation can be discussed. Following that, the findings underline the importance of complementary measures to address both muscular performance and kinematic characteristics in outcome assessments and functional rehabilitation of the cervical spine. Notwithstanding our findings of a moderate correlation of muscle endurance capacity and motor output in healthy subjects, no systematic interrelationship among muscle fatigue, performance, and motion characteristics was shown. Although speculative, one therefore can suggest that muscular stiffness and endurance programs neglecting neuromuscular control may be insufficient to influence neck kinematics. Thus, improvements in kinematics may be reached providing immediate feedback on movement performance in addition to the muscular stiffness and endurance training. Another reason for the possible relevance to address and assess muscle performance and motor capacity simultaneously in the rehabilitation of idiopathic neck pain is the suggested association of both muscle strength and ROM with the level of pain in CNPP (Hagen, Harms-Ringdahl, Enger, Hedenstad, & Morten, 1997; Takala, 2002). This as well is of importance due to the impaired isometric cervical muscle endurance described in Journal of Motor Behavior
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Cervical Kinematics and Muscle Fatigue
CNPP (Armijo-Olivo et al., 2010; Lee et al., 2005; Peolsson & Kjellman, 2007). However, due to the suggested altered muscle fiber properties in CNPP, which may be induced by pain (Falla, Farina, Kanstrup Dahl, & Graven-Nielsen, 2008), our results’ assignability for CNPP may be limited. Thus, further research is warranted to elucidate potential interrelationships of motor function and muscular capacity with changes in pain perception in CNPP, likewise, to ensure an optimal treatment approach for CNPP. In addition, extending the measures to other planes (horizontal and transversal plane) as well as to multiplane movements or even 3D acceleration might have revealed further information on the topic and should be considered by future researchers, likewise. Although a potential influence of occupancy and the physical activity behavior on motion characteristics and cervical muscle endurance in unimpaired subjects is supposable, these relations have not been proven yet (Carroll et al., 2008; Domenech et al., 2011). Nevertheless, further research on this suggested relation is warranted and may influence or expand our findings. CONCLUSIONS While a linear association between strength testing duration and end ROM might be suggested, no systematic influence of local muscle fatigue on cervical movement patterns was observed. These findings may be of importance for outcome assessments in unimpaired subjects attending for high-load tasks and underline the importance of complementary measures to address both muscular performance and kinematic characteristics in outcome assessment of the cervical spine. FUNDING The present study was initiated and funded by the German Federal Institute of Sport Science and realized within MiSpEx—the National Research Network for Medicine in Spine Exercise. REFERENCES Abt, J. P., Sell, T. C., Chu, Y., Lovalekar, M., Burdett, R. G., & Lephart, S. M. (2011). Running kinematics and shock absorption do not change after brief exhaustive running. Journal of Strength and Conditioning Research, 25, 1479–1485. Allison, G. T., & Fukushima, S. (2003). Estimating three-dimensional spinal repositioning error: The impact of range, posture, and number of trials. Spine, 28, 2510–2516. Alricsson, M., Harms-Ringdahl, K., Sch€uldt, K., Ekholm, J., & Linder, J. (2001). Mobility, muscular strength and endurance in the cervical spine in Swedish Air Force pilots. Aviation, Space, and Environmental Medicine, 72, 336–342. Armijo-Olivo, S., Fuentes, J. P., da Costa, B. R., Major, P. W., Warren, S., Thie, N. M., & Magee, D. J. (2010). Reduced endurance of the cervical flexor muscles in patients with concurrent temporomandibular disorders and neck disability. Manual Therapy, 15, 586–592.
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