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Title: Neck muscle strength training in the risk management of concussion in contact sports: Evidence supporting practice. 

Authors: Ian Gilchrist, 1,2 Michael Storr,3 Elizabeth Chapman, 4 Lucie Pelland1,2

Affiliations: 1School of Rehabilitation Therapy, Queen�s University, Kingston; 2The Human Mobility Research Centre at Queen�s University and Kingston General Hospital, Kingston; 3Kingston General Hospital, Department of Pediatrics, Kingston; 4BTE Technologies Inc., Milton; Ontario, CANADA.

Corresponding Author: 	
Lucie Pelland, PT, Ph.D. Associate Professor, 
Queen�s University, School of Rehabilitation Therapy, Louise D. Acton Building, 
Kingston, Ontario, Canada. K7L 3N6. 
Telephone: +1-613-533-3237; E-mail: Lucie.Pelland@queensu.ca

Acknowledgement
This work was supported, in part, by financial support from the DND-DTAES Human System Integration/Human Factors Section. 

Abstract
Background: Within the context of contact sports, resistance training of the neck musculature is increasingly being promoted as a player-specific strategy to reduce the risk and severity of concussion. A critical review was conducted to identify and analyze the evidence supporting this recommendation, as well as to evaluate the relative effectiveness of different resistance training programs in producing absolute gains in neck strength and the specificity of identified strength training programs in modifying concussion biomechanics and risk. Methods: Structured search of five electronic databases (Ovid MEDLINE, CINAHL, PubMED, EMBASE, and AMED), combining MeSH and generic search terms relating neck strength to concussion biomechanics, risk and incidence. Level of research evidence (Oxford Centre of Evidence-based Medicine) and methodological quality (PEDro Scale, Newcastle- Ottawa Scale) were determined. Results: Absolute gains in peak static neck strength with resistance training do not predict post-impact kinematics of the head (level 1b, 3b, 4). Significant attenuating effects are produced by short-latency increases in neck force (level 1b, 3b, 4). Effects of resistance training on parameters of short-latency neck force generation were evaluated in only one study, with isotonic training improving the rate of muscle force development, resulting in a 14% to 48% attenuation of the post-impact kinematics of the head. Conclusion: Current evidence supports training of short-latency parameters of neck strength as a player-specific factor to modify concussion risk. Standardization of neck strength measurement, reporting of short-latency variables of strength, and measurement of post-impact kinematics need to be established to identify most effective parameters of strength training of the neck in contact sport. 

Keywords
Concussions, neck strength, resistance training, concussion biomechanics, concussion risk, dynamic head-neck stability

Abbreviations
HN: Head-neck; PEDro: Physiotherapy Evidence Database; RCT: randomized controlled trial; Non-RCT: non-randomized controlled trial; NOS: Newcastle Ottawa Scale; MDC95%: Minimum detectable change with 95% confidence; lbs.: pound; Kg: kilogram; N: Newton; MADYMO: Mathematical Dynamic Modeler; HIC: Head Injury Criterion; ACSM: American College of Sports Medicine; CI: confidence interval; SCM: sternocleidomastoid; UFT: upper fibers of trapezius; RFD: rate of force development; EMG: electromyography; RM: repetition maximum; NCAA: National Collegiate Athletics Association

Introduction
With increasing evidence of the acute effects of concussions on neurocognitive function, as well as the possibility for persistent impairment in brain function [1-3], the design and implementation of effective risk management strategies for concussions in sport has become a focus of effort by healthcare professionals, scientists and sport governing bodies [4-8]. Within the context of contact sports, strength training of the neck musculature is increasingly being promoted as a player-specific strategy to reduce the incidence and severity of concussion [9, 10]. This recommendation is based on a fundamental principle of mechanics that stronger necks improve the coupling of the head-neck (HN) segment to the torso, increasing its mass-moment of inertia and, therefore, its capacity to resist external forces [9, 11]. The capacity of the HN segment to resist external forces has been quantified as dynamic stiffness [12], with greater dynamic stiffness associated with lower peak magnitudes of post-impact linear and rotational acceleration of the head, which therefore lowers the risk of concussion [13].

While the scientific community has cautiously supported neck strength training as one component of a comprehensive risk management strategy for concussions in contact sport [1], resistance training programs for the neck musculature are widely popularized in the media (e.g.,  HYPERLINK "http://www.si.com/college-football/2012/09/28" www.si.com/college-football/2012/09/28;  HYPERLINK "http://www.keepingscore.blogs.time.com/2013/02/21" www.keepingscore.blogs.time.com/2013/02/21) with a large number of web-based programs being readily available to consumers (e.g. Concussion prevention for football: Strengthening the neck;  HYPERLINK "http://www.sports-upgrade.com/blog/2012/09/08/" www.sports-upgrade.com/blog/2012/09/08/). Healthcare professionals and trainers are also increasingly making use of web-based media as a platform to market and promote sport injury prevention programs to athletes, coaches and parents, including preventive neck strengthening programs for concussions (e.g.,  HYPERLINK "http://www.elitefts.com" www.elitefts.com;  HYPERLINK "http://www.momsteam.com" www.momsteam.com;  HYPERLINK "http://www.fightmedicine.com" www.fightmedicine.com) Some claim their evidence-based neck strength training program can �conclusively and unequivocally� increase neck muscle size, with �100% guarantee with respect to its ability to positively enhance an individual�s chances in preventing and/or reducing the severity of cervical spine and traumatic brain injury� ( HYPERLINK "http://www.coachaprotraining.com" www.coachaprotraining.com).

Considering that the generic phrase �neck muscle strengthening for concussion prevention� yielded 558,000 hits in Google and 17,300 in Google Scholar in March, week 4, 2014, there is a definite need to inform sport specialists, and the consumers of their strength training programs, on the current level of evidence supporting strengthening of the neck musculature as a risk-reduction strategy for concussion. To this end, a scoping review was conducted to, first, identify and analyze the evidence relating strength capacity of the neck to concussion biomechanics and risk; second, to evaluate the relative efficacy of different resistance training programs in producing absolute gains in neck strength; and third, to evaluate the specificity of identified resistance training programs for the neck musculature in modifying concussion biomechanics and risk. 

Methods 
Comprehensive searches were executed using the methods for a scoping review outlined by Arksey and O�Malley [14] and Anderson et al. [15]. Five online databases were used to identify relevant data for analysis - Ovid MEDLINE, CINAHL, PubMED, EMBASE, and AMED. The searches were conducted in March 2014 and a full description of search strategies is provided in Tables 1 and 2. In agreement with the scoping nature of the review, the search was not limited by study design; all experimental and quasi-experimental designs, and systematic reviews outlined by the Oxford Center for Evidence-based Medicine (www.cebm.net) were included.
The first search focused on the relationship between neck strength and concussion biomechanics and risk of concussion (Table 1). Of the 278 articles identified by the search, 245 were excluded after review of their abstract as they either did not specifically relate neck strength to head or neck injury, or they addressed neck strength training within the context of intervention studies for clinical populations. Of the thirty-three remaining articles, eleven titles were redundant, and eight general review articles were excluded as they did not present either original, or systematically reviewed data, and one study could not be retrieved, leaving thirteen unique articles for full review. Eight of these articles were excluded from the analysis after full review as they contributed to the general context for interpreting research evidence on concussion risk and biomechanics but did not provide specific data relating neck strength to concussion biomechanics. Seven additional articles were identified through a manual search of the reference list of retrieved articles and google scholar alerts of new articles on concussion up to June, week 4, 2014, resulting in twelve articles retained for review and critical appraisal. 
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The second search focused on resistance training programs for the neck musculature in non-clinical populations (Table 2). Of the 128 articles identified by the search, 122 were excluded as they evaluated strength training programs for the shoulder girdle in relation to the incidence and management of neck pain, evaluated effectiveness of resistance training programs for the neck in clinical populations, or focused on evaluating effects of different strength training modalities using repeated measures analysis within a single session. Of the six remaining studies, two were redundant and one could not be retrieved. Seven additional studies were identified through manual search strategy, resulting in ten resistance training studies being retained for review and critical appraisal.  
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Data analysis
Research articles were appraised using the guidelines of Law and MacDermid [16], with summaries of experimental design and methods, statistical comparison, measured outcomes, and findings provided. Methodological quality of the studies was evaluated using the Physiotherapy Evidence Database (PEDro) scale for randomized controlled trials (RCTs), and non-RCTs [17, 18], and the Newcastle-Ottawa scale (NOS) for case-series and cohort studies [19]. On the PEDro scale, studies with scores > 6/10 is considered to be of high quality, with a maximum score of 8/10 possible for non-RCTs [17, 18]. The NOS provides a continuous grade of methodological quality from 0 to 9 for cohort studies and case-series studies with no cut-off criteria to define high-quality methodology. The level of research evidence was determined using the Oxford Levels of Evidence Scale (www.cebm.net) and the methodological quality of the studies evaluated. 

As appropriate, effect size (Cohen�s d) was calculated to assess the clinical relevance of changes in strength and kinematics of the HN segment measured after completion of a resistance training program or between groups with differences in initial baseline static neck strength capacity. A Cohen�s d value d" 0.2 is considered a  small  effect size, 0.5 d" d d" 0.8 a  medium  effect size, and e" 0.8 a  large  effect size [20]. Minimum detectable change (MDC95%) values were also calculated to determine the magnitude of change necessary for a resistance training program to produce a statistically meaningful effect on neck strength [21].

Results
The association between static neck strength and concussion risk was evaluated in two prospective, level 1b, studies. Mihalik et al. [22] related pre-season measures of peak static strength of the anterior and anterolateral neck flexors, posterolateral neck extensors and cervical rotators muscle groups prior to the kinematics of the head for on-ice collisions recorded over 98 games and 99 practices in 37 minor hockey players. Higher peak static strength did not predict lower magnitudes of linear and rotational acceleration of the head (P e" 0.06) or lower head impact severity profile (P e" 0.22). More recently, Collins et al. [23] reported results of a large prospective pilot study of 6,662 high-school athletes in the United States with the aim of relating pre-season measures of peak static neck strength in flexion, extension and bilateral side flexion, the ratio of neck-to-head circumference, and the ratio of neck length-to-head circumference to the incidence of concussion. After adjusting for sex and sport, the linear regression analysis identified total neck strength as a predictor of concussion incidence (P = 0.004), with odds of concussion decreasing by 5% for every one pound increase in peak static neck strength. These results need to be evaluated within the context of the study. The regression analysis was based on the data of 179 athletes who sustained a concussion during the study period (2.7% of the study population), with no clear definition of concussion diagnosis provided, and a higher proportion of female to male athletes (P < 0.001). As well, the reported difference of 1.5 lbs. between concussed and uninjured athletes represents a small effect size of neck strength (Cohen's d = 0.29); with the large sample size of this study (N = 6458 uninjured and N = 179 concussed athletes respectively), the MDC95% would yield a significant change in peak neck strength of only 0.16 lbs. for uninjured athletes and 1.0 lbs. for concussed athletes, which may explain the high statistical significance from a relatively small mean difference in neck strength. 

While research on the prospective evaluation of the role of peak static neck strength on concussion incidence is limited, the functional association between neck strength and the dynamic stability the HN segment has been evaluated in controlled lab-based studies using between-subject [12, 24, 25] and within-subject [12, 26] experimental designs. This evidence is summarized in Table 3.
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Mansell et al. [12] and Tierney et al. [24] compared the kinematic response of the head to a controlled application of a 50N force along the sagittal plane of neck motion in females and males, with the a priori assumption of a lower static neck strength capacity in females. The 42% to 49% lower peak static strength in females was associated with a 29% lower dynamic HN stiffness compared to males, and 19% to 30% higher peak magnitudes of angular acceleration of the head post-impact. Eckner et al. [25] extended these results, adapting the methods of Mansell et al. [12] to scale the magnitude of the applied external force to participants� body mass and quantifying the relationship of peak strength to dynamic stiffness of the HN segment in all three planes of motion of the neck, flexion-extension, lateral bending and axial rotation. In their study group of 46 athletes, 8 to 30 years old, peak strength was 31% lower in adult females compared to males, with a 19% higher peak magnitude of change in angular velocity of the head post-impact in females. Similarly, peak strength was 32% lower in younger (high school age or younger) versus older males and 53% in younger versus older females. This strength difference was associated with 43% to 51% higher magnitude of change in peak angular velocity of the head post-impact in younger males and females, respectively, compared to adults. Eckner et al. [25] reported peak strength to vary linearly with dynamic HN stiffness (r = 0.42 to 0.61, P < 0.01), with peak static strength explaining 42% to 55% of the variance in the linear velocity of the head post-impact and 46% to 60% of the variance in angular velocity. This linear relationship was influenced by a significant independent effect of age (P < 0.001). 

Therefore, there is level 3b and 4 evidence of a positive effect of higher peak static neck strength on dynamic stiffness of the HN segment using between-subject comparisons. Reported between-group differences could be mediated, in part, by differences in the underlying neuromuscular control of dynamic HN stiffness (see Table 3) [12, 24]. 

Positive findings of a relationship between peak static neck strength and dynamic HN stability in between-subject studies are not supported by within-subject studies evaluating the effects of resistance training of the neck musculature on the dynamic stiffness of the HN segment [12, 26]. Both Mansell et al. [12] and Lisman et al. [26] used an isotonic strength-training program with individualized training stimulus of 55% to 70% of 10 repetitions maximum and 60% to 80% of 10 repetitions maximum, respectively. Resistance training produced direction-specific increases in peak strength: 15% increase in neck flexor strength (P < 0.001) [12], 7% in neck extensor strength (P < 0.05) [26] and 10% in left lateral flexion strength (P < 0.05) [26]. These gains in static peak strength did not correlate to higher dynamic HN stiffness. Lisman et al. [26] reported no attenuation of the acceleration profile of the head, during a standardized football tackle, with higher static neck strength (P e" 0.051), while Mansell et al. [12] reported an increase in peak magnitudes of the linear acceleration of the head along the sagittal plane of neck motion post-training (P = 0.03). Therefore, there is level 3b and 4 evidence that gains in peak static strength with resistance training do not correlate specifically with higher dynamic HN stiffness.

While there is no clear evidence of a protective effect of absolute peak static strength on concussion risk, there is level 1b [27], 3b [12], and 4 [24, 25, 28-30] evidence of a modifying influence of neck force developed prior to, or early after, application of an external force on dynamic stiffness of the HN segment, with resulting attenuation of the kinematic response of the head. This positive effect of short-latency neck force has been evaluated through comparison of the kinematic response of the head to an applied external force when the time of impact is �known� versus �unknown,� with the assumption that knowledge of impact allows for pre-tensing of the neck musculature. This evidence is summarized in Table 4.
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Insert Table 4
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The positive effects of anticipatory pre-tensing of neck muscles on dynamic HN stiffness in-situ game play are reported in one prospective cohort study measuring the influence of knowledge of upcoming on-ice collisions on peak magnitudes of linear and rotational acceleration of the head for 16 minor ice-hockey players over 54 games [27]. Anticipation of impact, measured from video review of on-ice collisions, did not modify post-impact kinematic response of the head for high head impact severity collisions (P > 0.05). However, a protective effect of anticipation was reported for impacts within the 50th to 75th percentile of head impact severity profile, resulting in 17% attenuation of peak rotational acceleration of the head for anticipated compared to unanticipated collisions (P = 0.006; Cohen�s d = 0.37) and an average 2% lowering of the head impact severity profile (P = 0.03; Cohen�s d = 0.27). Similar results were reported by Shewchenko et al. [30], quantifying the kinematic response of the head to four natural soccer heading maneuvers performed for low (6.2 m/s) and high speed (7.5 m/s) ball impacts. For low speed head impacts, anticipatory pre-tensing of the neck musculature yielded a 2% attenuation in peak linear acceleration of the head (Cohen�s d = 2.12) and 5% attenuation of peak rotational acceleration (Cohen�s d = 0.34), resulting in a 25% reduction of the head impact severity profile (Cohen�s d = 1.20). Short-latency neck force did not influence the kinematics of the head for high speed impacts, with a 5% increase in the head impact severity profile. Therefore, for low to medium head impact severity events, short-latency neck force contributes small to large protective effects on concussion risk (range of Cohen�s d, 0.34 to 2.12). This level 1b evidence is supported by level 3b and 4 evidence from controlled studies [12, 24, 25, 28, 29].

Anticipatory knowledge of impact correlated with attenuation of the post-impact head kinematics along all three planes of neck motion, flexion-extension, side flexion and axial rotation (r = 0.42 to 0.66, P < 0.001) [25]. Several general positive effects of short-latency neck force on post-impact HN mechanics were reported. With application of an impulse force to the head along the sagittal plane [12, 24, 25], short-latency neck force generally yielded a 13% to 21% increase in dynamic HN stiffness (P d" 0.05) [24], 7% to 24% attenuation of peak magnitudes of angular acceleration of the head (P d" 0.001) [12, 24], and 22% to 39% attenuation of peak angular displacement of the head (P d" 0.001) [12]. These modifying effects of short-latency force on post-impact HN mechanics are considered to be small to medium, with Cohen�s d values ranging between 0.03 to 0.70. Similarly, short-latency neck force yielded a 40% attenuation of peak angular acceleration of the head into extension with an applied inertial load transmitted to the head via whole body acceleration using a pneumatic sled [28, 29], with the attenuating effects of short-latency neck force scaled to the magnitude of the inertial load applied (R2 = 0.66; P < 0.05). Inclusion of short-latency neck force improved the fit of Eckner et al.�s regression model, explaining an additional 1.3% to 20.3% of the variance in the post-impact kinematics of the head than when peak static strength is considered as a unique factor.

These attenuating effects of short-latency neck force were validated by computational studies of the biomechanics of the HN segment with application of standardized external forces [11, 31]. This evidence is summarized in Table 5.
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Insert Table 5
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Both studies used simulation of a physical model of the HN segment, a 50th percentile Hybrid III dummy [11] and MADYMO (6.0.1), including 68 pairs of muscles of the neck [31], to predict effects of varying the level of pre-impact HN stiffness on post-impact kinematics of the head with application of a standardized external force. In the study by Viano et al. [11], the three-dimensional impact velocity and orientation parameters of the external force used were determined from video review of thirty-one collisions in 25 players of the National Football League who sustained a concussion resulting from helmet-to-helmet and helmet-to-ground impacts. Pre-impact stiffness of the HN segment was varied between 30 N/mm, representative of a 10 year-old child, and 240 N/mm, representative of a well-conditioned male elite athlete. Increasing pre-impact stiffness from 80 to 180 N/mm produced a 14% attenuation in peak linear acceleration of the head and an associated 35% lowering of the Head Injury Criterion (HIC), which is analogous to the head impact severity index. Model-based simulations predicted an exponential relationship between pre-impact HN stiffness and the HIC, such that for lower magnitudes of baseline neck strength, small increases in pre-impact neck stiffness will produce large decreases of the HIC. As an example, a 10 N/mm increase in neck stiffness for a 10 year-old child is predicted to yield a 23% lowering of the HIC.

In their study, Shewchenko et al. [31] manipulated pre-impact neck stiffness by assigning muscle activation values to neck flexors, extensors and sternocleidomastoid muscles. Pre-impact muscle activity levels were assigned to the neck flexor muscle group a priori, due to their primary role in flexing the head and neck towards the ball prior to impact. The relative activation of extensor muscle group and sternocleidomastoid muscles was then scaled in iterative fashion to achieve realistic post-impact kinematics of the HN segment previously recorded during performance of controlled ball-heading maneuvers [30]. Model-based simulations were then used to predict effects of increasing pre-impact muscle activity of the neck flexors to 125% and 150% of their predicted maximum on the post-impact kinematics of the HN and forces acting on the upper cervical spine. Increase of pre-impact activation of neck flexors to 125% of maximum yielded a 1% attenuation of peak linear acceleration of the head along the sagittal plane in combination with a 20% increase in peak angular acceleration of the head and 7% higher Head Impact Power, also an index analogous to the head impact severity profile. Further increase in activation of the flexors to 150% yielded 7% attenuation in peak linear acceleration, but with 48% increase in peak angular acceleration of the head and 6% in head impact power. The model also predicted 44% increase in anterior-posterior shear forces at C0-C1 and a 63% increase in axial compression when pre-impact activation of neck flexors was set at 125%, with these values rising to 79% and 119%, respectively, when pre-impact flexor activation level was increased to 150%. Therefore, the effects of short-latency neck force on dynamic HN stiffness are influenced by multiple factors, including individualized neuromuscular coordination developed through learning.

Resistant training programs for the neck musculature were critically appraised to evaluate their overall effectiveness on improving general strength and more specifically to evaluate their specificity in modifying short-latency static neck strength parameters. Relevant details of the twelve resistance training programs, including parameters of training - frequency, intensity and type [32] � are summarized in Table 6. Comparison of the efficacy of strength training programs, stratified by the method of training stimulus (isotonic, elastic, isometric/isokinetic), is represented by standardized effect size of changes in peak static strength with training, with their corresponding 95% confidence intervals (95% CI), in Figure 1, with the associated MDC95% for the programs reported in Table 7. The overall Cohen�s d and MDC95% values could not be calculated for the study by Leggett et al. [33], due to the absence of sufficient detailed information of measured strength outcomes provided, and the overall Cohen�s d for Taylor et al. [34], due to the small number of participants (N = 5) in the control and strength training groups.
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Insert Table 6, Figure 1, Table 7
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Both isotonic and isometric/isokinetic resistance training programs produced medium to large effect sizes of change between pre- and post-training measures of static neck strength, with an overall Cohen�s d value of 0.65 (95% CI, 0.37 to 0.93) for isotonic programs and 0.76 (95% CI, 0.31 to 1.21) for isometric/isokinetic programs. In contrast, elastic resistance training programs produced small effect sizes of change in peak static strength capacity of the neck, with an overall Cohen�s d value of 0.47 (95% CI 0.16 to 0.77). 

Of the twelve resistance training programs appraised, only three produced gains in static strength exceeding the MDC95%�threshold for clinical significance in at least 75% of the direction-specific measurements [34-36]. Two studies evaluated the effects of strength gains on dynamic HN stiffness [12, 26]. Effect size of strength gains with resistance training varied significantly between these two studies, with Cohen�s d values ranging between -0.56 to 0.54 for males and 1.16 to 1.83 for females in the study by Mansell et al. [12], including a 10% decrease in peak neck extensor strength post-training in males for which the authors did not provide an explanation. In contrast, Lisman et al.�s program yielded small strength training effects, ranging between 0.13 and 0.34. These small to large strength gains did not translate to increased dynamic stiffness of the HN segment. Only one study published data that allowed for the evaluation of neck strength training on short-latency neck force [12]. Strength training produced a 14% to 48% decrease in the ratio of peak angular acceleration of the head between �known� and �unknown� force applications, indicating a positive effect of the isotonic resistance training program used in this study on short-latency neck force [12].
Discussion
Attenuating the kinematic and kinetic response of the head to an externally applied force is fundamental to reducing the risk for concussion in contact sport [37]. Our critical appraisal of current research evidence supports a role for neck muscle strength training to enhance absorption of kinetic energy applied either as a direct impulsive force to the head or transferred to the head from impacts to the body. Level 1b, 3b and 4 evidence indicates short-latency neck force to be the effective variable of neck strength, which explains, to some extent, the absence of a direct association between peak static neck strength and concussion risk in-situ game play [22] and dynamic stability of the HN segment [12, 24-26]. 

Studies on the role of anticipatory knowledge of impact [12, 24, 25, 27-30] demonstrated short-latency neck force to exert small to large attenuating effects on post-impact head kinematics (range of Cohen�s d, 0.34 to 2.12) and lowering the severity of the head impact [27, 30]. Model-based simulations by Shewchenko et al. [31] predicted this protective effect to be mediated by the contribution of short-latency neck force to aligning the head, neck and torso with the line of force application, rather than resulting from pre-tension of the neck musculature in isolation. Therefore, the effectiveness of short-latency neck force in mitigating concussion risk would be dependent on two variables, the selective recruitment of those muscles of the neck that are optimally aligned to resist the applied load and the rate at which sufficient force can be developed in these muscles. 

Assessment of the muscle coordination underlying dynamic stability of the HN segment has been limited, to date, to the monitoring of activity of two superficial muscle groups of the neck, the sternocleidomastoid (SCM) and the upper fibers of trapezius (UFT). The temporal coordination of the activity of these muscles was addressed in one study, through the performance of various heading maneuvers by female soccer players [38]. A sequential pattern of activation of the SCM and UFT was reported, with the SCM activated 300 to 500 ms prior to ball contact, followed by a period of co-activation with UFT over a 150 ms window around the time of contact with the ball, and ending with selective activation of UFT for 300 to 500 ms after ball contact. Bauer et al. [38] hypothesized that this coordination of activation would serve to stabilize the HN segment, creating a rigid system to propel the ball, while maximizing absorption of the impact. These results are important as they indicate the possible need for motor learning programs to be implemented in combination with strength training. However, the contribution of muscle coordination to dynamic HN stiffness remains to be clarified by experimental studies. Currently, other studies that have included muscle activity profiles in their assessment of dynamic stiffness of the HN segment have reported large between-subject variation in activity profiles, including sex-specific effects (see Table 3 and 4) [12, 24, 25, 30]. Of these, the results of Shewchenko et al. [30] and Mansell et al. [12] are important as they indicate that dynamic stability of the HN segment may be sensitive to the relative balance of activation between the SCM and UFT. A systematic approach for the measurement of muscle activity patterns is needed to advance understanding of basic neuromuscular mechanisms underlying differential responses of the neck to applied external loads. 
The second neuromuscular parameter of interest is rate of force development (RFD), a velocity-dependent parameter of muscle strength that reflects the efferent neural drive to muscles [39, 40]. RFD is a relevant parameter to concussion biomechanics and risk that can be enhanced by resistance training, allowing higher levels of muscle force to be reached in the early-phase of muscle contraction [39-43]. The effective training stimulus is a muscle contraction performed with ballistic intent [44]. These contractions are characterized by high firing rates, high force production and brief contraction times [39, 41, 44], resulting in an increase in the absolute magnitude of force generated, specifically in the early phases of a muscle contraction [39, 45, 46] that is not modulated by sensory feedback [46]. Training programs that emphasize high-velocity muscle contractions, for example, explosive contractions for plyometric movements have been shown to facilitate neural drive to effector muscles and increase short-latency muscle strength output [47, 48]. The gains in RFD are associated to increases in the rate of rise and mean amplitude of the electromyography signals (EMG), reflecting plastic changes in the efferent neural drive with learning [39, 40]. However, actual mechanical shortening of the muscle is not necessary to elicit short-latency neuromuscular adaptations, rather, it is the intention to produce a high-velocity movement [45]. Therefore, isometric contractions performed with ballistic intent would be a safe and appropriate strategy to rapidly increase anticipatory early-phase neck muscle tension to increase dynamic HN stiffness. Ballistic intent contractions could be integrated into existing isometric resistance program with demonstrated effectiveness in producing clinically meaningful changes in peak muscle strength, as for example, the program by Portero et al. [36] appraised in our review. This eight-week isometric strength training program in lateral side flexion produced a 35% increase in peak static strength in seven adult males, 24 and 30 years, representing a large effect size of (Cohen�s d value, 2.10, 95% CI, 0.74 to 3.41). 

The effects of strength training programs on RFD, however, have yet to be systematically investigated within the context of concussion risk management. In our critical review, RFD was considered in only one study [25], where RFD was expressed as the maximum absolute instantaneous slope of the force-time curve and, therefore, not limited to short-latency period of importance for concussion biomechanics. In this study, RFD measures were reported to vary linearly with dynamic HN stiffness along the sagittal plane and axial rotation (r = 0.41 to 0.60; P < 0.05). A standard to report RFD measures for discrete time intervals from the time of force onset (e.g., 0 to 25 ms, 0 to 50 ms, 0 to 100 ms) should be adopted that would allow for meaningful evaluation of the effectiveness of strength training designed to enhance anticipatory short-latency dynamic HN stiffness. Almosnino et al. [49, 50] reported that short-latency variables of static neck muscle strength, including RFD, could be measured with sufficient degree of reliability, using standardized methods, to measure effects of programs in controlled and natural studies. 

A clinically relevant question that remains, is how much of an increase in short-latency static neck capacity would be required to produce a significant modifying influence on concussion biomechanics? In the absence of experimental data, estimates can only be based on predictions from computational studies [11, 31]. Shewchenko et al. [31] predict the need for large increases in RFD based on their simulations showing a 7% reduction in peak linear acceleration of the head when pre-impact muscle activity of the SCM is increased to 150% of its maximum activation. Previous training studies have examined the relationship between resistance training and short-latency strength and muscle activation. Following a 14-week, high-intensity training study of the lower extremities, Aagaard et al. [39] showed a 17% (P < 0.001) increase in peak isometric knee extensor strength, and a 26%, 22%, and 17% (all P < 0.05) increase in ballistic-intent, isometric RFD at time intervals of 0 to 30 ms, 0 to 50 ms, 0 to 100 ms, respectively. They also reported short-latency increases of 22 to 143% (P < 0.05 to P < 0.01) in mean average EMG response within 0 to 100 ms of force onset; an increase of 41 to 106% (P < 0.01 to P < 0.001) in the rate of EMG signal rise within 0 to 75 ms of EMG onset, but showed no significant change in absolute peak EMG amplitude. While achieving these changes in RFD of the neck muscles with specific training could be possible, the implications for reducing the incidence of concussion are not straightforward in the absence of a clear threshold for concussive injuries [51]. Prospective studies including RFD as a predictor variable for concussion incidence would be necessary to establish population norms of MDC95% required to produce a protective effect for concussion.

Limitations
The appraisal of evidence on the role of peak and short-latency neck strength in concussion risk management is currently restricted by a number of methodological limitations that need to be addressed and standards developed to advance this field of study. First and foremost, strength training programs need to adhere to the guidelines of the American College of Sports Medicine [32]. The ACSM publishes evidence-based guidelines in regards to strength training parameters � frequency, intensity, type and time � designed to optimize strength gains. Of the twelve resistance strength training programs appraised, only three applied the frequency and intensity parameters recommended by the ACSM, while utilizing different type of resistance, isotonic [34, 35] and isometric [36]. These programs had participants train three to four times per week at a loading intensity of 75% 1 repetition maximum (RM) or 80% maximal isometric strength. These studies increased the loading intensity when participants could complete one or more dynamic repetitions beyond the target number [34, 35], or when there was an increase in maximal isometric strength [36]. All three of these programs produced gains in static strength exceeding the MDC95%�threshold for clinical significance in at least 75% of the direction-specific measurements. Conversely, the training intensities used by Mansell et al. [12] and Lisman et al. [26] were conservative by ACSM guidelines, with training intensities of 41 to 53% 1 RM (equivalent to 55 to 70% 10 RM), and 45 to 60 % 1 RM (equivalent to 60 to 80% 10 RM), respectively. In addition, the training programs of Mansell et al. [12], and Lisman et al. [26], consisted of two training sessions per week and were four weeks shorter than the programs of Taylor et al. [34] and Conley et al. [35]. The loading intensities in the programs by Mansell et al. [12] and Lisman et al. [26] were, therefore, too low to effect maximal strength gains and may explain the absence of transfer to dynamic HN stiffness. As a standard, resistance training programs for the neck should report MDC95% values to permit assessment of the contribution of neck strength to concussion biomechanics and risk beyond the probability of measurement error. 

There is also a need to develop standard methods for the measurement of both peak and short-latency neck strength variables that would allow for systematic comparison of results across different studies. Measurement varied between studies, using hand-held dynamometry [12, 22, 24] and tensile scale [23], and custom or commercial fixed-frame dynamometry that incorporate digital strain gauge load cells [25, 26]. Neck strength was also measured in various positions, with participants seated and fully restrained below the neck [12, 24, 25], restrained at the pelvis [26], unrestrained in sitting [23], and unrestrained in prone and supine [22]. Differences in position will influence the contribution of other muscles to measured force variables of the neck. Also, neck strength was most commonly reported only along the sagittal plane and frontal plane, with Eckner et al. [25] including measures in axial rotation. However, the contribution of individual muscles to the stability of the cervical spine varies as a function of the change in their mechanical advantage about all three axes of rotation at each intervertebral joint [52]. Therefore, relating neck strength to dynamic HN stiffness is not straightforward and standards should be developed both for the multi-directional measurement of neck strength, and dynamic HN stiffness. As well, while computational studies and experimental studies manipulating knowledge of time of impact have demonstrated the importance of short-latency neck muscle strength to dampen the kinematic response of the head, strength outcomes are almost exclusively reported only as peak magnitudes (e.g. lbs., kg, N). This may be a factor of limitations of commercial data acquisition systems (e.g., hand-held dynamometers, strain gauge load cells). The validity of using these peak strength measures to investigate the role of neck strength in concussion risk management needs to be critically considered. It has been reported that it takes 400 to 600 ms to generate absolute peak force in skeletal muscles [53, 54]. For athletes participating in contact sports, they may be unable to generate maximal tension in their neck muscles prior to impact. 

Determining standards of neck strength from current research is further limited by the methodological quality of available research. Studies identified by our search evaluated neck strength and its relationship to dynamic stability of the HN segment and concussion incidence in small study groups from specific populations, for example, NCAA soccer players, former high-school football players, and male minor hockey players. Within these limited study designs, effects of neck strength have most commonly been evaluated between two groups, including females and males or adults and children, with a priori assumptions of between-group difference in strength used to explain statistical differences in dynamic HN stiffness and concussion risk. This approach has been useful to identify the higher risk for concussion in females and children when compared to adult males. However, making inferences on the contribution of neck strength to concussion risk based on such between-group comparisons should be guarded. Differences in response of the HN segment to externally applied loads may be related to multiple factors, including differences in neuromuscular coordination and learning [12, 24, 30, 38]. Within-subject designs, using resistance training to manipulate neck strength, should be adopted as a standard to investigate the effects of neck strength on concussion risk. 

Lastly, the modeling work by Shewchenko et al. [31] is critical to consider in the study of neck strength to concussion biomechanics. Their model-based simulations predicted that while higher activation of neck muscles was effective in attenuating the linear acceleration of the head, this was associated to a 70% increase in peak magnitude of shear force and 119% of axial compression force at C0-C1. Therefore, there is a need for continued research using computational models to identify potentially injurious consequences of neck strength training programs on structures of the cervical spine. 

Application of evidence to practice and conclusions
While the relationship between peak static strength capacity of the neck and concussion risk is commonly discussed in popular media, analysis of current evidence does not support popular claims of a protective effect of higher peak static neck strength capacity for concussion in contact sport. However, the limited experimental research currently available is encouraging, particularly in regards to the role of short-latency neck strength. Controlled studies are needed to clarify the neural response of the neck to multidirectional resistive strength training using short-latency variables of muscle activation and force, including RFD. Combining these with measures of dynamic stability, as used in previous studies [12, 24, 25], would further clarify the relationships of increased short-latency neck stiffness to impulse response of the head-neck system under conditions of external loading. 

Considering the predicted functional role of short-latency neck strength in positively modifying impact biomechanics of the head and neck segment [11, 31], standardized assessment of short-latency neck strength capacity should be integrated into assessment of return-to-play readiness. The adoption of a standardized neck strength assessment platform would be a significant step forward in the field concussion biomechanics, allowing for systematic assessment of neck strength characteristics, including RFD, for baseline screening, as well as identifying most effective parameters of strength training of the neck in contact sport. There is also a need for multi-center prospective studies to evaluate effectiveness of strength training programs emphasizing short-latency neck strength in modifying concussion risk in-situ gameplay, as well as to identify reliable cutoffs for MDC95%.

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H�kkinen K, Komi P, Al�n M (1985) Effect of explosive strength training on isometric force- and relaxation time, electromyographic and muscle fiber characteristics of leg extensor muscles. Acta Physiol Scand 125: 587-600. (http://www.ncbi.nlm.nih.gov/pubmed/4091002)
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