SYNOPSIS
Sports-related concussions (SRC) occur due to biomechanical forces to the head or neck that can result in pathophysiological changes in the brain. The musculature of the cervical spine has been identified as one potential factor in reducing SRC risk as well as underlying sex differences in SRC rates. Recent research has demonstrated that linear and rotational head acceleration, as well as the magnitude of force, upon impact is influenced by cervical spine biomechanics. Increased neck strength and girth is associated with reduced linear and rotational head acceleration during impact. Past work has also shown that overall neck strength and girth are lower in athletes with SRC. Additionally, differences in cervical spine biomechanics are hypothesized as a critical factor underlying sex differences in SRC rates. Specifically, compared to males, females tend to have less neck strength and girth which is associated with increased linear and rotational head acceleration. Although our ability to detect SRC has greatly improved, our ability to prevent SRCs from occurring and decrease the severity of clinical outcomes post-injury is limited. However, we suggest, along with others, that cervical spine biomechanics is a modifiable factor in reducing SRC risk. We review the role of the cervical spine in reducing SRC risk, and how this differs dependent on sex. We discuss clinical considerations for the examination of the cervical spine and the potential clinical relevance for SRC prevention. Additionally, we provide suggestions for future research examining cervical spine properties as modifiable factors in reducing SRC risk.
Keywords: head injury, mild traumatic brain injury, neck
INTRODUCTION
According to the most recent consensus statement on concussion in sport, sports-related concussion (SRC) is a traumatic brain injury that results from biomechanical forces to the body including the head and neck47. These forces induce pathophysiological changes in the brain, leading to somatic, physical, cognitive, and emotional symptoms, as well as sleep disturbances47. Although pathophysiological changes are typically transient, with symptoms often resolving within 10–14 days in adults47, a percentage of individuals with SRC experience persistent symptoms resulting in prolonged activity and participation limitations45–47. Impacts to the head or body can result in linear and rotational head acceleration, which in some cases can lead to damage to brain tissue21, 25, 41, 63. The force (g’s) and duration of an impact (seconds) influences the magnitude of an impact25; however, the magnitude of force associated with SRC is extremely variable, with no consistent findings between impact magnitude and clinical outcomes26. Musculoskeletal function, particularly neck strength and activation of neck muscles, may serve as a key mediator of the relationship between impact magnitude and the resulting transfer of energy from the head to the brain7, 25, 33.
Epidemiological studies have demonstrated higher rates of SRC in female university athletes compared to their male counterparts when competing in comparable sports13, 15, 17, 49. Relative to males, females also experience more severe symptoms and longer recovery patterns post-SRC12, 48. Sex differences in cervical spine biomechanics are one hypothesis put forth regarding differences in SRC rates and clinical outcomes post-SRC in males and females12, 14, 66. This article focuses on the role that cervical spine biomechanics and function play in SRC risk, specifically with regard to neck strength, neck girth, neck strength imbalances, and cervical spine posture. We address how the aforementioned risk factors differ based on sex. Additionally, we provide considerations for clinical examination and clinical relevance to highlight the potential role that physical therapists, athletic trainers, and other sports medicine personnel can play in SRC risk reduction. Since there is limited evidence to support specific recommendations, the goal of this paper is to highlight the importance of assessing the cervical spine with respect to SRC risk, and potential ways of incorporating these measures into clinical practice and future research.
CERVICAL SPINE BIOMECHANICS AND FUNCTION IN SRC RISK
Neck Strength and Girth
Neck strength and girth have been described as potential modifiable risk factors in SRC prevention, with research demonstrating a relationship between lower neck strength and neck girth being associated with increased head acceleration during impact5, 8, 9, 20. Whereas most studies to date have assessed the relationship between neck strength and girth on linear rotation and acceleration, only one has prospectively assessed this relationship with SRC risk. Collins and colleagues11 found that neck strength values at baseline were lower in high school athletes who subsequently sustained a SRC relative to those who did not, and further that for every one-pound (approximately 0.45 kilogram) increase in neck strength, SRC risk decreased by 5 percent 11. The proposed mechanism by which neck strength decreases SRC risk relates to the ability of the neck to decelerate head movement, decreasing the transfer of energy to the brain during impact. A stronger neck can decrease head acceleration8, 27 and is associated with reduced head velocity, peak acceleration, and displacement during impact in human and simulation studies9, 20, 33, 71. Sternocleidomastoid (SCM) muscle strength may be of particular importance in reducing SRC risk, as SCM strength specifically has been shown to be predictive of linear and rotational head acceleration when heading a soccer ball8.
Furthermore, past work suggests that males have significantly greater neck strength than females in neck extension, flexion, and lateral flexion, even after accounting for differences in body mass10, 20, 29, 67, and that females have significantly smaller head-neck segment mass and neck girth compared to males5, 20. These sex differences in neck muscle strength and girth are thought to contribute to females experiencing increased head acceleration during impact9, 65. However, it should be noted that whereas Collins et al11 found that male athletes who sustained a concussion had lower overall baseline neck strength as compared to the uninjured athletes, this was not significant in female athletes.
Muscle strength imbalances in the cervical spine may also play an important role in head acceleration and SRC risk16, 29. Isometric tests demonstrate that cervical extension strength is generally greater than flexion strength50. It has been suggested however, that when extension and flexion strength production are similar, the head and neck may be more protected during impact16, 29. This suggestion is supported by research showing that, regardless of sex, a flexion-extension strength ratio close to one correlates with lower head acceleration during impact16.
Cervical Spine Posture
Cervical spine posture may affect the force generating capacity of neck muscles which could influence SRC risk29. A common structural alteration in head positioning is forward head posture (FHP), defined as the external auditory meatus being positioned anterior to the shoulder joint37. FHP alters the normal mechanics of the neck69 and is generally more common in females54. FHP also increases activation of the SCM and upper trapezius and subsequently inhibits the deep muscles responsible for segmental stability and neck proprioception2, 40, 43, 44. Further, FHP is associated with a decreased flexion-extension strength ratio3 which, as mentioned previously, has an impact on head acceleration forces16. Thus, FHP may result in increased head acceleration during impact due to the muscle imbalances noted in this posture.
POTENTIAL CLINICAL CONSIDERATIONS FOR SRC PREVENTION
Neck Strength, Girth, and Endurance
To-date, only one study has linked greater neck strength with decreased SRC risk, and no studies have shown what age- and sex-specific degree of neck strength is critical for risk reduction. However, based on the studies discussed above, it is suggested that head acceleration during impact is affected by head and neck size/girth as well as neck strength8, 16. Thus, increasing neck strength and potentially girth, and reducing neck strength imbalances, may in turn reduce SRC risk. Based on this research, we suggest that clinicians consider performing a thorough cervical spine strength assessment for athletes who are at risk for SRC (see TABLE). Where normative strength values exist, clinicians can use these values to identify reduced strength and potential areas of focus8, 10, 11, 51, 57, 68. Where normative values do not exist in the literature, clinicians should still consider collecting baseline strength and girth values to identify changes over time or in response to a specific strengthening protocol.
TABLE 1.
Factor of Interest |
Potential Examinations to Consider |
Measurements to Consider |
Clinical Relevance | Avenues for Future Research |
---|---|---|---|---|
Neck Strength and Girth |
Isometric neck strength measures in all three planes of motion to quantify flexion, extension, lateral flexion, rotation, and flexion in rotation (sternocleidomastoid). |
Isometric strength measurements with a: • Hand-held dynamometer5, 10, 19, 68, 70. • Fixed dynamometer16, 19, 51, 57. • Hand-held tension scale11. |
Lower neck strength is associated with increased head linear and rotational accelerations during impact5, 8, 9, 20 as well as increased SRC risk11. Additionally, every one- pound (approximately 0.45 kilogram) increase in neck strength, decreased concussion risk by 5 percent11. |
• Development of age- and sex- specific strength normative values. • Relationship between neck strength and SRC risk, including reducing linear and rotational head acceleration. • Relationship between neck strength and clinical outcomes post- SRC. |
Neck circumference measurement. |
Circumference measurement above10 or below11 the thyroid cartilage. |
Lower neck girth is associated with increased head linear and rotational accelerations during impact5, 8 as well as increased SRC risk11. |
• Relationship between girth and SRC risk, including reducing linear and rotational head acceleration. • Relationship between girth and isometric neck strength. |
|
Neck Endurance |
Neck muscle endurance measures. |
Cervical flexor24, 28, 34 and extensor35, 59 endurance tests. |
Since increased activation of the deep cervical flexors is thought to enhance stability and posture in the cervical spine22, 39 and possibly play a role in controlling head accelerations32, 61, 72, there is potential for increases in neck endurance in these muscles to be associated with decreased risk of SRC. |
• Relationship between deep muscle endurance and SRC risk. • Relationship between deep muscle endurance and clinical outcomes post- SRC. |
Strength Imbalances |
Asymmetry in neck strength measures across the three planes of motion. |
Calculation of a strength imbalance score within planes of motion16. |
A flexion-extension ratio that is close to one correlates with lower head accelerations during impact16 which may allow for more neck protection16, 29. |
• Relationship between neck muscle asymmetries and SRC risk. |
Posture | Observation for forward head posture (FHP). |
Craniovertebral angle measurement56. |
It is speculated that since FHP is associated with a decreased flexion- extension strength ratio3, more extreme postural impairments may be associated with SRC risk. Obtaining this specific measure may be important as smaller craniovertebral angles are associated with FHP impairments73. |
• Relationship between head-neck posture and linear and rotational head acceleration. • Relationship between head-neck posture and severity of clinical outcomes post- SRC. |
An examination of standard isometric cervical spine strength should be considered in all three planes of movement to quantify flexion/extension, lateral flexion, and rotation. Additionally, isolated SCM strength can be measured by isometrically resisting flexion with the neck rotated to the contralateral side30. To measure cervical spine strength, we recommend the use of a hand-held dynamometer (HHD) or other devices that allow for clear quantification of muscle strength and strength imbalances (see TABLE). If the HHD is the device of choice, we further recommend the HHD be strapped to the table to optimize stability and minimize inconsistencies in clinician force19 (FIGURE). With this strength assessment, we recommend clinicians also consider assessing the flexion-extension strength ratio, as a ratio close to one correlates with lower head acceleration during impact16. Additionally, clinicians should consider screening for pain during strength testing, as baseline reports of neck pain have been correlated with increased SRC risk in youth athletes58. The type and severity of pain may influence the examination values obtained. We suggest that clinicians consider addressing patients’ reports of neck pain or headaches and be cognizant of pain characteristics (e.g. acute versus chronic, radiating versus localized) when determining baseline strength values or prior to implementing a strengthening protocol.
There is evidence that isolated strengthening of the neck may serve to protect against SRC31 and reduce functional impairments in the cervical spine4. Further, isometric neck strengthening has been shown to reduce neck injury and SRC risk in sport31. Thus, we recommend clinicians consider implementing a pre-athletic participation strengthening program. This strengthening program should be targeted to increase neck strength in an effort to modify the risk factors associated with SRC. Given the busy nature of a pre-season schedule, clinicians should use their own judgment when determining the volume and intensity of the exercises.
With regard to neck girth, one can hypothesize that since increased neck girth is correlated with lower head linear and rotational accelerations during impact5, 8, interventions to increase neck girth would create a protective advantage for reducing SRC risk. Some research has sought to create reference values for neck girth10, 11, however, given the variety of anatomical structures that influence neck circumference (e.g. subcutaneous fat and individual muscle volumes), the best interventions for increasing neck girth are not clear at this time.
We similarly hypothesize that in addition to an isometric protocol for superficial cervical muscles, increasing the endurance capacity of the deep cervical flexors and extensors may be important for reducing SRC risk. Deep cervical flexor activation is thought to enhance stability and improve posture in the cervical spine22, 39 and when activated properly can help to decrease reliance on superficial muscles for controlled movement of the cervical spine23. Additionally, research has suggested that some of the deep muscles of the neck may play a role in decreasing head accelerations32, 61, 72. Although the majority of studies have assessed cervical flexor endurance, reliable measures for both cervical flexor endurance1, 24, 28, 34 and cervical extensor endurance35, 59 exist. Normative data have been developed for the cervical flexor endurance test18, 36 and can be utilized for reference values; we are not aware of normative values for neck extensor endurance. While we recommend that cervical spine assessment and strengthening protocols be performed for both sexes, we believe they are of particular importance for the female athlete, given the previously mentioned sex differences in neck muscle strength.
Cervical Spine Posture
A thorough postural assessment should be considered as part of an athlete’s examination. FHP can be observed clinically from the sagittal direction with the athlete in a standing or sitting position. Measuring the craniovertebral angle with a goniometer may further assist with quantifying FHP56. Smaller craniovertebral angles have been significantly associated with FHP impairments73. Intervening on postural impairments often implies correcting FHP and normalizing associated muscular imbalances. When the postural assessment is complemented by the strength assessment, an individualized intervention plan can be put into place to correct postural imbalances. This plan will vary based on the athlete’s individual presentation, however, there are some general practices for reducing FHP that are supported by the literature. Exercises combining cervical retraction and axial extension are commonly prescribed to restore the muscle balances in individuals with FHP42. We also recommend taking note of the muscles that are commonly affected by FHP, including the SCM55, upper trapezius6, levator scapulae6, and suboccipital muscles6.
QUESTIONS FOR FUTURE RESEARCH
Most studies to date have examined linear and rotational head acceleration in laboratory situations or have related neck strength to a past history of concussion. Given the relationship between neck strength and girth with reduced head acceleration and rotational forces, coupled with Collins and colleagues11 work demonstrating overall neck strength is lower in those who experience an SRC, the evidence is strong enough to warrant future prospective, highly-powered studies that further examine the role of neck strength as a preventative measure for SRC, as well as a potential intervention for SRC-related symptoms. That is, studies should include measurements of cervical spine characteristics in athletes before SRCs occur to determine whether those with increased neck strength and girth, less neck muscle asymmetry, greater endurance, and neutral alignment of the head and neck, experience fewer SRCs. Furthermore, cervical spine characteristics may impact clinical outcomes post-SRC by reducing the number of symptoms, symptom severity, and recovery timelines. Thus, it is important to collect data on these variables and understand their relationship to clinical outcomes.
Furthermore, although the magnitude of acceleration and rotation forces on impact may be a proxy for expected SRC risk, due to the range of magnitude of forces that result in concussive injuries25, the amount of force required to cause a SRC is not known. We also do not know if these forces have direct effects on clinical outcome measures post-injury (e.g., symptoms, symptom severity, and recovery timelines) or on the severity of potential brain tissue damage post-impact. Thus, prospective studies are needed that examine for relationships between cervical spine characteristics such as neck strength and endurance, neck girth, and posture as well as biomechanical factors thought to increase SRC risk such as head acceleration and rotation. Baseline biomechanical measures are likely to be of particular importance in contact and collision sports where SRC risk is greater and have the potential to provide additional information about SRC risk and clinical outcomes. Given what is known about differences in head acceleration and rotational forces between males and females, coupled with observations that female athletes incur more SRCs, experience a greater number of symptoms and severity, as well as prolonged recovery timelines, it is important that studies are adequately powered to examine sex differences.
In addition, it is imperative to develop sex-specific norms for neck strength that are associated with reduced risk of SRC. Normative data of isometric strength for cervical flexion, extension, side-bending and rotation have been published for males and females51, 57 with females having weaker necks compared to men, even when accounting for body weight, body mass index, height and neck length51, 57, 68. However, what is not known is whether there are specific strength values in male and female athletes that are associated with fewer SRCs, or maybe more importantly, fewer clinical symptoms, reduced symptom severity, and reduced recovery timelines. Additionally, the influence of innate anatomical variations of the cervical spine between males and females warrants further investigation62. Specifically, females tend to have increased ligamentous laxity52, 53, 60, smaller vertebral body width64 and less consistent vertebral coupling64 which have been suggested to decrease dynamic stability of the cervical spine62. These geometric differences between male and female necks68 along with factors such as the ratio of muscle strength around the cervical spine also needs further investigation with respect to their roles in SRC risk or prevention. If sex-specific strength targets and muscle strength balance goals can be identified, then pre-activity training programs can be designed to meet those targets.
Finally, future research examining the relationship between cervical spine characteristics and SRC risk should consider sport-specific factors and level of competition. That is, greater neck strength and girth, reduced muscle asymmetries, and neutral alignment of the head and neck may be of greater importance for athletes participating in high-impact sports associated with greater magnitude of impacts to the head and body. Athletes participating in sports with no, or limited, contact may not need to incorporate these protocols in pre-athletic participation assessments. Nonetheless, we believe it is still important to collect normative values and understand differences in cervical spine characteristics in athletes who compete in collision, contact, limited, and non-contact sports.
CONCLUSION
Significant advancements have been made in the diagnosis and management of SRC, yet we are still falling short in preventing and reducing the risk of these injuries occurring. As such, an important focus moving forward is to determine ways to prevent SRC and reduce the severity of their impact when they do occur. Neck strength, girth, and cervical spine posture have been identified as potential factors that reduce SRC risk by decreasing linear and rotational head acceleration and the magnitude of force upon impact. Further, it is speculated that biomechanical differences in the cervical spine between males and females may impact sex differences in SRC rates. Thus, we suggest that focusing on biomechanical properties of the cervical spine are important as they may represent a modifiable factor in reducing SRC risk. Clinically, it is important to comprehensively assess the cervical spine, including strength, girth, and postural assessments, prior to engagement in sport, and particularly in those where there is a high risk of impact, to determine who would benefit from pre-activity cervical spine interventions. Established normative values and baseline measurements would be helpful to in implementing intervention and preventative measures. Furthermore, future research is needed which focuses on: how cervical spine biomechanics influence SRC risk, sex differences in SRC rates, and whether reductions in head acceleration and rotation forces directly impact SRC outcomes.
ACKNOWLEDGMENTS
Financial support was provided to C.E. through Rutgers University School of Health Professions.
Footnotes
The authors disclose no conflicts of interest.
REFERENCES
- 1.Araujo FX, Ferreira GE, Scholl Schell M, Castro MP, Silva MF, Ribeiro DC. Measurement properties of the craniocervical flexion test: a systematic review protocol. BMJ open. 2018;8:e019486. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Blouin JS, Descarreaux M, Belanger-Gravel A, Simoneau M, Teasdale N. Attenuation of human neck muscle activity following repeated imposed trunk-forward linear acceleration. Exp Brain Res. 2003;150:458–464. [DOI] [PubMed] [Google Scholar]
- 3.Bokaee F, Rezasoltani A, Manshadi FD, Naimi SS, Baghban AA, Azimi H. Comparison of isometric force of the craniocervical flexor and extensor muscles between women with and without forward head posture. Cranio : the journal of craniomandibular practice. 2016;34:286–290. [DOI] [PubMed] [Google Scholar]
- 4.Borisut S, Vongsirinavarat M, Vachalathiti R, Sakulsriprasert P. Effects of strength and endurance training of superficial and deep neck muscles on muscle activities and pain levels of females with chronic neck pain. J Phys Ther Sci. 2013;25:1157–1162. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Bretzin AC, Mansell JL, Tierney RT, McDevitt JK. Sex Differences in Anthropometrics and Heading Kinematics Among Division I Soccer Athletes. Sports Health. 2017;9:168–173. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Brody LT, Hall CM.. Therapeutic Exercise: Moving Toward Function. 3 Philadelphia, PA: Lippincott Williams & Wilkins, a Wolters Kluwer business; 2011. [Google Scholar]
- 7.Broglio SP, Surma T, Ashton-Miller JA. High school and collegiate football athlete concussions: a biomechanical review. Annals of biomedical engineering. 2012;40:37–46. [DOI] [PubMed] [Google Scholar]
- 8.Caccese JB, Buckley TA, Tierney RT, et al. Head and neck size and neck strength predict linear and rotational acceleration during purposeful soccer heading. Sports biomechanics. 2017;1–15. [DOI] [PubMed] [Google Scholar]
- 9.Caccese JB, Buckley TA, Tierney RT, Rose WC, Glutting JJ, Kaminski TW. Sex and age differences in head acceleration during purposeful soccer heading. Res Sports Med. 2017;1–11. [DOI] [PubMed] [Google Scholar]
- 10.Catenaccio E, Mu W, Kaplan A, et al. Characterization of Neck Strength in Healthy Young Adults. PM & R : the journal of injury, function, and rehabilitation. 2017; [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Collins CL, Fletcher EN, Fields SK, et al. Neck strength: a protective factor reducing risk for concussion in high school sports. J Prim Prev. 2014;35:309–319. [DOI] [PubMed] [Google Scholar]
- 12.Covassin T, Elbin RJ, Crutcher B, Burkhart S. The management of sport-related concussion: considerations for male and female athletes. Translational stroke research. 2013;4:420–424. [DOI] [PubMed] [Google Scholar]
- 13.Covassin T, Moran R, Elbin RJ. Sex Differences in Reported Concussion Injury Rates and Time Loss From Participation: An Update of the National Collegiate Athletic Association Injury Surveillance Program From 2004–2005 Through 2008–2009. J Athl Train. 2016;51:189–194. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Covassin T, Savage J, Bretzin A, Lafevor M. Sex differences in sport-related concussion long-term outcomes. International journal of psychophysiology : official journal of the International Organization of Psychophysiology. 2017; [DOI] [PubMed] [Google Scholar]
- 15.Davis-Hayes C, Gossett JD, Levine WN, et al. Sex-specific Outcomes and Predictors of Concussion Recovery. The Journal of the American Academy of Orthopaedic Surgeons. 2017;25:818–828. [DOI] [PubMed] [Google Scholar]
- 16.Dezman ZD, Ledet EH, Kerr HA. Neck strength imbalance correlates with increased head acceleration in soccer heading. Sports Health. 2013;5:320–326. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Dick RW. Is there a gender difference in concussion incidence and outcomes? Br J Sports Med. 2009;43 Suppl 1:i46–50. [DOI] [PubMed] [Google Scholar]
- 18.Domenech MA, Sizer PS, Dedrick GS, McGalliard MK, Brismee JM. The deep neck flexor endurance test: normative data scores in healthy adults. PM & R : the journal of injury, function, and rehabilitation. 2011;3:105–110. [DOI] [PubMed] [Google Scholar]
- 19.Dvir Z, Prushansky T. Cervical muscles strength testing: methods and clinical implications. Journal of manipulative and physiological therapeutics. 2008;31:518–524. [DOI] [PubMed] [Google Scholar]
- 20.Eckner JT, Oh YK, Joshi MS, Richardson JK, Ashton-Miller JA. Effect of neck muscle strength and anticipatory cervical muscle activation on the kinematic response of the head to impulsive loads. Am J Sports Med. 2014;42:566–576. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Elkin BS, Elliott JM, Siegmund GP. Whiplash Injury or Concussion? A Possible Biomechanical Explanation for Concussion Symptoms in Some Individuals Following a Rear-End Collision. The Journal of orthopaedic and sports physical therapy. 2016;46:874–885. [DOI] [PubMed] [Google Scholar]
- 22.Falla D, Jull G, Russell T, Vicenzino B, Hodges P. Effect of neck exercise on sitting posture in patients with chronic neck pain. Physical therapy. 2007;87:408–417. [DOI] [PubMed] [Google Scholar]
- 23.Ghaderi F, Jafarabadi MA, Javanshir K. The clinical and EMG assessment of the effects of stabilization exercise on nonspecific chronic neck pain: A randomized controlled trial. Journal of back and musculoskeletal rehabilitation. 2017;30:211–219. [DOI] [PubMed] [Google Scholar]
- 24.Grimmer K Measuring the endurance capacity of the cervical short flexor muscle group. Aust J Physiother. 1994;40:251–254. [DOI] [PubMed] [Google Scholar]
- 25.Guskiewicz KM, Mihalik JP. Biomechanics of sport concussion: quest for the elusive injury threshold. Exercise and sport sciences reviews. 2011;39:4–11. [DOI] [PubMed] [Google Scholar]
- 26.Guskiewicz KM, Mihalik JP, Shankar V, et al. Measurement of head impacts in collegiate football players: relationship between head impact biomechanics and acute clinical outcome after concussion. Neurosurgery. 2007;61:1244–1252; discussion 1252–1243. [DOI] [PubMed] [Google Scholar]
- 27.Gutierrez GM, Conte C, Lightbourne K. The relationship between impact force, neck strength, and neurocognitive performance in soccer heading in adolescent females. Pediatr Exerc Sci. 2014;26:33–40. [DOI] [PubMed] [Google Scholar]
- 28.Harris KD, Heer DM, Roy TC, Santos DM, Whitman JM, Wainner RS. Reliability of a measurement of neck flexor muscle endurance. Physical therapy. 2005;85:1349–1355. [PubMed] [Google Scholar]
- 29.Hildenbrand KJ, Vasavada AN. Collegiate and high school athlete neck strength in neutral and rotated postures. Journal of strength and conditioning research. 2013;27:3173–3182. [DOI] [PubMed] [Google Scholar]
- 30.Hislop HJ, Montgomery J. Daniels and Worthinghams Muscle Testing: Techniques of Manual Examination 8th. St. Louis, Missouri: Saunders Elsevier; 2007. [Google Scholar]
- 31.Hrysomallis C Neck Muscular Strength, Training, Performance and Sport Injury Risk: A Review. Sports Med. 2016;46:1111–1124. [DOI] [PubMed] [Google Scholar]
- 32.Jarman NF, Brooks T, James CR, et al. Deep Neck Flexor Endurance in the Adolescent and Young Adult: Normative Data and Associated Attributes. PM & R : the journal of injury, function, and rehabilitation. 2017;9:969–975. [DOI] [PubMed] [Google Scholar]
- 33.Jin X, Feng Z, Mika VH, Li H, Viano D, Yang KH. The Role of Neck Muscle Activities on the Risk of Mild Traumatic Brain Injury in American Football. Journal of biomechanical engineering. 2017; [DOI] [PubMed] [Google Scholar]
- 34.Jull GA, O’Leary SP, Falla DL. Clinical assessment of the deep cervical flexor muscles: the craniocervical flexion test. Journal of manipulative and physiological therapeutics. 2008;31:525–533. [DOI] [PubMed] [Google Scholar]
- 35.Juul T, Langberg H, Enoch F, Sogaard K. The intra- and inter-rater reliability of five clinical muscle performance tests in patients with and without neck pain. BMC musculoskeletal disorders. 2013;14:339. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36.Kelly M, Cardy N, Melvin E, Reddin C, Ward C, Wilson F. The craniocervical flexion test: an investigation of performance in young asymptomatic subjects. Man Ther. 2013;18:83–86. [DOI] [PubMed] [Google Scholar]
- 37.Kendall P Muscles Testing and Function with Posture and Pain. Baltimore, MD: Lippincott Williams and Wilkins; 2005. [Google Scholar]
- 39.Kim JY, Kwag KI. Clinical effects of deep cervical flexor muscle activation in patients with chronic neck pain. J Phys Ther Sci. 2016;28:269–273. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 40.Kim MS. Neck kinematics and sternocleidomastoid muscle activation during neck rotation in subjects with forward head posture. J Phys Ther Sci. 2015;27:3425–3428. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 41.Krave U, Al-Olama M, Hansson HA. Rotational acceleration closed head flexion trauma generates more extensive diffuse brain injury than extension trauma. Journal of neurotrauma. 2011;28:57–70. [DOI] [PubMed] [Google Scholar]
- 42.Lee J, Kim D, Yu K, Cho Y, You JH. Comparison of isometric cervical flexor and isometric cervical extensor system exercises on patients with neuromuscular imbalance and cervical crossed syndrome associated forward head posture. Bio-medical materials and engineering. 2018;29:289–298. [DOI] [PubMed] [Google Scholar]
- 43.Lee KJ, Han HY, Cheon SH, Park SH, Yong MS. The effect of forward head posture on muscle activity during neck protraction and retraction. J Phys Ther Sci. 2015;27:977–979. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 44.Lee MY, Lee HY, Yong MS. Characteristics of cervical position sense in subjects with forward head posture. J Phys Ther Sci. 2014;26:1741–1743. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 45.McCrea M, Guskiewicz K, Randolph C, et al. Incidence, clinical course, and predictors of prolonged recovery time following sport-related concussion in high school and college athletes. J Int Neuropsychol Soc. 2013;19:22–33. [DOI] [PubMed] [Google Scholar]
- 46.McCrea M, Guskiewicz KM, Marshall SW, et al. Acute effects and recovery time following concussion in collegiate football players: the NCAA Concussion Study. Jama. 2003;290:2556–2563. [DOI] [PubMed] [Google Scholar]
- 47.McCrory P, Meeuwisse W, Dvorak J, et al. Consensus statement on concussion in sport-the 5th international conference on concussion in sport held in Berlin, October 2016 Br J Sports Med. 2017; [DOI] [PubMed] [Google Scholar]
- 48.Neidecker JM, Gealt DB, Luksch JR, Weaver MD. First-Time Sports-Related Concussion Recovery: The Role of Sex, Age, and Sport. The Journal of the American Osteopathic Association. 2017;117:635–642. [DOI] [PubMed] [Google Scholar]
- 49.O’Connor KL, Baker MM, Dalton SL, Dompier TP, Broglio SP, Kerr ZY. Epidemiology of Sport-Related Concussions in High School Athletes: National Athletic Treatment, Injury and Outcomes Network (NATION), 2011–2012 Through 2013–2014. J Athl Train. 2017;52:175–185. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 50.O’Leary S, Fagermoen CL, Hasegawa H, Thorsen AS, Van Wyk L. Differential Strength and Endurance Parameters of the Craniocervical and Cervicothoracic Extensors and Flexors in Healthy Individuals. Journal of applied biomechanics. 2017;33:166–170. [DOI] [PubMed] [Google Scholar]
- 51.Peolsson A, Oberg B, Hedlund R. Intra- and inter-tester reliability and reference values for isometric neck strength. Physiotherapy research international : the journal for researchers and clinicians in physical therapy. 2001;6:15–26. [DOI] [PubMed] [Google Scholar]
- 52.Pollard CD, Braun B, Hamill J. Influence of gender, estrogen and exercise on anterior knee laxity. Clin Biomech (Bristol, Avon). 2006;21:1060–1066. [DOI] [PubMed] [Google Scholar]
- 53.Quatman CE, Ford KR, Myer GD, Paterno MV, Hewett TE. The effects of gender and pubertal status on generalized joint laxity in young athletes. Journal of science and medicine in sport. 2008;11:257–263. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 54.Ruivo RM, Pezarat-Correia P, Carita AI. Cervical and shoulder postural assessment of adolescents between 15 and 17 years old and association with upper quadrant pain. Brazilian journal of physical therapy. 2014;18:364–371. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 55.Ruivo RM, Pezarat-Correia P, Carita AI. Effects of a Resistance and Stretching Training Program on Forward Head and Protracted Shoulder Posture in Adolescents. Journal of manipulative and physiological therapeutics. 2017;40:1–10. [DOI] [PubMed] [Google Scholar]
- 56.Salahzadeh Z, Maroufi N, Ahmadi A, et al. Assessment of forward head posture in females: observational and photogrammetry methods. Journal of back and musculoskeletal rehabilitation. 2014;27:131–139. [DOI] [PubMed] [Google Scholar]
- 57.Salo PK, Ylinen JJ, Malkia EA, Kautiainen H, Hakkinen AH. Isometric strength of the cervical flexor, extensor, and rotator muscles in 220 healthy females aged 20 to 59 years. The Journal of orthopaedic and sports physical therapy. 2006;36:495–502. [DOI] [PubMed] [Google Scholar]
- 58.Schneider KJ, Meeuwisse WH, Kang J, Schneider GM, Emery CA. Preseason reports of neck pain, dizziness, and headache as risk factors for concussion in male youth ice hockey players. Clinical journal of sport medicine : official journal of the Canadian Academy of Sport Medicine. 2013;23:267–272. [DOI] [PubMed] [Google Scholar]
- 59.Sebastian D, Chovvath R, Malladi R. Cervical extensor endurance test: a reliability study. Journal of bodywork and movement therapies. 2015;19:213–216. [DOI] [PubMed] [Google Scholar]
- 60.Shultz SJ, Sander TC, Kirk SE, Perrin DH. Sex differences in knee joint laxity change across the female menstrual cycle. The Journal of sports medicine and physical fitness. 2005;45:594–603. [PMC free article] [PubMed] [Google Scholar]
- 61.Siegmund GP, Blouin JS, Brault JR, Hedenstierna S, Inglis JT. Electromyography of superficial and deep neck muscles during isometric, voluntary, and reflex contractions. Journal of biomechanical engineering. 2007;129:66–77. [DOI] [PubMed] [Google Scholar]
- 62.Stemper BD, Derosia JJ, Yogananan N, Pintar FA, Shender BS, Paskoff GR. Gender dependent cervical spine anatomical differences in size-matched volunteers - biomed 2009. Biomedical sciences instrumentation. 2009;45:149–154. [PubMed] [Google Scholar]
- 63.Stemper BD, Shah AS, Pintar FA, et al. Head rotational acceleration characteristics influence behavioral and diffusion tensor imaging outcomes following concussion. Annals of biomedical engineering. 2015;43:1071–1088. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 64.Stemper BD, Yoganandan N, Pintar FA, et al. Anatomical gender differences in cervical vertebrae of size-matched volunteers. Spine. 2008;33:E44–49. [DOI] [PubMed] [Google Scholar]
- 65.Tierney RT, Higgins M, Caswell SV, et al. Sex differences in head acceleration during heading while wearing soccer headgear. J Athl Train. 2008;43:578–584. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 66.Tierney RT, Sitler MR, Swanik CB, Swanik KA, Higgins M, Torg J. Gender differences in head-neck segment dynamic stabilization during head acceleration. Med Sci Sports Exerc. 2005;37:272–279. [DOI] [PubMed] [Google Scholar]
- 67.Valkeinen H, Ylinen J, Malkia E, Alen M, Hakkinen K. Maximal force, force/time and activation/coactivation characteristics of the neck muscles in extension and flexion in healthy men and women at different ages. European journal of applied physiology. 2002;88:247–254. [DOI] [PubMed] [Google Scholar]
- 68.Vasavada AN, Danaraj J, Siegmund GP. Head and neck anthropometry, vertebral geometry and neck strength in height-matched men and women. J Biomech. 2008;41:114–121. [DOI] [PubMed] [Google Scholar]
- 69.Vasavada AN, Li S, Delp SL. Influence of muscle morphometry and moment arms on the moment-generating capacity of human neck muscles. Spine. 1998;23:412–422. [DOI] [PubMed] [Google Scholar]
- 70.Versteegh T, Beaudet D, Greenbaum M, Hellyer L, Tritton A, Walton D. Evaluating the reliability of a novel neck-strength assessment protocol for healthy adults using self-generated resistance with a hand-held dynamometer. Physiother Can. 2015;67:58–64. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 71.Viano DC, Casson IR, Pellman EJ. Concussion in professional football: biomechanics of the struck player--part 14. Neurosurgery. 2007;61:313–327; discussion 327–318. [DOI] [PubMed] [Google Scholar]
- 72.Vibert N, MacDougall HG, de Waele C, et al. Variability in the control of head movements in seated humans: a link with whiplash injuries? The Journal of physiology. 2001;532:851–868. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 73.Yip CH, Chiu TT, Poon AT. The relationship between head posture and severity and disability of patients with neck pain. Man Ther. 2008;13:148–154. [DOI] [PubMed] [Google Scholar]