Table of Contents Author Guidelines Submit a Manuscript
Journal of Sports Medicine
Volume 2016, Article ID 1590161, 20 pages
http://dx.doi.org/10.1155/2016/1590161
Review Article

Cervical Spine Involvement in Mild Traumatic Brain Injury: A Review

1Department of Human Kinetics, Université du Québec à Trois-Rivières (UQTR), Trois-Rivières, QC, Canada G9A 5H7
2Research Group on Neuromusculoskeletal Dysfunctions (GRAN), UQTR, Trois-Rivières, QC, Canada G9A 5H7
3Cortex Médecine et Réadaptation Concussion Clinic, Quebec City, QC, Canada G1W 0C5
4Department of Rehabilitation, Faculty of Medicine, Laval University, Quebec City, QC, Canada G1V 0A6
5Research Center in Neuropsychology and Cognition (CERNEC), Montreal, QC, Canada H3C 3J7

Received 1 March 2016; Revised 30 May 2016; Accepted 19 June 2016

Academic Editor: S. John Sullivan

Copyright © 2016 Michael Morin et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Background. There is a lack of scientific evidence in the literature on the involvement of the cervical spine in mTBI; however, its involvement is clinically accepted. Objective. This paper reviews evidence for the involvement of the cervical spine in mTBI symptoms, the mechanisms of injury, and the efficacy of therapy for cervical spine with concussion-related symptoms. Methods. A keyword search was conducted on PubMed, ICL, SportDiscus, PEDro, CINAHL, and Cochrane Library databases for articles published since 1990. The reference lists of articles meeting the criteria (original data articles, literature reviews, and clinical guidelines) were also searched in the same databases. Results. 4,854 records were screened and 43 articles were retained. Those articles were used to describe different subjects such as mTBI’s signs and symptoms, mechanisms of injury, and treatments of the cervical spine. Conclusions. The hypothesis of cervical spine involvement in post-mTBI symptoms and in PCS (postconcussion syndrome) is supported by increasing evidence and is widely accepted clinically. For the management and treatment of mTBIs, few articles were available in the literature, and relevant studies showed interesting results about manual therapy and exercises as efficient tools for health care practitioners.

1. Introduction

Mild traumatic brain injury (mTBI) is commonly known as concussion [1]. In a recent study, Statistics Canada estimated mTBI annual incidence to be 600 per 100,000 people [1]. The pediatric TBI population is the patients’ subgroup who consulted the most often in the emergency room [1]. An estimated 1.6 to 3.8 million sport and recreation-related brain injuries occur in the United States annually, and up to 75% of them are classified as mild [2]. About 70 to 90 percent of all TBI cases are thought to be of mild severity, and the related symptoms usually resolve within 7 to 10 days [3, 4]. However, as many as 50% of concussions may go unreported [5]. In an epidemiologic study, Tator et al. (2007) reported that the highest incidence for TBI is in the age group under 18 years, with almost 45%. Additionally, approximately one-quarter of all patients with TBI are aged between 19 and 29 years [1]. The Centers for Disease Control and Prevention (CDC) describes mTBI as a silent epidemic [2].

Concussion in sports was defined in 2012 at the international consensus on concussion in sport held in Zurich as

a brain injury and is defined as a complex pathophysiological process affecting the brain, induced by biomechanical forces. Several common features that incorporate clinical, pathologic and biomechanical injury constructs may be utilized in defining the nature of a concussive head injury. This is caused by a direct blow to the head, face, neck or elsewhere on the body with an “impulsive” force transmitted to the head. [4]

The number of reported concussions has increased in recent years for multiple reasons. Recent studies identified an increased awareness of the potential complications following concussion and repeated head trauma in the population [6] and higher involvement of health professionals in sports and in concussions recognition and follow-up [7]. Even though it is believed that most concussions usually resolve in between 7 and 10 days [3, 4], the symptoms may persist longer for up to 33 percent of cases [8]. Symptoms persisting for a few weeks to more than six months are defined in the literature as postconcussion syndrome (PCS) [8].

PCS is a complex medical subject that few articles and studies in the scientific literature explore concretely [4]. Considering that mTBI is a multifaceted injury, many signs and symptoms complicate its diagnosis [3]. Multiple impairments linked to this condition such as cognitive, vestibular, cervical, physical, and psychological dysfunctions [3, 4]. Therefore, with a multitude of clinical theories in the literature, it is difficult to determine clinical guidelines for PCS [3]. Current consensus identifies that a multidisciplinary approach is essential to the progress of the patient suffering from PCS [4].

One of the major challenges in the medical management of concussion is that there is no “gold standard” for assessing and diagnosing the injury [9]. It has been shown by Schneider et al. (2014) that a combination of cervical and vestibular physiotherapy decreased time to medical clearance for the return to sport in a cohort of 31 patients (12–30 years old) with persistent symptoms of dizziness, neck pain, and/or headaches following a sport-related concussion [10]. However, little research has been published on this very specific topic.

2. Problem

The problem targeted by this review of literature is the lack of data regarding the association between mTBI and cervicogenic impairment. The majority of scientific publications focus on diagnosing mTBI, and there is little evidence on the possible involvement of the cervical region [4]. Cervical spine examination after a cranial trauma is essential, but the association between symptoms and mTBIs is poorly described in the literature. A literature review will improve the medical knowledge of all medical professionals and help the diagnosis and treatment of mTBI.

3. Goals

The aim of this review was to target scientific articles describing mTBI and those involving cervicogenic headache (CGH) cases in order to look at the connections and similarities between these two types of injuries. The specific goals of this paper are (1) to determine the common signs and symptoms of mTBI (including PCS) and cervical dysfunctions, (2) to describe the mechanism of cranial trauma injury and link it with the impact on the cervical spine, and (3) to give an update on the various types of effective treatments for these conditions.

4. Methods

The following electronic resources were searched from January 1, 1990, to May 19, 2015: PubMed, Index to Chiropractic Literature (ICL), SportDiscus, Physiotherapy Evidence Database (PEDro), Cumulative Index to Nursing and Allied Health Literature (CINAHL), and Cochrane Library databases. The following keywords were used in different combinations: concussion, neck, TBI, mTBI, cervical, physiotherapy, physical therapy, athletic training, treatment, chiropractic, manipulation, manual therapy, and guideline. For the complete list of combinations, see Table 1. Three data collections were carried out at different dates: February 16, 2014, May 15, 2014, and May 19, 2015. Reference lists of articles meeting the selection criteria were also collected. All abstracts in English and French dealing with concussion involving the neck were selected for a full reading of the article. A total of 4,854 abstracts were found on search engines. Following this search, the articles were selected according to three main streams:(1)mTBI’s and PCS symptoms related to the cervical spine.(2)Mechanism of injury.(3)Therapies of the cervical spine with symptoms related to mTBI.

Table 1: Preliminary search of literature (total results/abstracts (Abs) selection/articles (Art) for review).

Inclusion criteria, based on the precited keywords, were original data articles, literature reviews, and clinical recommendations, available in English and/or French, based on the objectives of this research. Exclusion criteria were foreign language papers other than English or French, case studies, magazine articles, and expert and editorial comments. The selection of articles is shown in Figure 1, and combinations are explained in Table 1.

Figure 1: Research method for this review.

5. Results

After a careful screening of 4,854 data entries, 82 abstracts met the inclusion criteria of our research and were reviewed. All these articles were read and analyzed. Thirty-eight articles were excluded because the main topic did not match the three topics of this study () or were case studies (), magazine articles (), and expert commentary (). Finally, 43 papers were included in this literature review. Each selected article is described in Table 2 (see Appendix). These articles were analyzed and assigned to the different categories of topics discussed: (1) the association between cervical spine sprain and mTBI signs and symptoms, (2) mechanism of injury, and (3) treatments. Results are represented in Figure 1 and Table 1.

Table 2: Included studies description.

6. Discussion

6.1. The Association between Cervical Spine Sprain and mTBI Signs and Symptoms

The 2012 Zurich consensus on concussion in sports led by McCrory et al. (2013) defined a list of 22 common symptoms of mTBI divided into 4 main categories, as described in Table 3 [4, 6, 1113]. The majority of mTBIs (80–90%) are resolved in 7 to 10 days [4, 14, 15]. However, in the remaining 10 to 20%, symptoms may persist for more than 10–14 days, and even for several months after trauma [4, 16]. This clinical picture is diagnosed as PCS and the etiology for PCS is not well defined in the literature [11, 14, 17].

Table 3: Most common symptoms of mTBI according to their categories [4, 6, 1113].

As mentioned previously, the most common symptom in subjects after mTBI is posttraumatic headache (PTH) [18, 19]. The incidence of PTH varies between 5 and 90% [16, 20]. Their prevalence in children with mTBI is from 73 to 93% [19]. The diagnosis of PTH can be difficult to address in subjects with a history of preexisting headaches. However, PTH syndrome diagnosis is considered when the intensity or frequency of headaches increases after trauma [19]. PTH is defined as a headache that occurs within 1 week after regaining consciousness or within 1 week following head trauma [17]. The majority of PTH resolve within 6 to 12 months, and it is caused by cervical muscle tension and posture impairment [17]. Because headache is one of the major causes of morbidity in mTBI subjects, health care professionals should manage this symptom with a high level of priority [17].

Biologically, concussions usually resolve 7 to 10 days after trauma in adults [4, 21]. PCS related symptoms are nonspecific. Professionals must consider other pathologies as alternative explanations to persistent symptoms [4, 17]. Meanwhile, a recent study suggests that even at 1 month or more after concussion, the cerebral blood flow is decreased in 36% of 11- to 15-year-old subjects who suffered mTBI compared to a nonconcussed control group [22]. Further studies are needed to clarify this phenomenon.

Rather than a structural problem, PCS would be related to a brain dysfunction problem [15]. This would explain the negative results on most of the medical imaging prescribed in emergencies [15]. In addition, a prospective Norwegian study of 348 participants identified through a questionnaire that headaches persisting for more than 3 months after trauma and diagnosed as PCS are often related to a musculoskeletal pathology. In other words, the head or brain injury does not cause the persistent symptoms [23]. These results show the importance of potential cervical impairment in patients with mTBI [4, 14, 16, 17].

6.2. Mechanism of Injury

Recent studies correlated mTBI with whiplash occurrence [12, 16, 24, 25]. Furthermore, Schneider et al. (2013) demonstrated in a prospective study with 3,832 male ice hockey players (11–14 years old) that the presence of headache and neck pain in a preseason evaluation increases the risk of concussions during the season [26]. Consequently, a neck examination should be part of the postconcussion follow-up in addition to the neurological screening examination [6].

Whiplash is defined as a mechanism of acceleration-deceleration transferred to the cervical spine [6, 20, 27, 28] (see Table 4). With its large range of motion, the upper cervical spine is the most mobile part of the spine. During a whiplash, cervical structures are stressed at their end ranges of motion which can lead to neck injuries [29]. The impact generates stresses and injuries in the bones and soft tissues of the cervical spine, causing clinical manifestations [24]. Among those, whiplash symptoms include neck pain, cervicogenic headaches, chest pain, memory and concentration disturbances, muscle tension, sleep disturbances, dizziness, fatigue, cervical range of motion restrictions, irritability, tinnitus, and visual disturbances [12, 17, 20, 24, 25]. A preliminary study has demonstrated that low velocity impacts between 4 and 12 km/h can provoke neck and head injuries causing dysfunctions and pain [12]. These symptoms are often similar to those listed for mTBI, which leads to confusion for the medical community [12, 14, 16, 25].

Table 4: Summary table of the Whiplash-Associated Disorder (WAD) classifications and concussion symptoms that can manifest themselves in any grade of WAD [6, 20, 27, 28].

The pathophysiology related to the patient’s symptoms originates from one or several structures of the cervical spine. After a trauma involving the cervical region, the involvement of muscles, ligaments, arteries, nerves, the esophagus, the temporomandibular joint, intervertebral discs, zygapophysial joints, vertebrae, and the atlantooccipital joint creates a complex challenge for clinicians [16, 17, 20].

One of the hypotheses raised in the literature for the origin of neck pain is the involvement of the cervical zygapophysial joints [30]. Zygapophysial joints have been shown to be the source of neck pain, headaches, visual disturbances, tinnitus, and dizziness in patients who have sustained whiplash [14, 24, 25]. In this following order, the C1-C2, C2-C3, C0-C1, and C3-C4 levels are the most often described in association with cervical symptoms following mTBI [16, 24, 26, 31]. More specifically, cervical zygapophysial joint pain is expressed by a hypersensitivity and hyperexcitability of the spinal cord reflexes, causing an increase of nociceptive processes in the central nervous system [32]. The cross-sectional study of Smith et al. (2013) recruited 58 adults (18–52 years old) with chronic whiplash disorder and provided a facet joint block to all participants [32]. They analyzed characteristics of responders and nonresponders to facet joint block and concluded that patients with chronic Whiplash-Associated Disorder (WAD) show similar sensory disturbances, motor dysfunction, and psychological distress [32]. Another study published by Treleaven et al. (1994) supports the implication of the cervical region by a precise physical examination in differential diagnosis of 12 patients suffering of persistent postconcussion headache [31].

Following a whiplash, the cervical spine is often the source of a patient’s pain [4, 10]. The neck received the transmitted force of the impact and the same acceleration-deceleration mechanism that produces mTBI [28]. During the whiplash, the cause of cervicogenic and brain induced symptoms could be caused by either the mTBI or the cervical spine involvement or both at the same time [10]. There are similarities between the symptoms of neck disorders and the symptoms of mTBI [19]. The most common posttraumatic symptom is headache [4]. Cervicogenic headache and posttraumatic headache are well-known conditions [4, 13, 19, 33]. In fact, those upper cervical impairments, if not diagnosed and treated, can lead to chronicity of postconcussion headaches [10].

Cervicogenic headaches are common after a whiplash injury [16, 34]. Different studies showed that 3 to 4.6% of patients will develop chronic daily headaches after whiplash and 2% will be permanently disabled [34]. Upper cervical spine pain can arise from various anatomical structures such as muscles, joints, ligaments, and nerves [34]. Tensions in cervical muscles (trigger points) are the most common diagnosed type of headache [16, 23]. Becker (2010) explained that headaches related to cervical spine disorders (CGH) remain one of the most controversial areas of headache medicine [34]. Dysfunctions of the craniocervical zygapophysial (C0 to C4) joints can also cause headaches [16, 30]. In patients with headaches following a whiplash injury, dysfunctions of the C2-C3 zygapophysial joint are highly prevalent, particularly if there is tenderness over the C2-C3 facet joint [34]. Cervicogenic headaches may be unilateral or bilateral with the dominance depending on one or more of the structures that are affected [16]. Pain location usually begins in the occipital region of the neck [34]. After a whiplash injury, zygapophysial joints are clinically identified as the single most common source of pain in at least 50% of neck pain. Furthermore, facet joints appear to be the most common source of pain in the neck, with or without headache [34]. King et al. (2007) showed in their retrospective study, which included 173 patients, that manual examination had a high degree of sensitivity during zygapophysial joint pain evaluation [35]. Tension in the cervical muscles has the potential effect of reducing neck movement and generating local pain [16, 18]. A bad posture or sleeping position as well as physical activity performed with a faulty motor strategy can lead to neck pain and pain irradiating to the head [19]. In 2013, the Cervicogenic Headache International Study Group (CHISG) developed the diagnostic criteria for CGH [33] (see the following).

Summary of the Cervicogenic Headache (CGH) Diagnostic Criteria [33]Unilaterality of pain, although it is recognized that bilateral cervicogenic headache may occur.Restriction in range of motion in the neck.Provocation of usual head pain by neck movement or sustained awkward neck positions.Provocation of usual head pain with external pressure over the upper cervical or occipital region on the symptomatic side.Ipsilateral neck, shoulder, or arm pain, usually of a vague nonradicular nature, occasionally radicular.

Posttraumatic headaches are a serious contributor to disability following cranial, cerebral, and cervical injury. Therefore, evaluating the cervical region after a head trauma is recommended [4]. This recommendation will highly contribute to limiting morbidity of mTBI and, furthermore, to help clinicians identify the International Headache Society (IHS) cervicogenic characteristics on mTBI patients. One of the improvements of SCAT3 and Child-SCAT3 compared to the SCAT2 is the introduction of the cervical assessment in posttrauma evaluation [4]. Knowing that the mechanism of mTBI is an external force transmitting energy to the head, it is possible that the neck, supporting the head, can also be injured during such an external force [11, 12, 16]. The Zurich consensus for concussion in sports (2012) recommended a multidisciplinary approach for patients who suffer PCS symptoms, such as headaches lasting longer than 6 weeks [4].

6.3. Treatments

The majority of articles in the literature currently focus on the diagnosis of mTBI, but few are dedicated to its management and treatments [7]. The 2012 Zurich consensus on concussion in sport suggested physical and cognitive rest until the end of the acute symptoms after trauma and a multidisciplinary approach involving experienced health care professionals when treating mTBI [4]. In their retrospective analysis, Moser et al. (2012) analyzed 49 high school and collegiate athletes (mean = 15.0 years old) and suggested that a period of cognitive and physical rest may be a useful mean of treating concussion-related symptoms [21]. This recovery time allows for a period of 7 to 10 days before the athlete returns to competition [2]. During this period, the symptoms should be evaluated daily and all activities that increase these symptoms should be stopped [4]. A Cochrane study mentioned that, based on present literature, no acutely initiated intervention has been clearly associated with a positive outcome for patients who sustain mTBI [36].

Return-to-play is allowed when athletes are symptom-free at rest, are able to do a full practice with contact without symptoms, no longer take any medications, and have returned to their baseline levels of cognitive functioning and postural stability [6].

The evaluation of the cervical region has been included as a new part of the SCAT3/Child-SCAT3, and a full clearance is essential before return-to-play [4]. According to some authors, post-mTBI subjects must have no pain in the neck, full mobility, and an adequate bilateral general strength to restart their sporting activities [12].

Treatments such as vertebral manual therapy, cervical tractions, manipulations, and exercises can relieve neck pain [16]. Brolinson (2014) has demonstrated that interventions of spinal manual therapy, physiotherapy, and neuromotor/sensorimotor training are more effective for mTBI recovery compared to a program of rest and exercises [7]. Another study demonstrated that the physical status of individuals with neck pain is improved with an exercise program combining manipulation, proprioceptive neuromuscular facilitation, acupressure on trigger points, and range of motion exercises, along with proprioceptive exercises compared to a neck pain control group of similar patients treated with information and advice [29]. Treatment of the cervical spine (sustained natural apophyseal glides) has been shown to be effective in 17 individuals with suspected cervicogenic dizziness compared to a control group (17 adults) [37]. Schneider et al. (2014) established that a significantly higher proportion of post-mTBI individuals (more than 3 weeks after trauma) were medically cleared to return to sport within 8 weeks of initiating treatment if they were treated in physiotherapy with cervical spine and vestibular rehabilitation compared to a control group [10]. Another study recruited 128 mTBI adults with either PCS or cervicogenic/vestibular symptoms [27], who completed the 22-symptom postconcussion symptoms scale questionnaire. Their results demonstrated that the questionnaire does not reliably discriminate between both types of patients. They concluded that clinicians should consider specific testing of exercise tolerance and perform a physical examination of the cervical spine and the vestibular/ocular systems to determine the etiology of postconcussion symptoms and to consider treating these accordingly [27]. Assessment and treatment of the cervical spine and vestibular system in the presence of persistent dizziness, neck pain, and/or headaches may facilitate functional and symptomatic improvements and shorten recovery in post-mTBI subjects [7, 10].

There is little evidence in clinical trials on the treatment of PTH. A study by Bonk et al. (2000) has shown that physiotherapy treatments decrease pain and increase cervical range of motion compared to a control group in a cervical collar for a period of 6 and 12 weeks after trauma [38]. The physiotherapy programs consisted of active and passive mobilizations, postural strengthening, the application of ice, and exercises that are efficient for PTH.

Regarding the cervical muscular system, several changes are observed following a trauma such as mTBI or whiplash. There is still nonempirical support that stronger neck muscles could reduce the risks of mTBI on the field [11, 39]. In fact, Mihalik et al. (2011) evaluated the effect of cervical strength on head impact in 37 hockey players (average 15 years old) and they concluded that the hypothesis of neck strength decreasing head acceleration was not supported [39]. Recent publications identify the importance of neck musculature in the prevention of concussions. Two hypotheses are presently under debate in the literature. The potentially modifiable risk factors for concussion are neck strength and impact anticipation [40]. Tierney et al. (2005) demonstrated that males have a better head-neck segment dynamic stabilization than females when angular acceleration is sustained by the head in a study including 20 males and 20 females [41]. Furthermore, a descriptive study demonstrated that greater neck strength and anticipatory cervical muscle activation (bracing for impact) can reduce the magnitude of the head’s kinematic response in a population of 46 contact sport athletes (male and female) aged between 8 and 30 years [40]. Another study on a group of 49 football players (high school/collegiate) has shown that the odds of sustaining higher magnitude head impacts are reduced with better cervical strength and lower angular displacement following impact [42]. However, their findings did not show that stronger and larger neck muscles in players decreased head impact severity [42]. Meanwhile, Collins et al. (2014) concluded, in their study, which included 6704 high school athletes, that neck strength can be a valuable screening tool to prevent concussion [43]. Further research is needed to clarify these hypotheses and the actual role of neck strength in reducing risk of concussion.

A study by Leddy et al. (2012) for mTBI subjects slow to recover shows that a lightweight level of exercise can be beneficial [44]. Kozlowski et al. (2013) recently published a cross-sectional study about the exercise impact on 34 patients with PCS and a control group of 22 patients [3]. Conclusions showed that patients with PCS had a symptom-limited response to exercise, and the treadmill test was a potentially useful tool to monitor the recovery from PCS [3].

Other physiotherapy treatments, such as vestibular rehabilitation, visual training, cardiovascular training, and the treatment of cervical dysfunctions, have shown some promising avenues, but further studies are needed [4, 10, 14, 17, 20].

7. Conclusion

In conclusion, mTBI is a complex injury and needs to be taken care of by different medical specialists working together toward the same goal, recovery [4]. The evidence of cervical spine involvement in mTBI is becoming apparent, but there is a lack of sound evidence in the literature [25]. Our findings have implications for further research. The hypothesis of cervical spine involvement in post-mTBI symptoms and in PCS is supported by increasing evidence and largely accepted. Health professionals should consider assessing the cervical spine of patients affected by mTBI. Some original data articles support this theory and show that persistent headache and postconcussion syndrome are often related to musculoskeletal pathology of the cervical spine. For the mTBI management and treatment, few articles in the literature are available, but well-defined studies showed interesting results about manual therapy (cervical and vestibular) and exercises as effective tools for health care practitioners. Further studies are needed to establish an adequate evaluation and determine guidelines for treatments. The evaluation and treatment of the cervical region are a major step to improve mTBI rehabilitation.

Appendix

See Figure 1 and Tables 1, 2, 3, and 4, and also see “Summary of the Cervicogenic Headache (CGH) Diagnostic Criteria [33]” in Section 6.2.

Abbreviations

mTBI:Mild traumatic brain injury
ICL:Index to Chiropractic Literature
PEDro:SportDiscus, Physiotherapy Evidence Database
CINAHL:Cumulative Index to Nursing and Allied Health Literature
CDC:Centers for Disease Control and Prevention
TBI:Traumatic brain injury
PCS:Postconcussion syndrome
MRI:Magnetic Resonance Imaging
WAD:Whiplash-Associated Disorder
IHS:International Headache Society
PTH:Posttraumatic headache
CGH:Cervicogenic headache
GCS:Glasgow Coma Score
SAC:Standardized Assessment of Concussion
BESS:Balance Error Scoring System.

Competing Interests

The authors declare that they have no competing interests.

References

  1. C. Tator, G. Bray, and D. Morin, “The CBANCH report—the burden of neurological diseases, disorders, and injuries in Canada,” The Canadian Journal of Neurological Sciences, vol. 34, no. 3, pp. 268–269, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. M. R. Borich, K. L. Cheung, P. Jones et al., “Concussion: current concepts in diagnosis and management,” Journal of Neurologic Physical Therapy, vol. 37, no. 3, pp. 133–139, 2013. View at Publisher · View at Google Scholar · View at Scopus
  3. K. F. Kozlowski, J. Graham, J. J. Leddy, L. Devinney-Boymel, and B. S. Willer, “Exercise intolerance in individuals with postconcussion syndrome,” Journal of Athletic Training, vol. 48, no. 5, pp. 627–635, 2013. View at Publisher · View at Google Scholar · View at Scopus
  4. P. McCrory, W. H. Meeuwisse, M. Aubry et al., “Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport held in Zurich, November 2012,” British Journal of Sports Medicine, vol. 47, pp. 250–258, 2013. View at Publisher · View at Google Scholar
  5. K. G. Harmon, J. A. Drezner, M. Gammons et al., “American Medical Society for Sports Medicine position statement: concussion in sport,” British Journal of Sports Medicine, vol. 47, no. 1, pp. 15–26, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. E. Hanson, A. Stracciolini, R. Mannix, and W. P. Meehan, “Management and prevention of sport-related concussion,” Clinical Pediatrics, vol. 53, no. 13, pp. 1221–1230, 2014. View at Publisher · View at Google Scholar · View at Scopus
  7. P. G. Brolinson, “Management of sport-related concussion: a review,” Clinical Journal of Sport Medicine, vol. 24, no. 1, pp. 89–90, 2014. View at Publisher · View at Google Scholar · View at Scopus
  8. M. Makdissi, R. C. Cantu, K. M. Johnston, P. McCrory, and W. H. Meeuwisse, “The difficult concussion patient: what is the best approach to investigation and management of persistent (>10days) postconcussive symptoms?” British Journal of Sports Medicine, vol. 47, no. 5, pp. 308–313, 2013. View at Publisher · View at Google Scholar · View at Scopus
  9. K. M. Guskiewicz, J. Register-Mihalik, P. McCrory et al., “Evidence-based approach to revising the SCAT2: introducing the SCAT3,” British Journal of Sports Medicine, vol. 47, no. 5, pp. 289–293, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. K. J. Schneider, W. H. Meeuwisse, A. Nettel-Aguirre et al., “Cervicovestibular rehabilitation in sport-related concussion: a randomised controlled trial,” British journal of sports medicine, vol. 48, no. 17, pp. 1294–1298, 2014. View at Publisher · View at Google Scholar · View at Scopus
  11. C. M. Marshall, “Sports-related concussion: a narrative review of the literature,” The Journal of the Canadian Chiropractic Association, vol. 56, no. 4, pp. 299–310, 2012. View at Google Scholar
  12. L. M. Hynes and J. P. Dickey, “Is there a relationship between whiplash-associated disorders and concussion in hockey? A preliminary study,” Brain Injury, vol. 20, no. 2, pp. 179–188, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. K. A. Scorza, M. F. Raleigh, and F. G. O'Connor, “Current concepts in concussion: evaluation and management,” American Family Physician, vol. 85, no. 2, pp. 123–132, 2012. View at Google Scholar · View at Scopus
  14. F. Kennedy, Guideline 2013—Post-Concussion Treatment Guidelines 2013, 2013.
  15. S. Signoretti, G. Lazzarino, B. Tavazzi, and R. Vagnozzi, “The pathophysiology of concussion,” PM&R, vol. 3, no. 10, supplement 2, pp. S359–S368, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. J. S. Hecht, “Occipital nerve blocks in postconcussive headaches: a retrospective review and report of ten patients,” Journal of Head Trauma Rehabilitation, vol. 19, no. 1, pp. 58–71, 2004. View at Publisher · View at Google Scholar · View at Scopus
  17. M. M. Weightman, R. Bolgla, K. L. McCulloch, and M. D. Peterson, “Physical therapy recommendations for service members with mild traumatic brain injury,” Journal of Head Trauma Rehabilitation, vol. 25, no. 3, pp. 206–218, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. J. C. Pelletier, “Sports related concussion and spinal injuries: the need for changing spearing rules at the National Capital Amateur Football Association (NCAFA),” The Journal of the Canadian Chiropractic Association, vol. 50, no. 3, pp. 195–208, 2006. View at Google Scholar
  19. S. Lucas, “Headache management in concussion and mild traumatic brain injury,” PM&R, vol. 3, no. 10, supplement 2, pp. S406–S412, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. T. K. Watanabe, K. R. Bell, W. C. Walker, and K. Schomer, “Systematic review of interventions for post-traumatic headache,” PM&R, vol. 4, no. 2, pp. 129–140, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. R. S. Moser, C. Glatts, and P. Schatz, “Efficacy of immediate and delayed cognitive and physical rest for treatment of sports-related concussion,” The Journal of Pediatrics, vol. 161, no. 5, pp. 922–926, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. T. A. Maugans, C. Farley, M. Altaye, J. Leach, and K. M. Cecil, “Pediatric sports-related concussion produces cerebral blood flow alterations,” Pediatrics, vol. 129, no. 1, pp. 28–37, 2012. View at Publisher · View at Google Scholar · View at Scopus
  23. L. J. Stovner, H. Schrader, D. Mickevičiene, D. Surkiene, and T. Sand, “Headache after concussion,” European Journal of Neurology, vol. 16, no. 1, pp. 112–120, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. C. Fernández De Las Peñas, L. Palomeque Del Cerro, and J. Fernández Carnero, “Manual treatment of post-whiplash injury,” Journal of Bodywork and Movement Therapies, vol. 9, no. 2, pp. 109–119, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. O. Leslie and N. Craton, “Concussion: purely a brain injury?” Clinical Journal of Sport Medicine, vol. 23, no. 5, pp. 331–332, 2013. View at Publisher · View at Google Scholar · View at Scopus
  26. K. J. Schneider, W. H. Meeuwisse, J. Kang, G. M. Schneider, and C. A. Emery, “Preseason reports of neck pain, dizziness, and headache as risk factors for concussion in male youth ice hockey players,” Clinical Journal of Sport Medicine, vol. 23, no. 4, pp. 267–272, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. J. J. Leddy, J. G. Baker, A. Merchant et al., “Brain or strain? Symptoms alone do not distinguish physiologic concussion from cervical/vestibular injury,” Clinical Journal of Sport Medicine, vol. 25, no. 3, pp. 237–242, 2015. View at Publisher · View at Google Scholar · View at Scopus
  28. W. O. Spitzer, M. L. Skovron, L. R. Salmi et al., “Scientific monograph of the Quebec Task Force on Whiplash-Associated Disorders: redefining ‘whiplash’ and its management,” Spine, vol. 20, no. 8, pp. 1S–73S, 1995. View at Google Scholar · View at Scopus
  29. E. Kristjansson and J. Treleaven, “Sensorimotor function and dizziness in neck pain: implications for assessment and management,” Journal of Orthopaedic and Sports Physical Therapy, vol. 39, no. 5, pp. 364–377, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. N. Bogduk, “On cervical zygapophysial joint pain after whiplash,” Spine, vol. 36, no. 25, supplement, pp. S194–S199, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. J. Treleaven, G. Jull, and L. Atkinson, “Cervical musculoskeletal dysfunction in post-concussional headache,” Cephalalgia, vol. 14, no. 4, pp. 273–279, 1994. View at Publisher · View at Google Scholar · View at Scopus
  32. A. D. Smith, G. Jull, G. Schneider, B. Frizzell, R. A. Hooper, and M. Sterling, “A comparison of physical and psychological features of responders and non-responders to cervical facet blocks in chronic whiplash,” BMC Musculoskeletal Disorders, vol. 14, article 313, 2013. View at Publisher · View at Google Scholar · View at Scopus
  33. Headache Classification Committee of the International Headache Society, “The International Classification of Headache Disorders, 3rd edition (beta version),” Cephalalgia, vol. 33, no. 9, pp. 629–808, 2013. View at Publisher · View at Google Scholar
  34. W. J. Becker, “Cervicogenic headache: evidence that the neck is a pain generator,” Headache, vol. 50, no. 4, pp. 699–705, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. W. King, P. Lau, R. Lees, and N. Bogduk, “The validity of manual examination in assessing patients with neck pain,” Spine Journal, vol. 7, no. 1, pp. 22–26, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. J. Gravel, A. D'Angelo, B. Carrière et al., “Interventions provided in the acute phase for mild traumatic brain injury: a systematic review,” Systematic Reviews, vol. 2, article 63, 2013. View at Publisher · View at Google Scholar · View at Scopus
  37. S. A. Reid, D. A. Rivett, M. G. Katekar, and R. Callister, “Sustained natural apophyseal glides (SNAGs) are an effective treatment for cervicogenic dizziness,” Manual Therapy, vol. 13, no. 4, pp. 357–366, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. A. D. Bonk, R. Ferrari, G. D. Giebel, M. Edelmann, and R. Huser, “Prospective, randomized, controlled study of activity versus collar, and the natural history for whiplash injury, in Germany,” Journal of Musculoskeletal Pain, vol. 8, no. 1-2, pp. 123–132, 2000. View at Google Scholar · View at Scopus
  39. J. P. Mihalik, K. M. Guskiewicz, S. W. Marshall, R. M. Greenwald, J. T. Blackburn, and R. C. Cantu, “Does cervical muscle strength in youth ice hockey players affect head impact biomechanics?” Clinical Journal of Sport Medicine, vol. 21, no. 5, pp. 416–421, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. J. T. Eckner, Y. K. Oh, M. S. Joshi, J. K. Richardson, and J. A. Ashton-Miller, “Effect of neck muscle strength and anticipatory cervical muscle activation on the kinematic response of the head to impulsive loads,” American Journal of Sports Medicine, vol. 42, no. 3, pp. 566–576, 2014. View at Publisher · View at Google Scholar · View at Scopus
  41. R. T. Tierney, M. R. Sitler, C. B. Swanik, K. A. Swanik, M. Higgins, and J. Torg, “Gender differences in head-neck segment dynamic stabilization during head accelaration,” Medicine and Science in Sports and Exercise, vol. 37, no. 2, pp. 272–279, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. J. D. Schmidt, K. M. Guskiewicz, J. T. Blackburn, J. P. Mihalik, G. P. Siegmund, and S. W. Marshall, “The influence of cervical muscle characteristics on head impact biomechanics in football,” The American Journal of Sports Medicine, vol. 42, no. 9, pp. 2056–2066, 2014. View at Publisher · View at Google Scholar · View at Scopus
  43. C. L. Collins, E. N. Fletcher, S. K. Fields et al., “Neck strength: a protective factor reducing risk for concussion in high school sports,” Journal of Primary Prevention, vol. 35, no. 5, pp. 309–319, 2014. View at Publisher · View at Google Scholar · View at Scopus
  44. J. J. Leddy, H. Sandhu, V. Sodhi, J. G. Baker, and B. Willer, “Rehabilitation of concussion and post-concussion syndrome,” Sports Health, vol. 4, no. 2, pp. 147–154, 2012. View at Publisher · View at Google Scholar · View at Scopus