Review Article

Cervical Spine Involvement in Mild Traumatic Brain Injury: A Review

Table 2

Included studies description.

Authors/sectionsStudy objectivePopulationMethods Main outcomes/findings

Becker [34]This review was developed as part of a debate and takes the “pro” stance that abnormalities of structures in the neck can be a significant source of headacheAdultLiterature review(i) Clinical treatment trials involving patients with proven painful disorders of upper cervical zygapophysial joints have shown significant headache relief with treatment directed at cervical pain generators
(ii) Headaches related to cervical spine disorders (cervicogenic headache and chronic headache attributed to whiplash injury) remain one of the most controversial areas of headache medicine
(iii) Diagnostic criteria for cervicogenic headache have been developed by the CHISG

Bogduk [30]To summarize the evidence that implicates the cervical zygapophysial joints as the leading source of chronic neck pain after whiplashAdultNarrative review
Data were retrieved from studies that addressed the postmortem features and biomechanics of injury to the cervical zygapophysial joints and from clinical studies
(i) Clinical studies have shown that zygapophysial joint pain is very common among patients with chronic neck pain after whiplash
(ii) The fact that multiple lines of evidence, using independent techniques, consistently implicate the cervical zygapophysial joints as a site of injury and source of pain strongly implicates injury to these joints as a common basis for chronic neck pain after whiplash

Bonk et al. [38]To evaluate the effectiveness of conservative management for acute Whiplash-Associated DisorderAdultSystematic review and meta-analysis of randomized controlled trialsImprovement of cervical movement in the horizontal plane short term could be promoted by the use of a conservative intervention. The use of a behavioral intervention (e.g., act-as-usual, education, and self-care including regular exercise) may be an effective treatment in reducing pain and improving cervical mobility in patients with acute WADII in the short-medium term

Borich et al. [2]In this special interest article, we discuss the definition and risk factors associated with concussion, summarize and highlight some of the most widely used assessment tools, and critique the evidence for current principles of concussion managementAdultLiterature review(i) Disease Control and Prevention describes mild traumatic brain injury (mTBI which includes concussion) as a silent epidemic
(ii) An estimated 1.6 million to 3.8 million sport- and recreation-related brain injuries occur in the United States annually, and up to 75% are classified as mild
(iii) “Rest” in the form of delaying return to competitive sports may be better served by a universal period of 7 to 10 days than by symptom monitoring, primarily to prevent the potential for reinjury

Brolinson [7]To systematically review the evidence for rest, treatment, and rehabilitation after sport-related concussionSports
Adult
Pediatric
Systematic review(i) From 749 articles evaluating rest and 1,175 evaluating treatment, 2 studies met criteria for the effect of rest and 10 abstracts met criteria for treatment. Three further treatment articles were identified by the authors
(ii) Health professionals are more involved in sports and in the concussions follow-up
(iii) Interventions included manual spinal therapy, physiotherapy, and neuromotor and sensorimotor retraining compared with rest and graduated exercise, for up to 8 weeks

Collins et al. [43]To develop and validate a cost-effective tool to measure neck strength in a high school setting and to determine if anthropometric measurements captured by ATs can predict concussion risk6,704 high school athletes in boys’ and girls’ soccer, basketball, and lacrosseFeasibility study
Pilot study
(i) Differences in overall neck strength may be useful in developing a screening tool to determine which high school athletes are at higher risk of concussion. Once identified, these athletes could be targeted for concussion prevention programs

Eckner et al. [40]The purpose of this study was to determine the influence of neck strength and muscle activation status on resultant head kinematics after impulsive loading 46 contact sport athletes
24 males; 22 females
aged 8 to 30 years
Descriptive laboratory study (i) Neck strength and impact anticipation are 2 potentially modifiable risk factors for concussion
(ii) The results of this study suggest that greater neck strength attenuates the head’s dynamic response to external forces

Fernández De Las Peñas et al. [24]The aims of the present paper are to detail a manual approach developed by our research group, to help in future studies of the management of the sequels to whiplash injury, and to suggest explanations for the mechanisms of this protocol AdultLiterature review(i) The clinical syndrome of whiplash injury includes neck pain, upper thoracic pain, cervicogenic headache, tightness, dizziness, restriction of cervical range of motion, tinnitus, and blurred vision
(ii) Spinal manipulation/mobilization and soft tissue mobilization techniques are manual therapies commonly used in the management of neck disorders

Kennedy [14]This document is intended to provide the user with instruction and direction in the rehabilitation of PCSOntario Hospital
Canada
Adult
PCS and treatment
guidelines
(i) Cervicogenic
(ii) Autonomic
(iii) Vestibular
(iv) Vision
(v) Education
(i) Anatomically, the cervical spine is closely linked to structures that can cause many of the same symptoms as concussion
(ii) PCS treatment has traditionally consisted of rest, education, neurocognitive rehabilitation, and antidepressants with limited effectiveness
(iii) Balance deficits and postural instability are commonly reported after concussion

Gravel et al. [36]This systematic review investigated the effectiveness of interventions initiated in acute settings for patients who experience mTBIAdultSystematic review
Cochrane’s risk of bias assessment tool
(i) According to the published literature, no intervention initiated acutely has been clearly associated with a positive outcome for patients who sustain mTBI, and there is little evidence suggesting that follow-up interventions may be associated with a better outcome
(ii) There is a paucity of well-designed clinical studies for patients who sustain mTBI. The large variability in outcomes measured in studies limits comparison between them

Guskiewicz et al. [9]To review the current literature to identify the most sensitive and reliable concussion assessment components for inclusion in the revised version: the SCAT3 Adult Literature review(i) One of the major challenges in the medical management of concussion is that there is no single “gold standard” for assessing and diagnosing the injury
(ii) Balance deficits or instability are often observable in patients following concussion and the presence of these deficits may be an indicator of vestibular disruption

Hanson et al. [6]The purpose of this article is to review the current literature in the management and prevention of concussion PediatricsReview(i) The rise in the number of concussion diagnoses may be due, in part, to increased awareness regarding the potential for complications of concussions and sequelae of multiple concussions, as opposed to an actual increase in the incidence of concussion alone
(ii) Typical signs and symptoms of concussion

Harmon et al. [5]To provide an evidence-based, best practices summary to assist physicians with the evaluation and management of sports concussionAdult
Children
Statement of the American Medical Society for Sport Medicine Review(i) However, as many as 50% of the concussions may go unreported
(ii) Headache is the most commonly reported symptom with dizziness the second most common

Headache Classification Committee of the International Headache Society (IHS) [33]The International Classification of Headache Disorder may be reproduced freely for scientific, educational, or clinical uses by institutions,
societies, or individuals
Adult
Children
Review
guideline
(i) Cervicogenic
headache from () migraine and () tension-type headache
includes side-locked pain, provocation of typical headache by digital pressure on neck muscles and by head movement, and posterior-to-anterior radiation of pain
(ii) Diagnostic criteria

Hecht [16]This article reviews the literature on management of posttraumatic headaches, presents an approach to the assessment and treatment of individuals with headaches following TBI that appear to be cervicogenic, focuses specifically on identifying occipital neuralgia, and discusses the technique of occipital nerve blocks7 males
(18–42 yo)
3 females
(22–64 yo)
Retrospective review
&
Report of ten patients
(i) While there are a variety of different posttraumatic headaches, clinicians must be aware of all potential presentations including those emanating from the cervical spine and its affiliated structures (e.g., cervicogenic)
(ii) Injury to these structures (innervated by afferent fibres of the 3 sup. cervical roots)
(iii) These include but are not limited to muscles, ligaments, vessels, somatic and sympathetic nerves, esophagus, temporomandibular joint, discs, zygapophyseal joints, cervical vertebrae, and the atlantoaxial complex
(iv) Whiplash syndrome may be the primary factor in many postconcussive headaches

Hynes and Dickey [12]To examine the relationship between the occurrence of Whiplash-Associated Disorders and concussion symptoms in hockey playersHigh school, college/university, Ontario Hockey League, and men’s recreational teams
(15–35 yo)
20 teams
Prospective study(i) 183 players were registered for this study; 13 received either a mechanical whiplash injury or a concussion injury
(ii) There is a strong association between whiplash-induced neck injuries and the symptoms of concussion in hockey injuries
(iii) Acceleration and deceleration of the head and neck complex occurs in sports and can potentially create injuries similar to those incurred in low velocity motor vehicle accidents, as stated in a recent literature review focused on Whiplash-Associated Disorders

King et al. [35]The objective was to determine the sensitivity, specificity, and likelihood ratio of manual examination for the diagnosis of cervical zygapophyseal joint pain173 patients with neck pain in whom cervical zygapophyseal joint pain was suspectedRetrospective study(i) Manual examination had a high sensitivity for cervical zygapophyseal joint pain, at the segmental levels commonly symptomatic, but its specificity was poor
(ii) The present study found manual examination of the cervical spine to lack validity for the diagnosis of cervical zygapophyseal joint pain

Kozlowski et al. [3]To assess exercise intolerance in male and female patients with PCS34 patients (PCS)
17 males,
17 females
Age = 25.9 ± 10.9
22 uninjured individuals
Cross-sectional study(i) Symptoms from concussion typically resolve within 7 to 10 days
(ii) The definition of PCS given by the World Health Organization includes a history of traumatic brain injury and 3 or more symptoms
(iii) No cognitive testing, exclusion of other disorders, or symptom threshold exists for the diagnosis of PCS
(iv) 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

Kristjansson and Treleaven [29]The purpose is to review dizziness in neck pain: implications for assessment and management AdultReview(i) Disturbances to the afferent input from the cervical region in those with neck pain may be a possible cause of symptoms such as dizziness, unsteadiness, and visual disturbances, as well as signs of altered postural stability, cervical proprioception, and head and eye movement control

Leddy et al. [27]The objective was to compare symptoms in patients with physiologic postconcussion disorder (PCD) versus cervicogenic/vestibular PCD128 adultsRetrospective review
Questionnaire
(i) 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
(ii) Concomitant injury to the cervical spine resembling whiplash may occur as a result of the acceleration, deceleration forces sustained in concussive trauma
(iii) Structural and functional injury to the cervical spine can be associated with prolonged symptoms such as headache, dizziness, blurred vision, and vertigo

Leddy et al. [44]This review focuses on rehabilitation of concussion and postconcussion syndrome Adult
Children
Review(i) Early education, cognitive behavioral therapy, and aerobic exercise therapy have shown efficacy in certain patients but have limitations of study design

Leslie and Craton [25]Based on the current medical evidence, we would suggest that the constellation of symptoms presently defined as concussion does not have to involve the brainAdult Editorial comment(i) Concussion symptoms can emanate from the cervical spine
(ii) Whiplash mechanisms of injury are identical to the “impulsive forces” described in concussive injuries
(iii) Notably, symptoms such as headache, neck pain, disturbance of concentration or memory, dizziness, irritability, sleep disturbance, and fatigue have been described in both concussion and whiplash patients
(iv) Cervical zygapophysial joints have been implicated as generators of headache and dizziness
(v) The overlap with neck/whiplash injuries is evident

Lucas [19]This article reviews the literature on headache management in concussion and mTBIAdult
Pediatric
United States
Literature review(i) Reports of headache after concussion or mTBI in children ranged from 72% to 93%
(ii) Headache is one of the most common symptoms after TBI and PTH may be part of a constellation of symptoms that is seen in the postconcussive syndrome

Makdissi et al. [8]The objectives of the current paper are to review the literature regarding difficult concussion and to provide recommendations for an approach to the investigation and management of patients with persistent symptomsAdult
Sport
Qualitative review (i) Cases of concussion in sport where clinical recovery falls outside the expected window (i.e., 10 days) should be managed in a multidisciplinary manner by health care providers with experience in sports-related concussion

Marshall [11]This paper is a review of recent literature on the topic of concussion, consisting of biomechanics, pathophysiology, diagnosis, and sideline managementAthletes
United States
Narrative review (i) The cervical spine not only is a potential source of injury that we must be aware of but also is implicated as a factor in the concussion itself
(ii) Signs and symptoms of concussion from the Association of Sport College of Medicine (ACSM) updated consensus statement

Maugans et al. [22]The goal of this investigation was to explore cerebral blood flow fluctuation after pediatric sport-related concussionTwelve children
Ages 11 to 15 years
Control group
Clinical study(i) Statistically significant alterations in cerebral blood flow were documented in the sport-related concussion group, with reduction in cerebral blood flow predominating. Improvement toward control values occurred in only 27% of the participants at 14 days and 64% at >30 days after sport-related concussion

McCrory et al. [4]The new 2012 Zurich Consensus statement is designed to build on the principles outlined in the previous documents and to develop further conceptual understanding of this problem using a formal consensus-based approachInternational consensus
(i) Adults
(ii) Pediatric
International consensus
Sport concussion
(i) An initial period of rest may be of benefit
(ii) Multimodal physiotherapy treatment for individuals with clinical evidence of cervical spine and/or vestibular dysfunction may be of benefit
(iii) Persistent symptoms (>10 days) are generally reported in 10–15% of concussions. In general, symptoms are not specific to concussion and it is important to consider other pathologies
(iv) PCS should be managed in a multidisciplinary manner by health care providers with experience in sports concussion

Mihalik et al. [39]The objective was to evaluate the effect of cervical muscle strength on head impact biomechanics 37 volunteer ice hockey players
Age = 15.0 ± 1.0 years
Prospective cohort study(i) The hypothesis that players with greater static neck strength would experience lower resultant head accelerations was not supported
(ii) There is still nonempirical support for the role neck musculature may play in reducing the risk of mild TBI that is worthy of investigation in a young at-risk sample

Moser et al. [21]The objective of this article is to evaluate the efficacy of cognitive and physical rest for the treatment of concussionHigh school and collegiate athletes ()
Range = 14–23 yo 
Mean = 15.0 yo
67% male
33% female
Retrospective analysis (i) Participants showed significantly improved performance on Immediate Post-Concussion Assessment and Cognitive Testing and decreased symptom reporting following prescribed cognitive and physical rest
(ii) These preliminary data suggest that a period of cognitive and physical rest may be a useful means of treating concussion-related symptoms, whether applied soon after a concussion or weeks to months later

Pelletier [18]The purpose of this paper is to present a review of the diagnosis and treatment of the potentially catastrophic neck and head injuries caused by spearing in Canadian amateur football Amateur football United States and CanadaLiterature review(i) Associated cervical trauma with concussion may include one or several of neck pain, reduced cervical range of movement, cervicogenic headache, cervicogenic vertigo, and occipital neuralgia
(ii) Several manual techniques for the treatment of posttraumatic concussion syndrome have been described as either “direct” or “indirect”

Reid et al. [37]This study aimed to determine the efficacy of sustained natural apophyseal glides (SNAGs) in the treatment of this condition34 adults
17 SNAGs
17 Placebo
Double-blind randomized controlled clinical trial(i) The SNAG treatment had an immediate clinically and statistically significant sustained effect in reducing dizziness, cervical pain, and disability caused by cervical dysfunction

Schmidt et al. [42]The purpose of this study was to compare the odds of sustaining higher magnitude in-season head impacts between athletes with higher and lower preseason performance on cervical muscle characteristics49 high school and collegiate American football playersCohort study (i) The study findings showed that greater cervical stiffness and less angular displacement after perturbation reduced the odds of sustaining higher magnitude head impacts; however, the findings did not show that players with stronger and larger neck muscles mitigate head impact severity
(ii) Male athletes also exhibit greater stiffness and capacity to store elastic energy compared with female athletes

Schneider et al. [26]The objective of this study was to determine the risk of concussion in youth male hockey players with preseason reports of neck pain, headaches, and/or dizziness3832 males
Ice hockey players
(11–14 yo)
280 teams
Prospective study (i) Preseason reports of neck pain and headache were risk factors for concussion
(ii) Dizziness was a risk factor for concussion in the Pee Wee nonbody checking
(iii) A combination of any 2 symptoms was a risk factor in the Pee Wee nonbody checking cohort and the Bantam cohort
(iv) Neck pain is the third most commonly reported baseline symptom in varsity athletes

Schneider et al. [10]The objective of this study was to determine if a combination of vestibular rehabilitation and cervical spine physiotherapy decreased the time until medical clearance in individuals with prolonged postconcussion symptoms18 males
13 females
12–30 years
Randomized controlled trial (i) A combination of cervical and vestibular physiotherapy decreased time to medical clearance to return to sport in youth and young adults with persistent symptoms of dizziness, neck pain, and/or headaches following a sport-related concussion
(ii) The cervical spine is cited as a source of pain in individuals with whiplash
(iii) The upper cervical spine can cause cervicogenic headaches
(iv) A combination of manual therapy and exercise has been shown to be more effective than passive treatment modalities in individuals with neck pain

Scorza et al. [13]Current concepts in concussionChildren adolescentsLiterature review(i) Initial evaluation involves eliminating cervical spine injury and serious traumatic brain injury
(ii) Selected symptoms of concussion

Signoretti et al. [15]The following review represents the authors’ effort to piece together the current concepts and the most recent findings about the complex basic physiology underlying the injury processes of this particular type of brain trauma and to emphasize the nuances involved in conducting research in this area European countries
United States
Adult
Literature review(i) Postconcussive symptoms may be prolonged in a small percentage of cases, but the acute clinical symptoms largely reflect a functional disturbance rather than a structural injury, which usually is confirmed by the absence of abnormalities on standard neuroimaging studies
(ii) The symptoms of concussion reflected a functional disturbance rather than a structural damage such as contusion, hemorrhage, or laceration of the brain

Smith et al. [32]This preliminary study examined a sample of individuals who did and did not respond to facet block as well as healthy controls to determine whether there were differences in their physical and psychological features once the effects of the blocks had abated and symptoms had returned 58 adults
(18–65 yo)
Calgary, Canada
Cross-sectional study (i) Following FB procedures, both WAD groups demonstrated generalized hypersensitivity to all sensory tests, decreased neck ROM, and increased superficial muscle activity with the CCFT compared to controls
(ii) Both WAD groups demonstrated psychological distress
(iii) Chronic WAD responders and nonresponders to feedback (FB) procedures demonstrate a similar presentation of sensory disturbance, motor dysfunction, and psychological distress. Higher levels of pain catastrophization and greater medication intake were the only factors found to differentiate these groups

Spitzer et al. [28]The purpose was to expose the clinical classification of Whiplash-Associated DisordersAdultGuideline(i) Grades 0 to 4 (clinical presentation)

Stovner et al. [23]A main objective of this study was to assess the validity of this diagnosis by studying the headache pattern of concussed patients that participated in one historic () and one prospective cohort () study 200 patients
(18–67 yo)
Trauma involving LOC of < 15 min.
Kaunas, Lithuania
Questionnaires study
(after 3 months & 1 year)
(i) Existence of pretraumatic headache was a predictor of posttraumatic headache, although pretraumatic headache seems to have been underreported among the concussed patients
(ii) This is negative correlation, and the lack of specificity indicates that headache occurring 3 months or more after concussion is not caused by the head or brain injury
(iii) Rather it may represent an episode of one of the primary headaches, possibly induced by the stress of the situation

Tator et al. [1]This report is intended to improve understanding of the epidemiology of neurological conditions and the economic impact on the Canadian health care system and society Adult
Children
Canada
Statistical report(i) Cerebral concussions are commonly known as mild traumatic brain injury (mTBI)
(ii) By contrast, Statistics Canada estimated in recent studies that the annual incidence for mTBI is 600 per 100,000 persons and 11.4 per 100,000 inhabitants for a traumatic brain injury (TBI)
(iii) However, the highest age group incidence is between 19 and 29 years, representing approximately one-quarter of patients with cranial trauma
(iv) Children (18 years and younger) represented almost 45% of the patients with head injury

Tierney et al. [41]The purpose was to determine whether gender differences existed in head-neck segment kinematic and neuromuscular control variables responses to an external force application with and without neck muscle preactivation20 females
20 males
Adult
Cohort study (i) Gender differences existed in head-neck segment dynamic stabilization during head angular acceleration
(ii) Females exhibited significantly greater head-neck segment peak angular acceleration and displacement than males despite initiating muscle activity earlier (SCM only) and using a greater percentage of their maximum head-neck segment muscle activity

Treleaven et al. [31]This study measured aspects of cervical musculoskeletal function in a group of patients (12) with postconcussional headache (PCH) and in a normal control group 8 males
(15–48 yo)
4 females
(20–44 yo)
Retrospective study(i) Twelve of the 15 eligible patients consented to enter the study
(ii) The most frequent major symptomatic segments were C1-C2, C2-C3, C0-C1, and C3-C4.
Signs of cervical articular and muscular dysfunction distinguished the PCH group from the control group
(iii) As upper cervical joint dysfunction is a feature of cervicogenic causes of headache, the results of this study support the inclusion of a precise physical examination of the cervical region in differential diagnosis of patients suffering persistent headache following concussion

Watanabe et al. [20]The specific goals of this review include
(1) determination of effective interventions for PTH
(2) development of treatment recommendations
(3) identification of gaps in the current medical literature regarding PTHA treatment
(4) suggestions for future directions in research to improve outcome for persons with PTHA
Adult
Child
Literature review
The level of evidence: American Academy of Neurology criteria
(i) Head pain may be related to direct damage to the skull or brain tissue; muscular, tendinous, and/or ligamentous injury to the cervical spine; and injuries to peripheral nerves. Other nervous system injuries, such as visual and vestibular system damage, also may contribute to headache syndromes
(ii) Biologically based interventions included a variety of biofeedback mechanisms, physical therapy and manual therapy, immobilization devices, ice, and injections

Weightman et al. [17]The purpose of this article is to provide a summary of the development process and to share specific recommendations for PT practice with service members who sustain MTBI Military and civilian populations Literature review
MTBI-related, evidence-based reviews and guidelines
(i) Determine the disability and its severity related to the neck, jaw, and headaches
(ii) Physical therapy interventions with the strongest evidence in the treatment of PTH include a multimodal approach of specific training in exercise and postural retraining, stretching and ergonomic education, and manipulation and/or mobilization in combination with exercise