Cervical Spine Involvement in Mild Traumatic Brain Injury: A Review

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.


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]

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.

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.

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, andMay 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.
(3) Therapies of the cervical spine with symptoms related to mTBI.
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.

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 ( = 34) or were case studies ( = 2), magazine articles ( = 2), and expert commentary ( = 1). 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 3 [4,6,[11][12][13]. 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].
As mentioned previously, the most common symptom in subjects after mTBI is posttraumatic headache (PTH) [18,19].  Total  Abs  Art  Total  Abs  Art  Total  Abs  Art  PubMed  Concussion, Neck  180  12  8  10  0  0  21  5  1  PubMed  T B I ,N e c k ,T r e a t m e n t  5 6  0  0  0  0  0  7  2  1  PubMed  T B I ,C e r v i c a l  8 3  0  0  3 3  0  0  1 7  0  0  PubMed  Concussion, Chiropractic  12  4  1  2  0  0  2  0  0  PubMed  Concussion, Physiotherapy  53  3  2  3  0  0  12  2  1 PubMed Concussion, Physical Therapy ---  t i c  2 2  0  0  0  0  0  0  0  0  Total  4510  48  31  201  5  1  143  29  11 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].

Mechanism of Injury.
Recent studies correlated mTBI with whiplash occurrence [12,16,24,25]  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 accelerationdeceleration 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].
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 Systematic review and meta-analysis of randomized controlled trials Improvement 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 management Adult Literature 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 6 Journal of Sports Medicine     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 concussion

Twelve 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  Literature review (i) Initial evaluation involves eliminating cervical spine injury and serious traumatic brain injury (ii) Selected symptoms of concussion

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 14 Journal of Sports Medicine 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 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 Fracture and/or dislocation 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 accelerationdeceleration 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].

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 symptomfree 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].

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.