Characterization of headache after traumatic brain injury - CiteSeerX

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William Walker3 and Sureyya Dikmen2,4,5. Abstract ... Sylvia Lucas, Department of Neurology, University of Washington, Box. 356097, Seattle, WA 98195–6097 ...
Original Article

Characterization of headache after traumatic brain injury

Cephalalgia 0(0) 1–7 ! International Headache Society 2012 Reprints and permissions: sagepub.co.uk/journalsPermissions.nav DOI: 10.1177/0333102412445224 cep.sagepub.com

Sylvia Lucas1,2, Jeanne M Hoffman2, Kathleen R Bell2, William Walker3 and Sureyya Dikmen2,4,5 Abstract Background: Headache is a common and persistent symptom following traumatic brain injury (TBI). Headaches following TBI are defined primarily by their temporal association to injury, but have no defining clinical features. To provide a framework for treatment, primary headache symptoms were used to characterize headache. Methods: Three hundred and seventy-eight participants were prospectively enrolled during acute in-patient rehabilitation for TBI. Headaches were classified into migraine/probable migraine, tension-type, or cervicogenic headache at baseline and 3, 6, and 12 months following TBI. Results: Migraine was the most frequent headache type occurring in up to 38% of participants who reported headaches. Probable migraine occurred in up to 25%, tension-type headache in up to 21%, then cervicogenic headache in up to 10%. Females were more likely to have endorsed pre-injury migraine than males, and had migraine or probable migraine at all time points after injury. Those classified with migraine were more likely to have frequent headaches. Conclusions: Our data show that most headache after TBI may be classified using primary headache criteria. Migraine/ probable migraine described the majority of headache after TBI across one year post-injury. Using symptom-based criteria for headache following TBI can serve as a framework from which to provide evidence-based treatment for these frequent, severe, and persistent headaches. Keywords Headache, traumatic brain injury, TBI, post-traumatic headache, PTH, migraine, probable migraine, tension-type headache, cervicogenic headache, secondary headaches Date received: 30 December 2011; revised: 5 March 2012; accepted: 18 March 2012

Introduction The Centers for Disease Control and Prevention (CDC) estimates that between 1.4 and 1.8 m civilians in the USA sustain a traumatic brain injury (TBI) each year (1). Approximately 20% of Operation Enduring Freedom (OEF) and Operation Iraqi Freedom (OIF) veterans are thought to have experienced a TBI (2). In civilian and military populations, headache is not only one of the most commonly reported symptoms following TBI (3,4), but is also often persistent (5). The reported prevalence of post-traumatic headache (PTH) in the literature has been broad (i.e. 30–90%), most likely due to patient sampling biases such as using patients treated in specialty clinics who have complicated recoveries versus prospectively studied representative TBI samples. In a 2006 review of the available literature, Lew et al. (3) found PTH to be often

persistent, reporting that 18–22% of PTH lasted longer than one year. In a recent prospective longitudinal investigation of over 450 individuals with TBI, we found the prevalence of PTHs to be 47% following

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Department of Neurology, University of Washington, USA Department of Rehabilitation Medicine, University of Washington, USA 3 Department of Physical Medicine and Rehabilitation, Virginia Commonwealth University, USA 4 Department of Psychiatry and Behavioral Medicine, University of Washington, USA 5 Department of Neurological Surgery, University of Washington, USA 2

Corresponding author: Sylvia Lucas, Department of Neurology, University of Washington, Box 356097, Seattle, WA 98195–6097, USA Email: [email protected]

2 TBI, and prevalence remained consistently high at over 40% up to one year post-injury (5). The study of headache was significantly advanced by the development of a classification system by the classification subcommittee of the International Headache Society in 1988, subsequently revised and titled the International Classification of Headache Disorders, 2nd edition (ICHD-2) criteria (6). The ICHD-2 divides headache disorders into primary and secondary headaches. Primary headache disorders, such as migraine, probable migraine (formerly migrainous headache), cluster headache, and tension-type headache among others, are thought to have no known underlying treatable cause and are primarily defined as syndromes using clinical symptoms such as severity, duration, pain characterization, and associated autonomic features for inclusion into a particular headache category. As secondary headaches, PTHs are defined based on a close temporal relationship with an antecedent TBI with severity, latency, and duration criteria, but with no defining clinical features as is found in the primary headache syndromes. Classification into primary headache phenotypes has been used to characterize PTH (7) primarily in an effort to provide a framework for treatment decisions. The similarities in neurochemical changes reported after TBI with those found in migraine suggest shared pathophysiological pathways, possibly involving the trigeminovascular system that may allow the same effective treatments despite different causation (8,9). The primary purpose of this prospective, longitudinal study was to characterize and classify headache syndromes after TBI at multiple time points up to one year following injury.

Methods Study participants A total of 378 participants with a diagnosis of TBI, who had the cognitive and communication ability to give valid responses to questions, were enrolled during acute in-patient rehabilitation. Recruitment to the study occurred within the TBI Model Systems (TBIMS) from seven centers between February 2008 and June 2009. All follow-up assessments were completed by July 2010. Criteria for inclusion and exclusion were the same as for the TBIMS. Inclusion criteria required participants to: (a) present to the designated TBIMS acute care hospital within 72 h of injury; (b) receive both acute medical and acute rehabilitation care within the same system;

Cephalalgia 0(0) (c) sustain a TBI with at least one of the following characteristics: (i) Glasgow Coma Scale (GCS) (10) score < 13 on emergency room admission (not due to intubation, sedation, or intoxication); (ii) loss of consciousness > 30 min (not due to sedation or intoxication); (iii) post-traumatic amnesia (PTA) > 24 h; or (iv) trauma-related intracranial abnormality on neuroimaging. (d) be aged 16 years or older. Exclusion criteria were participant incarceration or no telephone access for follow-up. Informed consent was obtained as approved by the institutional review boards of all seven institutions. Initial data were collected on headache during or within 1 week after discharge from in-patient rehabilitation. Follow-up interviews were conducted by telephone by trained research assistants using structured interviews at 3, 6, and 12 months after injury.

Measures Demographic data included age at injury, sex, race (white, black, Asian/Pacific Islander, native American, Hispanic, and other), education (completed high school/did not complete high school), and cause of injury (moving vehicle-related, violence, sports, fall, hit by object, and other). Prospectively assessed PTA duration was used as a marker of brain injury severity [categorized as mild (PTA < 24 h), moderate (PTA 1– 7 days), severe (PTA > 8 days] and unknown. A headache survey included detailed questions about current headache at initial evaluation during in-patient rehabilitation, history of headache prior to injury, and headache at follow-up time points. Questions were asked specifically about headache intensity, location, duration, disability and associated symptoms such as nausea, vomiting, and neurological accompaniments including visual disturbance, disability, and neck pain to classify each headache by its symptoms.

Headache characterization Headaches were classified into the following categories for primary headache disorders: migraine, probable migraine, tension-type headache and cervicogenic headache (a symptom-defined secondary headache). If the headaches did not fit into one of these categories at a given time point, they were deemed unclassifiable. Specific decisions for classification were based on answers to the headache questionnaire, ICHD-2 criteria, and expert review (KB, SL) using an ordered

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Lucas et al. decision tree. A headache was considered to be a migraine if the pain rating was moderate to severe and at least two of the following criteria were met: 1. 2. 3. 4.

the headache had a significant disabling impact; the headache was unilateral; the headache was throbbing/pulsating; the headache was worsened by movement or physical activity.

Finally, each participant had to endorse nausea and/ or vomiting or sensitivity to light and sound. A headache was classified as probable migraine if the participant endorsed moderate to severe pain, but met only one of the other criteria for migraine headache classification. A headache was classified as tension-type if it was bilateral, vice-like, squeezing or tight, and the pain was rated as mild to moderate. A headache was classified as cervicogenic if it was unilateral, neck pain was endorsed, and the headache did not meet the criteria for migraine, probable migraine, or tension-type headache. All headaches that did not fit into the four classifications were considered unclassifiable. Two random samples of headaches (N ¼ 10 and 18 respectively) defined as unclassifiable were reviewed by experts (KB, SL) when initial classification was started and prior to final data analysis. All reviewed cases were missing at least one or more symptoms to meet diagnostic classification in one of the four headache types. The classification was ordered in that it gave precedence to migraine headache with or without aura at a given time point if the criteria were met. Only if the criteria were not met for migraine would probable migraine, followed by tension-type, and finally cervicogenic, be the primary given headache for a participant.

Statistical analysis Descriptive statistics are the statistics we used in the manuscript (summarizing what we found in our study sample) rather than testing a hypothesis (inferential statistics). In our paper, the descriptive statistics we use are means (SD), percentages, and counts which are all descriptive.

Results Demographics of the 378 participants are presented in Table 1. The majority of the participants were male, white, completed high school, and were injured in motor vehicle accidents. Injury severity based on length of PTA varied, with the vast majority of participants meeting moderate to severe brain injury severity criteria.

Table 1. Demographics Variable Total number of subjects Age at injury (mean  SD) Male Female Race White Black Asian-Pacific Islander Native American Hispanic Other Education (years; mean  SD) Completed high school PTA < 24 h 1–7 days > 8 days Unknown Cause of injury Motor vehicle Violence Sports Fall Hit by object Other

N (%) 378 42.6  19.3 267 (71%) 111 (29%) 283 (75%) 55 (15%) 10 (3%) 3 (1%) 25 (7%) 2 (1%) 12.6  2.7 264 (70%) 25 73 275 5

(7%) (19%) (73%) (1%)

211 32 15 98 7 15

(56%) (8%) (4%) (26%) (2%) (4%)

Headache characteristics Sixty-six participants (17.5%) reported a history of headaches prior to TBI, with a majority endorsing symptoms consistent with migraine or probable migraine headaches (57%). The occurrence of each headache type over the first year is shown in Table 2. Migraine was the most frequent headache type occurring in up to 38% of participants who reported having headaches at 6 months after injury. Nearly one-third of headaches were not classifiable into one of the four headache types at baseline, but became more classifiable over time after injury. The occurrence of headache over the first year after TBI for those without a history of headache is found in Table 3. Migraine was the most frequent headache type occurring in up to 40% of individuals who reported headaches at 6 months after injury. Migraine and probable migraine headaches were more frequent and more likely to be classifiable early after injury. In contrast, tension-type and cervicogenic headache became slightly more classifiable over time.

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Table 2. Headache classification over the first year following traumatic brain injury Pre-injury N (% of column) Migraine Probable migraine Tension-type Cervicogenic Unclassifiable

30 8 9 2 17

(45%) (12%) (14%) (3%) (26%)

Baseline N (% of column) 51 35 11 17 49

3 months N (% of column)

(31%) (21%) (7%) (10%) (30%)

44 36 26 8 29

6 months N (% of column)

(31%) (25%) (18%) (6%) (20%)

51 30 24 4 26

(38%) (22%) (18%) (3%) (19%)

12 months N (% of column) 48 36 33 6 32

(31%) (23%) (21%) (4%) (21%)

Table 3. Headache classification over the first year after traumatic brain injury in individuals without a history of headache Baseline N (% of column) Migraine Probable migraine Tension-type Cervicogenic Unclassifiable

34 29 9 14 37

3 months N (% of column)

(28%) (24%) (7%) (11%) (30%)

26 27 15 5 21

Table 4. Classification of migraine/probable migraine by sex across all time points Male Pre-injury Baseline 3 months 6 months 12 months

20 51 50 44 52

(54%) (50%) (54%) (56%) (50%)

Female 18 35 30 37 32

(62%) (57%) (61%) (67%) (61%)

In a prior study examining the natural history of PTH in this cohort, female sex was found to be significantly related to higher rates of headache at all time points. Table 4 shows the classification of migraine or probable migraine headache by sex across all time points. Females were more likely to endorse migraine pre-injury than males, and were more likely to have migraine or probable migraine at all time points after injury compared to males. Headache frequency was higher for those who endorsed migraine or probable migraine over other headache types after injury (Figure 1). Participants whose headaches were classified as migraine were more likely to have frequent headaches (several days per week or daily) than did those whose headaches met the criteria for other headache phenotypes.

Discussion The most frequent primary headache phenotype found in this study was migraine headache, occurring at baseline in 31% of individuals with headache after TBI.

(28%) (29%) (16%) (5%) (22%)

6 months N (% of column) 36 16 16 3 20

(40%) (18%) (18%) (3%) (22%)

12 months N (% of column) 34 24 23 5 22

(31%) (22%) (21%) (5%) (20%)

Probable migraine was next in frequency with a baseline occurrence of 21% of headache types. These headache types were consistent over one year post-injury indicating that moderate to severe headaches of migraine phenotype are common and persistent following TBI. Unclassifiable headaches tended to become more ‘classifiable’ largely because the number of tension-type headaches increased from the unclassifiable pool. Despite this, tension-type headaches were described in only about one-fifth of persons with headache after TBI. Cervicogenic headaches were also infrequent, a surprising finding given the high incidence of vehicle accidents as the cause of injury. Our findings are similar to the work of others using primary headache criteria to characterize headache after TBI. Theeler et al. (11) in a questionnaire-based study of US soldiers with a history of concussion during deployment in Iraq or Afghanistan found that 58% of PTH had a migraine phenotype according to the ICHD-2 criteria remarkably similar to headache characterization in our civilian population. A later retrospective, chart-based review by Theeler and Erickson (12) in a mild TBI population sustaining head or neck trauma while deployed to Iraq, found that 78% of all headaches presenting to a specialty neurology clinic met the criteria for migraine with and without aura or probable migraine, and only 18% met criteria for tension-type headache. Other studies attempting to classify headache following mild head injury have not found the higher prevalence of migraine that this and other studies found (11,12). Haas (13) found that 75% of a clinic sample of patients, over 80% with mild TBI, met the criteria

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Lucas et al.

Headache frequency at 12 months

45 40 35 30 25 20 15 10 5 0 Migraine

Probable migraine