The Association Between Fear of Pain and Sports-Related Concussion Recovery in a Pediatric Population

Abstract

Objective:

Determine if an association exists between fear of pain and recovery time from sports-related concussion in a pediatric population.

Design:

Prospective observational study.

Setting:

Primary outpatient sports medicine clinic of a large pediatric hospital.

Patients:

128 pediatric patients aged 8 to 18 years who presented to clinic with a primary diagnosis of concussion from September 2018 – March 2020. Inclusion criteria included presentation within two weeks of injury and symptomatic on initial visit. Patients who sustained a concussion due to motor vehicle collisions or assault were excluded.

Independent Variables:

There was no intervention. Study participants who met inclusion criteria were administered the Fear of Pain Questionnaire (FOPQ) at their initial visit.

Main Outcome Measures:

Time to clinical recovery was the main outcome measure and was determined by the fellowship trained sports medicine physician based on resolution of concussion symptoms, resumption of normal physical and cognitive daily activities, no use of accommodations or medications, and normalization of physical exam.

Results:

There was a significant difference in FOPQ scores for those with prolonged recovery (M = 33.12, SD = 18.36) compared to those recovering in fewer than 28 days (M = 26.16, SD = 18.44; t(126) = −2.18, p = .036).

Conclusions:

Consistent with the adult literature, we found that pediatric patients are more likely to have a prolonged recovery from concussion when they have higher fear of pain.

INTRODUCTION

In the United States, an estimated 27 million youth aged 6–18 years old participate in team sports annually.¹ Participation in youth sports can pose an increased risk of sustaining a sports-related concussion (SRC), a subset of mild traumatic brain injury. Mild traumatic brain injury is a traumatically induced transient disturbance of brain function that involves a complex physiological process.² Annually, 1–1.8 million SRCs occur in the pediatric population in the United States.³

Most SRCs in young athletes resolve within an expected time frame of 2–4 weeks,² but 30% of pediatric patients have a prolonged recovery (defined in the pediatric population as symptoms lasting longer than 28 days), with persistent post-concussive symptoms.^4,5 Symptoms include physical dysfunction such as headaches and dizziness. In addition, prolonged recovery can cause psychosocial issues resulting from decreased participation in sports and withdrawal from social encounters.^6,7 Risk factors for prolonged recovery include female, young age, history of prior concussion, mood disorders, learning disabilities, attention-deficit/hyperactivity disorder (ADHD), and history of migraines.^8–10 Identifying these risk factors allows the medical provider to counsel patients and their families appropriately on the expected recovery timeline.

A combination of non-specific post-concussive symptoms may be associated with preexisting and coexisting factors, rather than a single pathophysiological entity or an ongoing physiological injury to the brain.¹¹ A biopsychosocial explanation may capture the complex interactions of underlying features that support the variable recovery outcomes of patients with SRCs.¹² One such biopsychosocial factor is fear-avoidance behaviors. Young patients may develop a maladaptive response (fear and catastrophizing) to pain when symptom-provoking activities worsen their concussion symptoms. The fear-avoidance model shows that catastrophizing the pain experience results in increased future fear of pain. Fear of pain leads to hypervigilance and avoidance of pain-provoking activity, causing persistent disability and disuse, further exacerbating the fear-avoidance cycle.¹³ Examples of fear-avoidance behaviors in pediatric patients with concussions include refusing to complete schoolwork due to worsening headache, refusing to leave the bedroom due to noise in the house that increases symptoms, and avoiding aerobic exercise due to exacerbation of symptoms despite the benefits of sub-maximal aerobic activity for faster recovery.

Pain-related fear is complex and difficult to assess, as it may involve fear of reinjury, cognitive activity, physical activity, or a combination of these factors. Fear of pain or re-injury has been studied in both musculoskeletal injuries and chronic medical conditions.^14,15 High fear of pain predicts greater chronic disability in individuals with chronic neck pain¹⁶ and low back pain.¹⁷ Likewise, fear avoidance and post-concussion symptoms are positively correlated,¹⁸ and fear avoidance predicts greater symptom severity and disability in adult patients with mild traumatic brain injury.¹² Anderson et al.¹⁹ recently showed that adolescents with high fear of re-injury after an SRC were more symptomatic and more likely to exhibit vestibulo-ocular symptoms.

The most recent sports concussion consensus statement discussed the paucity in the literature regarding pediatric patients with SRC.¹¹ It is important to be able to determine if fear of pain is a risk factor for prolonged recovery in young athletes with sports concussion, as early interventions may improve recovery. Measures developed to assess pain-related fear for adults include the Tampa Scale for Kinesiophobia^20,21 and the Fear-Avoidance Belief Questionnaire (FOPQ).²² The FOPQ is a validated measure in the pediatric population for patients aged 8–18 years old.²³. The purpose of our study is to determine if a relationship exists between fear of pain and recovery from concussion within a pediatric population. Our hypothesis is that patients with higher FOPQ scores will experience prolonged recovery from concussions. To our knowledge, this is the first study to evaluate this relationship in the pediatric population.

METHOD

Design and Participants

This prospective observational study was performed in the sports medicine subspecialty clinic of a tertiary care children’s hospital and approved by the institutional review board. Patients aged 8–18 years who presented to the sports medicine clinic with primary diagnoses of concussion from September 2018 – March 2020 were considered for this study. Inclusion criteria included presentation within 2 weeks of sustaining the injury and symptomatic on initial visit. Patients who sustained a concussion due to motor vehicle collisions or assault were excluded from this study. History of severe traumatic brain injury and brain surgery were not a priori exclusion criteria, but no patient in this study had a history of these experiences. Written consent was obtained from the parent or patient’s legal guardian, and verbal assent was obtained from the study participant.

Procedures

Study participants who met inclusion criteria were administered the FOPQ at their initial visit. The FOPQ is a validated questionnaire for children aged 8–18 years and consists, of 24 statements regarding pain-related fear that are rated on a 5-point Likert-type scale, ranging from “strongly disagree” to “strongly agree”.²³ (α_chronbach = .92). The FOPQ was completed by the patient only at the initial visit. Total score (out of 96) is calculated by summing all items. Higher scores on the FOPQ indicate greater avoidance of activities and pain related fear.

After completing the FOPQ on the initial visit, the patient went through a normal concussion assessment. The parent filled out a concussion intake form, and the patient completed an age-appropriate checklist of symptoms from the Child Sport Concussion Assessment Tool 5^th edition (Child SCAT5) for ages 5–12 or the Sports Concussion Assessment Tool 5^th edition (SCAT5) for ages 13 and above.²⁴ For those patients younger than 13 years of age filling out the child SCAT5, both patient and parent filled out checklists of symptoms; however, only the child’s responses were recorded for this study.

A standardized physical examination was performed by a fellowship trained sports medicine physician, and findings were documented in a standardized template in an electronic medical record (Epic Systems, Verona, Wisconsin). The initial exam included a detailed neurological exam including evaluation of cranial nerves, deep tendon reflexes, and muscle strength in all extremities. Balance was evaluated using the modified balance error scoring system from the SCAT5.¹¹ The examination also included a standardized vestibulo-ocular motor screen (VOMS),^25,26 to identify any provocation of symptoms (i.e., headache, dizziness, nausea, or fogginess) with smooth pursuits, saccades, vestibulo-ocular reflex, and vestibulo-ocular reflex cancellation testing. Near point convergence was measured using a standard Astron accommodative ruler (Gulden ophthalmics, Elkins Park, Pennsylvania) with a single-column 20/30 card. Abnormal near point convergence was defined as greater than or equal to 6 cm, measured from the nasal bridge. Change in scores from baseline (> 2 on any VOMS item) determined a positive finding on VOMS. The VOMS has high internal consistency (alpha_Chronbach = .92) and differentiated between SRC and healthy controls.^25,27

Based on a chart review of study participants, additional categorical variables were collected and included age, sex, insurance type (private versus Medicaid), concussion injury details, time to presentation in clinic, initial concussion symptom score (symptom severity and total number of symptoms), VOMS findings (positive or negative), and self/parent reported history of anxiety, depression, ADHD, prior concussions, and migraine.

Patients continued with follow-up visits until there was clinical recovery, defined as resolution of concussion symptoms, resumption of normal daily physical and cognitive activity, and normalization of physical examination findings to functional levels. The majority of follow-up visits occurred weekly or bi-weekly, depending on the treating physician’s recommendation. Patients were encouraged to return to clinic earlier if the family and patient felt they had fully recovered from the concussion.

Outcome Measures

The main outcome measure was time to clinical recovery. Clinical recovery was determined by the sports medicine physician based on resolution of concussion symptoms, resumption of normal physical and cognitive daily activities, no use of accommodations or medications, and normalization of physical exam. The date of recovery was defined as the date of discharge and clearance to initiate or complete the state-specific, return-to-sport protocol.

Statistical Analysis:

Descriptive statistics were used to describe medians, mean values, and ranges. Categorical variables included sex, insurance type (Private vs Medicaid), positive VOMS at initial visit, self-reported history of anxiety, depression, ADHD, and self-reported history of prior concussions and migraines. Chi square tests measured relationships between prolonged recovery and categorical independent variables. Independent sample t-tests measured relationships between prolonged recovery and continuous variables. Relationships between days to recovery and continuous variables were measured by Pearson correlations. The analyses were conducted using IBM SPSS software version 18. Thresholds for statistical significance were set to α = .05. We conducted a post-hoc power analysis for our focal t-test of the association between prolonged recovery and FOPQ using G*Power version 3.1.9.2.²⁸ Given the observed noncentrality parameter δ = 2.74, 126 degrees of freedom, and a two-tailed α of .05, the t-test to detect the present difference of d = .49 achieved Power (i.e., 1 - β) = .78.

RESULTS

One hundred twenty-eight patients were included in the study sample.ⁱ Sixty-two percent were female, and the mean age was 14.19 years (SD = 2.15). Patients sustained concussions during a range of sports-related activities, but the majority occurred from football (27%), soccer (14%), basketball (9%), and cheerleading (6%). Sixteen percent of patients sustained a concussion in non-organized sports (e.g., recess or physical education class). Patients presented to the sports medicine clinic an average of 5.68 days (SD = 3.46) after sustaining an injury. Patients endorsed on average 10.95 symptoms at their initial visit (SD = 5.78, range = 0 – 22). Average number of days to recovery was 42.57 (SD = 43.72, range = 3 – 343). Seventy-three (57%) patients had a prolonged recovery (> 28 days).

Fear of Pain

Patients endorsed a range of scores on the FOPQ from 0–90 with a mean score of 30.13 (SD = 18.65). Those with prolonged recovery had significantly higher FOPQ scores (M = 33.12, SD = 18.36) than those without prolonged recovery (M = 26.16, SD = 18.44; t(126) = −2.18, p = .036, CI [−13.46, −46]). FOPQ scores were not related to a self/parent reported history of anxiety or depression, and there were no significant differences in FOPQ scores between males and females. Separate independent sample t-tests measured whether patients with prolonged recovery indicated higher mean scores on specific items of the FOPQ compared to patients without prolonged recovery (See Table 2). Patients with prolonged recovery indicated higher scores at their initial sports medicine visit for six items: “I find it difficult to calm my body down when having pain” (t(126) = −2.34, p = .021, CI [−1.02, −.08]), “When I hurt I can’t stop thinking about the pain” (t(126) = −2.70, p = .008, CI [−1.08, −.17]), “I begin shaking/trembling when doing an activity that increases pain” (t(126) = −2.21, p = .029, CI [−.92, −.05]), “I can’t think straight when I feel pain” (t(126) = −2.60, p = .010, CI [−1.08, −.14]), “I cannot go back to school until my pain is treated” (t(126) = −3.34, p = .001, CI [−.89, −.23]), and “I do not think I will ever be able to go back to a normal school schedule” (t(126) = −2.34, p = .042, CI [−.59, −.01]).

Table 2:

FOPQ Item analysis by recovery

Item	M (SD) score for patients without prolonged recovery (<27days; N = 55)	M (SD) score for patients with prolonged recovery (> 27 days; N = 73)	t(df)
When I feel pain, I am afraid that something terrible will happen.	1.29 (1.27)	1.55 (1.25)	−1.14 (126)
I worry when I am in pain.	1.73 (1.35)	1.92 (1.21)	−.84 (126)
Feelings of pain are scary for me.	1.24 (1.18)	1.61 (1.28)	−1.63 (123)
I find it difficult to calm my body down when having pain.	1.31 (1.26)	1.86 (1.38)	−2.34 (126)*
I think that if my pain gets too bad it will never get better.	.91 (1.20)	1.11 (1.21)	−.95 (123)
When I hurt I can’t stop thinking about the pain.	1.56 (1.33)	2.18 (1.25)	−2.70 (125)**
Pain causes my heart to beat fast or race.	1.55 (1.37)	1.58 (1.34)	−.12 (126)
I’m afraid that when the pain starts it’s going to be really bad.	1.42 (1.26)	1.71 (1.28)	−1.27 (125)
I walk around in constant fear of hurting.	.64 (1.06)	.69 (1.08)	−.30 (125)
I begin shaking/trembling when doing an activity that increases pain.	.76 (1.12)	1.25 (1.36)	−2.21 (123.7)*
I can’t think straight when I feel pain.	1.76 (1.32)	2.37 (1.31)	−2.60 (125)*
When I sense pain, I feel dizzy or lightheaded.	1.38 (1.33)	1.84 (1.42)	−1.84 (126)
I can’t do all the things normal people do because it’s so easy to hurt my body.	.60 (1.08)	.82 (1.11)	−1.13 (126)
I put things off because of my pain.	1.16 (1.30)	1.44 (1.29)	−1.19 (126)
I cancel plans when I am in pain.	1.20 (1.31)	1.51 (1.25)	−1.38 (125)
I do not go to school because it makes my pain worse.	.98 (1.06)	1.33 (1.36)	−1.62 (125.8)
I cannot go back to school until my pain is treated.	.51 (1.15)	1.07 (1.15)	−3.34 (123.5)**
I choose to miss things that are important to me so that I won’t feel my pain.	.64 (.97)	.73 (1.08)	−.49 (126)
I go immediately to lie down or rest when I feel really bad pain.	1.09 (1.38)	2.48 (1.28)	−1.59 (126)
I stop any activity if I start to hurt or my pain becomes worse.	1.98 (1.28)	2.18 (1.26)	−.87 (126)
When I am in pain, I stay away from other people.	.91 (1.11)	1.14 (1.23)	−1.09 (125)
My pain controls my life.	.45 (.90)	.38 (.84)	.46 (126)
I do not think that I will ever be able to go back to a normal school schedule.	.24 (.64)	.53 (1.00)	−2.05 (122.88)*

Note: FOPQ responses are rated on a 5-point Likert scale, ranging from “strongly disagree” to “strongly agree”.

^*p < .05,

^**p < .01,

Age

Those with prolonged recovery tended to be younger (M = 13.75, SD = 2.31) than those without prolonged recovery (M = 14.76, SD = 1.78; t(126) = 2.79, p = .006, CI [.29, 1.73]). In addition to being more likely to have a prolonged recovery, younger patients tended to have higher scores for fear of pain (r(126) = −.18, p = .039). Age is significantly related to scores such that younger patients are more likely to have higher FOPQ score (r = −.18, p = .039).

Other Factors

Approximately 20% of the sample reported experiencing at least one prior concussion (range = 1 – 6). Twelve percent of the patients reported a history of depression or anxiety, and 19% reported a history of a diagnosis of ADHD. Approximately 8% of the patients reported a history of migraines. Sex, insurance type, mental health, concussion, and migraine history were not related to recovery outcomes (days to recovery and prolonged recovery). See Table 1 for summary of study variables in relationship to recovery outcomes and FOPQ score.

Table 1:

Demographic, medical, and physical health factors in relation to FOPQ and Recovery Outcomes

Variable (N) or (M; SD)	Days to Recovery (42.57; 43.72,range : 3–343)	Prolonged recovery (N =73)	FOPQ Total Score (30.13:18.65, range 0–99)
Male (61)	t (120) =.52	χ2 = 1.84	t (126)=.50
Age (14.19; 2.15)	r = −.06	t (126) =2.79**	r = −.18*
History of previous concussion (25)	t (120) = −1.34	χ2 =.11	t (126) =.33
History of anxiety diagnosis (15)	t (120) = −1.71	χ2 = 3.66	t (126) = −.31
History of depression diagnosis (15)	t (120) = −1.06	χ2 =.64	t (126) = .29
History of ADHD diagnosis (24)	t (120) = −.93	χ2 =.36	t (126) = −1.13
History of migraines (10)	t (120) = −2.19	χ2 = 2.34	t (126) = − .95
Private insurance (107)	t (120) = −.17	χ2 =.11	t (126) = 1.70
Symptom severity score at initial visit (27.68; 22.63)	r = .34***	t (126) = −4.24***	r = .16
FOPQ at initial visit (30.13; 18.65)	r = .47	t (126)=−2.18*	--
Positive VOMS at initial visit (102)	t (120) = −3.14**	χ2 = 4.59*	t (126) = −.68

Note:

^*p < .05,

^**p < .01,

^***p < .001; Delayed recovery is defined as ≥ 28 days.

Initial Visit Findings Affecting Recovery

Eighty percent (N = 102) of the patients had a positive VOMS screen at initial visit. Positive VOMS was related to days to recovery such that those with a positive VOMS took significantly longer to recover (M days = 46.71, SD = 46.79) compared to those without (M = 26.52, SD = 23.29; t (120) = −3.14, p = 0.003, CI [−33.44, −6.95]) and were more likely to have a prolonged recovery (χ² = 4.59, p = .03). Symptom-severity score at initial visit was related to both number of days to recovery (r = .34, p < .001) and prolonged recovery (M = 34.32, SD = 24.13) compared to those with recovery < 28 days (M = 18.87, SD = 17.01; t (126) = −4.24, p < .001, CI [−22.64, −8.24]).ⁱⁱ

DISCUSSION

This study is the first, to our knowledge, to examine fear of pain as it relates to recovery from concussion in the pediatric population. Consistent with the adult literature, we found that pediatric patients were more likely to have a prolonged recovery from concussion when they had higher fear of pain. Importantly, a history of anxiety, depression, or ADHD was not associated with recovery outcomes, suggesting that fear of pain may be a unique phenomenon separate from generalized anxiety. These findings emphasize that a history of mental illness alone may not necessarily predispose a child to having a prolonged recovery from a concussion.

Our results were consistent with previous studies indicating that younger athletes take longer to recover than do older adolescent patients.^29–31 There are several theories as to why this is the case, including the stage of brain development when the concussion occurs or age-dependent physiological responses to the concussion.³² In our cohort, younger patients who sustained their first concussion may have inappropriately interpreted exacerbation of symptoms as worsening the injury, possibly leading to fear avoidance behaviors. Similar to previous studies, a high score for severity of symptoms and a positive VOMS on initial visit were additional risk factors for prolonged recovery.³³ Interestingly, our findings did not show a relationship between high scores for severity of symptom and elevated FOPQ scores. This finding also was not consistent with previous findings showing a relationship between positive VOMS and fear of re-injury.¹⁹

Previous studies evaluating fear avoidance after sports-related injuries in the adolescent and adult population looked at fear of physical movement using the Tampa Scale of Kinesiophobia.^19,34 Unlike pain due to musculoskeletal injuries, symptoms related to concussion can be exacerbated by cognitive stress in addition to physical demands, for which the Tampa Scale of Kinesiophobia may not account. The FOPQ assesses not only fear of movement but also the patient’s ability to manage the body’s pain response due to cognitive demands. Several items within the FOPQ related to psychological interpretations of one’s self-efficacy in physical pain management were statistically significantly different for patients with and without prolonged recovery. For instance, the items “I find it difficult to calm my body down when having pain”; “When I hurt I can’t stop thinking about the pain”; and “I can’t think straight when I feel pain” were rated higher at initial appointments by patients who had a prolonged recovery.

Returning to school or learning is a key aspect of managing a pediatric concussion. SRC can affect attention, cognitive speed, and short-term memory that affects learning.³⁵ Headaches are among the most common symptoms seen after a concussion.³⁶ Cogniphobia is similar to fear of pain as it involves avoidance of mental exertion for fear of developing or exacerbating a headache.³⁷ This fear will contribute to diminished cognitive effort and performance, as well as self-imposed restrictions for cognitively demanding activities, leading to increased disability.³⁸

Students do not need to be symptom-free to return to school, and minimizing the length of school absences is beneficial.^39,40 Counseling young patients that concussions are functional injuries may help decrease cogniphobia-related avoidance, especially as cogniphobia has been associated with avoidance of physical activity and traumatic stress.⁴¹

Perhaps the FOPQ could be used as a risk factor for cogniphobia, especially given that items such as “I cannot go back to school until my pain is treated” and “I do not think I will ever be able to go back to a normal school schedule.” were found to be related to prolonged recovery.

Strict physical rest is also not recommended, as it has detrimental effects including worsening anxiety, self-perpetuation of symptoms, and social isolation, which prolong overall recovery.^11,42,43 There is benefit, including reducing recovery time, to performing sub-symptom threshold activities, such as cognitive activities and noncontact aerobic exercise, after a short period of relative rest.^11,44–47 Some elements of fear of pain may mirror the detrimental effects of strict physical rest by affecting willingness to engage in activities of daily living, schooling, and socializing with family and friends, thereby leading to prolonged recovery. Therefore, it is important to identify those patients with elevated fear of pain to work to prevent these consequences.

Initial education and counseling should include expected symptoms, recovery time frame, and acute management to help reduce persistent concussion symptoms.^48,49 In addition, it is important to help patients and families understand the relationship between physical and mental health symptoms and provide counseling for some associated mood and anxiety symptoms that occur in the short term of recovery from concussion.

Moreover, if patients are screened for FOP at their initial sports medicine appointment after sustaining a concussion, patients may benefit from brief clinical interventions to address fear of pain that would reduce severity of symptoms and speed recovery and return to sports. For instance, a brief clinical intervention aimed at psychoeducation about fear of pain and tools for managing pain avoidance, such as exposure and response prevention,⁵⁰ could prove effective. Specific content of these brief interventions could include helping patients to understand the mind-body relationship. Cognitive Behavioral Therapy strategies such as cognitive restructuring, relaxation, and other coping skills⁵¹ could be provided and practiced in sessions with patients so that when they experience post-concussion symptoms they can begin to tolerate and accept some level of discomfort both physically and/or psychologically through their recovery.⁵² Psychoeducation could be given to families, as well, in how best to support patients following a concussion, including emphasizing what a patient is capable of doing instead of focusing on what symptoms they are experiencing and what they should avoid. With guidance from their physicians, parents can also begin to help their children manage symptoms as they are cleared to participate in more activities of daily living and sports.⁵¹ Future clinical research initiatives could target the creation and implementation of brief clinical interventions that could occur immediately after medical visits to determine if these interventions speed recovery and reduce severity of symptoms over time.

There is emergent interest in the role that fear of pain plays in recovery from SRC, but no measurable instrument has been established to evaluate the psychometric properties in the pediatric or adolescent population. Recently, Snell et al,⁵³ developed the fear avoidance behavior after traumatic brain injury questionnaire (FAB-TBI) to evaluate fear avoidance behaviors in adults with mild traumatic brain injury. Further research is needed to evaluate the FAB-TBI’s validity in the pediatric population.

Study Limitations:

Patients were asked to answer the questionnaire only on their initial visit and not on subsequent visits. It is not known if patient’s FOPQ scores changed throughout the recovery process. Normative scores for the FOPQ have, to our knowledge, not been established; therefore, how to categorize patients (i.e., mild, moderate, severe scores) is unclear. Bebe (2021)⁵⁴ did establish moderate and severe scores for the subscales of the FOBQ through statistical, rather than clinical, calculations with a small sample (n=16) for which the Fear of Pain subscale was rated moderate for >20 and severe for >30.2 and Avoidance of Activities subscale was rated >15 for moderate and >25 for severe. Still, given the small sample of that study, we lack confidence in relying on those cutoffs as being normative. An additional limitation of the study is the lack of standardized mental health screening measures; patients reported only whether they had a history of anxiety, depression, or ADHD. A standardized generalized anxiety measure or sports-specific anxiety measure would have been beneficial for helping to differentiate different types of anxiety from fear of pain.

Conclusion

In conclusion, higher fear-of-pain scores on the FOPQ were prospectively associated with prolonged recovery from concussion in a pediatric patient population. Clinicians will benefit from future research examining if fear of pain can be modified with educational interventions and potentially reduce the time to recovery in patients with concussion. SRC is a unique injury, as symptoms are exacerbated by physical, cognitive, and emotional stressors, and recovery has a multifaceted trajectory. It is important for clinicians to evaluate and monitor for maladaptive fears avoidance behaviors (e.g., fear of pain; cogniphobia) throughout the recovery process to most effectively treat patients.