Athletic Fear Avoidance in Athletes Receiving Rehabilitation for Sport-Related Concussion: A Preliminary Study

Abstract

Background:

Fear avoidance after musculoskeletal injury is avoiding activity due to fear of pain and contributes to persistent symptoms, depression, and disability. Little is known about fear avoidance for sport (athletic fear avoidance) in athletes with sport-related concussion (SRC).

Hypothesis:

Athletic fear avoidance after SRC would be elevated at the start of rehabilitation, improve over time, and be associated with postconcussion recovery outcomes.

Study Design:

Observational study.

Level of Evidence:

Level 4.

Methods:

Athletes in rehabilitation after SRC participated. Testing at initial and discharge visits and 6-month follow-up included Athletic Fear Avoidance Questionnaire (AFAQ), Postconcussion Symptom Scale (PCSS), Profile of Mood States (POMS), and Dizziness Handicap Inventory (DHI). Differences were explored in AFAQ score at initial testing based on sex or age (<18 or ≥18 years). Change in questionnaire scores over time was examined. Association of AFAQ score with other questionnaire scores was determined at each timepoint.

Results:

A total of 48 athletes participated: 28 completed initial testing only (INITIAL ONLY), and 20 completed all testing (LONGITUDINAL). Across cohorts, the mean (SD) AFAQ score at initial testing was 24.3 (7.6) points, with no significant difference by sex or age. AFAQ, PCSS, POMS, and DHI scores improved in LONGITUDINAL; the effect size was large from initial to discharge testing (1.0, 1.0, 1.0, and 1.2, respectively) and variable from discharge to follow-up testing (0.52, -0.34, -0.08, and 0.02, respectively). AFAQ scores increased from discharge to follow-up in 3 athletes and were consistently above the mean value in 2 athletes. AFAQ score was significantly correlated to the other questionnaire scores at each timepoint (range, r = 0.36-0.75).

Conclusion:

Athletic fear avoidance was elevated at the start of SRC rehabilitation, improved over time in most patients, and was associated with postconcussion symptoms, mood, and disability.

Clinical Relevance:

Athletic fear avoidance may impact recovery after SRC.

Sport-related concussion (SRC) is a mild traumatic brain injury in athletes caused by biomechanical forces directly to head or impulse through the body. ²⁶ SRC results in a host of clinical signs (eg, loss of consciousness, amnesia, neurological deficits), symptoms (eg, headache, dizziness, fogginess), and disturbances in function (eg, altered gait and balance or intolerance of exercise or physical activity) that vary from person to person.^10,26 Clinical recovery is considered complete when the neurological examination is normal and postconcussion symptoms and functional assessments have returned to baseline status. ²⁶ Many of the athletes who sustain SRC meet these criteria within 2 weeks of injury ²¹ ; however, the remaining 25% to 30% continue to report symptoms and require clinical care at 4 weeks postconcussion or longer.^13,21,39,44 Understanding why recovery after SRC is delayed in some athletes is important as it can negatively affect their health-related quality of life.^11,43

Aside from ongoing neurophysiologic and neuroanatomic changes in the brain,^7,19 protracted recovery could be related to psychological factors.^{5,22,35,36,43} An “anxiety/mood” subtype of SRC has been identified and is typified by ruminative thinking, hypervigilance, anxiety, panic, depressed mood, apathy, sleep disruption, and symptom endorsement on psychological inventories. ³⁶ Interestingly, many of the characteristics align with the fear avoidance model for chronic pain development after musculoskeletal injury. ²³ According to the model, patients who perceive musculoskeletal injury related pain as a threat will catastrophize the pain (ie, magnification and ruminative thinking) and exhibit pain-related fear avoidance behavior (hypervigilance and kinesiophobia), resulting in disuse, disability, and depression. ²³ It is therefore plausible that fear avoidance underlies the development of persistent symptoms after SRC.

Studies have begun to show the relevance of the fear avoidance model in people with concussion. Experiencing symptoms for >3 months after mild traumatic brain injury was found to be associated with symptom catastrophizing. This in turn was associated with elevated cogniphobia (fear of cognitive activity), which has been linked to depression, disuse, and functional disability.^38,41,42 Cogniphobia is a form of fear avoidance behavior. Subjects in these studies were older than the typical age of athletes with SRC, and testing was conducted months or years after injury. However, a recent study in athletes with SRC found that those with elevated kinesiophobia - another form of fear avoidance - at the initial clinical visit had a higher symptom score than those with lower kinesiophobia; yet, there were no group differences in the time to medical clearance or in the symptoms score at medical clearance. ³ These studies support further examination of fear avoidance in athletes with SRC.

Athletes who experience persistent symptoms after SRC may be referred to rehabilitation for vestibular therapy, musculoskeletal management of the cervical spine, aerobic exercise, and/or a sport-specific return to activity progression.^14,20,26,34 Fear avoidance is not assessed or addressed routinely in typical SRC rehabilitation.^26,34,38 The purpose of this study was to examine athletic fear avoidance and its association with postconcussion symptoms, mood disturbance, and disability in athletes receiving rehabilitation for SRC. It was hypothesized that athletic fear avoidance would be elevated at the start of rehabilitation, improve over time, and be associated with more severe symptoms, mood disturbance, and disability in athletes with SRC.

Methods

Subjects

Athletes aged 15 to 30 years who were evaluated by a physician or neuropsychologist and referred to rehabilitation within a multidisciplinary sports concussion program were eligible to participate in this study. Exclusion criteria included a lack of intention to return to sport participation within 6 months after completing physical therapy or an inability to fully participate in exertion activity. Adults who agreed to participate in the study gave written informed consent, while minors gave written assent and a parent or guardian provided written consent, on a form approved by the Institutional Review Board at the University of Minnesota.

Study Protocol

Demographic information and questionnaire responses were collected at the initial visit, discharge from rehabilitation, and 6 months after discharge (follow-up). Questionnaires were Athletic Fear Avoidance Questionnaire (AFAQ), Postconcussion Symptom Scale (PCSS), Profile of Mood States (PMD), and Dizziness Handicap Inventory (DHI).

Demographic Information

Demographic variables included age, sex, body mass index (BMI), history of previous concussions, psychological disorder, attention deficit-hyperactivity disorder/learning disability, migraine, oculomotor disorder, and car sickness.

Rehabilitation

Six physical therapists with board certification as orthopaedic clinical specialists and postgraduate training in vestibular therapy provided rehabilitation. A standard evaluation consisted of tests and measures for the vestibular, oculomotor, and musculoskeletal systems (Table 1). An impairment was considered present if symptoms and/or an abnormal result were revealed during the examination. A formal exertion tolerance assessment was performed at the initial visit only if impairments in these systems were mild or absent.

Table 1.

Overview of physical examination and typical interventions in SRC rehabilitation

Assessment	Test or Measure	Typical Interventions
Vestibular system	• Vestibulo-ocular reflex • Vestibulo-ocular reflex cancellation • Computerized dynamic visual acuity test • Gaze stabilization test	• Adaptation/habituation exercise • Motion sensitivity retraining
	Benign paroxysmal positional vertigo assessment (Dix-Hallpike or Roll test)	Repositioning maneuver
Oculomotor system	• Saccades • Smooth pursuit • Nearpoint convergence	• Oculomotor exercises • Referral to vision therapy when indicated
Musculoskeletal system	• Upper cervical spine ligamentous stability screening • Cervical and thoracic ROM • Joint mobility • Joint position sense • Strength/endurance	• Manual therapy • Cervical strengthening • Flexibility exercise • Neuromuscular re-education
Exertion tolerance	• Buffalo concussion treadmill test • Sport-specific functional activities • Standardized functional exertion assessment	• Graded aerobic exercise • Sport-specific functional activities • Resistance training

ROM, range of motion; SRC, sport-related concussion.

The treatment plan addressed the impairments identified. Typical rehabilitation interventions are summarized in Table 1. It is common for concussed athletes to have impairments in more than 1 system. In these instances, the individualized pragmatic approach was taken with prioritization of the more involved system. Rehabilitation in the first week to 10 days after concussion often prioritized cervical spine management since athletes often cannot tolerate vestibular/oculomotor exercises due to symptom provocation. Thereafter, impairments of the vestibular and oculomotor systems were often prioritized, as these impairments often affect the ability to move. Patients were reassessed at subsequent visits to document impairment resolution and/or inform the ongoing treatment plan. Criteria for discharge included resolution of vestibular, oculomotor, and musculoskeletal impairments; and asymptomatic status with strenuous physical exertion including the Buffalo concussion treadmill test and sport-related conditioning drills. The time from concussion to initial rehabilitation visit, impairments at initial visit, number of rehabilitation visits, and rehabilitation duration were recorded.

Questionnaires

Fear avoidance related to sport injury was assessed with the 10-item AFAQ. ¹² Example items are “I will never be able to play as I did before” and “I worry if I play too soon I will make my injury worse.” Each item is scored on a 5-point scale (5, completely agree; 1, not at all). Total score ranges from 10 to 50 points, and a higher score indicates a higher level of fear avoidance. The questionnaire has good internal consistency (α = 0.805), and concurrent validity has been established with the pain catastrophizing scale and fear avoidance belief questionnaires. ¹² Minimal clinically important difference (MCID) and minimal detectable change have not been established for AFAQ.

Postconcussion symptoms were reported on the 22-item PCSS, which is part of the Sport Concussion Assessment Tool, fifth edition. ⁹ Example items include headache, trouble falling asleep, irritability, feeling more emotional, and difficulty remembering. Each item is scored on a 7-point Likert scale (0, none; 6, severe). The symptom score is the number of items out of 22 with a score >0. The severity score is the sum of the score on each item, with a range from 0 to 132 points. A higher severity score represents greater symptom severity. Internal consistency for this measure is reported to be high (r = 0.88-0.94). ²⁷ MCID is 6.8 points with an 80% CI.^2,24

Mood disturbance was measured with the 40-item abbreviated POMS, which contains subscales for tension, anger, fatigue, depression, esteem-related affect, vigor, and confusion. Each item is scored on a 5-point Likert scale (0, not at all; 4, extremely). The POMS-total mood disturbance score is a measure used to indicate the overall mood state and it is calculated by summing up the negative subscale values including tension, anger, fatigue, depression, and confusion, then subtracting the summed values from the 2 positive subscales (esteem-related affect and vigor) and a constant of 100 was added to be consistent with previous literature. ¹⁷ Scores range from 56 to 216 points, and higher scores indicate greater mood disturbance. Internal consistency of the questionnaire is reported to be good (α = 0.798), and the validity has also been established. ¹⁷ MCID has not been established for POMS.

The 25-item DHI measures the self-perceived level of disability associated with dizziness in physical, emotional, and functional domains. Each item has 3 response levels (0, no; 2, sometimes; 4, always). The total score ranges from 0 to 100 with a higher score indicating greater perceived disability associated with dizziness. Content validity, construct validity, and criterion validity have been established in vestibular disorder population.^18,33 Excellent test-retest reliability (r = 0.97), and internal consistency (α = 0.89) have been reported. ¹⁸ MCID is 18 points at 95% CI. ¹⁸

Statistical Analysis

This was a pilot study of athletic fear avoidance in the SRC population. The target enrollment was initially set at 30 patients to detect a correlation between AFAQ score and scores on the concussion recovery questionnaires of at least r = 0.5 with 80% power and P < 0.05 (https://sample-size.net/correlation-sample-size/). However, the study was disrupted due to COVID-19, and it was decided when research operations resumed to halt the study and move to analysis due to the novel line of inquiry.

Analyses were conducted with SPSS Version 29 (IBM SPSS Statistics). Descriptive statistics were generated for demographic variables, rehabilitation variables, and questionnaire scores. Demographic variables were compared between athletes who completed initial testing and were missing data at the other timepoints (INTITIAL ONLY) and those who completed all testing (LONGITUDINAL) using independent samples t test or chi-square test, as appropriate. Statistical significance was set at P < 0.05.

Normality of questionnaire scores was examined with Kolmogorov-Smirnov test, and non-normal distribution was found in multiple questionnaires at different time points. INITIAL and LONGITUDINAL were combined to explore differences in AFAQ score based on sex or age (<18 and ≥ 18 years) using chi-square test. Change in questionnaire scores across testing time points was assessed in LONGITUDINAL with Wilcoxon signed rank test. Effect size for the change in questionnaire scores between adjacent time points was calculated with Cohen’s d. Pearson correlation coefficients examined the association of AFAQ score with PCSS, POMS, and DHI scores at each testing timepoint. An effect size or correlation of 0.2 was considered small, 0.5 considered moderate, and >0.8 considered large. ³⁰

Results

A total of 48 athletes with SRC (29 females and 19 males) enrolled in the study. Of these, 28 athletes were in INITIAL ONLY, and 20 athletes were in LONGITUDINAL (Figure 1). Demographic information is presented in Table 2. The cohorts were not significantly different in age, sex, or BMI (P > 0.05); however, the time from injury to rehabilitation, number of physical therapy visits, and physical therapy duration were higher in INITIAL ONLY (P < 0.05). Most athletes (90%) had impairments in >1 system. Only 5 of 48 athletes completed exertion assessment at the initial visit, with 2 athletes demonstrating exertion impairment.

Figure 1.

Participant flow. SRC, sport-related concussion.

Table 2.

Demographic and rehabilitation variables

Variable		INITIAL ONLY (n = 28)	LONGITUDINAL (n = 20)
Age, y [range]		17.3 (2.6) [15, 25]	17.1 (2.7) [15, 27]
Sex, n		17 Female 11 Male	12 Female 8 Male
BMI, kg/m2		24.3 (5.7) [16.9, 45.2]	24.0 (4.0) [19.1, 34.8]
Past medical history, n (%)	Concussion	17 (61)	13 (65)
	Psychological	6 (21)	3 (15)
	ADHD/learning disability	5 (18)	5 (25)
	Migraine	11 (39)	3 (15)
	Oculomotor disorder	8 (29)	5 (25)
	Car sickness	13 (47)	10 (50)
Concussion to initial visit, days [range]		41.8 (45.5) [10, 220]	18.0 (11.6) [7, 56]
Rehabilitation visits, n		4.4 (2.5) [1, 10]	3.0 (1.9) [1, 10]
Rehabilitation duration, weeks [range]		5.4 (4.7) [0.0, 15.9]	2.7 (2.2) [0.0, 9.6]
Impairments at initial visit, n (%)	Vestibular	28 (100)	20 (100)
	Oculomotor	26 (93)	15 (75)
	Cervical spine	20 (71)	8 (40)
	Exertion	2 (7) a	0 b

ADHD, attention deficit-hyperactivity disorder; BMI, body mass index.

Continuous variables are mean (SD) [Range].

^aOnly 2 of 28 patients underwent Buffalo concussion treadmill test at initial visit, and both patients demonstrated exertion impairment.

^bOnly 3 of 20 patients underwent the Buffalo concussion treadmill test at initial visit, and those patients successfully completed the test.

Questionnaire scores are found in Table 3. AFAQ score was higher in INITIAL ONLY compared with LONGITUDINAL (P > 0.05). With both cohorts combined, the mean (SD) AFAQ score was 23.8 (6.7) points. The exploratory analysis revealed no difference in AFAQ score at initial testing by sex or age-group (P > 0.05). In LONGITUDINAL, all questionnaire scores significantly improved over time (P < 0.05). Effect sizes were large from initial to discharge testing for all questionnaires (range, 1.0-1.2). Conversely, effect size from discharge to follow-up testing was moderate and in the direction of improvement for AFAQ, small and in the direction of improvement for DHI, and small and in the direction of worsening for PCSS and POMS. Exploration of individual AFAQ scores showed that scores increased between discharge and follow-up testing in 3 athletes (4, 5, and 8 points, respectively), and in 2 athletes the AFAQ scores were higher than the mean value at each testing time point (Appendix Figure A1, available in the online version of the journal).

Table 3.

Questionnaires scores at initial visit, discharge visit, and 6-month follow-up ^a

Questionnaire	INITIAL ONLY (n = 28)	LONGITUDINAL (n = 20)
		Initial Testing	Discharge Testing	Follow-up Testing	Initial to Discharge Effect Size	Discharge to Follow-up Effect Size
AFAQ, points	26.5 (8.2) [16, 44]	21.0 (5.1)* [10, 34]	17.8 (5.6) [10, 33]	15.3 (6.0) [10, 32]	1.0 [0.5, 1.54]	0.52 [0.05, 0.98]
PCSS symptoms, n	13.9 (5.9) [0, 22]	10.9 (5.2)* [2, 21]	3.6 (3.6) [0, 11]	4.5 (5.7) [0, 20]	1.4 [0.73, 2.0]	-0.21 [-0.65, 0.23]
PCSS severity, points	39.9 (25.4) [0, 95]	22.4 (16.7)* [2, 64]	4.9 (5.5) [0, 20]	9.4 (15.9) [0, 63]	1.0 [0.48, 1.6]	-0.34 [-0.79, 0.12]
POMS, points	110.8 (23.5) [80, 166]	99.2 (14.9)* [75, 142]	82.6 (11.9) [64, 107	83.5 (14.2) [64, 127]	1.0 [0.44, 1.5]	-0.08 [-0.51, 0.37]
DHI, points	34.8 (15.1) [0, 58]	23.6 (14.8)* [0, 50]	5.2 (7.1) [0, 28]	5.1 (7.7) [0, 30]	1.2 [0.61, 1.8]	0.02 [-0.42, 0.46]

^aScores are mean (SD) and [range]. Effect size calculations are value and [95% CI].

AFAQ, Athlete Fear-Avoidance Questionnaire; DHI, Dizziness Handicap Inventory; PCSS, Postconcussion Symptom Scale; POMS, Profile of Mood States - total mood disturbance.

^*Significant change across timepoints (P < 0.01).

At initial testing, the AFAQ score was significantly and positively correlated with PCSS severity (P < 0.01), POMS (P < 0.01), and DHI (P < 0.05) scores with INITIAL and LONGITUDINAL cohorts combined, but no significant correlation was found at initial testing in LONGITUDINAL by itself. In addition, AFAQ score was significantly and positively correlated with POMS and DHI scores at discharge testing and with all questionnaire scores at follow-up testing in LONGITUDINAL (P < 0.05; Appendix Table A1, available online).

Discussion

This pilot study examined athletic fear avoidance and the association with postconcussion symptoms, mood disturbance, and disability in athletes receiving rehabilitation after SRC. As hypothesized, AFAQ score was elevated at initial testing and improved (decreased) significantly over time. Also, AFAQ score was associated significantly with PCSS, DHI, and POMS scores at initial and follow-up testing and with DHI and POMS scores at discharge testing. The direction of association was for higher fear avoidance to be associated with worse postconcussion symptoms, mood disturbance, and disability. These findings suggest that athletic fear avoidance is elevated after SRC and associated with SRC recovery.

Results of this study contribute to emerging literature on athletic fear avoidance. The magnitude of the AFAQ score at the initial visit approximates the score in athletes with musculoskeletal injury (21.8-26.0 points).^{12,15,25,31,32} This finding affirms research that has shown similarities in the psychological response of athletes with concussion or musculoskeletal injuries. ⁴⁰ In LONGITUDINAL, the mean AFAQ score decreased over time, which has been reported in athletes with musculoskeletal injury. ²⁵ However, AFAQ scores increased in 3 athletes (15%) between discharge and follow-up and 2 athletes had AFAQ scores higher than the mean value at all timepoints. An increase in fear of reinjury and fear avoidance is common when the return to sport participation is imminent,^6,8 and it is possible that these athletes might require a different treatment approach. ⁴ The effect size for change in AFAQ score from initial to discharge testing and discharge to follow-up testing were large (1.0) and moderate (0.52), respectively. Because MCID has not been established for AFAQ, it is unclear what amount of increase or decrease in score has clinical relevance. Regardless, it appears important to measure athletic fear avoidance serially because it can change over time.

Correlations of athletic fear avoidance with postconcussion symptom severity, disability, and mood disturbance align with correlations of fear avoidance with physical and mental function in patients with musculoskeletal injury,^16,25 and the mild traumatic brain injury population.^38,41,42 No correlation was found at initial testing in LONGITUDINAL only, in part because several questionnaires had less variation in the scores. The magnitude of correlations increased over time, possibly because athletic fear avoidance becomes more relevant when athletic activity is imminent. ⁶ Sport participation was not tracked in this study; therefore, it cannot be ascertained to what degree sport participation was performed in the follow-up time interval. These data suggest that athletic fear avoidance coexists with poorer recovery and may be a rehabilitation target.

It is important to recognize that AFAQ is based on the fear avoidance model, which was created to explain the development of chronic pain. ²³ As such, AFAQ includes questions regarding pain. Based on the results of this study, the fear avoidance model has relevance to the SRC population as it does for athletes with musculoskeletal injury. Fear avoidance could be triggered by injury-related fears besides fear of pain. ³⁰ Future research can ascertain injury-related fears after SRC and evaluate how these contribute to athletic fear avoidance to better understand the specific needs of the SRC population. Moreover, future research may determine if any patient characteristics impact athletic fear avoidance after SRC.

Current standard of care after SRC does not involve routine assessment and treatment of athletic fear avoidance. ²⁶ Psychological factors such as athletic fear avoidance and psychological readiness for sport are emerging as contributors to secondary injury and reduced physical function in athletes with musculoskeletal injury.^15,29 Based on these findings, addressing athletic fear avoidance may also be important from physical function and injury prevention perspective in athletes recovering from SRC. Various interventions, such as cognitive behavioral therapy, meditation, yoga, and relaxation, have been shown to be effective in improving psychological outcome and postconcussive symptoms in the acute and chronic stages after concussion; however, further research is needed to improve the quality of the evidence.^1,28,37

Limitations

A primary limitation of this study is the small sample size, which does not allow robust statistical analysis, such as multifactorial modeling or analysis of fear avoidance based on other patient characteristics. This study focused on athletes referred for rehabilitation after SRC; it is unknown how fear avoidance is acutely after SRC, and results may not generalize to those athletes who show symptom recovery in a shorter time span. Rehabilitation was not controlled in this study and so it cannot be ascertained if any intervention had a direct effect on athletic fear avoidance.

Conclusion

Athletic fear avoidance was elevated in patients with SRC at the start of rehabilitation and generally decreased over time, except in some patients. Athletic fear avoidance was associated with postconcussion symptoms, mood disturbance, and disability. These findings support further inquiry into athletic fear avoidance after SRC, including treatment modifications for athletes with high athletic fear avoidance after SRC.