Brain Injury, November 2009; 23(12): 956–964

Active rehabilitation for children who are slow to recover followingsport-related concussion

ISABELLE GAGNON1,2, CARLO GALLI1, DEBBIE FRIEDMAN1, LISA GRILLI1, &GRANT L. IVERSON3

1Montreal Children’s Hospital, Montreal, Canada, 2McGill University, Montreal, Canada, and 3University of

British Columbia and British Columbia Mental Health & Addiction Services, Vancouver, Canada

(Received 25 February 2009; revised 29 August 2009; accepted 27 September 2009)

AbstractPrimary objective: To present an innovative approach to the management of children who are slow to recover after a sport-related concussion.Research design: The article describes the underlying principles and the development of specific interventions for a newrehabilitation programme as well as preliminary data on pre- and post-rehabilitation changes in outcome measures.Methods and procedures: Development of the intervention was done using multiple perspectives including that of theliterature, of experts in the field of traumatic brain injury and of experienced clinicians involved with the paediatric andadolescent MTBI clientele. A logic model was developed providing sound theoretical background to the intervention. Theintervention was implemented and evaluated with a sample of 16 children and adolescents.Main outcomes and results: The presented cases suggest that involvement in controlled and closely monitored rehabilitation inthe post-acute period may promote recovery in children and adolescents who present with atypical recovery following aconcussion. All 16 of the children and adolescents who participated in the programme experienced a relatively rapidrecovery and returned to their normal lifestyles and sport participation.Conclusions: A gradual, closely-supervised active rehabilitation programme in the post-acute period (i.e. after 1 monthpost-injury) appears promising to improve the care provided to children who are slow to recover.

Keywords: Concussion, mild traumatic brain injury, paediatric, rehabilitation, sports

Introduction

Sport-related concussions (i.e. mild traumatic braininjuries (MTBI)) occur fairly commonly, particularlyin football, soccer, rugby and hockey [1–3]. Themajority of the literature to date suggests thatathletes recover quickly from concussions, withsome recovering in 1–2 days and most recoveringwithin 7–10 days [4, 5]. There is concern, however,that concussions in children might be different [6]and might be associated with slower recovery.Professionals providing services to children andadolescents after a concussion have long recognizedthe need for coordinated care for this clienteleand, particularly, the need for individualized

interdisciplinary management of the paediatric ath-lete who sustains a concussion [7–10]. More focusedand specific research with children has been recom-mended [11, 12].

Agreement statements developed by governmentalorganizations [13], professional associations [10, 14]and research groups [11] set forth the recommen-dation that athletes, including children, should beasymptomatic at rest prior to engaging in physicalexertion. Without question, these agreement state-ments are designed to protect the health and welfareof the athlete, reduce the likelihood of the athleteexperiencing a set-back in the recovery process andminimize the chances that the athlete will be

Correspondence: Isabelle Gagnon, Montreal Children’s Hospital-McGill University Health Center, Trauma Programs, C-833, 2300 Tupper, Montreal,Canada, H3H 1P3. Tel: 514-412-4400 x23422. Fax: 514-412-4398. E-mail: isabelle.gagnon8@mcgill.ca

ISSN 0269–9052 print/ISSN 1362–301X online ! 2009 Informa Healthcare Ltd.DOI: 10.3109/02699050903373477

returned to sport prematurely and experience anoverlapping injury. The recommendation that ath-letes avoid exercise until completely asymptomatic atrest works well for most injured athletes, most of thetime. However, when athletes are very slow torecover, there is a risk that their symptoms anddeficits (cognitive, motor) will (1) become chronicand (2) be caused in whole or part by factors thatmight not be directly related to the neurobiology ofthe original concussion. Moreover, from a practicalperspective, it is very difficult to ensure that mildlysymptomatic children will not engage in physicalexertion (e.g. vigorous playing and running).Therefore, children and adolescents with persistentsymptoms represent a unique challenge to healthcareproviders.Over the past 2 years, clinicians at the Montreal

Children’s Hospital Trauma Programs have beendeveloping an individualized approach with paedia-tric athletes who sustain concussions and are slowto recover. The Montreal Children’s HospitalRehabilitation After Concussion (MCH-RAC) pro-gramme consists of gradual, closely monitored phys-ical conditioning, general coordination exercises,visualization, as well as education and motivationactivities. These are performed in the presence ofpersistent symptoms in order to contribute to theirresolution as well as to improve children’s generalphysical condition and mood. The programme isindividualized and is designed to last until completesymptom resolution at rest. At that time, children andadolescents are eligible to resume the standard returnto activity protocols, part of the Montreal Children’sHospital MTBI/Return to Sports Program. Othergroups, working with an adult population, have alsodescribed similar approaches in the domain of reha-bilitation post-concussion with both athletes andnon-athletes [15, 16].The purpose of this paper is to present an

innovative approach to the rehabilitation of childrenwho are slow to recover after a sport-relatedconcussion. The article describes the principlesunderlying the MCH-RAC as well as its interventionmodalities. A series of cases concerning the impact ofthis rehabilitation strategy on the resolution of post-concussion symptoms as well as children’s perspec-tive on their experience with the intervention willalso be discussed.

Development of the intervention andunderlying principles

Designing successful interventions requires theunderstanding of challenges facing the targetedpopulation as well as elements on which one canhope to have an impact. Three broad principles were

used to guide the design of the MCH-RAC: (1) thenon-specificity of post-concussion symptoms, (2) themulti-dimensional impacts of injury on athletes and(3) the effects of exercise as an interventionmodality.

First, post-concussion-like symptoms are non-specific [17–19]. They can be associated with avariety of things, such as school-related stress,relationship stress, mild depression, anxiety condi-tions, Attention-Deficit Hyperactivity Disorder(ADHD) and sleep disturbances. Therefore, thelonger the athlete is symptomatic the more likely,statistically, that some of the symptoms will becaused or maintained (at least in part) by factorsother than the neurobiology of the concussion.

Secondly, athletes can have adverse psychologicalreactions to being injured and to being kept out ofsports [20–24]. These psychological reactionsinclude denial, mild depression, anxiety, worry,anger, diminished vigour, loneliness, worthlessness,impatience and general overall negativity [25].According to models of psychological reaction tosport injury, these reactions are mediated in part bypersonal and situational factors, but also on cogni-tive appraisal of the situation [24]. These psycho-logical reactions can underlie what appear to bepost-concussion symptoms, especially when thesymptoms persist for several weeks. Moreover,improvement in the psychological condition of thephysically injured athlete (not concussed athlete) isassociated with perceived progress in rehabilitation[26, 27].

Thirdly, there is evidence that exercise has positiveeffects on mental health and that it could be used asa treatment for depression in adults [28]. There isalso evidence that depressed mood after a concus-sion could reflect pathophysiology consistent witha limbic-frontal model of depression [29, 30].Therefore, it is possible that exercise could have abeneficial effect on symptoms in children if theirsymptoms are related to depressed mood or mentalhealth issues. Furthermore, there is evidence in theanimal literature that exercise is good for the brainand promotes neuroplasticity, even after fluid-percussion induced MTBI in rats [31, 32].However, there appears to be a temporal windowin which exercise does not promote neuroplasticityand the literature suggests that exercise could,theoretically, slow down recovery if done too soonafter injury [33]. In fact, the molecular markers aresuppressed if the injured rat is allowed to engage involuntary exercise during the first week post-injurybut not in the post-acute phase (3–4 weeks post-injury). Most children and adolescents do notreceive follow-up interventions beyond the initialmanagement period, even though their deficits(balance, response time, cognitive) may last up to

Rehabilitation after concussion 957

3 months [34–36]. Furthermore, for the group ofindividuals who fail to return to pre-injury statusafter the expected initial recovery period, treatmentrecommendations usually are broad, do not suggestspecific evidence-based interventions and are notvery helpful to the professionals who have todetermine the best way to address the needs ofthese children.Starting from these principles, a systematic search

of the English and French literature on paediatric andadolescent MTBI as well as on exercise-inducedchanges to neurological function performed using thefollowing six databases: MEDLINE (1980–2008),CINHAL (1982–2008), ERIC (1980–2008),PsychINFO (1980–2008) and SportsDiscus (1980–2008). This review led to the theoretical rationale forthe components of the programme set out in Table I.

The MCH-RAC

The Montreal Children’s Hospital (MCH) is atertiary care paediatric teaching Hospital affiliatedwith McGill University in Montreal, Canada. It isone of two designated paediatric Trauma centres inthe Province of Quebec, Canada. The MCHTrauma mandate consists of five different pro-grammes (Trauma, Neurotrauma, MTBI/Return toSports, Burns and Injury Prevention). The manage-ment of children who sustain a concussion within theinstitution is a comprehensive multilevel programme

involved with children who require admission to thehospital and for those who are cared for directly inthe Emergency Department (ED) or on an out-patient basis when referred from community part-ners (paediatricians, family doctors, schools andsports teams).

The physician in the MCH-ED uses a standar-dized form to assess children presenting withconcussion. This form was designed to ensure thatall injury variables useful for diagnostic and prog-nostication purposes are collected systematically.The form also contains clear criteria for referral tofurther services, namely the MCH NeurotraumaProgramme, following discharge from the ED, usu-ally after a few hours of assessment/observation.Before leaving the ED, children receive standardeducation and documentation regarding the natureof the injury, reassurance and instructions for returnto school and physical activities, as well as contactinformation should they need further information.For those children referred to the NeurotraumaProgramme (see Table II), follow-up phone callsensure individualized education/information andreturn to activities instructions.

The MTBI/Return to Sports Clinic is part ofthe MCH Trauma Programs and was created toprovide children and adolescents with the opportu-nity to follow a closely monitored, stepwise pro-gramme to ensure that their return to sport andschool is a positive and safe one. Children seen in thecontext of this clinic are at least 7 years old and belongto one of two categories: elite athletes (defined aspracticing more than 8 hours of competitive levelsports per week) and children who are slow torecover, defined here as presenting with symptomsor impairments lasting more than 4 weeks (Figure 1).The latter slow to recover group is the focus of thispaper.

Intervention

The MCH-RAC programme is therefore an inter-vention for children and adolescents who do not

Table I. Theoretical rational for the Montreal Children’sHospital Rehabilitation After Concussion (MCH-RAC)Programme.

I. Aerobic ActivityIncrease brain-derived neurotrophic factor (BDNF)SynaptogenesisIncreased cardiovascular activityAltered cerebral vascular function and brain perfusionIncreased endorphin releaseImproved brain autoregulationImprove overall fitness levelReduce fatigue/improve energy levelsReduce stress, worry and anxietyImprove moodImprove cognitionImprove self-efficacy and performance

II. Coordination/Skill Practice (Enjoyed Activity)Increased endorphin releaseImprove mood

III. Visualization of Positive and Successful Activities Related toPreferred Physical Activity

Reassurance and increased confidence relating to ability topractice sport

Activated brain regions linked to motor activitiesImprove self-efficacy and performance

IV. Education and MotivationEducation and reassurance leads to empowerment andimproved coping

Increased confidence in services provided

Table II. Criteria for referral to the Montreal Children’s HospitalNeurotrauma Programme.

Prolonged loss of consciousness (>1 minute) at time of injuryConcussive convulsionsSkull fracturePatients given Miami-J collar to rule out neck injuriesPersistent symptoms with no improvement lasting >1 weekPersistent deficits or cognitive impairmentsMultiple concussions (>2 in the same year) or occurring with less

impact forcesElite athletes (practice >8 hours/week competitive sport)Delayed Emergency Department visit with confirmed skull

fracture

958 I. Gagnon et al.

recover in the initial days or weeks following theinjury, either because they may have a more severeinjury than initially thought or they may present withpre-injury characteristics placing them at risk ofdeveloping more chronic symptoms.Before being considered eligible for this interven-

tion, children undergo an evaluation by theNeurotrauma Program Coordinator of the MCH.Following this initial evaluation, they are providedwith standard education and reassurance material,ongoing telephone follow-up, as well as referrals toany other services (e.g. neuropsychology, schoolservices, neurology or neurosurgery) thought to benecessary for their condition. All children are alsorequired to have been evaluated by a physician, mostoften in the MCH ED, where an algorithm is inplace to ensure a coherent and consistent approachin the medical management of these cases.Prior to their entry into the MCH-RAC pro-

gramme, children complete several assessment mea-sures. These measures include: (1) standardneurological and physical examination, (2) balance,using the Bruininks-Oseretsky Test of MotorProficiency (BOTMP-2) [37] and in some cases

the Balance Error Scoring System (BESS) [4],(3) coordination testing using the BOTMP-2 and(4) a post-concussion symptoms checklist [38].

After the assessment, they initiate a gradedrehabilitation, as presented in Figure 2. They beginwith sub-maximal (50–60% maximal capacity) aer-obic training either on a treadmill or a stationarybicycle for up to 15 minutes. Children are thenintroduced to light coordination exercises that aretailored to the child’s favourite or main sport. Forexample, basketball players will be introduced tolight coordination drills including ball activities andfootwork as used in usual sports practices. These willbe performed for up to 10 minutes. The purpose ofthese exercises is to continue light aerobic activitiesbut also to reintroduce familiar activities in asuccessful context, one of the means of increasingself-efficacy. Self-efficacy is a key element of perfor-mance and satisfaction with the practice of physicalactivities [39, 40] and found to be decreased follow-ing concussion [41]. Children are monitored closelyfor any increase in symptoms during the physicalactivities. An increase in symptoms is the pointwhere activities are stopped.

-Return appointment for re-evaluation

-Education and weekly follow-up

Remains symptom free

Gradual return to sports guidelines

Referral to Concussion/Return to Sports clinic(team members include: trauma coordinator, clinic coordinator, physiotherapist, psychologist, neurosurgeon, other

consultants as needed)

Physical and cognitive exertion testing

Initial evaluation:History, physical, and appropriate cognitive

evaluation

Elite athletes symptom free at rest for 1 week

Children with slow recovery

Initial evaluation:History, physical, and appropriate

cognitive evaluation

Asymptomatic for 1 week

-Graded rehab (MCH-RAC) until asymptomatic for 1 week

-Management by team: PT, psychologist, MD, etc.

Discharge from clinic

Gradual return to sports

NoYes

Figure 1. The MCH MTBI/Return to Sports Clinic. Children seen in this clinic belong to one of two categories: Elite athletes (defined aspracticing more than 8 hours of competitive level sports per week) and children who are slow to recover, defined here as presenting withsymptoms or impairments lasting more than 4 weeks.

Rehabilitation after concussion 959

Throughout the aerobic and coordination phase ofthe intervention, children and parents are providedwith education, reassurance and motivation toaddress knowledge, attitudes and behaviourstowards the injury and further normalize theirsituation to facilitate recovery. They are also taughtsport-specific visualization and imagery techniques.This is also thought to improve confidence and self-efficacy towards the ability to recover as well as toreturn to sports/activities.The final but essential phase of the MCH-RAC

intervention is the inclusion of a home programmedesigned to allow children to continue trainingoutside the clinic, thus facilitating school attendanceand minimizing disruptions to their daily life. Thehome programme consists of sub-maximal aerobictraining and coordination exercises, chosen amongthe child’s usual activities, for the duration the childwas able to tolerate without his symptoms increasingduring the supervised session. The child and parentsare also instructed to interrupt the home session andcontact the Neurotrauma Programme if any deteri-oration occurs. Finally, the child is followed weeklyand this goes on until he or she reports beingsymptom-free at rest for 1 week. At that time, thechild enters the standard return to activity protocol,including exertion testing and graded returnto activities. A schematic representation of theprogramme is presented in Figure 2.

Case studies

In an initial effort to assess the process and impact ofthe intervention, the authors reviewed the outcome

of the children who had received the interventionduring the first 17 months of its implementation.This was completed as part of an evaluative processaiming to review new interventions within the MCHTrauma Programmes.

Participants

All children/adolescents aged 10–17 years whosustained a concussion and experienced post-concussion symptoms for more than 4 weekspost-injury were seen in the initial months ofimplementation of the MCH-RAC at the MontrealChildren’s Hospital. They were followed prospec-tively for the duration of their involvement in theprogramme. All children had been referred tothe programme after having been seen by a physicianand, for some of them, by a concussion clinicelsewhere. The reason for their referral was theincomplete resolution of their symptoms after theexpected recovery period.

Data collection

The MCH Trauma Programs maintain a centraldatabase of all children and adolescents referred forservices, whether admitted to hospital or treatedsolely in the ED. The medical records of all childrenseen in the MCH-RAC programme between 1 July2007 and 15 December 2008 were reviewed afterInstitutional authorization was obtained. For eachchild, data was collected using a standardized formby a single investigator. Variables of interestincluded information about the injury sustained,course of recovery, time of referral to MCH-RACprogramme, assessments done in rehabilitation and

Figure 2. Schematic representation of the MCH-RAC programme.

960 I. Gagnon et al.

course while in the MCH-RAC until recovery anddischarge.

Results

Over the initial 17 months of implementation, 142children were seen in the MTBI/Return to Sportsclinic. A total of 16 children and adolescents withslow recovery were seen in the MCH-RAC pro-gramme over the covered period. This correspondsto 11.2% of children and is consistent with thereported prevalence of persistent symptoms in theliterature [42]. A summary of the children’s char-acteristics is presented in Table III. Children wereable to participate in 5–15 minutes (mean9.3 minutes) of aerobic activity at their initial visitbefore an increase in symptoms was reported. Thistolerance gradually increased over time with a meanof 12.2 minutes at the second visit and of14.2 minutes at the third visit.Children reported being motivated to engage in

physical activities after the rest period imposed onthem following their injury. All participants forwhom data were collected showed significant andrapid improvement of symptoms. Indeed, the meanPost-Concussion Scale-Revised Score [43] at initialassessment was 30.0 (SD!20.8) and decreased to6.7 (SD! 5.7) at discharge from the programme. Allchildren were able to resume their normal physicalactivity participation at the end of the programme.Mean duration of the MCH-RAC intervention was

4.4 (SD! 2.6) weeks after a mean of 7.0 (SD! 4.1)weeks of persistent symptoms. Parents qualitativelyreported high satisfaction with the programme andthe comprehensive nature of the follow-up, empha-sizing the positive impact of the intervention on theirchild’s mood, as illustrated by the following quote:‘. . . it was like there was a light in her eyes, her wholeface changed after the exercise’. Parents alsodiscussed their feelings of empowerment in relationto the active nature of the intervention and the factthat ‘. . . finally something was being done for mychild’.

The results from a single case are presented indetail to illustrate the application of the programme.A 13-year old male soccer player sustained aconcussion in early March 2007. Immediately afterthe hit, he felt dizzy. He did not seek medicalattention at the time. It was only 4 weeks later, aftercontinuing to experience severe headaches andsensitivity to light and sounds that he was seen inthe MCH Emergency Department. A CT scan wasdone (negative). He was given a dose of IVMetoclopramide with some headache relief. Hewas also referred to the MTBI/Return to SportsClinic of the MCH.

He was seen at the beginning of May withcomplaints of persistent headaches since the injury.He often felt very tired and missed playing soccer.He rated his constant headaches at 2–3 on a 10-pointvisual analogue scale. His neurological exam wasnormal, as were his balance and coordination skills.

Table III. Characteristics and outcome of children involved in the Montreal Children’s Hospital Concussion Rehabilitation Intervention(MCH-RAC).

CaseAge

(years) GenderCause ofinjury LOC

Time toMCH-RAC(weeks)

Main complaint atpresentation toMCH-RAC

Duration ofinitial aerobic

session(before increase

in symptoms) (min)

Durationof involvementin MCH-RAC

before resolutionof symptoms

(weeks)

1 16 M Rugby yes 6 Feeling depressed, fatigue 12 62 14 F Soccer no 8 Headache 15 23 17 M Kayak no 5 Feeling depressed, fatigue 8 54 13 M Soccer no 9 Fatigue 15 25 13 M Football no 6 Fatigue 12 26 17 F Cheerleading no 6 Headache 13 37 15 M Hit, assault no 6 Fatigue, headache 12 48 17 F Fall on the street no 4 Headache 8 29 13 F Skiing no 4 Headache 15 2

10 8 M Soccer no 5 Poor endurance 5 511 15 M Hockey no 4 Headache 12 1212 12 M Football no 4 Fatigue, headache 10 413 13 M Hockey no 4 Headache 5 414 16 M Football no 16 Headache 10 815 14 F Soccer no 18 Headache 10 516 15 M Hockey no 7 Headache 9 5

Rehabilitation after concussion 961

Because of current management guidelines thatrequire children to be symptom-free before initiatingreturn to activity protocols, he had been restingfor more than 9 weeks without majorimprovements. After the assessment, he began lightaerobic training on the treadmill at 3.6 kmh"1 for10 minutes (60–70% of max HR). He did notexperience any increase in symptoms and stated thatit ‘felt good to move’. He also began light jumpingdrills as well as 10 pushups. He was sent home withinstructions to continue with 15 minutes of dailylight aerobic activity for 1 week.Five days later he returned to clinic reporting

improvement. Headaches were now only sporadicand rated as 2/10. He reported no increase insymptoms with activity and felt he had moreenergy. After being reassessed (had no symptomsat the time of the visit), he proceeded to the aerobictraining now consisting of 15 minutes of treadmill at3.6 kmh"1. He also performed ball activities specificto soccer and light jumping drills under supervision.He was sent home with instructions to continue with20–30minutes of daily light aerobic activity for1 week. Foot handling drills with ball on his ownwere added to the home programme.His next visit was a month later because he was

studying for exams and could not attend clinic.Throughout that month, phone contacts were doneand rehabilitation had progressed. He had beensymptom-free at rest for more than 1 week andphysical exertion did not trigger symptoms. He wasready to enter progressive return to play protocols, asper concussion management guidelines.

Conclusion

The presented cases suggest that involvement incontrolled and closely monitored rehabilitationin the post-acute period may promote recovery inchildren and adolescents who are slow to recoverfollowing a concussion. The MCH-RAC was createdout of a clinical need to better care for children andadolescents who are slow to recover following aconcussion. It is an individualized interventiondeveloped for children to address persistent symp-toms and other issues related to the injury. All 16 ofthe children and adolescents who participated in theprogramme experienced a relatively rapid recoveryand they returned to their normal lifestyles and sportparticipation. In the recent months, multiple out-come measures were added to the clinical follow-upof these patients in order to better monitor theirmood, anxiety, fatigue level, cognitive abilities andpostural stability. Those outcome measures willfurther enlighten one’s understanding of recoveryin this clientele and allow one to possibly identify

sub-groups of patients for whom the interventionwill be more or less effective.

It is understood that active rehabilitation forchildren and adolescents who remain symptomaticfollowing a concussion is somewhat controversial.Several published agreement statements [10, 11,14, 44] emphasize that athletes should be asympto-matic at rest prior to engaging in exercise.This model works very well for the majority ofinjured children and adolescents. However, a minor-ity have persistent symptoms for many weeks. Forthem, significant lifestyle restrictions, includingavoiding physical activity, can actually contributeto symptom maintenance over time. That is, thelonger a person has symptoms, the more likely it isthat other factors that are separate from or onlypartially related to the neurobiology of the originalinjury are causing or maintaining the symptoms.Thus, at some point, active rehabilitation seemsindicated. Exercise has been shown to have positiveeffects on mood and self-esteem and it promotes ageneral sense of well-being [45–48]. In adults,exercise can be an effective treatment for milddepression [28, 49, 50]. Exercise promotes neuro-plasticity in animal studies [51] and exercise doneafter a period of recovery in animal studies involvingconcussion is also associated with neuroplasticity[31–33]. Active rehabilitation and exercise is usedwith older adults following stroke. Therefore, it isbelieved that a gradual, closely-supervised activerehabilitation programme for children and adoles-cents in the post-acute period (i.e. after 1 month postinjury) is appropriate.

The theoretical rationale presented in this paper(Table I) is presently the object of an external expertconsultation and validation process. This will likelycontribute to further improvement in the interven-tion, ensure solid theoretical bases for its implemen-tation and assist with the preparation of a clinicaltrial to formally investigate the effectiveness of thisapproach with children and adolescents who areslow to recover after a concussion.

Acknowledgements

Part of this manuscript was presented at the 7thWorld Congress on Brain Injury, Lisbon, 2008 andat the 3rd International Conference on Concussionin Sport, Zurich, 2008. Dr Gagnon is presentlyfunded by a Clinician-Scientist Career Award fromthe Fonds de la Recherche en Sante du Quebec.Further development of the MCH-RAC Programis supported by a research grant from the Fonds de laRecherche en Sante du Quebec RehabillitationResearch Network.

962 I. Gagnon et al.

Declaration of interest: The authors report noconflicts of interest. The authors alone are respon-sible for the content and writing of the paper.

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