Dysautonomia after traumatic brain injury: aforgotten syndrome?

Ian J Baguley, Jodie L Nicholls, Kim L Felmingham, Jenelle Crooks, Joseph A Gurka,Lauren D Wade

AbstractObjectives—To better establish the clini-cal features, natural history, clinical man-agement, and rehabilitation implicationsof dysautonomia after traumatic braininjury, and to highlight diYculties withprevious nomenclature.Methods—Retrospective file review on 35patients with dysautonomia and 35 sexand Glasgow coma scale score matchedcontrols. Groups were compared on injurydetails, CT findings, physiological indices,and evidence of infections over the first 28days after injury, clinical progress, andrehabilitation outcome.Results—the dysautonomia group weresignificantly worse than the control groupon all variables studied except duration ofstay in intensive care, the rate of clinicallysignificant infections found, and changesin functional independence measure(FIM) scores.Conclusions—Dysautonomia is a distinctclinical syndrome, associated with severediVuse axonal injury and preadmissionhypoxia. It is associated with a poorerfunctional outcome; however, both thecontrols and patients with dysautonomiashow a similar magnitude of improvementas measured by changes in FIM scores. Itis argued that delayed recognition andtreatment of dysautonomia results in apreventable increase in morbidity.(J Neurol Neurosurg Psychiatry 1999;67:39–43)

Keywords: traumatic brain injury; dysautonomia; auto-nomic dysfunction; dystonia

Alterations in autonomic function are wellrecognised in the acute recovery phase aftertraumatic brain injury. These transient changesinclude 33% of patients with tachypnoea greaterthan 30 breaths/min, 25% with tachycardiaabove 120 beats/min, and 15% with systolicblood pressures above 160 mm Hg.1 However, asyndrome of prolonged episodes of autonomicabnormalities has been reported to follow a widevariety of diVerent cerebral pathologies. Fea-tures of the syndrome include severe, paroxys-mal increases in heart rate, respiratory rate, tem-perature, and blood pressure, with decerebrateor decorticate posturing, increased muscle tone,and profuse sweating. This syndrome has beenvariously termed autonomic dysfunctionsyndrome,2 3 autonomic or sympatheticstorming,3–5 dysautonomia,4 6 brainstem attack,7

hyperpyrexia associated with musclecontraction,8 hypothalamic-midbrain dysregula-tion syndrome,9 acute midbrain syndrome,10 anddiencephalic seizure.11 12 The syndrome willhenceforth be referred to as dysautonomia.

Despite the dramatic presentation of the con-dition, literature reports of dysautonomia aftertraumatic brain injury consist of five papersrecording details of 11 patients (table 1). Giventhe lack of a systematic nomenclature, acomprehensive literature review was performedfor all aspects of altered autonomic function ortone after traumatic brain injury. This processyielded a further six patients in four papers withfeatures consistent with dysautonomia, but inwhom dysautonomia was not identified (table1). These papers focused on isolated aspects ofthe overall syndrome—for example, metabolicexpenditure,13 hypertension,14 early onset dysto-

Table 1 Summary of literature cases of dysautonomia

Author

CaseNo inStudy

Age,Sex GCS

Temp°C

HeartRate/min

BPmm Hg

RespRate/min Posturing Sweating

Outcome(GOS)

Time ofAssessment CT

Rossitch et al2 1 Y Y Y Y Y Y <33 Y Y Y Y N Y <35 Y Y Y Y Y Y 5

Rossitch et al2 11 2 24, M 6 39.6 165 160/100 52 Y Y 4 6 CC, blocked cisterns4 24, M <8 39.6 103 170/80 60 Y Y <3 3 Normal

Boeve et al5 1 17, F <8 42 190 170/− 40 Y Y 3 8 SAH, IVH, CCStrich et al7 1 28, M 5 Y Y 3 8

2 32, F <8 Y Y Y Y 3 44 27, M <8 Y Y Y Y 3 6

Pranzatelli et al9 2 7, M <8 39.3 160 150/105 45 Y Y <3 DiVuse SAH3 19, M <8 40 140 160/115 40 Y Y <3 SAH, generalised oedema

Chiloero et al13 1 26, M 6 155 Y 1 6 SDH, CCSandel et al14 1 17, M 8 Y 130 170/120 N Y Y 4 3 SAH, CCSilver et al15 1 27, M 6 Y Y Y Y Y Y 2-3 12 CC

2 25, F 4 Y Y Y Y Y Y 3 SAH, IVHMeythaler et al16 1 20, F 3 38.9 Y Y 3 Normal

3 15, F 4 40.6 Y Y IVH, DAI

GCS=Glasgow coma scale; BP=blood pressure; GOS=Glasgow outcome score; SAH=subarachnoid haemorrhage; IVH=intraventricular haemorrhage;SDH=subdural haemorrhage; CC=cortical contusion.When available, the values of the various indices are reported. Y=the reporting, but not the severity, of hyperthermia, tachycardia, hypertension, tachypnoea, postur-ing or sweating. N=absence of the symptom. Blank fields are included when data were not reported. Age is in years, time of assessment in months after injury.

J Neurol Neurosurg Psychiatry 1999;67:39–43 39

Brain InjuryRehabilitation Service,Westmead Hospital,Westmead, NSW 2145,AustraliaI J BaguleyJ L NichollsK L FelminghamJ CrooksJ A GurkaL D Wade

Department ofRehabilitationMedicine, Universityof Sydney, AustraliaI J Baguley

Correspondence to:Dr Ian J Baguley, BrainInjury Rehabilitation Service,Westmead Hospital,Westmead, NSW 2145,Australia Telephone 006129845 7941; fax 00612 96358892; emailianb@biru.wsahs.nsw.gov.au

Received 25 October 1998and in revised form23 December 1998Accepted 10 February 1999

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nia after traumatic brain injury,15 and fever ofcentral origin.16

The literature on traumatic brain injury anddysautonomia focuses on small series of casereports or on anecdotal responses to a particu-lar drug therapy. Minimal attention has beenpaid to the natural history, patterns of physi-ological changes, or outcomes of patients withdysautonomia. The limited outcome data(table 1) indicates a poor functional prognosis.Therefore, the aims of this study were to betterestablish the clinical features of dysautonomiain a larger series of patients, to evaluate the rolethat cerebral pathology, infection, and medica-tions have in the aetiology of the condition, andto examine aspects of management and out-come of dysautonomia by comparison ofpatient groups with traumatic brain injury withand without dysautonomia.

MethodsPATIENTS

A retrospective file review was performed on 35patients with traumatic brain injury with dysau-tonomia admitted to a rehabilitation service overa 10 year period. For the purposes of the study,dysautonomia was defined as simultaneous,paroxysmal increases in at least five out of theseven reported features of dysautonomia (heartrate, respiratory rate, temperature, blood pres-sure, posturing, dystonia, and sweating), withepisodes persisting for at least 2 weeks afterinjury. The control group consisted of 35subjects matched for sex and Glasgow comascale (GCS) severity taken from a database of121 consecutive inpatients with severe traumaticbrain injury (maximum GCS score<8 in thefirst 24 hours). Data were recorded on personaland injury related details, clinical progress, andrehabilitation outcome. Day of injury CT wasused to diagnose brain stem and diVuse axonalinjuries. Evidence supporting the diagnosis ofdiVuse axonal injuries included intraventricularhaemorrhage, diVuse cerebral oedema, andmultiple subcortical white matter or brainstemhaemorrhages. Ambulance and emergency de-partment reports were used to determine thepresence or otherwise of preadmission hypoten-sion and hypoxia. Physiological findings, haema-tology, and microbiology reports were reviewedfor the first 28 days after injury. The dates thatmedications, particularly antibiotics, sedatives,and central acting drugs, were started or endedwere also recorded.

STATISTICAL ANALYSIS

Analyses compared the dysautonomia groupand the matched control group on baselinecharacteristics (age, sex, mode, and severity ofinjury), acute physiological and clinical presen-tation (maximum temperature and heart andrespiratory rate, and white blood cell countover a 4 week acute recovery period; thepresence or absence of tone, sweating, postur-ing, diVuse axonal injuries, brainstem injury,and preadmission hypotension and hypoxia)and outcome data (duration of stay in intensivecare unit, rehabilitation and total time inhospital, Glasgow outcome scale (GOS),17

duration of post-traumatic amnesia (PTA; uti-

lising the Westmead PTA scale)18 and func-tional independence measure (FIM)19 scoreson admission and discharge).

All continuous variables were corrected foroutliers and non-normal distributions. Agedistributions were compared using one wayanalyses of variance (ANOVAs) whereas con-tinuous physiological records were analysedwith two way repeated measures ANOVAs withgroup (dysautonomia v control) as the betweenfactor and time (weekly epochs) the within fac-tor. Greenhouse-Geissner corrections wereused to control for sphericity. Ordinal data(GCS, GOS, FIM) were analysed with thenon-parametric Mann-Whitney U test. Cat-egorical data relating to sex and the presence orabsence of clinical features were comparedbetween groups using Fisher’s exact ÷2 test.Finally, the matched control group was com-pared on age, sex, and GCS criteria with thecomplete database of 121 patients with severetraumatic brain injury to test for representa-tiveness of the sample.

ResultsBASELINE CHARACTERISTICS

Table 2 presents the baseline characteristics foreach group. There were no significant diVer-ences between the dysautonomia group andthe matched control group for age, GCS score,sex, or mode of injury. All patients in thedysautonomia group and 34 out of 35 patientsin the control group had closed head injuries.No patient in either group had evidence of spi-nal cord injury. Comparisons between the con-trol group and the complete severe traumaticbrain injury database did not show significantdiVerences in sex (÷2=0.31, p>0.05) or GCSscore (U(1,138)=1.83, p=0.177). A significantdiVerence was found for age (F(1,138)=29.6,p=0.000) with the control mean age of 20.7years significantly younger than the totalsample mean of 35.1 years.

ACUTE PHYSIOLOGICAL AND CLINICAL

PRESENTATION

The figure shows continuous physiologicalrecords for the dysautonomia and matchedcontrol group over the first 28 days after injury.Repeated measures ANOVAs showed thatmaximum temperature (F(1,57)=44.8,p=0.000), heart rate (f(1,59)=51.4, p=0.000),and respiratory rate (F(1,48)=9.1, p=0.004)were significantly higher for the dysautonomiagroup than the control group. These maineVects were qualified by significant time bygroup interactions in each of these measures.Maximum temperatures were significantlygreater for the dysautonomia group in each ofthe four weekly epochs, with maximal groupdiVerences during weeks 2 and 3. Maximum

Table 2 Demographic and injury related data fordysautonomia group and control group

Dysautonomia Control Significance

Mean age (y) 20.5 20.7 NSGCS score (median) 4.0 3.0 NSMale/female ratio 25/10 25/10 NSMode of injury:

Motor vehicle/other 25/10 22/13 NS

40 Baguley, Nicholls, Felmingham, et al

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heart rates were significantly higher in the dys-autonomia group during weeks 2, 3, and 4.Respiratory rates were lower for the dysautono-mia group during the first week, but becamesignificantly higher than controls in weeks 2and 3.

By contrast, the maximum white cell countdid not diVer significantly between groups atany time period (F(1,59)=0.26, p=0.6099).Neither the mean number of microbiologicallyconfirmed infections/patient (dysautono-mia=1.9, control=1.5; F(1,52)=0.86, p=0.36)

nor antibiotic use (dysautonomia=2.7, con-trol=3.0 courses of antibiotics/patient;F(1,53)=0.49, p=0.49) diVered significantlybetween groups.

Table 3 presents categorical data comparingthe presence or absence of clinically relevantsymptoms for each group. Patients with dysau-tonomia presented with significantly greaterreports of sweating, posturing, hypertension,and dystonias during recovery. Brain CTshowed that patients with dysautonomia hadsignificantly greater frequency of diVuse axonal

Physiological indices over the first 4 weeks. Error bars indicate the 95% CI for each index identified.

20.0

16.0

18.0

14.0

12.0

8.0

10.0

286 7 8 9 104 5

Days after injury

M

ean

max

imu

m w

hit

e b

loo

d c

ell

cou

nt

(109 /l)

321 11

DysautonomiaControl

12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27

30

25

20

10

15

286 7 8 9 104 5 M

ean

max

imu

m r

esp

irat

ory

rat

e (

/min

)

321 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27

130

120

110

80

100

286 7 8 9 104 5

M

ean

max

imu

m h

eart

rat

e (

/min

)

321 11

90

12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27

39.0

38.5

38.0

36.5

37.5

286 7 8 9 104 5

Mea

n m

axim

um

tem

per

atu

re(°

C)

321 11

37.0

12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27

Dysautonomia after traumatic brain injury 41

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injuries and brain stem injuries than controls.There were significantly more reports ofpreadmission hypoxia, but not hypotension, inthe dysautonomia group relative to controls.

OUTCOME DATA

Thirty one patients in the dysautonomia grouphad outcome data. Of the remaining fourpatients, two died in hospital, and two remainas inpatients. Table 4 presents outcome datafor the two groups. The dysautonomia grouphad significantly longer rehabilitation and stayin hospital, but not duration of stay in theintensive care unit. The dysautonomia grouphad a significantly greater mean duration ofPTA and greater number of subjects withchronic amnesia (those who do not emergefrom PTA) or who could not be reliably tested.The outcome at discharge from rehabilitationwas significantly worse for the dysautonomiagroup as reflected by scores on both the GOSand the FIM. Change in FIM scores (dischargeminus admission FIM) were calculated for thedysautonomia and control groups. Both groupsshowed functional improvement during reha-bilitation using the FIM as a dependent meas-ure. Mann-Whitney U tests on change in FIMscores found no significant diVerences betweenthe two groups.

DRUG MANAGEMENT

Aside from medications used for sedation andparalysis, the use of centrally acting medica-tions in the two groups varied dramatically. Inthe intensive care unit morphine and mida-zolam infusions were used in all patients inboth dysautonomia and control groups. Afterstopping regular sedation, a wide range ofdrugs was used in an attempt to control dysau-tonomic features. These included, in decreas-ing order of frequency, chlorpromazine (14patients), clonidine (nine), benzodiazepines(eight), propanolol (two), hydrallazine (one),and carbidopa/levodopa (one). This contrasts

with the control group, in which medicationsused were diazepam (five), chlorpromazine(one), and haloperidol (one). Twenty eightpatients in the control group did not receivecentrally acting agents.

DiscussionThis paper provides supportive evidence thatdysautonomia is a distinct clinical syndromeaVecting a subgroup of patients with severetraumatic brain injury. It extends previousmedical literature by noting consistencies inthe clinical presentation of 35 patients and bycomparing outcome with a matched controlgroup. Patients with the condition have adiVerent course of hospital stay and worsefunctional outcome. Both groups showed asimilar magnitude of improvement asmeasured by change in FIM scores, albeit theimprovement occurred at a slower rate in thedysautonomia group.

The data suggest that dysautonomia can bedivided into three phases. During the firstphase there is little to distinguish between thedysautonomia group and the control group. Onaverage, this phase lasted 1 week and seemed toend with the cessation of regular paralysis orsedation. Phase two sees the onset of the physi-ological changes recognised as dysautonomia.This phase was taken to end with the cessationof sweating, with an average duration of 74days after injury (SD 47.9, range 15–204). Inphase three the paroxysmal episodes haveburnt out, leaving dystonia and spasticity ofvarying severity. Two dysautonomic patientsdeveloped “locked in” syndrome20 on the basisof severe generalised dystonias, when commu-nication only became possible due to voluntarycontrol of an isolated muscle group (thumb inpatient 20, eye blink in 28). It would be possi-ble to misinterpret such a patient’s physicalinability to communicate as evidence of absentcognitive function, resulting in an inappropri-ate diagnosis of persistent vegetative state.

Dysautonomia was particularly associatedwith severe diVuse axonal injury, preadmissionhypoxia, younger age and, to a lesser extent,brainstem injury. The striking proportion ofpatients with both diVuse axonal and hypoxicinjuries has not been previously reported. Theresults of the study do not support a role forinfection in the aetiology of the syndrome, asthere were no diVerences in white cell countpatterns, infection rates, or antibiotic usagebetween the control group and the dysauto-nomia group. Similarly, medications withautonomic activity were not responsible forcausing dysautonomia, as they were invariablyprescribed after the onset of dysautonomiaand in an attempt to minimise autonomicabnormalities.

Many of the features reported in this paperhave the potential to increase secondary braininjury. An example of such an eVect may bepostinjury hyperthermia. In animal models, thethreshold for secondary neuronal injury falls to38°C.21 How long the injured brain remainssensitive to hyperthermia has yet to be deter-mined. In this study, 73% of patients withdysautonomia continued to have core tempera-

Table 3 Number of clinical features present and absent in dysautonomia group andcontrol group

Clinical feature

Dysautonomia Control

÷2 ResultPresent Absent Present Absent

Sweating 34 1 5 29 ÷2=47.6, p<0.005**Tone 35 0 1 33 ÷2=64.8, p<0.005**Posturing 25 10 6 29 ÷2=20.9, p<0.005**Hypertension >2 weeks 22 11 11 21 ÷2=6.8, p<0.05*DiVuse axonal injury 32 3 23 11 ÷2=6.03, p<0.025*Brainstem injuries 11 24 4 30 ÷2=3.9, p<0.05*Pre-admission hypoxia 22 13 9 26 ÷2=9.9, p<0.005**Pre-admission hypotension 7 16 12 18 ÷2=0.53, p>0.05

*p <0.05; **<0.005.

Table 4 Outcome data for dysautonomia group and control groups

Dysautonomiagroup

Controlgroup Significance

Mean hospital DOS (days) 267.9 69.2 F(1,64)=38.6, p=0.000**Mean ICU DOS (days) 13.3 11.6 F(1,64)=0.413, p=0.58Mean rehabilitation DOS (days) 206.8 44.1 F(1,58)=42.9, p=0.000**Mean PTA duration (days) 124.4 36.6 F(1,43)=50.4, p=0.000**Median GOS score 3 2 U(1,67)=84, p=0.000**Median discharge FIM 60 119 U(1,48)=16, p=0.000**Mean FIM change score 44.4 51.8 U(1,48)=232, p=0.41Persistent amnesia (yes/no) 21/12 2/33 ÷2=25.3, p<0.005**

DOS=Duration of stay; ICU=intensive care unit.**p<0.005.

42 Baguley, Nicholls, Felmingham, et al

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tures above 38°C 2 weeks after injury, falling to24% at 4 weeks. In controls, these values were18% and 3% respectively. Thus, temperatureloading poses a much greater threat for second-ary brain injury in patients with dysautonomia.In addition, “posturing” patients have dramati-cally increased energy expenditure, measured at150%-200% in the first week, increasing to200% to 250% in the second week.22 23 Althoughnot identified as dysautonomia, these extremeenergy expenditure figures were from “invari-ably sweating, hypertonic patients who usuallyremained vegetative”.22 The metabolic changes24

and posturing21 25 are associated with increasednoradrenaline concentrations. Noradrenalineproduces permanent cardiac and skeletal musclefibre damage and is an independent predictor ofpoor outcome after traumatic brain injury.26

Thus early recognition and treatment of dysau-tonomia has the potential to minimise second-ary brain injury.

Although our findings extend previous litera-ture, this study had several limitations. Dataacquisition was retrospective and relied ondocumentation within medical records. It isconsidered that such documentation mayunderrepresent the frequency and severity ofdysautonomic episodes after traumatic braininjury. Furthermore, the retrospective natureof our data prevented estimation of itsincidence; nor was there an objective way ofdetermining eYcacy of the medications used.This study was limited to a single rehabilitationfacility and the findings would benefit fromconfirmation in multicentre studies. Futureresearch should focus on prospective analysesto improve understanding of the pathophysiol-ogy and aetiology of dysautonomia, thusoptimising pharmacotherapy and rehabilita-tion interventions.

ConclusionThis paper describes the symptoms and clinicalcourse of dysautonomia after severe traumaticbrain injury. Dysautonomia seems to be a dis-tinct clinical syndrome associated with apoorer outcome. It is argued that the featuresof dysautonomia may result in a preventableand unnecessary increase in morbidity. Earlyrecognition and treatment of the condition isrecommended to reduce long term disability.Research has been hampered by a lack ofstandardised diagnostic criteria and nomencla-ture. Systematic evaluation of treatment re-gimes are required to optimise the outcome ofpatients with dysautonomia.

This study did not receive funding in any form.

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Dysautonomia after traumatic brain injury 43

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doi: 10.1136/jnnp.67.1.39 1999 67: 39-43J Neurol Neurosurg Psychiatry

 Ian J Baguley, Jodie L Nicholls, Kim L Felmingham, et al. forgotten syndrome?Dysautonomia after traumatic brain injury: a

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