Brain Injury

ISSN: 0269-9052 (Print) 1362-301X (Online) Journal homepage: http://www.tandfonline.com/loi/ibij20

Anosmia and olfactory outcomes following

paediatric traumatic brain injury

Kathleen Bakker, Cathy Catroppa & Vicki Anderson

To cite this article: Kathleen Bakker, Cathy Catroppa & Vicki Anderson (2015): Anosmia
and olfactory outcomes following paediatric traumatic brain injury, Brain Injury, DOI:
10.3109/02699052.2015.1089597

To link to this article: http://dx.doi.org/10.3109/02699052.2015.1089597

Published online: 30 Nov 2015.

Submit your article to this journal

Article views: 33

View related articles

View Crossmark data

Full Terms & Conditions of access and use can be found at

http://www.tandfonline.com/action/journalInformation?journalCode=ibij20

Download by: [137.189.170.231] Date: 11 December 2015, At: 09:50

 http://tandfonline.com/ibij
ISSN: 0269-9052 (print), 1362-301X (electronic)

Brain Inj, Early Online: 1–8

© 2015 Taylor & Francis Group, LLC. DOI: 10.3109/02699052.2015.1089597

Anosmia and olfactory outcomes following paediatric traumatic brain injury

Kathleen Bakker1,2,3, Cathy Catroppa2,3,4,5, & Vicki Anderson2,3,4,5
1
Victorian Paediatric Rehabilitation Service, Royal Children’s Hospital, Melbourne, Australia, 2Murdoch Childrens Research Institute, Melbourne,
Australia, 3Department of Paediatrics, University of Melbourne, Australia, 4Psychology Department, Royal Children’s Hospital, Melbourne, Australia,
and 5School of Psychological Sciences, University of Melbourne, Australia

Abstract Keywords
Objective: Research into olfactory dysfunction (OD) following paediatric traumatic brain injury Traumatic brain injury, child, anosmia,
(TBI) is limited. The current study investigated the frequency of OD following paediatric TBI and olfactory dysfunction, smell
the relationship between OD and injury characteristics including severity, site of impact and
cause of injury. It was hypothesized that children with moderate/severe TBI would demonstrate History
greater OD than those with mild TBI.
Design/method: Thirty-seven children aged 8–16 with TBI were recruited to a prospective Received 23 March 2015
Revised 27 July 2015
Downloaded by [] at 09:50 11 December 2015

longitudinal study at a metropolitan children’s hospital. Olfactory assessment, using the

University of Pennsylvania Smell Identification Test, was completed at 0–3 months post-injury. Accepted 30 August 2015
Published online 27 November 2015
Results: Nineteen per cent of participants demonstrated impaired olfaction, while a small
number (5%) were anosmic. A significant relationship between OD and severity of injury was
found. No other injury variables demonstrated a significant relationship with olfactory
outcomes.
Conclusions: OD was relatively common in this paediatric TBI cohort and the hypothesized
relationship with severity of injury was supported. It is recommended that information about
OD after TBI be routinely provided to children and families. Further research is needed in larger
cohorts to support the implementation of routine clinical assessment, understand the relation-
ship between OD and other injury characteristics, determine the functional implications of OD
and document recovery trajectories.

Introduction In early research post-traumatic OD was estimated to

effect ~ 24–30% of adults with severe TBI, 15–19% with
Post-traumatic anosmia was first described in the scientific
moderate TBI and 0–16% with mild TBI [9]. More recent
literature over 150 years ago [1]. Despite the early identifi-
studies have reported prevalence rates in adult TBI, ranging
cation of this clinical phenomenon, understanding of olfac-
from 22–65% [10–13] in mixed severity samples. In mild TBI
tory dysfunction (OD) following paediatric TBI remains
cohorts, prevalence rates of 25% have been reported [14].
incomplete. OD is commonly used as an umbrella term
Interestingly, despite these high rates on testing, reduced
that encompasses a full spectrum of olfactory deficits, with
awareness of olfactory deficits via self-report is common
anosmia (complete loss of smell) at one extreme, through to
[10–12,15].
hyposmia or microsmia (reduced sense of smell) and nor-
Significantly less research has been conducted in paedia-
mosmia (or normal olfactory function) at the other [2]. The
tric TBI cohorts and variable prevalence rates from as little as
lack of knowledge of post-traumatic OD is surprising given
3% to as many as 58% have been reported in this age group
documentation of its significant negative impact on activ-
[15–17]. Studies in paediatric cohorts with OD of mixed
ities of daily living, diet, hygiene, leisure and relationships
aetiology have identified head trauma as the most common
[3–5]. Health and safety risks have also been linked to OD,
cause of olfactory impairment in children and adolescents
with individuals at increased risk of cooking accidents,
[18]. Deficits in olfactory function have also been reported
ingestion of spoiled food and toxic substances and failure
in a range of paediatric neuropsychiatric disorders such as
to detect gas leaks or fires [6]. Disruptions to olfactory
attention deficit hyperactivity disorder and autism spectrum
function during early development have also been identified
disorder, with the integrity of orbitofrontal cortex and the
as impacting on development of olfactory and gustatory
dopaminergic system identified as possible underlying
systems [7,8].
mechanisms [19,20].
A number of underlying neuropathological mechanisms
Correspondence: Kathleen Bakker, MSc, Senior Clinical
have been proposed for the presence of post-traumatic OD.
Neuropsychologist, Victorian Paediatric Rehabilitation Service, Royal Mechanical injury to the nasal passages, causing obstruction
Children’s Hospital, Flemington Road, Parkville 3052, Australia. E-mail: or nasal deviations, may limit the passage of odour molecules
kath.bakker@rch.org.au
 2 K. Bakker et al.
reaching the olfactory neuroepithelium and reduce olfactory
function [9,17]. Most commonly post-traumatic OD is
ascribed to shearing injuries to the olfactory filaments as
they enter the skull via the cribriform plate. The location of
the olfactory nerves immediately below and their connection
directly to the inferior surface of the frontal lobes [21] makes
them particularly vulnerable to damage from the rotational
and mechanical forces of TBI [9]. Cortical injury to olfactory
centres in the brain has also been implicated in post-traumatic
OD. Damage to temporal lobe structures and contusions to
the olfactory bulb, tract and orbitofrontal cortex have all been
identified in anosmia, with volume loss documented in both
the olfactory bulb and tract and inferior frontal cortex in
neuroimaging studies [22,23].
There is inconsistent evidence of the role of injury vari-
ables as possible clinical predictors of OD in TBI research.
While some research in adult cohorts has indicated a relation-
ship between severity of injury and OD [9,11,24–26] such
findings are not consistently replicated [10,12,13,27,28]. It
has been argued that other injury characteristics, including
site of impact, are better predictors of post-traumatic olfac-
tory function in adult TBI samples [28]. Posterior impacts
Downloaded by [] at 09:50 11 December 2015
have been found to result in greater impairment in olfaction
than frontal impacts in adults [27,29], with this linked to
contre-coup injury mechanisms. Base of skull fractures, facial
fractures and frontal neuropathology have also been identified
as possible predictors of OD in adult cohorts [28,30].
In paediatric TBI the relationships between injury vari-
ables and OD are similarly unclear and the limited number of
studies in paediatric cohorts make conclusions difficult [31].
While there appears to be support for a relationship between
severity of injury and OD in children [15–17], study findings
are limited by methodological issues [31] such as use of non-
standardized or poorly validated measures of olfactory func-
tion, unclear clinical sample source, retrospective or unclear
recruitment methodology and variability in time since injury
at testing [15,16]. A prospective study in a largely mild
paediatric TBI cohort by Sandford et al. [17] found a positive
relationship between injury severity and OD; however, those
with TBI did not differ from controls in terms of OD. Wide
variability in time since injury to assessment in their sample
and the largely mild severity of their TBI cohort limit the
generalizability of their findings.
Little can be concluded about the predictive value of other
injury-related variables such as site of impact, neuropathol-
ogy, cause of injury and presence of skull fracture from the
existing paediatric literature. The studies cited above report
some evidence of positive relationships between occurrence
of frontobasal injuries [16], fracture [17], presence of intra-
cranial injury [17] and OD.
Post-traumatic OD has the potential for significant func-
tional impact in a paediatric setting, yet research in this age
group to date is limited. Given the known differences in child
and adult TBI outcomes in other neurocognitive areas, extra-
polating findings directly from adult outcome studies may not
be appropriate, highlighting the importance of further
research in paediatric TBI cohorts [32,33].
The aim of this study was to determine the frequency of
OD within the first 3 months of injury, in a prospectively
recruited mixed severity paediatric TBI cohort, using a
Brain Inj, Early Online: 1–8
standardized measure of olfactory function. Further, the
aim was to investigate the relationship between OD and
injury variables, including severity, site of impact, cause of
injury, location of neuropathology and skull fracture. The
relationship between self-report of OD and its relationship
to objective test results was also examined. Based on exist-
ing paediatric literature it was hypothesized that those
children with moderate/severe TBI would demonstrate
greater impairment in olfactory function than those with
mild TBI.
Materials and methods
Design
This is a prospective, longitudinal, single site, observational
study.
Participants
Participants were 37 children aged 8–16 years with documen-
ted evidence of TBI who presented to the Emergency
Department (n = 19) or were referred as an inpatient (n =
7) or outpatient (n = 11) to the Rehabilitation Department, at
a major metropolitan children’s hospital in Australia, between
April 2010 and August 2012. Of the 37 participants, 25 were
male and 12 female, a ratio of ~ 2:1. Mean age was 12.40
years (SD = 1.96). TBI was defined as documented evidence
of closed head injury with either period of altered or loss of
consciousness, period of coma, period of post-traumatic
amnesia or retrograde amnesia and/or neuroimaging evidence
of brain trauma [34]. Children with a history of documented
prior brain injury, developmental, learning, neurological or
neuropsychiatric disorder or self-reported pre-morbid diffi-
culties with smell or taste were excluded.
Invitations to participate in the study were made to 223
children and their families. Sixty-two families were not able
to be contacted following initial invitation. As Australian
privacy laws did not allow for the collection of further
information on these children they were excluded from the
study as no determination was able to be made about elig-
ibility. A further 42 children were excluded based on pre-set
exclusion criteria and five failed to attend follow-up appoint-
ments and were excluded. Seventy-seven families declined
participation.
Those declining participation were compared with enrolled
participants on available demographic and injury data (age,
gender, injury severity and residential suburb) to ensure that
the large non-participation rate did not introduce any systema-
tic bias into the sample. The un-enrolled potentially eligible
group did not differ significantly from the enrolled group in
terms of age at injury, t(112) = –0.38, p = 0.71; gender, χ2(2)
= 0.08, p = 0.83; injury severity, χ2(2) = 5.23, p = 0.07; or
socio-economic factors, as measured by Index of Relative
Social Advantage and Disadvantage [35], Z = –0.6, p = 0.55.
Enrolled children were assigned to two groups on the basis
of severity of injury. Mild TBI (n = 22) was defined as initial
Glasgow Coma Scale (GCS) score [36] 13–15 and/or period
of post-traumatic amnesia (PTA) < 24 hours, with or without
neuroimaging evidence of intracranial injury not requiring
 DOI: 10.3109/02699052.2015.1089597
surgical intervention. Moderate/severe TBI (n = 15) was
defined as initial GCS of ≤ 12 and/or period of PTA ≥ 24
hours.
Materials
Demographic information
Data relating to gender, age at injury, pre-morbid medical,
developmental history, parental education, occupation and
income were collected from parents via questionnaire.
Injury indices
Injury indices including initial GCS, period of PTA, evidence
of intracranial injury, location of neuropathology on clinical
neuroimaging (CT/MRI), site of impact (frontal, occipital,
parietal, temporal), cause of injury, need for neurosurgical
intervention, presence or absence of skull fracture and dys-
phagia were collected from the child’s medical record.
Socio-economic status
Downloaded by [] at 09:50 11 December 2015
For both recruited and non-recruited groups residential sub-
urb was used to calculate socio-economic status using the
Socio-economic Indexes for Areas (SEIFA) data from the
Australian Bureau of Statistics (ABS) 2011 Census [35].
The Index of Relative Socio-economic Advantage and
Disadvantage (IRSAD) was chosen to compare the group
who did not consent to participate with the final study cohort
to examine any differences across the groups. The IRSAD
includes measures that tap into relative advantage and disad-
vantage and includes variables that relate to income, educa-
tional attainment, occupation, family structure and home
ownership. A low score indicates relatively greater disadvan-
tage and lack of advantage, whereas a high score indicates
greater advantage and a relative lack of disadvantage. Scores
range from 300–1250. The IRSAD is an ordinal value as it
represents rank.
The Social Risk Index (SRI) [37] was used for the
clinical sample as a measure of relative pre-injury social
risk. This measure has been used in developmental and
acquired brain injury research as a measure of socio-eco-
nomic status and incorporates information on family
income, caregivers’ educational level and ethnicity [37,38].
The social risk index uses six aspects of social status to give
a numeric value of social risk (range = 0–12) utilizing the
following variables: maternal age at child’s birth (0 = > 21
years, 1 = 18–21 years, 2 = < 18 years); level of education
of primary care giver (0 = tertiary educated, 1 = completed
11–12 years of formal schooling, 2 = < 11 years formal
schooling completed); occupation of primary wage earner (0
= skilled/professional, 1 = semi-skilled, 2 = unskilled);
employment status of primary wage earner (0 = full time,
1 = part time, 2 = unemployed/pension), family constella-
tion (0 = two caregivers at home, 1 = separated with dual
custody, 2 = single parent family); primary language spoken
at home (0 = English only, 1 = some English spoken, 2 =
no English spoken). A higher score represents increased
social risk.
Anosmia and olfactory outcomes in paediatric TBI 3
Primary outcome measure (smell identification)
The University of Pennsylvania Smell Identification Test
(UPSIT) [2] was administered as the primary outcome mea-
sure to assess smell identification. The UPSIT is a 40-item
multiple choice ‘scratch and sniff’ smell test for assessing
olfactory functions. It consists of four booklets of 10 micro-
encapsulated odourant patches on separate cards (40 odour-
ants in total). Each card also provides a forced choice of four
written options for identifying the smell. Possible scores
range from 0–40.
The UPSIT provides an absolute index of smell loss as well
as percentile data for 5–90 year olds. Normative data are stra-
tified into gender groups and for age intervals from 5–9, 10–14
and 15–19 years. The UPSIT also provides classification into
the following descriptive groups on the basis of age corrected
performance: normosmia (normal smell identification), mild
microsmia, moderate microsmia, severe microsmia and anos-
mia. The UPSIT has high test–re-test reliability (r = 0.92) over
a 6 month test interval and strong correlations (r = 0.73–0.78)
between the scores on each of the four test booklets [2].
Due to cultural and language differences in performance
previously identified between Australian cohorts and the
North American standardization sample a correction was
made to participants raw scores by adding 2 raw score points
[39]. A cut-off score of performance below the 5th percentile
was taken to indicate impairment in olfactory function and
this was the primary outcome score. Standard UPSIT categor-
izations were also reported to allow for more detailed descrip-
tion of participant olfactory performance.
The administration procedure for the UPSIT was as fol-
lows. The four test booklets were presented to all children in
order from 1–4. Prior to presentation children were told that
they would be asked to smell 40 smells. After presentation of
each odourant children were asked which of the four options
it smelt most like. Children were instructed to choose an
option even if they were unsure of the smell or if no smell
was present. Each item was presented to the child after the
examiner scratched the microencapsulated label with a pencil.
Each odour was presented to both nostrils. Due to variability
in age of the cohort, the four alternative answers were read
aloud by the examiner—and children were also able to read
the options.
Procedure
The data reported in this study are from stage 1 (0–3 month
follow-up) of a larger prospective longitudinal study. The
study was approved by the hospital’s Human Ethics
Research Committee and carried out in accordance with
National Privacy Legislation and the Code of Ethical
Principles for Medical Research Involving Human Subjects
of the World Medical Association (Declaration of Helsinki).
Eligible children were identified and recruited via three
strategies.
Recruitment via Emergency Department
Potential eligible participants meeting age and injury inclusion
criteria were identified after presentation to the Emergency
 4 K. Bakker et al.
Department during the recruitment period. A letter outlining
details of the study was sent to all potentially eligible families,
inviting them to participate in the research project.
Recruitment via inpatient rehabilitation programme
Potential participants meeting age and injury inclusion cri-
teria were identified after admission to the Rehabilitation
Department by the principal investigator. Families were
approached directly on the ward once medically stable and
out of post-traumatic amnesia as deemed by the treating
clinical team. Families were provided with detailed informa-
tion sheets and consent forms.
Recruitment via outpatient brain injury clinic
Potential participants meeting age and injury inclusion cri-
teria were identified after referral to outpatient ABI clinic for
initial 4–8 week clinic follow-up post-injury. Families were
approached at their clinic appointment and provided with
detailed information and consent forms.
For consenting families in all three recruitment strategies,
Downloaded by [] at 09:50 11 December 2015
children were screened for exclusion criteria and those deemed
eligible were scheduled for completion of initial testing.
Assessments were carried out at ~ 0–3 months (M = 1.58,
SD = 0.63) post-injury. At time of assessment children were
required to be free of pathology that could impact on smell
abilities, such as diagnosis of sinusitis or upper respiratory
tract infection (URTI). Assessments were conducted at the
hospital either on the ward or in a separate clinic room. Prior
to testing, children were asked if they had experienced a loss
or change of sense of smell or taste since their injury. If they
answered yes, details of that change were recorded.
While children were assessed, parents completed the
demographic questionnaire
Statistical analysis
Data analysis was conducted using SPSS (Version 22.0). Chi
square test for independence (using Fisher’s exact test) and
independent t-tests were conducted to examine any differ-
ences across severity groups on demographic and injury vari-
ables. Effect sizes for analyses were calculated using phi (ϕ)
coefficient and r, respectively, where 0.1 = small, 0.3 =
moderate and 0.5 = large [40].
To investigate the hypothesis that children with moderate/
severe TBI would demonstrate poorer olfactory function than
those with mild TBI, Mann Whitney U for independent sam-
ples (with exact significance calculated) was conducted to
compare olfactory performance (UPSIT corrected percentile
score) across the mild and moderate/severe groups. Univariate
linear regression was conducted to investigate effects of age at
injury on olfactory performance. Mann Whitney U for inde-
pendent samples (with exact significance calculated) was
performed to compare those with ‘impaired’ and ‘unimpaired’
olfactory function on severity variables (GCS and PTA) with
effects size, r, reported [40].
Chi-square test for independence was calculated (using
Fisher’s exact test) to investigate the relationship between injury
characteristics and olfactory function. Due to small n and
Brain Inj, Early Online: 1–8
variability on clinical neuroimaging (CT/MRI), the rela-
tionship between location of neuropathology and OD was
not able to be analysed. Effect size was determined using
phi (ϕ) coefficient [40].
Results
Demographics and injury characteristics
Demographic and injury data for the participant group are
provided in Table I. The moderate/severe TBI group (mean
age = 13.45, SD = 1.74) were significantly older at time of
injury than the mild TBI group (mean age = 11.68, SD =
1.81). There was, however, no significant difference between
the groups in terms of socio-economic factors as measured by
social risk index.
As expected, the mild and moderate/severe TBI groups
differed on many of the injury variables. The moderate/severe
group demonstrated significantly lower GCS and longer per-
iods of PTA than the mild group. The moderate/severe TBI
group also demonstrated a higher frequency of abnormal
neuroimaging, presence of dysphagia and need for acute
neurosurgical intervention and a tendency towards greater
likelihood of skull fracture (although this result did not
meet significance). Motor vehicle accidents were the most
common cause of injury for the moderate/severe group and
sporting injury the most common for those with mild TBI.
Interestingly, sports-related injuries were the most common
cause of injury in the sample, accounting for a third of all
injuries.
Site of impact varied between the two severity groups,
with occipital impacts the most common for those with
moderate/severe TBI (53%). The mild TBI group showed
more equal distribution between frontal and occipital
impacts. For the entire sample, frontal and occipital
impacts accounted for 80% of impacts in those with docu-
mented site of impact.
Frequency of olfactory dysfunction in paediatric TBI
Analysis of participant performance on the UPSIT revealed a
high rate of OD post-TBI. Using corrected raw scores and a
cut-off score of performance below the 5th percentile as
indicative of impaired olfaction, 19% of the total sample
were found to demonstrate impaired olfaction. Without raw
score correction for an Australian sample, this percentage
increased to 41% of participants meeting criteria for impaired
olfaction.
Participants performance on the UPSIT was also investi-
gated in relation to clinical categorical assignments outlined
in the test manual. Using uncorrected scores, 8% of partici-
pants were categorized as anosmic, this reduced to 5% when
the two point (+2) correction was applied to raw scores.
Interestingly, after assigning participants to UPSIT category
groups on the basis of their corrected raw score performance
only 38% of participants demonstrated normal olfactory func-
tion, with 57% of participants categorized as microsmic.
Details of UPSIT performance using corrected scores are
outlined in Table II.
 DOI: 10.3109/02699052.2015.1089597 Anosmia and olfactory outcomes in paediatric TBI 5
Table I. Participant demographics and injury characteristics.

Variables Total Mild Moderate/severe Significance

n 37 22 15
Gender, females, n (%) 12 (32) 6 (27) 6 (40) χ2(1) = 0.66, p = 0.32
Age at injury (years), M (SD) 12.40 (1.96) 11.68 (1.81) 13.45 (1.74) t(35) = –2.97, p = 0.005
SRI*, M (SD) 1.89 (2.16) 1.48 (1.91) 2.47 (2.42) t(34) = –1.37, p = 0.18
Injury characteristics
GCS, M (SD) 13.25 (2.66) 14.59 (0.60) 11.14 (3.26) t(34) = 4.88, p < 0.0005
PTA days, M (SD) 4.76 (9.07) 0.10 (0.16) 11.6 (11.28) t(35) = –4.81, p < 0.0005
Positive neuroimaging, n (%) 16 (43) 4 (18) 12 (80) χ2(1) = 5.1, p = 0.04
Neurosurgery, n (%) 5 (14) 0 5 (33) χ2(1) = 8.48, p = 0.007
Dysphagia, n (%) 5 (14) 0 5 (33) χ2(1) = 8.48, p = 0.007
Skull fracture, n (%) 10 (27) 3 (14) 7 (47) χ2(1) = 4.93, p = 0.06
Cause of injury
MVA# passenger, n (%) 7 (19) 1 (5) 6 (40)
MVA# pedestrian, n (%) 2 (5) 1 (5) 1 (7)
Bike/scooter, n (%) 4 (11) 3 (14) 1 (7)
Skateboard, n (%) 7 (19) 3 (14) 4 (27)
Fall, n (%) 4 (11) 4 (18) 0
Sport, n (%) 12 (32) 9 (41) 3 (20)
Assault, n (%) 1 (3) 1 (5) 0
Injury impact
Frontal, n (%) 11 (30) 9 (41) 2 (13)
Temporal, n (%) 4 (11) 4 (18) 0
Parietal, n (%) 2 (5) 0 2 (13)
Occipital, n (%) 15 (41) 7 (32) 8 (53)
Undocumented, n (%) 5 (14) 2 (9) 3 (20)
Downloaded by [] at 09:50 11 December 2015

#
* Social Risk Index, Motor vehicle accident.

Table II. Olfactory performance of mild and moderate/severe TBI p = 0.01, r = 0.42, with the moderate/severe TBI group
groups. demonstrating poorer olfactory function. As the TBI severity
groups differed in age at injury, univariate regression with age
Total Mild Moderate/severe at injury as the predictor was conducted to determine if this
n 37 22 15 better explained differences in olfactory function. Age at injury
Age, years, M (SD) 12.54 (1.96) 11.81 (0.39) 13.62 (0.44) was not a significant predictor of olfactory performance, with
UPSIT, M (SD) 20.08 (20.17) 25.68 (21.95) 11.87 (14.22) this explaining 2.7% of the variance (r2 = –0.01), p = 0.4 in
Anosmia, n (%) 2 (5) 1 (5) 1 (7)
UPSIT scores.
Micrsomia, n (%) 21 (57) 11 (50) 10 (66)
Normosmia, n (%) 14 (38) 10 (45) 4 (27)

Predictors of impaired olfaction

Self-report of olfactory deficits
Injury severity
On questioning at the time of assessment the majority of
To further explore the relationship between severity of injury
participants indicated that they had experienced no change
and impaired olfaction, participants were assigned to
in sense of smell or taste (86%). Four participants identified
impaired (n = 7; corrected UPSIT score < 5th percentile) or
change in sense of smell and one indicated changes in taste.
unimpaired (n = 30; corrected UPSIT score ≥ 5th percentile)
Of the five reporting changes, descriptions included: com-
groups. Children with moderate/severe TBI were significantly
plete loss of smell (n = 1); diminution in smell (n = 1); initial
over-represented in the impaired group compared to those
change in sense of smell which had recovered prior to assess-
with mild TBI, χ2(1) = 7.31, p = 0.01, ϕ = 0.44.
ment (n = 1); qualitative change in odours where items smell
Analysis of specific severity indices provided further sup-
unpleasant or different (n = 1); and change in taste only (n =
port for the positive relationship between OD and severity of
1). Analysis of UPSIT performance for those reporting olfac-
injury. Participants with impaired olfaction had a significantly
tory and gustatory deficits revealed the following categoriza-
longer period of PTA, Z = –2.44, p = 0.01, r = 0.4 and
tions: anosmic (n = 1), moderate microsmia (n = 2), mild
significantly lower initial GCS, Z = –2.33, p = 0.02, r = 0.39
microsmia (n = 1) and normosmia (n = 1). Interestingly, of
than those categorized as unimpaired.
the seven participants demonstrating impaired performance
on the UPSIT, only one self-reported any change in olfaction.
Injury characteristics
To explore differences in olfactory function relative to injury
Hypothesis: Children with moderate/severe TBI will dem-
characteristics, participants were stratified into groups based
onstrate poorer olfactory function than those with mild TBI
on categorical injury variables. Groups were determined on
Results of analysis indicated a significant difference the basis of skull fracture: positive (n = 10) or negative (n =
between the mild and moderate/severe group, Z = –2.55, 27); evidence of intracranial injury (in those with
 6 K. Bakker et al.
neuroimaging): positive (n = 16) or negative (n = 10); site of
injury impact: frontal (n = 11) or occipital (n = 15); acute
dysphagia: positive (n = 5) or negative (n = 32); acute
neurosurgical intervention: positive (n = 5) or negative (n =
32); and cause of injury: vehicular accidents (n = 9) or sports
injury (n = 11).
No significant differences were found between the
impaired and unimpaired group for any of the injury charac-
teristics using chi-square analysis. Despite this, examination
of effects size statistics indicated a moderate-to-large effect
size for both skull fracture, χ2(1) = 3.97, p = 0.07, ϕ = 0.33,
and those with evidence of intracranial injury, χ2(1) = 4.88,
p = 0.05, ϕ = 0.43. Effects sizes for site of impact, χ2(1) =
0.11, p = 0.1, ϕ = 0.07, cause of injury, χ2(1) = 0.79, p =
0.61, ϕ = 0.19, need for acute neurosurgical intervention, χ2
(1) = 3.73, p = 0.14, ϕ = 0.32 or acute dysphagia, χ2(1) =
1.68, p = 0.23, ϕ = 0.21 were small-to-moderate.
Discussion
Using a prospective design and standardized, age normed
olfactory function assessment, the results indicate that OD
Downloaded by [] at 09:50 11 December 2015
was relatively common in this paediatric TBI sample, with
almost one-fifth of children demonstrating impaired olfaction
(defined as performance below the 5th percentile on UPSIT)
within the first 3 months post-injury. In total, 5% of the
sample were classified as anosmic according to standard
UPSIT categorizations. Interestingly, when using UPSIT cate-
gorizations, only 38% of the sample demonstrated normal
olfactory function, with 57% being categorized as microsmic.
Despite these findings, self-report of OD in this TBI cohort
was low, with only 14% of children identifying change via
self-report prior to testing.
The frequency of OD in the mixed severity sample is
generally within the range of the variable frequencies reported
from previous paediatric literature. Sandford et al. [17], using
a standardized measure of olfaction, found 8% of their sample
had impaired olfaction, in comparison to 19% in this cohort.
The greater proportion of mild injuries in their cohort and
longer time post-injury may explain the differences with these
results. In contrast to the 19% of this sample having impaired
olfaction, Roberts and Simcox [15] reported OD in 58% of
their cohort, although their olfactory assessment method,
differences in time post-injury and retrospective recruitment
methodology may explain their much higher rates and incon-
sistencies with these findings. Their findings are more in
keeping with the 57% of participants in this cohort categor-
ized as microsmic according to UPSIT classifications. The
rate of impaired olfaction is higher than the 3% reported by
Jacobi et al. [16] in their large mixed severity sample. These
differences may be due to the use of standardized olfactory
assessment, differences in recruitment methodology and clin-
ical sample source. Additionally this may reflect differences
in the definition of OD between studies. Their finding of 3%
of participants with ‘loss of smell’ would certainly be con-
sistent with the finding of 5% of the sample being categorized
as anosmic. In general, these results are in keeping with
incidence rates of 22–25% reported in contemporary adult
TBI studies using standardized assessments and investigating
olfaction in the acute post-injury period [13,14].
Brain Inj, Early Online: 1–8
The hypothesis that those with moderate/severe TBI would
demonstrate greater impairment in olfactory function than
those with mild TBI was supported. A significant relationship
between severity of injury and olfactory function was found,
in line with previous literature in children [15–17]. Moreover,
severity of injury appeared to be a significant factor in the
prediction of olfactory impairment following TBI, with a
longer period of PTA and lower initial GCS significantly
and positively related to impairment in olfaction. While the
results here are consistent with previous paediatric research,
severity effects have not been uniformly supported in adult
TBI literature [13,28].
Other injury-related variables did not demonstrate any
significant relationship with post-traumatic OD. The moder-
ate-to-large effect sizes observed when the impaired and
unimpaired group were compared on presence of skull frac-
ture and evidence of intracranial injury indicate that a possi-
ble significant relationship may have been obscured by low
power related to the small sample size. Such a relationship
has been documented in a mild paediatric TBI cohort [17]
and these relationships have been documented in previous
studies of adult TBI [28,30].
To the authors’ knowledge, this is the first study to inves-
tigate the relationship of multiple injury characteristics,
including site of impact, need for neurosurgery and presence
of dysphagia to OD in a paediatric TBI cohort. No evidence
was found of significant relationships between these variables
and OD in this cohort. Site of impact has previously been
identified as related to OD in adult TBI [27,29] and Haxel
et al. [28] concluded that this may be a better predictor of
post-traumatic OD than severity of injury. Variability in site
of impact and the small sample size, as well as differences in
source of TBI recruitment and the paediatric cohort may have
impacted on the differences in these results.
There were clear disparities in this sample between UPSIT
performance and participants self-report of olfactory pro-
blems. These differences between self-report or self-aware-
ness of OD and objective results have been frequently
reported in the literature in both paediatric and adult post-
traumatic cohorts, with individuals likely to significantly
under-report OD [15,27]. The robustness of this finding has
implications for clinical practice, as it raises significant ques-
tions about the reliability of self-report as a valid method in
clinical screening practices [17].
While the UPSIT is considered a gold standard in the
field [10,11,27,41], the findings identified some inconsis-
tencies across scoring methods. Nineteen per cent of parti-
cipants were classified as having impaired olfaction using
the cut-off score. However, when using UPSIT classifica-
tions, 57% of participants were categorized as miscrosmic—
exhibiting non-normal olfactory performance. In keeping
with some previous literature [15] using non-standardized
olfactory assessment methods, this represents a large pro-
portion of the sample. Given the absence of previous
research using the UPSIT in paediatric TBI populations it
is difficult to determine whether this represents an over-
estimate of incidence of OD post-paediatric TBI. It will be
important for future studies to continue to validate its use-
fulness in paediatric TBI cohorts. These results also high-
light the importance of clear operational definitions of OD
 DOI: 10.3109/02699052.2015.1089597
and anosmia to allow for comparison of study results to
build an accurate picture of the incidence of OD post-pae-
diatric TBI.
The original small sample size and high variability in
location of neuropathology on CT/MRI in the sub-set of
participants with CT/MRI evidence of neuropathology
meant that this study was not able to meaningfully investigate
the relationship between neuropathology and olfactory func-
tion. The possible mechanisms responsible for post-traumatic
OD, understanding of olfactory networks and evidence from
neuroimaging studies would certainly indicate that a relation-
ship is likely to exist in children, as has been demonstrated in
previous research in adult cohorts [22,28], and this would
certainly be an area for future investigation.
It is important to note a number of other limitations with
the current study. The small sample size limits the power of
this study and so a lack of significant relationships between
injury characteristics and OD should be interpreted with cau-
tion. Given the moderate-to-large effect sizes observed
between skull fracture and presence of intracranial injury
and OD, studies with larger samples may well find a signifi-
cant relationship here. A combined moderate/severe TBI
Downloaded by [] at 09:50 11 December 2015
group may also have obscured results, by diluting severity
groupings—resulting in a reduction in the strength of rela-
tionship between severity and OD.
The current study did not use a control group for compar-
ison, which may limit the robustness of the findings with
relation to the frequency of OD in the paediatric TBI cohort
—and this would be recommended in future larger studies.
The inclusion, however, of a well validated standardized test
of smell identification with age norms as the main outcome
measure is a strength of the study and allows for assessment
of olfactory function relative to the normal paediatric popula-
tion and across clinical groups [7,41,42]. The inclusion of a
standardized age-normed assessment builds on previous stu-
dies using un-validated or unknown assessment methods
[15,16] and provides more convincing evidence for the fre-
quency of OD in paediatric TBI.
The low rate of participation in this study from potentially
eligible subjects raises the question of the representativeness
of the cohort. Analysis indicates that those who declined
participation did not differ from the enrolled cohort on avail-
able demographic and injury variables and as such the sample
is felt to be representative of the general paediatric TBI
cohort. It will be important that future studies improve
recruitment procedures to maximize participation so that
results can be replicated in larger samples.
This study has provided further support for the frequency
of post-traumatic OD in a paediatric population, but there is
still a sizeable gap in knowledge in this area. Identified links
between OD and executive function in children with TBI [15]
raise questions about whether OD may be a useful predictor
of later executive or behaviour change in children with TBI.
Little is known about the longer-term functional implications
of OD in a paediatric TBI. Evidence of important health and
safety risks, implications for quality-of-life, hygiene, voca-
tional options and developmental implications in previous
research [4–7] highlight the clinical significance of post-TBI
OD and support the importance of gaining a better under-
standing of the functional implications of OD for this group.
Anosmia and olfactory outcomes in paediatric TBI 7
Larger longitudinal studies are needed to better explore and
identify those variables that may be useful predictors of the
relative risk of OD post-injury. This would be important in
identifying those at risk in a clinical setting and providing further
follow-up screening to identify those with OD. Such knowledge
will assist with clinical management and rehabilitative education
for families and children, around expected recovery patterns,
compensatory strategies and the need for safety and health
precautions.
There is also a real need for accurate, reliable and acces-
sible olfactory assessment measures for clinical and research
use. While this is a growing area, with a number of measures
being developed in the last few years [42,43], issues of
clinical feasibility around cost and normative data still require
further exploration.
Conclusion
OD was apparent in almost one in five of the mixed severity
paediatric TBI cohort, with evidence of a significant relation-
ship with severity of injury. Clinical screening of olfaction
and appropriate education and clinical management strategies
(particularly around health and safety) should be provided to
children with TBI and their families. Further research is
needed to support the implementation of routine clinical
assessment. Given the frequency of occurrence and signifi-
cant health and safety implications of OD, there is a need for
further investigation of the natural history of OD post-pae-
diatric TBI, potential functional impacts and the development
of guidelines around clinical assessment and rehabilitative
management for children.
Acknowledgements
The authors thank Dr. Kevin Dunne, Dr. Peter Barnett, Mr.
Ken Robinson and staff of the Emergency Department and
Victorian Paediatric Rehabilitation Service, Royal Children’s
Hospital, for assistance with recruitment and Dr. Stephen
Hearps for statistical analysis advice.
Declaration of interest
The authors report no conflicts of interest. The project
received funding from the Victorian Neurotrauma Initiative,
Murdoch Childrens Research Institute, the Victorian
Government Operational Infrastructure Scheme and The
University of Melbourne, Australia.
References
1. Jackson JH. Illustrations of diseases of the nervous system. Clinical
Lectures and Reports by the Medical and Surgical Staff of the
London Hospital 1864;1:470.
2. Doty RL. The smell identification test administration manual.
Haddon Heghts, NJ: Sensonics, Inc.; 1995.
3. Zasler ND, McNeny R, Heywood PG. Rehabilitative management
of olfactory and gustatory dysfunction following brain injury.
Journal of Head Trauma Rehabilitation 1992;7:66–75.
4. Drummond M, Douglas J, Olver J. Anosmia after traumatic brain
injury: a clinical update. Brain Impairment 2007;8:31–40.
5. Miwa T, Furukawa M, Tsukatani T, Costanzo RM, DiNardo LJ,
Reiter ER. Impact of olfactory impairment on quality of life and
 8 K. Bakker et al.
disability. Archives of Otolaryngology Head and Neck Surgery
2001;127:497–503.
6. Santos DV, Reiter ER, DiNardo LJ, Costanzo RM. Hazardous
events associated with impaired olfactory function. Archives of
Otolaryngology Head and Neck Surgery 2004;130:317–319.
7. Dalton P, Mennella JA, Cowart BJ, Maute C, Pribitkin EA, Reilly
JS. Evaluating the prevalence of olfactory dysfunction in a pedia-
tric population. Annals of the New York Academy of Sciences
2009;1170:537–542.
8. Mennella JA, Jagnow CP, Beauchamp GK. Prenatal and postnatal
flavor learning by human infants. Pediatrics 2001;107:E88.
9. Costanzo RM, Zasler ND. Epidemiology and pathophysiology of
olfactory and gustatory dysfunction in head trauma. Journal of
Head Trauma Rehabilitation 1992;7:15–24.
10. Callahan CD, Hinkebein J. Neuropsychological significance of
anosmia following traumatic brain injury. Journal of Head
Trauma Rehabilitation 1999;14:581–587.
11. Callahan CD, Hinkebein JH. Assessment of anosmia after trau-
matic brain injury: Performance characteristics of the University of
Pennsylvania Smell Identification Test. Journal of Head Trauma
Rehabilitation 2002;17:251–256.
12. Neumann D, Zupan B, Babbage DR, Radnovich AJ, Tomita M,
Hammond F, Willer B. Affect recognition, empathy, and dysosmia
after traumatic brain injury. Archives of Physical Medicine
Rehabilitation 2012;93:1414–1420.
13. Sigurdardottir S, Jerstad T, Andelic N, Roe C, Schanke A-K.
Olfactory dysfunction, gambling task performance and intracranial
lesions after traumatic brain injury. Neuropsychology
Downloaded by [] at 09:50 11 December 2015
2010;24:504–513.
14. de Kruijk JR, Leffers P, Menheere PPC, Meerhoff S, Rutten J,
Twijnstra A. Olfactory function after mild traumatic brain injury.
Brain Injury 2003;17:73–78.
15. Roberts MA, Simcox AF. Assessing olfaction following pediatric
traumatic brain injury. Applied Neuropsychology 1996;3:86–88.
16. Jacobi G, Ritz A, Emrich R. Cranial nerve damage after paediatric
head trauma: a long-term follow-up study of 741 cases. Acta
Paediatrica Hungarica 1986;27:173–187.
17. Sandford AA, Davidson TM, Herrera N, Gilbert P, Magit AE,
Haug K, Gutglass D, Murphy C. Olfactory dysfunction: a sequela
of pediatric blunt head trauma. International Journal of Pediatric
Otorhinolaryngology 2006;70:1015–1025.
18. Harris R, Davidson TM, Murphy C, Gilbert PE, Chen M. Clinical
evaluation and symptoms of chemosensory impairment: one thou-
sand consecutive cases from the Nasal Dysfunction Clinic in San
Diego. American Journal of Rhinology 2006;20:101–108.
19. Schecklmann M, Schwenck C, Taurines R, Freitag C, Warnke A,
Gerlach M, Romanos M. A systematic review on olfaction in child
and adolescent psychiatric disorders. Journal of Neural
Transmission 2013;120:121–130.
20. Karsz FR, Vance A, Anderson VA, Brann PG, Wood SJ, Pantelis C,
Brewer WJ. Olfactory impairments in child attention-deficit/hyper-
activity disorder. Journal of Clinical Psychiatry 2008;69:1462–
1468.
21. Martzke JS, Swan CS, Varney NR. Posttraumatic anosmia and
orbital frontal damage: Neuropsychological and neuropsychiatric
correlates. Neuropsychology 1991;5:213–225.
22. Yousem DM, Geckle RJ, Bilker WB, McKeown DA, Doty RL.
Posttraumatic olfactory dysfunction: MR and clinical evaluation.
American Journal of Neuroradiology 1996;17:1171–1179.
Brain Inj, Early Online: 1–8
23. Levin HS, High WM, Eisenberg HM. Impairment of olfactory
recognition after closed head injury. Brain 1985;108:579–591.
24. Costanzo RM, Becker DP. Smell and taste disorders in head injury
and neurosurgery patients. In: Meiselman HL, Rivlin RS, editors.
Clinical measurements of taste and smell. New York: Macmillan
Publishing Company; 1986. p 565–578.
25. Fujiwara E, Schwartz ML, Gao F, Black SE, Levine B. Ventral
frontal cortex functions and quantified MRI in traumatic brain
injury. Neuropsychologia 2008;46:461–474.
26. Green P, Rohling ML, Iverson GL, Gervais RO. Relationships
between olfactory discrimination and head injury severity. Brain
Injury 2003;17:479–496.
27. Doty RL, Yousem DM, Pham LT, Kreshak AA, Geckle R, Lee
WW. Olfactory dysfunction in patients with head trauma. Archives
of Neurology 1997;54:1131–1140.
28. Haxel BR, Grant L, Mackay-Sim A. Olfactory dysfunction after head
injury. Journal of Head Trauma Rehabilitation 2008;23:407–413.
29. Sumner D. Post-traumatic anosmia. Brain 1964;87:107–120.
30. Renzi G, Carboni A, Gasparini G, Perugini M, Becelli R. Taste and
olfactory disturbances after upper and middle third facial fractures:
a preliminary study. Annals of Plastic Surgery 2002;48:355–358.
31. Bakker K, Catroppa C, Anderson V. Olfactory dysfunction in
pediatric traumatic brain injury: a systematic review. Journal of
Neurotrauma 2014;31:308–314.
32. Crowe LM, Catroppa C, Babl FE, Rosenfeld JV, Anderson V.
Timing of Traumatic Brain Injury In Childhood And Intellectual
Outcome. Journal of Pediatric Psychology 2012;37:745–754.
33. Anderson V, Spencer-Smith M, Leventer R, Coleman L, Anderson
P, Williams J, Greenham M, Jacobs R. Childhood brain insult: can
age at insult help us predict outcome? Brain 2009;132:45–56.
34. Menon DK, Schwab K, Wright DW, Maas AI. Position statement:
definition of traumatic brain injury. Archives of Physical Medicine
& Rehabilitation 2010;91:1637–1640.
35. Pink B. Socio-economic indexes for areas (SEIFA). Canberra,
Australia: Australian Bureau of Statistics; 2011.
36. Teasdale G, Jennett B. Assessment of coma and impaired con-
sciousness. A practical scale. Lancet 1974;2:81–84.
37. Roberts G, Howard K, Spittle AJ, Brown NC, Anderson PJ, Doyle
LW. Rates of early intervention services in very preterm children
with developmental disabilities at age 2 years. Journal of
Paediatrics and Child Health 2008;44:276–280.
38. Greenham M, Spencer-Smith MM, Anderson PJ, Coleman L,
Anderson VA. Social functioning in children with brain insult.
Frontiers of Human Neuroscience 2010;4:1–10.
39. Mackay-Sim A, Doty RL. The University of Pennsylvania Smell
Identification Test: normative adjustment for Australian subjects.
Australian Journal of Otolaryngology 2001;4:174–177.
40. Volker MA. Reporting effect size estimates in school psychology
research. Psychology in the Schools 2006;43:653–672.
41. Doty RL. Assessment of olfaction. In: Brewer W, Castle D,
Pantelis C, editors. Olfaction and the Brain. Cambridge:
Cambridge University Press; 2006. p 235–258.
42. Cameron EL, Doty RL. Odor identification testing in children and
young adults using the smell wheel. International Journal of
Pediatric Otorhinolaryngology 2013;77:346–350.
43. Dalton P, Mennella JA, Maute C, Castor SM, Silva-Garcia A,
Slotkin J, Grindle CR, Parkes W, Pribitkin EA, Reilly JS.
Development of a test to evaluate olfactory function in a pediatric
population. Laryngoscope 2011;121:1843–1850.