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ABSTRACT.
also seen. However, the aetiology often
Purpose: To evaluate ophthalmological abnormalities in children with acute
remains unknown in up to 50% of the
encephalitis.
cases. The symptoms of acute
Methods: Thirty-six children included in a hospital-based prospectively and encephalitis are similar in children
consecutively collected cohort of children with acute encephalitis were investi- and adults with most cases presenting
gated for ophthalmological abnormalities. The investigation included clinical with fever, headache and altered sen-
ophthalmological examination, fundus photography, neuro-ophthalmological sorium. Focal neurological symptoms
examinations as well as visual and stereo acuity. Results on laboratory or seizures may also be present. The
examinations, clinical findings, neuroimaging and electroencephalography reg- long-term outcome after encephalitis in
istrations were recorded for all children. childhood varies from death or severe
Results: The median age was 4.0 years (Interquartile Range 1.9–9.8). The sequelae to full recovery. Predicting the
aetiology was identified in 74% of cases. Three of 36 patients were found to have prognosis after encephalitis in child-
abnormal ophthalmological findings related to the encephalitis. Transient sixth hood is difficult due to an often weak
nerve palsy was seen in a 15-year-old child and transient visual impairment was relationship between the clinical pic-
seen in a 3.5-year-old child. Bilateral miosis and ptosis, i.e. autonomic nerve ture in the acute phase and the preva-
system symptoms, were seen in an 11-month-old child, with herpes simplex 1 and lence of remaining sequelae (Fowler
et al. 2010; DuBray et al. 2013;
N-methyl-D-aspartate receptor antibody encephalitis. All three children recov-
Michaeli et al. 2014). Some correlation
ered and improved their ophthalmological function with time.
is seen with a worse outcome in agents
Conclusion: Only 3 of 36 children were found to have ophthalmological that cause necrosis or vasculitis, e.g.
abnormalities due to encephalitis and they all improved with time. Thus, HSV-1, but the individual variation in
ophthalmological consultation does not seem to fit in a screening programme for a given aetiology is large.
childhood encephalitis but should be considered in selected cases. Ophthalmological complications
have been reported in association with
Key words: central nervous system – infection – neurological – ophthalmological out- CNS infections and often seem to be
come – paediatric agent specific. Known ocular com-
plications in, for instance, herpetic
Acta Ophthalmol. 2017: 95: 66–73 viral infections include conjunctivitis,
ª 2016 Acta Ophthalmologica Scandinavica Foundation. Published by John Wiley & Sons Ltd dacryoadenitis, episcleritis, keratitis,
iritis and optic neuritis (Matoba 1990;
doi: 10.1111/aos.13305
Chong et al. 2004). Ophthalmoplegia
estimated to be 2–18/100.000 child- and cranial nerve palsies have also
Introduction years (Koskiniemi et al. 1997; Clarke been documented in association with
Infections in the central nervous system et al. 2006; Thompson et al. 2012). encephalitis in a limited amount of
(CNS) are relatively uncommon but Encephalitis is often caused by studies, and mostly in small case series
potentially devastating. viruses such as herpes simplex virus (Correll et al. 2015; Malcles et al.
The true incidence of encephalitis is (HSV), enterovirus, varicella zoster 2015). Ptosis and sixth nerve palsy
difficult to estimate due to differences virus (VZV), influenza virus or arthro- were reported in two cases with diag-
in reporting systems, but the highest pod-borne viruses, e.g. tick-borne nosed encephalitis due to influenza type
incidence is seen in young children and encephalitis (TBE) virus or West Nile A (Migita et al. 2001). In a case series
in the elderly. In the western world the virus, but cases due to bacteria, fungi of 24 patients with HSV caused brain-
incidence of childhood encephalitis is or autoimmune-mediated disease are stem encephalitis 81% had neuro-
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Acta Ophthalmologica 2017
ophthalmological symptoms such as Demographic characteristics, clinical magnetic resonance imaging (MRI)
abnormal ocular movements, nystag- signs and symptoms were recorded for was performed in 15/36.
mus, anisocoria, ptosis, spasmodic all children. All children included in the study
movements and oscillopsia (Livorsi Blood and cerebrospinal fluid underwent an EEG examination within
et al. 2010). Acute retinal necrosis is a (CSF) were prospectively sampled the first days of admission. Episodic or
well-known and feared sight-threaten- according to the study protocol as continuous, focal or generalized, slow
ing condition, which has been strongly well as when clinically motivated. All activity (delta and/or theta) with or
associated with HSV and in some cases children underwent routine laboratory without epileptiform discharges were
also to Epstein–Barr virus (EBV) tests of serum at the time of admis- considered as EEG abnormalities com-
caused neuroinflammation (Kim et al. sion including serology, CRP and patible with encephalitis.
2011; Papageorgiou et al. 2014). How- WBC. Antibody titres in blood were Visual acuity (VA) was evaluated
ever, few, if any, studies have described analysed for Borrelia Burgdorferi and with age appropriate methods and
ophthalmological findings in a paedi- TBE virus in all, and depending on according to general health condition.
atric population with clinical clinical symptoms some cases were Monocular VA was measured when
encephalitis of unselected origins. tested for enterovirus, adenovirus, possible. The youngest children were
The purpose of this study was to mycoplasma pneumoniae, HSV1 and assessed with the Teller Acuity Cards
evaluate ophthalmological findings at HSV2. Lumbar puncture (LP) was (Teller 1979) and the Cardiff Acuity
illness onset in a hospital-based con- performed during the acute phase Test (Adoh & Woodhouse 1994;
secutively recruited population of chil- with routine analysis of the CSF, Sharma et al. 2003). When these tests
dren with encephalitis of various and including WBC, levels of protein, were not possible to use, due to lack of
unselected aetiological origin. glucose, lactate and microbiological co-operation, the child0 s visual beha-
analyses. Microbiological analysis of viour was assessed using coloured
the CSF included bacterial culture sugar strands. For the preschool chil-
Materials and Methods and virological tests for HSV1, dren, the HVOT or LH symbols were
Children aged 28 days to 16 years with HSV2, VZV and enterovirus with used for evaluation of recognition acu-
acute encephalitis and meningoen- polymerase chain reaction (PCR) ity and, for school children, the KM
cephalitis who were admitted to our and/or intrathecal antibody produc- letter chart was used (Hedin et al.
primary and tertiary care hospital in tion. Depending on season and the 1980; Hyvarinen et al. 1980; Moutakis
northern Stockholm, between May clinical picture, the CSF was also et al. 2004). All numerical values of VA
2011 and May 2013, were enrolled in tested for other aetiologies, such as were transferred to decimal values,
this study. The diagnosis of encephali- Borrelia Burgdorferi, human herpes according to the literature, to facilitate
tis was based on the following criteria: virus 6, parechovirus, cytomegalovirus comparisons (Rydberg et al. 1999;
(1) signs of cerebral dysfunction either and EBV in some cases. Tests for Leone et al. 2014; Larsson et al. 2015).
as (i) encephalopathy defined as altered antibodies directed at neuronal anti- Stereo acuity was assessed with the
consciousness, personality or beha- gens, such as N-methyl-D-aspartate Lang (I or II) or the TNO stereo test
vioural changes lasting for more than receptor (NMDAR) antibodies, were (Ancona et al. 2014) and was defined
24 hr, or (ii) abnormal electroen- not routinely done. However, in chil- as present if at least one item was
cephalography (EEG) findings compat- dren where the initial aetiological identified, and absent if none was.
ible with encephalitis, plus at least one screening was negative and in whom A thorough clinical examination of
of the following: abnormal results of no clinical improvement was seen, the eyes was performed using slit
neuroimaging compatible with tests for neuronal antibodies were lamp and funduscopy. Fundus photog-
encephalitis, positive focal neurologi- considered. Nasopharyngeal aspirate raphy was taken when possible.
cal findings or seizures. Cases with was tested for respiratory viruses Neuro-ophthalmological examinations
abnormal EEG findings compatible when respiratory symptoms were pre- included pupils, ocular motility, nys-
with encephalitis but not showing sent. Faeces were analysed with PCR tagmus and ocular alignment.
abnormalities on neuroimaging, focal for enterovirus and if gastrointestinal
neurological findings, seizures or symptoms were present most children
Ethical approval
encephalopathy were classified as were also tested for norovirus, sapo-
meningoencephalitis. (2) Signs of virus and rotavirus. The detection of This study was approved by the
inflammation, defined either as pleocy- a viral agent in the CSF or intrathecal local ethics committee (Dnr 2010/
tosis (≥6 white blood cells/ll), fever production of antibodies and the 1206-31/1).
(>38°C) or elevated infectious parame- presence of antibodies against TBE
ters, C-reactive protein (CRP) and virus in serum was defined as con-
white blood cells (WBC). Catarrhalia firmed aetiologies, whereas other
Results
was considered not to be sufficient. agents found in blood, faeces or Thirty-six patients (26 girls and 10 boys)
Children with another verified cause of nasopharynx were labelled as proba- who fulfilled the inclusion criteria under-
symptoms such as bacterial meningitis ble aetiologies. went ophthalmological examinations on
or other underlying neurological or In children who underwent neu- at least one occasion at the time of onset.
metabolic disease that per se could roimaging, pathological changes com- Median age at first examination was
explain the symptoms were excluded. patible with encephalitis were recorded. 4.0 years (interquartile range 1.9–9.8,
Pure ataxia was not considered A computer tomography (CT) was distribution in years and gender is
sufficient neurology for inclusion. performed in 22/36 patients, whereas shown in Fig. 1).
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Acta Ophthalmologica 2017
Age at
onset
Years:
Case Agents Gender months VA RE VA LE VA Binoc Method Stereo Neurological signs CT/MRI
1 Rota- and M 03:07 0.16 0.2 0.25 LH linear Neg Visual impair, seizures, N
Sapovirus balance problems,
hallucinations
2 Influenza B F 03:11 0.25 0.4 LH linear Neg Seizures, esotropia N
3 Unknown M 15:10 1 1 KM 550″ Sixth nerve palsy N
4 HSV and F 00:11 Ptosis, miosis, seizures Abn
NMDAR ab
5 Enterovirus F 06:05 1 1 KM 60″
6 Unknown M 06:05 1 1 HVOT 60″ Seizures N
7 Unknown F 02:03 0.63 0.63 Cardiff Ataxia N
8 Mykoplasma F 02:05 0.4 LH single 200″ Seizures N
9 Unknown M 11:06 1 1 KM 30″ Seizures Abn
10 EBV F 16:00 15″ Seizures N
11 Unknown F 16:11 1 1 KM 550″ N
12 NMDAR ab F 07:11 60″ Seizures, dysphasia N
13 Rotavirus F 01:11 0.5 LH at near 200″ Seizures, balance
problems
14 Rotavirus M 02:11 0.65 LH single 550″ Balance problems N
15 Enterovirus F 01:09 16 c/d (appr 0.5) TAC 550″ Seizures, balance N
problems
16 TBE F 07:08 1 1 KM Pos N
17 Unknown F 09:03 27c/d (appr 0.9) TAC Seizures Abn
(Hashimoto)
18 Rotavirus F 03:00 0.63 0.63 LH linear 550″ Seizures N
19 Influenza B F 02:03 0,63 Cardiff 550″ Seizures, balance N
problems
20 TBE+Borrelia F 03:11 0.63 0.63 LH linear 200″
21 Rotavirus M 00:10 Truncal instability
22 Unknown F 12:03 0.3 0.8 KM
23 Norovirus F 01:09
24 Unknown F 15:11 1 1 KM 550″ Seizures, weakness N
left side
25 Rotavirus F 04:04 0.8 0.8 LH linear 200″
26 TBE F 06:09 1 1 KM 550″
27 Unknown M 03:09 0.63 LH linear 550″
(Kawasaki)
28 Unknown M 15:03 N
29 Sapovirus F 01:06 0.63 (6c/d) Cardiff (TAC) 550″ Seizures, balance N
problems
30 TBE M 06:04 0.4 0.4 0.8 LH linear Balance problems
31 Enterovirus F 00:05 600″ Seizures
32 Rotavirus F 00:11 550″ Seizures N
33 Enterovirus M 04:00 0.63 0.5 LH linear 550″ Seizures N
34 Unknown F 01:08 Seizures, balance N
problems
35 TBE F 12:04 1 1 KM 550″
36 EBV F 12:09 1.3 1.3 KM Seizures Abn
HSV = herpes simplex virus, NMDAR = N-methyl-D-aspartate receptor, ab = antibodies, EBV = Epstein–Barr virus, TBE = tick-borne encephali-
tis, m = male, f = female, VA = Visual acuity, RE = right eye, LE = left eye, Binoc = binocular, c/d = cycles per degree, TAC = Teller acuity cards,
neg = negative, pos = positive, visual impair = visual impairment, CT = Computer tomography of the brain, MRI = Magnetic resonance imaging of
the brain, N = normal, Abn = abnormal findings.
myopic. Fundus photographs are Case 4 monocytes/ll). Results from PCR of the
shown in Fig. 4. He received oral A previously healthy girl of 11 months CSF were positive for HSV1. The first
carbanhydrase-inhibitor (Diamox) was admitted to the hospital because of ophthalmological examination on day 2
treatment and recovered fast. The sixth generalized seizures preceded by gas- revealed bilateral miosis and a sluggish
nerve palsy had regressed completely troenteritis symptoms and high fever. pupillary reaction to light. No nystag-
on 1 month follow-up, with no remain- Initial CT brain scan was normal. EEG mus, palsy or other ocular motor dys-
ing strabismus and a positive stereo showed left-sided slow activity with function was noted and fundus
acuity. The aetiology to the encephali- spikes and sharp waves. CSF analysis examination was normal. Due to motor
tis remained unknown. revealed a monocytic pleocytosis (24 anxiety and lowered consciousness she
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Acta Ophthalmologica 2017
resolved quickly thereafter. This sug- In our study of an unselected Swed- pneumoniae in an ambulatory child. Case
gests that the cause was the increased ish paediatric cohort with encephalitis, Rep Neurol 3: 109–112.
intracranial pressure and not necessar- a wide distribution of different aetio- Chong EM, Wilhelmus KR, Matoba AY,
Jones DB, Coats DK & Paysse EA (2004):
ily the encephalitis per se. In one other logical agents was seen. There are,
Herpes simplex virus keratitis in children.
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Accepted on September 25th, 2016.
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Correspondence:
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Kerstin Hellgren
Menon V, Singh J & Prakash P (1984): strabismus. Strabismus 7: 1–24.
Department of Neuropediatrics
Aetiological patterns of ocular motor nerve Sharma P, Bairagi D, Kaur K, Khokhar S &
Astrid Lindgren Children’s Hospital
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Karolinska University Hospital, Solna
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S-171 76 Stockholm
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Sweden
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Tel: +468-517 77752
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Fax: +468-672 3330
Migita M, Matsumoto T, Fujino O, Takaishi Ocular manifestations of head injury and
Email: kerstin.hellgren@ki.se
Y, Yuki N & Fukunaga Y (2001): Two incidence of post-traumatic ocular motor
cases of influenza with impaired ocular nerveinvolvement in cases of head injury: a Financial support without any role in the design
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85. Teller DY (1979): The forced choice preferen- Stockholm County Council, IKEA Foundation,
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Nandi S & Biswas A (2014): Isolated bilateral Arch Dis Child 97: 150–161.
and Lena Falkman for help in examining the
abducent nerve palsy in infectious mononu- Vandercam T, Hintzen RQ, de Boer JH & Van
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