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Original Article

Predictors of Long Term Neurological Outcome in


Bacterial Meningitis
Pratibha Singhi, Arun Bansal, P. Geeta and Sunit Singhi

Department of Pediatrics, Postgraduate Institute of Medical Education and Research, Chandigarh.


[Received June 26, 2006; Accepted November 1, 2006]

ABSTRACT
Objective. To study the long-term neurological and developmental outcome and the clinical and laboratory predictors of
sequelae in children with acute bacterial meningitis (ABM).

Methods. Detailed clinical and demographic data was retrieved from the medical records of study children. Subsequently
they were followed up for a minimum of 12 months after discharge for development, neurological and hearing assessment.
All sequelae were identified and divided into minor or major. For analysis data was divided into 2 groups those with
sequelae and without sequelae at follow-up. Statistical analysis was done using SPSS version 10.00 and Epi Info version
2000.

Results. 61 boys and 19 girls, a mean age of 31.4±41.9 months at the time of ABM, were included in the study. Of these
62.5% children were infants. Mean age at follow-up was 58.6 ± 47.2 months. Sequelae were observed in 32 (40%) children
(8 (10%) minor and 24 (30%) major). Mean social quotient at follow-up was 92.8 ± 32.6. Developmentally 22 (37.9%)
children were normal and 20 (34.5%) had global delay. Seizures (P=0.015), cranial nerve palsy (P=0.0065), abnormal deep
tendon reflexes (P=0.002), Glasgow coma scale score (GCS) < 8 (P = 0.044) at admission, a CSF culture positive for
bacteria and abnormal findings on ultrasonography or computed tomography of head at admission had significant
association with sequelae at follow-up. All children (7/7) who had infarct on CT scan (P=0.001) and 12 (80%) of 15 patients
who had hydrocephalus (OR - 9.0, 95% CI – 2.03-45.6, P=0.001) diagnosed on CT scan developed severe sequelae. On
multiple regressions GCS score <8, presence of cranial nerve palsy and abnormal deep tendon reflexes were independent
predictors of sequelae.

Conclusion. Neurological and audiological sequelae and global developmental delay may be seen in about one third of
survivors of bacterial meningitis. GCS score <8, presence of infarct or cranial nerve palsy, or hydrocephalous on CT/
ultrasound at admission may help in identification of children most likely to need long term follow up and rehabilitation.
[Indian J Pediatr 2007; 74 (4) : 369-374] E-mail : dr_singhi@yahoo.com

Key words : Children; Acute bacterial meningitis; Neurological sequelae; Developmental delay; Outcome.

Acute bacterial meningitis remains an important countries, Baraff and colleagues 4 found an overall
problem in pediatric practice, marked by continuing mortality of 4.5% and a 15% incidence of major
significant mortality and morbidity in spite of adequate neurological sequelae. On comparing data from
treatment. The pathogens responsible for most cases of developed countries with that of developing countries,
meningitis in children in developing countries are they found lower mortality (4.8% vs 9.1%) in developed
Streptococcus pneumoniae and Hemophilus influenzae type countries. The probabilities of deafness (10.5% vs
b (Hib). 1-3 Neurological abnormalities occur with 11.1%); mental retardation (4.2% vs. 4.8%); spasticity
increased frequency in children who have had and/or paresis (3.5% vs 3.5%) and seizure disorder
meningitis. In a meta-analysis of 19 prospective studies (4.2% vs 5.0%) were also higher in developing
involving 1434 patients with meningitis in developed countries. Long-term complications range from subtle
forms of cognitive impairment to devastating
neurological handicaps. Various clinical and
laboratory parameters have been implicated in the
Correspondence and Reprint requests : Dr. Sunit Singhi,
Professor, Department of Pediatrics, Advanced Pediatric Centre, prognosis of acute bacterial meningitis. Almost all the
PGIMER, Chandigarh- 160 012. Phone : 0172- 2746699 (Office), published information regarding long term neuro­
0172-2715619 (Res.) developmental outcome has come from developed

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52

P. Singhi et al

countries5-12 with a few reports of systematic research age. Additionally, detailed neurodevelopment
regarding this from developing countries13-16 including assessment was done using the scheme from Amiel
India. 17, 18 The authors have studied the long-term Tison.19 This included neuro-motor status (active and
neurological and developmental outcome following an passive tone, reflexes and asymmetry), neuro­
episode of acute bacterial meningitis, and clinical and behavioral status (seizures, hyper excitability and
laboratory predictors of the long-term neurological lethargy), neuro-sensory status (vision and hearing test
outcome. Early prediction of poor neurological outcome audiometry and BERA, as indicated). Vineland Social
may help the physician in selecting children who may Maturity Scale (VSMS), Nagpur modification 20 was
require extensive follow-up and whose parents need to used for psychomotor testing.
be counseled.
All sequelae were identified and divided into minor
or major. Major sequelae included blindness,
MATERIALS AND METHODS hydrocephalus, microcephaly, quadriplegia, severe
mental retardation and uncontrolled seizures. Minor
sequelae included extra-pyramidal movements, hearing
This study was conducted in a tertiary care hospital of loss, hemiparesis, hyperactivity, peripheral facial palsy,
North India. The study was approved by Institutional mild mental retardation and language delay.
Ethics committee. Informed written consent was
obtained from the parents/guardian of the subjects. The Statistical analysis was performed with SPSS for
subjects eligible in the study were children between 2 Windows, version 10.0. Data from children having
months to 12 years old who were diagnosed and sequelae (minor sequelae and major sequelae) was
treated as meningitis during January 1990 to December compared with data from normal children to identify
1995. The diagnosis of meningitis was made based on the variables having significant association with
the clinical features and CSF findings. The suggestive sequelae using t-test. Comparison of means was done.
clinical features included presence of impaired Odds ratio and 95% confidence interval were
consciousness, convulsions and signs of meningeal calculated using Epi info version 2000. Multiple
irritation (such as bulging anterior fontanel, neck regressions were used to identify predictors of sequelae.
stiffness, Kernig’s sign, Brudzinski sign) in a febrile
child. The diagnosis of bacterial meningitis was made if
RESULTS
CSF grew bacteria on culture. Patients with a negative
culture were diagnosed to have bacterial meningitis if
they had presence of CSF polymorphonuclear (PMN) Eighty children (61 boys, 19 girls) were included in the
cell count > 6/mm3, CSF to blood glucose ratio <60% or study. They had meningitis at a mean age of 31.4 ± 41.9
CSF glucose < 40 mg/dl and proteins > 40 mg/dL with months (range 2 - 144 months); 30 children were > 1
either CSF gram stain positive or blood culture positive year of age, 50 (62.5%) were infants; of these 33 were ≤6
or in absence of both a normal chest X-ray and negative months of age. The mean age at follow-up was 58.6 ±
montoux test. Excluded from the study were children 47.2 months (range 14 - 189 months). Mean duration
having any other systemic or chronic disease, after which follow up was done was 27.2 ± 24.5 months
immunodeficiency, ventriculo-peritoneal shunt, (range 12-44 months; median 15 months).
developmental delay or hearing impairment prior to
diagnosis of acute bacterial meningitis. One hundred TABLE 1. Various Sequelae Seen at Follow-up in Survivors of
and eighty eight children with a diagnosis of bacterial Bacterial Meningitis (n-80, Total Affected Patients­
meningitis were admitted during study period. Forty 32)
three (23.8%) children died during the acute illness. Of Major sequelae n (%)
the 145 survivors only 80 survivors could be traced
through letters and personal visits; 65 could not be Blindness 2 (6.3)
contacted either because of change of address, or Hydrocephalus 6 (18.8)
Microcephaly 3 (9.4)
incomplete/wrong address. Quadriplegia 3 (9.4)
The minimum period after which follow-up was Severe mental retardation 17 (53.1)
Uncontrolled seizures 3 (9.4)
done was 12 months after discharge. In all children the Minor sequelae (%)
demographic and clinical data at the time of acute Extrapyramidal movements 1 (3.1)
illness was retrieved from medical records. Detailed Hearing loss 5 (15.6)
history including occurrence of seizures post discharge Hemiparesis 8 (25)
was recorded. Physical examination included Cranial nerve palsy 8 (25)
Mild mental retardation 7 (21.9)
anthropometry, general and systemic examination.
Language delay 8 (25)
Development was assessed using Denver Development
Screening Test (DDST) in 58 children below 6 years of Many patients had more than one sequelae.

370 Indian Journal of Pediatrics, Volume 74—April, 2007


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Predictors of Long term Neurological Outcome in Bacterial Meningitis

Neurological outcome: Of the 80 survivors, 32 (40%) charts was done, 22 (37.9%) were developmentally
children had sequelae on follow up, 24 (30%) major and normal, 20 (34.5%) had global delay, 4 (6.8%) were
8 (10%) minor sequelae. These are listed in Table 1. The abnormal in at least one sector and 12 (20.6%) had a
most common major sequela was severe psychomotor questionable one or two sectors.
retardation and minor sequela was speech delay.
Abnormal physical growth at follow-up was seen in 10 Predictors of sequelae
(14.3%) children, 9 of them had sequelae (Odds ratio
Clinical features: Seizures at admission had a significant
18.4, 955 CI- 2.1-411.3; P=0.0008).
association with sequelae at follow-up (Table 2).
Psychometric outcome: Mean social quotient (SQ) at Presence of cranial nerve palsy (P=0.0065) or abnormal
follow-up was 92.8±32.6; 17 children had an SQ <70, reflexes (P=0.002) was also associated significantly
and 56 had SQ >80. Neurological sequelae were seen in with sequelae on follow-up (Table 2). Almost half of the
all the 17 children with a SQ<70 (all minor) and 6 of 7 patients with a GCS of less than 8 (P=0.044), abnormal
children with an SQ between 70-80 (1 major and 5 tone (P=0.071) or abnormal power (P=0.076) at
minor). admission had severe sequelae on follow-up (Table 2).
Delayed physical growth (weight and height) and
Development outcome: Of 58 children below 6 years
microcephaly on follow-up correlated with poor
of age in whom developmental assessment using DDST
TABLE 2. Neurological Outcome with Respect to Demographic, Clinical and Laboratory Parameters at Admission

Variables n Affected Outcome at Follow-up


(%) No Sequelae Sequelae present Odds ratio P value
(n-48) (n-32) (95% CI)
Major Minor Total

Age < 1 year 80 5 0 (62.5) 32 2 16 18 0.64


(0.23-1.78) 0.479
Male Sex 80 6 1 (76.3) 36 7 18 25 1.19
(0.37-3.93) 0.957
Malnutrition 80 5 2 (65) 27 8 17 25 2.78
(0.91-8.71) 0.077
Seizures 80 5 1 (63.8) 25 5 21 26 3.99
(1.26-13.17) 0.015
GCS <8 80 2 7 (33.7) 12 2 13 15 2.7
(0.9-7.7) 0.044
Cranial nerve palsy 80 1 1 (13.8) 2 5 4 9 9.0
(1.6-66.0) 0.0065
Abnormal tone 80 2 8 (35) 13 1 14 15 2.38
(0.84-6.81) 0.071
Abnormal power 80 1 7 (21.2) 7 2 8 10 2.66
(0.79-9.17) 0.076
Abnormal reflexes 80 4 3 (53.7) 19 5 19 24 4.58
(1.55-13.95) 0.002
CSF culture
Sterile 56 (70) 36 7 13 20
S. pneumoniae 80 6 (7.5) 0 0 6 6 - 0.019
H. influenzae 13 (16.3) 9 0 4 4
Others 5 (6.2) 3 1 1 2

Blood culture
Sterile 66 (82.5) 44 8 14 22
S. pneumoniae 2 (2.5) 0 0 2 2
H. influenzae 80 4 (5.0) 2 0 2 2 - 0.06
S. aureus 1 (1.2) 0 0 1 1
Others 7 (8.8) 2 0 5 5

USG Head-Abnormal 3 8 1 7 (44.7) 7 1 9 10 2.7


(0.79-9.17) 0.011
CT scan Head­ 35 2 6 (74.3) 10 2 14 16 3.8
Abnormal (1.28-11.49) 0.006

Abbreviations: USG = ultrasonography, CT scan = Computed tomography


Results of clinical parameters, viz, fever, headache, vomiting, excessive crying, refusal to feed, impaired consciousness, meningeal signs
and papilledema and laboratory parameters, viz, CSF cell count, protein and sugar were non-significant when compared between the
above 2 groups (p>0.05)

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P. Singhi et al

neurological outcome. 13.3; p-0.429).


Laboratory features: CSF culture positive for bacteria Neurological-disability at discharge: Twenty-four
had a significant association with sequelae (Table 2). children had a disability at discharge and it persisted in
Abnormal findings on ultrasonography or computed 22 (91.7%). Of these, 6 had minor and 16 had major
tomography of head at admission had significant sequelae (OR – 50.6; 95% CI- 9.1-373.7; p-0.0000).
association with sequelae on follow-up (p < 0.05) Sequelae were not apparent at the time of discharge in a
(Table 2). All seven children who had infarct (P=0.001) number of children.
and 12 (80%) of 15 patients who had hydrocephalus
Multiple regressions: A GCS score < 8, presence of a
(OR- 9.0, 95% CI – 2.03-45.6, p-0.001) on CT scan,
cranial nerve palsy and abnormal deep tendon reflexes
developed severe sequelae. None of the other CSF or
were independent predictors of major/all sequelae and
blood parameters correlated with morbidity.
correctly predicted the outcome in about 80% cases
Complications: Thirty-six children had developed (Table-3)
complications during hospital stay, of these 13 were
without sequelae on follow-up, 3 had minor sequelae DISCUSSION
and 20 had major sequelae (OR - 6.9; 95% CI- 2.3 – 21.4;
P–0.00008). Seizures (n-12) after hospitalization were
associated with sequelae in 83% (10 of 12 patients, OR – The authors' have found that the overall prevalence of
10.5; 95% CI – 1.9-76.0; p-0.0024). Nosocomial infection neurological sequelae among the survivors of acute
(n-19) also had significant association with sequelae (14 bacterial meningitis was 40% and of major sequelae
of 19 patients, OR – 6.7; 95% CI – 1.9 – 25.3; p-0.001). 30%. The reported worldwide frequency of neurological
Ventriculitis, seen in 7 children, did not have an sequelae has varied from 10-50% ,21 but from the
association with sequelae (OR – 2.1; 95% CI – 0.4 – developed world it is around 10-20%.4-9 Various studies

TABLE 3. Multiple Regression Model Showing Predictors of Long Term Sequelae in Patients with Bacterial Meningitis

Variable β -weight S.E. Exp (B) 95% CI p-value

All Sequelae

GCS<8 -1.706 0.581 0.182 0.06-0.57 0.003


Cranial nerve palsy -2.487 0.958 0.083 0.01-0.54 0.009
Absent deep tendon reflexes -1.625 0.583 0.197 0.06-0.62 0.005
Major sequelae
GCS < 8 -1.696 0.599 0.185 0.06-0.60 0.005
Absent deep tendon reflexes -1.613 0.601 0.199 0.06-0.65 0.007

TABLE 4. Comparison of Long Term Neurological Outcome and Sequelae in Children with Bacterial Meningitis in Recently
Published Studies from India and Other Developing Countries

Index study George CN et al, Chinchankar N Goetghebuer T Wandi F


(n=80) 2002 17 , India et al18 , 2002, et al13 , 2000, et al14 , 2005,
(n=100) India Gambia Papua New
(n=31) (n=73) Guinea (n=80)

Mean age at the time of meningitis, months 31.4 - 13.7 # -


Mean age at follow-up, months 58.6 80 - - -
Length of follow–up, months 12-44
(Mean-27.2;
median 15) 55-90 12-36 10-93 38.4
Neurological sequelae
Major 32 (40%) * 17 (55%) 34 (47%) -
Minor 24 - - 14 -
8 - - 20 -
Global developmental delay 20 (34%) 23 (23%) 9 (29%) - 18 (23%)
Sensorineural hearing loss 5 (6%) 6 (6%) 4 (13%) 18 (25%) 23 (29%)
Persistent seizures 3 (4%) 13 (13%) 12 (39%) 14 (19%) 5 (6%)
Mental retardation 24 (30%) 20 (20%) 2 (6.5%) 16 (22%) -
Moderate-severe 17 2 - - -
Mild 7 18 - - -

• *Total children with neurological sequelae not mentioned in the study, but various sequelae noted were spasticity-6, hemiparesis-5,
quadriparesis-1, and ataxia-1.
• # Mean age in Pneumoccocal meningitis group: 12.5 months and in Haemophilus influenzae-b group: 9.8 months.

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Predictors of Long term Neurological Outcome in Bacterial Meningitis

from India have reported the incidence of neurological gender, low body temperature, seizures before
sequelae ranging from 40-55%17, 18 (Table 4). A higher presentation and duration of meningeal signs were
frequency of sequelae in their population could partly reported as predictors of outcome by Oostenbrink R et
be due to late presentation of patients (25% of their al. 10 However, in our study, gender, temperature,
patients were referred after pretreatment with meningeal signs, CSF cells > 100/cmm, high proteins
antibiotics). Another factor that could have been and hypoglycorrhachia did not have any impact on
responsible is the variation in method of classifying the outcome. Young age, delay in starting treatment,
sequelae in other studies: a clear categorization of presence of positive cultures of samples other than CSF
minor and major sequelae has been done in very few and malnutrition have also been reported as risk
studies.22-23 factors for poor outcome. 29, 30 We did not find any
association of outcome with any of these factors.
The spectrum of neurological sequelae in their
patients was similar to that reported in other studies Many studies have reported that the causative
viz, sensorineural hearing loss, motor problems, organism influences the outcome. Streptococcus
seizures and mental retardation. Wide variations in the pneumoniae has been implicated significantly with
rates of adverse sequelae associated with infection by neurological sequelae in many studies 8, 12, 25. In the
different organisms and also variations within groups present study, they found a statistically significant
of organisms have been reported. Most common difference in outcome between meningitis caused by
neurological sequelae seen in the present study was Streptococcus pneumoniae and those with H. influenzae b
severe mental retardation (21%). The reported or other organism. All 6 cases that had Streptococcus
frequency of mental delay has varied between 5-24% pneumoniae in CSF developed severe sequelae on follow-
worldwide 4, 10, 13. Incidence of severe sensorineural up. The choice of antibiotic did not make any significant
hearing loss seen in this study (6.2%) is lower than that difference in the long-term outcome. Similar observation
reported; worldwide it has varied between 5.6 – 23%8, 24, has been made by Peltola et al31 and Del Rio et al32
25
. Cherian B et al 26 from Ludhiana reported 28.1%
Seizures, and hydrocephalus and infarct on imaging
incidence of senserineural hearing loss. Two of the five
were associated with significantly poor outcome in the
cases with hearing impairment had H. influenzae b; one
present study. Grimwood et al 33 found that acute
pneumococcus and 2 had no identifiable organism in
neurologic complications (39%) in meningitis were
CSF. Kaplan et al 27 have noted greater incidence of
associated with an adverse outcome as compared to
deafness in children who had pneumococcal
uncomplicated meningitis (18%). Similar findings have
meningitis (33%) than in those with H. influenzae b (9%)
been reported by Taylor et al.34
or meningococcal (5%) meningitis.
The authors found that seizures at the time of
CONCLUSION
presentation, low GCS, cranial nerve palsy and
abnormal reflexes correlated significantly with poor
outcome. Seizures are a reflection of the underlying The authors conclude that in their population children
brain abnormality and many studies have reported with bacterial meningitis are at a high risk of abnormal
increased mortality and morbidity among patients who neurological and audiological sequelae. Presence at
had seizures during the acute phase of bacterial admission of coma (GCS score <8), focal neurological
meningitis.24 In one study of H. influenzae meningitis, deficits especially cranial nerve palsy and abnormal
50% of the patients who presented with seizures at the deep tendon reflexes, and presence of infarct or
time of admission went on to die or to have major hydrocephalous on radio imaging can help in
neurological sequelae.28 identifying children who are likely to have poor
Low GCS (<8) and focal nerve deficits at the time of neurological outcome. This can facilitate planning long-
acute illness were independent predictors of sequelae in term follow-up and ensure adequate rehabilitation of
this study; which is similar to some published data on survivors.
neurological sequelae. 29, 30 A study from Africa 29 has
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