Original Article

Journal of Child Neurology

1-6
Clinical Features of and Risk Factors ª The Author(s) 2018
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for Hydrocephalus in Childhood DOI: 10.1177/0883073818799155
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Bacterial Meningitis

Liang Huo, MD1, Yuying Fan, PhD1, Chunying Jiang, MD1, Jian Gao, MD2,
Meng Yin, MD3, Hua Wang, PhD1, Fenghua Yang, PhD1, and Qingjun Cao, PhD1

Abstract
Objective: To explore the clinical characteristics of and analyze the risk factors for hydrocephalus in children with bacterial
meningitis. Methods: Retrospective study of a sample of children with bacterial meningitis seen on the pediatric service of
Shengjing Hospital of China Medical University between January 1, 2010, and December 31, 2016. Results: Overall, 9.36%
(25/267) of patients presented with hydrocephalus. Among patients with hydrocephalus, the age at onset of bacterial meningitis
was usually <6 months, 15 patients had confirmed bacterial etiology, and 1 patient died. The most significant results of multivariate
analysis for hydrocephalus were a rural living situation, altered level of consciousness, previous treatment with antibiotics, initial
cerebrospinal fluid protein >2 g/L, C-reactive protein >100 mg/L, and dexamethasone use. Conclusions: A severe clinical
manifestation and significant laboratory index at admission are the most important predictors of hydrocephalus in children with
bacterial meningitis.

Keywords
hydrocephalus, meningitis, bacterial, children, risk factors

Received August 8, 2017. Received revised November 19, 2017. Accepted for publication November 28, 2017.

Meningitis is estimated to kill 164 000 children globally each cultures and Gram stain make treatment more difficult, partic-
year.1 According to population-based studies, the incidence of ularly in patients with neurologic complications.
acute bacterial meningitis in China ranges from 6.95 to 22.3 With the widespread use of medical imaging technology,
cases/100 000 children <5 years of age, and acute bacterial hydrocephalus caused by bacterial meningitis has recently
meningitis is more common in resource-poor settings.2 The attracted increasing concern. A meta-analysis of the global and
negative consequences of bacterial meningitis in developed regional risks for disabling sequelae from bacterial meningitis
countries has been significantly reduced by vaccination strate- found that since 2010 the overall increase in hydrocephalus in
gies, antibiotic treatment, and good-quality care facilities.3
Many developing countries are still facing cases of bacterial
meningitis in children, which is attributable to nonimplementa-
1
tion of vaccination programs against meningeal pathogens. Department of Pediatrics, Shengjing Hospital of China Medical University,
Although the mortality rate associated with bacterial meningi- Shenyang, China
2
Department of Radiology, Shengjing Hospital of China Medical University,
tis is lower than other major causes of childhood disease, it
Shenyang, China
continues to be high, and approximately 50% of children who 3
Department of Laboratory, Shengjing Hospital of China Medical University,
survive bacterial meningitis develop neurologic complications Shenyang, China
such as subdural effusions or empyemas, cerebral abscesses,
focal neurologic deficits, hydrocephalus, cerebrovascular Corresponding Authors:
Hua Wang, Pediatrics, Shengjing hospital of China Medical University, No.36,
abnormalities, altered mental status, and seizures. Accurate Sanhao Street, Heping District, Shenyang, Liaoning Province, China.
monitoring of pathogen-specific estimates of bacterial menin- Email: wangh1@sj-hospital.org
gitis is challenging in many countries because of the limited Liang Huo, Pediatrics, Shengjing hospital of China Medical University, No.36,
availability of laboratory-based surveillance and the misuse of Sanhao Street, Heping District, Shenyang, Liaoning Province, China.
antibiotics. Late and insufficient results for cerebrospinal fluid Email: 673561281@qq.com
2 Journal of Child Neurology XX(X)

children older than 1 month with bacterial meningitis is 7.1%,4

and hydrocephalus is the main factor of mortality.5
We conducted a single-center study to investigate the clin-
ical features of and risk factors related to hydrocephalus in
children with bacterial meningitis, in order to facilitate early
identification and accurate evaluation.

Materials and Methods

We retrospectively reviewed the records of children aged <14 years
who were treated for bacterial meningitis at the Shengjing Hospital of
China Medical University between January 1, 2010, and December 31,
2016. A confirmed bacterial etiology was based on a positive cere-
brospinal fluid culture, positive results on direct examination of the
cerebrospinal fluid with a negative culture, the presence of soluble
antigens in the cerebrospinal fluid, positive polymerase chain reaction
(PCR) results in the cerebrospinal fluid, or a positive blood culture Figure 1. Age distribution of 276 children with bacterial meningitis.
associated with cerebrospinal fluid pleocytosis (>10 cells/mm3).6-8
Probable bacterial meningitis was diagnosed based on the criteria of
the World Health Organization (WHO)9: clinical signs and symptoms
of meningitis, changes in the cerebrospinal fluid, and lack of an iden-
tifiable bacterial pathogen. Children who did not fulfill the criteria for
bacterial meningitis were excluded from the study, as were children
with tuberculous meningitis and neurobrucellosis.
The following clinical data were obtained and analyzed for every
child who fulfilled the inclusion criteria: demographic information,
clinical manifestations at onset, results of lumbar puncture, results of
laboratory examination (routine and biochemical cerebrospinal fluid
testing, cerebrospinal fluid culture, direct cerebrospinal fluid exami-
nation, blood culture, C-reactive protein level), results of computed
tomography (CT) or magnetic resonance imaging (MRI) of the head,
the therapeutic method used (number and type of antibiotics, use of
dexamethasone, surgery), and outcome. Every child underwent neu-
roimaging at admission and with any change in clinical presentation.
The diagnosis of hydrocephalus was based on neurologic examination
and the neuroimaging report. Evans index (a linear ratio between the
maximal frontal horn width and the maximal width of the inner Figure 2. The number of cases with confirmed bacterial etiology.
skull—normally <0.3)10 was calculated whenever possible if the (Note: Eco, Escherichia coli; Spn, Streptococcus pneumoniae; Kpn, Kleb-
radiologist’s report suggested hydrocephalus. siella pneumoniae; GBS, group B Streptococcus; Lmo, Listeria monocyto-
In order to determine association with the incidence of hydroce- genes; St, Staphylococcus; Nme, Neisseria meningitides; Sma, Serratia
marcescens; Ac, Acinetobacter; GAS, group A Streptococcus; P.Ae,
phalus in children with bacterial meningitis, 14 potentially relevant
Pseudomonas aeruginosa; Sa, Salmonella).
predictors were analyzed: (1) age <12 months; (2) sex; (3) place of
residence (urban vs rural); (4) birth (normal vs preterm); (5) occur-
rence of seizures prior to admission; (6) altered consciousness at the types of hydrocephalus, we used the w2 test. A P value of
time of presentation; (7) initial turbid cerebrospinal fluid with pleo- <.05 was considered statistically significant.
cytosis >5000 cells/mm3; (8) cerebrospinal fluid protein >2.0 g/L; (9)
cerebrospinal fluid glucose <1.1 mmol/L; (10) positive cerebrospinal
fluid culture; (11) C-reactive protein >100 mg/L; (12) previously anti- Results
biotic treatment; (13) initial treatment with dual-agent antibiotic ther- During the 6-year study period, 267 children aged <14 years
apy; and (14) use of dexamethasone. were treated for bacterial meningitis (28 days, n ¼ 99;
28 days–3 months, n ¼ 102; 3-12 months, n ¼ 36; 1-3 years,
n ¼ 13; 3-6 years, n ¼ 11; 6-14 years, n ¼ 6) (Figure 1). A total
Statistical Analysis of 156 patients were males, and 99 children had a confirmed
Data were analyzed using the Statistical Package for the Social bacterial etiology: Escherichia coli (n ¼ 20), Streptococcus
Sciences (SPSS), version 19.0. The odds ratios (ORs) with 95% pneumoniae (n ¼ 19), Klebsiella pneumoniae (n ¼ 14), group
confidence intervals (95% CIs) for an association between the B beta-hemolytic Streptococcus (n ¼ 13), Listeria monocyto-
14 potentially relevant predictors and the incidence of hydro- genes (n ¼ 10), Staphylococcus (n ¼ 8), Neisseria meningitides
cephalus were calculated using logistic regression. To identify (n ¼ 6), Serratia marcescens (n ¼ 4), Acinetobacter (n ¼ 2),
the relationships between laboratory findings and different group A beta-hemolytic Streptococcus (n ¼ 1), Pseudomonas
Huo et al 3

ventriculoperitoneal shunt. Of the patients with hydrocephalus,

12 survived, 1 died, and 12 were lost to follow-up.
On univariate analysis (Table 1), these differences were not
statistically significant (age <12 months, OR: 0.60, 95% con-
fidence interval [CI]: 0.19-1.90, P ¼ .39; male sex, OR: 1.04,
95% CI: 0.46-2.36, P ¼ .93; preterm delivery, OR: 0.56, 95%
CI: 0.22-1.46, P ¼ .23). An association with hydrocephalus
was noted in patients with living in rural areas (OR: 3.56,
95% CI: 1.30-9.80, P ¼ .009), seizures prior to admission
(OR: 15.99, 95% CI: 6.01-42.55, P < .001), altered mental
status (OR: 4.50, 95% CI: 1.93-10.48, P < .039), previous
antibiotic treatment (OR: 5.89, 95% CI: 2.50-13.86, P <
.001), initial cerebrospinal fluid pleocytosis >5000 cells/
mm3 (OR: 13.39, 95% CI: 5.40-33.20, P < .001), initial cere-
brospinal fluid protein >2 g/L (OR: 12.39, 95% CI: 3.61-
42.55, P < .001), initial cerebrospinal fluid glucose
Figure 3. Age distribution of 25 children with hydrocephalus. <1.1 mmol/L (OR: 7.63, 95% CI: 2.92-19.89, P < .001), a
positive bacterial culture (OR: 2.82, 95% CI: 1.22-6.55, P ¼
aeruginosa (n ¼ 1), and Salmonella (n ¼ 1) (Figure 2). Chil- .013), peripheral blood C-reactive protein >100 mg/L (OR:
dren with bacterial meningitis lived in rural (n ¼ 148) and 8.10, 95% CI: 3.10-21.16, P < .001), and dexamethasone use.
urban (n ¼ 119) areas in almost equal numbers. A total of These differences were statistically significant.
168 patients were treated for probable bacterial meningitis On multivariate analysis (Table 1), the risk factors most
(criteria mentioned in the Materials and Methods section). closely related to hydrocephalus were altered mental status
Initial single-agent antibiotic therapy was used in 52 chil- (OR: 7.59, 95% CI: 1.09-52.86, P ¼ .041), previous antibiotic
dren (19%), mainly meropenem (21/52 [40%]) or ceftriaxone treatment (OR: 36.28, 95% CI: 2.84-462.78, P ¼ .006), initial
cerebrospinal fluid protein >2 g/L (OR: 177.02, 95% CI: 3.53-
(12/52 [23%]), whereas 215 children (81%) were treated with
8866.51, P ¼ .010), peripheral blood C-reactive protein
initial dual-agent antibiotic therapy, typically a combination
>100 mg/L (OR: 52.29, 95% CI: 3.26-840.19, P ¼ .005), and
of vancomycin with meropenem or ceftriaxone (78/267
dexamethasone use (OR: 149.47, 95% CI: 2.56-8713.78, P ¼
[29%]). A total of 127 (59%) children were given dexametha-
.016). The observed difference for initial treatment with dual-
sone based on their clinical presentation (eg, altered mental
agent antibiotic therapy was statistically significant (OR: 0.06,
status, presence of seizures, focal neurologic deficit on admis-
95% CI: 0.01-0.62, P ¼ .018).
sion). The dose of dexamethasone was 0.15 mg/kg/d, given
Although the following factors showed a statistically sig-
every 6 hours for 4 consecutive days.
nificant association with bacterial meningitis and hydroce-
Of the 267 children treated for bacterial meningitis, 25
phalus, there was no statistically significant difference for
(9.4%) developed hydrocephalus. The age distribution of these the type of hydrocephalus: initial cerebrospinal fluid pleocy-
children was as follows: 28 days, n ¼ 6; 28 days–3 months, tosis >5000 cells/mm3 (P ¼ .165), initial cerebrospinal fluid
n ¼ 9; 3-6 months, n ¼ 5; 6-12 months, n ¼ 1; 1-3 years, n ¼ 2; protein >2 g/L (P ¼ .076), initial cerebrospinal fluid glucose
and 6-14 years, n ¼ 2 (Figure 3). Of these 25 children with <1.1 mmol/L (P ¼ .294), and peripheral blood C-reactive
hydrocephalus, 12 were boys. A higher incidence (80%, 20/25) protein >100 mg/L (P ¼ .91).
of hydrocephalus was recorded in rural children. The interval
from the first symptom to the diagnosis of hydrocephalus ran-
ged from 5 to 60 days (<2 weeks, n ¼ 9; 2-4 weeks, n ¼ 11; Discussion
4-8 weeks, n ¼ 3; 2, 8-9 weeks, n ¼ 2). Fifteen of the 25 Bacterial meningitis is a common and fatal disease of the cen-
patients with hydrocephalus had a confirmed bacterial etiology: tral nervous system.11,12 The number of studies on the neuro-
6 of the 20 patients with cultures positive for E coli had logic complications of bacterial meningitis have gradually
hydrocephalus, 2 of the 19 positive for S pneumoniae; 2 of the increased in recent years.13-15 Because early neurologic com-
8 with Staphylococcus; 2 of the 13 with group B beta-hemolytic plications are the first predictors of long-term sequelae of
Streptococcus; 2 of the 2 with Acinetobacter; and 1 of the 10 with childhood with bacterial meningitis, identifying the predictors
Listeria monocytogenes. There were 12 patients with obstructive of early neurologic complications is extremely important.
hydrocephalus (48%) and 13 with communicating hydrocephalus In a prospective study of 103 children surviving pneumo-
(56%). All patients with hydrocephalus had received initial coccal meningitis, 22 (21%) had evidence of hydrocephalus
conservative treatment. And later, 3 patients among them with on cranial CT or MRI at the time of hospital discharge.16 In
communicating hydrocephalus had undergone continuous lum- a Danish retrospective cohort study of bacterial meningitis
bar cerebrospinal fluid drainage; 2 with obstructive hydrocepha- in patients older than 14 years, hydrocephalus was identified
lus and 1 with communicating hydrocephalus had received a in 3 of 83 episodes (4%) of pneumococcal meningitis.4 In
4 Journal of Child Neurology XX(X)

Table 1. Association between Potentially Relevant Factors and the Incidence of Hydrocephalus (Results, P3).

Without With
hydrocephalus hydrocephalus
(n ¼ 242) (n ¼ 25) Univariate analysis Multivariate analysis

Potentially relevant factor n % n % P value OR (95% CI) P value OR (95% CI)

Age <12 mo 217 90 21 84 .39 0.60 (0.19 -1.90) .228 13.86 (0.19-995.34)
Male sex 144 60 12 48 .93 1.04 (0.46-2.36) .057 0.06 (0.00 -1.09)
Rural 128 53 20 80 .009 3.56 (1.30-9.80) .035 17.64 (1.23-252.86)
Preterm delivery 87 36 6 24 .23 0.56 (0.22 -1.46) .591 0.59 (0.09-4.00)
Seizures prior to admission 40 17 19 76 <.001 15.99 (6.01-42.55) .068 6.17 (0.87-43.51)
Altered level of consciousness 47 19 13 52 .039 4.50 (1.93-10.48) .041 7.59 (1.09-52.86)
Previous antibiotic treatment 43 18 14 56 <.001 5.89 (2.50-13.86) .006 36.28 (2.84-462.78)
Initial pleocytosis >5000 cells/mm3 21 9 14 56 <.001 13.39 (5.40-33.20) .059 5.95 (0.93-37.96)
Initial CSF protein >2 g/L 90 37 22 88 <.001 12.39 (3.61-42.55) .010 177.02 (3.53-8866.51)
Initial CSF glucose <1.1 mmol/L 71 29 19 76 <.001 7.63 (2.92-19.89) .933 1.09 (0.15-7.81)
Positive bacterial culture 84 35 15 60 .013 2.82 (1.22-6.55) .344 2.71 (0.34-21.44)
CRP >100 68 28 19 76 <.001 8.10 (3.10-21.16) .005 52.29 (3.26-840.19)
Initial treatment with dual-agent antibiotics 204 84 11 44 <.001 0.15 (0.06-0.35) .018 0.06 (0.01-0.62)
Dexamethasone use 104 43 23 92 <.001 15.26 (3.52-66.18) .016 149.47 (2.56-8713.78)
Abbreviations: CI, confidence interval; CRP, C-reactive protein; CSF, cerebrospinal fluid; OR, odds ratio.

our study, the incidence of hydrocephalus is 9.36%. This studies from developed10,22 and developing16,23-25 countries.
result is close to the incidence (7.1%) found in a systematic Our results agree, showing that altered mental status is a risk
review and meta-analysis on the global and regional risk of factor for hydrocephalus.
disabling sequelae from bacterial meningitis, reported by Hydrocephalus may occur at the beginning of the course of
Edmond in 2010.17 bacterial meningitis or after treatment with antibiotics for many
Age <2 years is considered an important prognostic factor days or weeks. In the present study, the interval from the first
for poor outcome of children with bacterial meningitis.18,19 The symptom to the diagnosis of hydrocephalus was typically less
younger age of patients have higher incidence of bacterial than 4 weeks, with a shortest recorded time of 5 days. This
meningitis with neurologic complication, especially the new- interval is significantly shorter than that seen in adults with
born.20 However, our study found that younger age and preterm hydrocephalus after bacterial meningitis.26 Although commu-
delivery (birth history) may not be the risk factor for hydro- nicating hydrocephalus is the most common type of hydroce-
cephalus. This is different from a study in Kosovo,21 which phalus after bacterial meningitis, and acute obstructive
found that age <12 months was a risk factor for both early hydrocephalus is rarely reported in adults with bacterial menin-
neurologic complications and long-term sequelae of bacterial gitis, acute obstructive hydrocephalus is more common in
meningitis in children. younger children.21 In our study, 52% of patients with hydro-
Many developing countries still have not implemented vac- cephalus have the communicating type, and the incidence of
cination programs against meningeal pathogens, and China is obstructive hydrocephalus is 48%, higher than the rate seen in
no exception. Especially in some remote areas, many children adults. This is especially true for children younger than
do not complete immunization in a timely fashion, despite the 6 months. This result is consistent with previous research.
fact that vaccination is free. This undervaccinated population Recently, alterations in cerebrospinal fluid parameters have
explains the high incidence of bacterial meningitis. Our study been identified as risk factors predicting hydrocephalus with
found that the incidence of bacterial meningitis in rural chil- bacterial meningitis.23,24,26 In our study, an increased cere-
dren is higher than that in urban children, with 80% of children brospinal fluid protein level (>2 g/L) and an increased C-
with bacterial meningitis and hydrocephalus coming from rural reactive protein level in the peripheral blood were identified
areas. In other words, the patient’s living environment is a risk as risk factors for hydrocephalus. Bacterial meningitis with
factor for hydrocephalus. Setting aside the nonimplementation hydrocephalus can be caused by a variety of pathogenic bac-
of vaccination programs, there may be other factors related to teria, including Streptococcus pneumonia, Neisseria meningi-
the high incidence in rural children, such as the quality of tidis, Haemophilus influenzae, and Staphylococcus aureus,
medical and health facilities, family awareness of health care, etc.27 In our study, 60% of patients with hydrocephalus have
and family economic conditions. a definite pathogenic diagnosis; 40% of these have E coli.
Serious clinical presentations, manifested as altered mental Pediatricians should pay close attention to the children with
status and seizures, are the strongest prognostic factors for positive bacterial cultures, because they are more likely to
neurologic complications of bacterial meningitis, in numerous develop hydrocephalus.
Huo et al 5

According to Namani et al,28 children with bacterial menin- Declaration of Conflicting Interests
gitis previously treated with antibiotics do not show an The author(s) declared no potential conflicts of interest with respect to
increased incidence of neurologic complications. Initial treat- the research, authorship, and/or publication of this article.
ment with 2 antibiotics is considered a risk factor for acute
neurologic complications, but adjunctive dexamethasone ther- Funding
apy does not reduce the incidence. In our study, previous anti- The author(s) disclosed receipt of the following financial support for
biotic treatment, initial therapy with dual-agent antibiotics, and the research, authorship, and/or publication of this article: Supported
dexamethasone use are all identified as statistically significant by the National Natural Science Foundation of China (No. 81501299)
factors for the development of hydrocephalus. This is likely
because patients receiving these therapies present with a severe Ethical Approval
clinical presentation from the onset. In the Cochrane meta- This study was approved by the Institutional Review Board at the
analysis, corticosteroids are found to decrease overall hearing Shengjing Hospital of China Medical University. Informed consent
loss and neurologic sequelae, but do not reduce mortality.29 was obtained by all from legal guardians of minor participants. Verbal
Conservative treatment is adopted in most children with and/or written assent was provided by all minor participants.
hydrocephalus. Invasive procedures are recommended in
patients with moderate or severe hydrocephalus with clinical References
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