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OBJECTIVE Central nervous system (CNS) infections cause significant morbidity and mortality and often require
neu- rosurgical intervention for proper diagnosis and treatment. However, neither the international burden of CNS
infection, nor the current capacity of the neurosurgical workforce to treat these diseases is well characterized. The
objective of this study was to elucidate the global incidence of surgically relevant CNS infection, highlighting
geographic areas for targeted improvement in neurosurgical capacity.
METHODS A systematic literature review and meta-analysis were performed to capture studies published between
1990 and 2016. PubMed, EMBASE, and Cochrane databases were searched using variations of terms relating to CNS
infection and epidemiology (incidence, prevalence, burden, case fatality, etc.). To deliver a geographic breakdown of
disease, results were pooled using the random-effects model and stratified by WHO region and national income status
for the different CNS infection types.
RESULTS The search yielded 10,906 studies, 154 of which were used in the final qualitative analysis. A meta-analysis
was performed to compute disease incidence by using data extracted from 71 of the 154 studies. The remaining 83
studies were excluded from the quantitative analysis because they did not report incidence. A total of 508,078 cases of
CNS infections across all studies were included, with a total sample size of 130,681,681 individuals. Mean patient age
was 35.8 years (range: newborn to 95 years), and the male/female ratio was 1:1.74. Among the 71 studies with
incidence data, 39 were based in high-income countries, 25 in middle-income countries, and 7 in low-income countries.
The
pooled incidence of studied CNS infections was consistently highest in low-income countries, followed by middle- and
then high-income countries. Regarding WHO regions, Africa had the highest pooled incidence of bacterial meningitis
(65 cases/100,000 people), neurocysticercosis (650/100,000), and tuberculous spondylodiscitis (55/100,000),
whereas Southeast Asia had the highest pooled incidence of intracranial abscess (49/100,000), and Europe had the
highest
pooled incidence of nontuberculous vertebral spondylodiscitis (5/100,000). Overall, few articles reported data on deaths
associated with infection. The limited case fatality data revealed the highest case fatality for tuberculous meningitis/
spondylodiscitis (21.1%) and the lowest for neurocysticercosis (5.5%). In all five disease categories, funnel plots
assess-
ABBREVIATIONS AFR = African Region; AMR-L = Region of the Americas–Latin America; AMR-US/Can = Region of the Americas–United States/Canada; BM =
bacterial meningitis; CNS = central nervous system; EMR = Eastern Mediterranean Region; EUR = European Region; HIC = high-income country; HIV = human
immunodeficiency virus; LIC = low-income country; LMICs = low- and middle-income countries; MIC = middle-income country; NCC = neurocysticercosis; SEAR =
Southeast Asia Region; TB
= tuberculosis; WPR = Western Pacific Region.
SUBMITTED March 16, 2017. ACCEPTED October 24, 2017.
INCLUDE WHEN CITING Published online June 15, 2018; DOI: 10.3171/2017.10.JNS17359.
* F.C.R. and J.R.L. contributed equally to this work and share first authorship.
©AANS 2018, except where prohibited by US copyright law J Neurosurg June 15, 2018 1
F. C. Robertson et
al.
ing for publication bias were asymmetrical and suggested that the results may underestimate the incidence of disease.
CONCLUSIONS This systematic review and meta-analysis approximates the global incidence of neurosurgically
rel- evant infectious diseases. These results underscore the disproportionate burden of CNS infections in the
developing world, where there is a tremendous demand to provide training and resources for high-quality
neurosurgical care.
https://thejns.org/doi/abs/10.3171/2017.10.JNS1735
9
KEYWORDS burden of disease; CNS infection; epidemiology; global surgery; neurocysticercosis;
neurosurgery
C
10 million people, of CNS infections v
advent of
although the expected mandate surgical i
antibiotics, involvement for diag-
ratio is at least e
vaccines, nosis and treatment, a
1 neurosurgeon per w
and other medical 100,000 people.52,147 better understanding of
therapies. The causative Our systematic
Moreover, only the global
organisms— bacteria, burden of CNS review was conducted
42% of African
viruses, parasites, fungi, infections requiring in accordance with the
countries and 75% of
and prions—can lead to Latin American neurosurgical inter- Preferred Reporting
meningitis, encephalitis, countries offer in- vention will elucidate Items for Systematic
spinal and cranial country training of the demand for Reviews
abscesses, discitis, neurosurgeons.146 capacity-building
epilepsy, and other Therefore, in an era in e
severe complications. In which CNS infections f
fact, neurocysticercosis remain a ma- f
(NCC) infection is the jor challenge, there may o
leading cause of be an imminent need to r
preventable epilepsy in increase t
the developing world14,109 the neurosurgical s
and is workforce, particularly
on the rise in developing in countries with i
nations.45,56 The spread the greatest disease n
of other burden. However,
CNS infections remains obtaining a reliable n
a concern in light of global estimate of the e
increased volume and burden of u
migration and tourism CNS infec- r
travel,68,95 drug-resistant tions has been difficult o
organisms, because population-wide s
and immunosuppressed data are u
individuals.50,51,112,134 limited, the r
While medi- heterogeneity in CNS g
cal treatment is infection type and loca- e
necessary for most CNS tion is tremendous, and r
infections, neuro- underdiagnosis and y
surgical involvement underreport- .
can be required for ing in
biopsy, debride- resource-
ment, M
limited
decom settings are e
pressio
n, or
suspected. t
The aim of this study
reconst was to assess the h
ruction
.
incidence and o
manifestation of CNS
Geographically, the infection at the national, d
burden of CNS regional, s
infection is un- and global levels to
equally distributed and S
further characterize the y
predominantly impacts global burden
low- and of neurological s
middle-income infection. Through a t
countries (LMICs); systematic review of e
unfortunately, these the literature, we have m
same countries face a
3 J Neurosurg June 15,
2018
F. C. Robertson et
al.
conducted. The WHO regions are classified as follows: meta-analysis. Potential publication bias was assessed
African Region (AFR), Region of the Americas–United using Egger’s lin- ear regression test and Begg’s
States/Canada (AMR-US/Can), Region of the correlation test. If publica- tion bias was indicated, the
Americas– Latin America (AMR-L), Southeast Asia number of missing studies was evaluated by the trim-
Region (SEAR), European Region (EUR), Eastern and-fill method. A p < 0.05 was con- sidered significant
Mediterranean Region (EMR), and Western Pacific unless otherwise indicated.
Region (WPR). The World Bank database (2016) was
used to characterize the in- come level for each country
using gross national income per capita. Country and
region populations were also ob- tained from World
Bank population metadata (https://data.
worldbank.org/data-catalog/population-projection-
tables).
Meta-
Analysis
Data were analyzed with Comprehensive Meta-
Analy- sis Version 3 (Biostat Inc.) and Stata 14.0
software (Stata- Corp). To account for variation between
and within stud- ies, the DerSimonian and Laird
random-effects model was used to obtain overall
incidence estimates and 95% con- fidence intervals.49
Forest plots allowed visualization of individual and
summary estimates. Heterogeneity among studies was
evaluated using Cochran’s Q test (p < 0.10) and I2 to
measure the proportion of between-study vari- ance. An
I2 value > 50% was considered high.31 Subgroup
analyses by categorical covariates were used to explore
potential sources of heterogeneity, that is, disease type
(NCC, bacterial meningitis [BM], intracranial abscess,
tuberculosis [TB] meningitis/osteomyelitis, and non-TB
spinal osteomyelitis), WHO region, and World Bank in-
come classification. Total world incidence of a
disease was estimated by multiplying our derived WHO
regional incidence by public WHO region population
data, and all seven regions were summed to provide a
global total.
The criteria for surgical versus nonsurgical CNS
infec- tious disease were decided unanimously among
the au- thors. Publications on cerebral malaria,
cryptococcal men- ingitis, unspecified CNS infections,
and human immuno- deficiency virus (HIV)-related
CNS infections were not included as those disease
entities are primarily managed medically, with less
relevance for neurosurgical interven- tion. To explore
sources of heterogeneity, stratification by WHO region
and income level was done for each disease category.
Once aggregate incidence data were obtained for each
disease category by WHO region and income level,
these values were summed to a total disease volume of
CNS infections. When published data were not available
for a disease in a given WHO region, the incidence was
estimated using the weighted proportion of HIC/MIC/
LIC within that region multiplied by the incidence rate
of the disease by income level. When this method
yielded an estimate greater than one deviation from the
averaged incidences, the value underwent logarithmic
transforma- tion to prevent significant outliers.124 There
were rare in- stances in which the literature provided no
incidence rate of a disease for a particular income level.
In these cases, the incidence was then removed from the
F. C. Robertson et
al.
FIG. 1. PRISMA diagram summarizing the search process. From a total of 10,906 studies, 154 were incorporated into the
review, with 71 in the quantitative analysis.
five from the Western rized in of 650 cases/100,000 Southeast Asia data were
Pacific, two from the Table people (95% CI 195– calculated as described
Eastern Medi- terranean, 4. 1333/100,000). Sixteen above in the Methods.
and one each from the studies were from MICs, The overall estimate of
US/Canada and Latin N four from LICs, and sev- the global population
America (Fig. 3). The e en from HICs (Fig. 6). affected by intracranial
estimate of individuals u The estimated incidence abscesses was 1,088,237
affected by BM r was 401 cases/100,000 each year (Table 3).
worldwide was o people in LICs (95% CI Reported incidence
2,907,146 each year c 16–1173/100,000), ranged from 0.15
(Table 3). Occurrence y 256/100,000 in MICs cases/100,000 people to
was highest in Africa, s (95% CI 54– 49/100,000. Incidence
with an incidence of t 569/100,000), and was lowest in the
65 cases/100,000 people 0.40/100,000 in HICs Western Pacific (0.15
i
(95% CI 13– (95% CI 0.11– cas- es/100,000 people,
155/100,000), and c 95% CI 0.05–0.25) and
0.83/100,000; p <
lowest in the e 0.001). Case fatality for highest in Southeast
US/Canada, with an r NCC was only available Asia (49/100,000, 95%
incidence of 2/100,000 c in two CI 6–62). Reported inci-
(95% CI 2–3; p- o studies,137,189 both of dence in HIC and MIC
interaction comparing s which came from the was similar at 0.54
the different groups < i US, with record- cases/100,000 and
0.001). Fifteen studies s ings of 1.2% and 9.8% 0.52/100,000,
were from HICs, five Twenty-seven studies (mean 5.5%, 95% CI respectively (p-
from MICs, and two on NCC were suitable 0.0%–60.5%). interaction = 0.19). Only
from LICs (Fig. 4). for inclu- sion (Fig. 5). one study from an LIC
Incidence was Six WHO regions were I was included and had a
85 cases/100,000 people included, with 14 studies n reported in- cidence of
in LICs (95% CI 78– from Latin America, t 240 cases/100,000
93/100,000), four from the r people (95% CI 86–
42/100,000 in MICs US/Canada, three each a 672).184
(95% CI 11–92/100,000; from Southeast Asia and c Case fatality data were
I2 = 99.1%; 5 Africa, two from the r not available for
studies), and 6/100,000 Eastern Mediterranean, a intracranial ab-
in HICs (95% CI 4– and one from Europe. n s
8/100,000; I2 = The overall estimate of i c
98.3%; the global population e
15 a
affected by NCC was s
studies; l s
24,743,893 people each
p- year (Table 3). The
interacti occurrence rate was A i
on < highest in Africa, with b n
0.001). an estimated incidence s
Case fatality was c t
available in 13 e h
studies,33,34,40,53,59,75,86, s e
98,107,113,140,148,198
giving an s
overall average of i
15.9% (95% Eight studies on n
CI 9.2%–22.5%), with intracranial abscesses, c
the highest rate of 32.7% which include extradural l
in Swazi- and subdural empyema, u
land59 and the lowest rate were suitable for inclu- d
of 2.4% in Singapore.34 sion, with two studies e
The most each from Africa and the d
common offending Western Pacific, and one
pathogens were reported each from Latin s
by 21 studies; America, US/Canada, t
these Eastern Mediterranean, u
results and Europe d
are (Supplemental Figs. 1 i
summa and 2); estimates for e
5 J Neurosurg June 15,
2018
F. C. Robertson et
al.
s
.
Hui et al., 2005 BM China WPR Middle 508,900 6.5 1992–2001 Retro Hosp 3 Tertiary only; adults only
Jamjoom et al., 1994 IA Saudi Arabia EMR High 500,000 3.6 1985–1991 Retro Hosp 4 Tertiary only
Jensen et al., 1998 SO-nonTB Denmark EUR High 5,000,000 13.3 1980–1990 Retro Pop 4 S. aureus only
Jensen et al., 1997 SO-nonTB Denmark EUR High 5,000,000 14.6 1980–1990 Pros Pop 4 S. aureus only
al.
F. C. Robertson et
Kalliola et al., 1999 BM Finland EUR High 63,816 8.1 1985–1994 Pros Pop 4 Neonates only (age <90 days)
Kehrer et al., 2014 SO-nonTB Denmark EUR High 483,123 192.0 1995–2008 Retro Pop 4
Klobassa et al., 2014 BM Austria EUR High 399,000 74.0 2001–2008 Retro Pop 3 Pneumococcal meningitis
Leshem et al., 2010 NCC Israel EMR High 2,400,000 4.25 1994–2009 Retro Pop 4
CONTINUED ON PAGE 6 »
5
» CONTINUED FROM PAGE 5
6
al.
F. C. Robertson et
TABLE 1. Review of 71 studies included in the quantitative meta-analysis
Disease Income Sample Incidence Study Study Study Method
J Neurosurg June 15, 2018
Authors & Year Category Country WHO Region Level Size (Nʹ) (nʹ) Period Design Scale Score Limitations/Considerations
Leshem et al., 2011 NCC Israel EMR High 2,400,000 6.8 1994–2009 Retro Pop 4 Travel episodes to endemic countries
Limcangco et al., 2000 BM Philippines WPR Middle 39 39.3 1994–1996 Retro Hosp 4 Haemophilus B meningitis only; children only
Lino et al., 1999 NCC Brazil AMR-L Middle 67 1.8 1974–1997 Retro Pop 4 Autopsy data
Looti et al., 2010 TB-s/c Cameroon AFR Middle 2,313 1.3 1999–2006 Retro Hosp 2 Neurology & neurosurgery database
Lu et al., 2002 IA Taiwan WPR High 5,441,000 8.2 1986–2000 Retro Hosp 3 Tertiary only
Lu et al., 2000 BM Taiwan WPR High 5,441,000 15.5 1986–1999 Retro Hosp 4
Mahmoud et al., 2002 BM UAE EMR High 225,970 12.8 1990–1999 Retro Pop 3
Menon & Serour, 2016 SO-nonTB Oman EMR High 2,120,000 15.5 2011–2015 Retro Hosp 4
Millogo et al., 2012 NCC Burkina AFR Low 888 11.0 2007 Cross Pop 4 Clustered random sampling.
Faso
Montano et al., 2005 NCC Peru AMR-L Middle 1,004 15.0 2004 Cross Pop 4 Epilepsy only
Moyano et al., 201221 NCC Peru AMR-L Middle 20,610 109.0 2006–2007 Pros Pop 5
Moyano et al., 2012 20
NCC Peru AMR-L Middle 20,197 109.0 2006–2007 Cross Pop 5 Door-to-door survey; imaged epilepsy suspects
Narata et al., 1998 NCC Brazil AMR-L Middle 2,554 236.0 1995–1996 Retro Hosp 3 Neurology/neurosurgery patients only
Nicoletti et al., 2005 NCC Bolivia AMR-L Middle 10,124 34.0 2003 Cross Pop 4 Epilepsy patients only
Nicolosi et al., 1991 IA USA AMR-US/Can High 93,532 0.8 1935–1981 Retro Pop 4
Nørgaard et al., 2003 BM Denmark EUR High 490,000 4.6 1984–1999 Retro Pop 5
Ong et al., 2002 NCC USA AMR-US/Can High 900,000 19.0 1996–1998 Pros Hosp 4
Østergaard et al., 2005 BM Denmark EUR High 5,404,624 93.5 1999–2000 Retro Pop 4 Pneumococcal meningitis only
Ptaszynski et al., 2007 NCC USA AMR-US/Can High 907,580 0.8 1990–2000 Retro Pop 4
Raina et al., 2012 NCC India SEAR Middle 2,209 10.0 2010 Cross Pop 4 Door-to-door survey; imaged epilepsy suspects
Rasit et al., 2001 TB-s/c Malaysia SEAR Middle 1,868,298 10.6 1994–1998 Retro Hosp 3
Reinert et al., 1993 BM France EUR High 131,786 17.7 1980–1989 Retro Hosp 4
Riise et al., 2008 SO-nonTB Norway EUR High 255,303 6.0 2004–2005 Cross Pop 5
Rodriguez-Gomez et al., 2002 TB-s/c Spain EUR High 483,000 2.5 1986–1999 Retro Hosp 4 Age >16 yrs only
Sakata, 2007 BM Japan WPR High 47,323 3.0 1996–2005 Retro Hosp 4 Children only age <10 yrs
Schuchat et al., 1997 BM USA AMR-US/Can High 10,281,746 248.0 1995 Cross Pop 5
Secka et al., 2011 NCC Senegal AFR Low 403 20.0 2009–2010 Pros Pop 5 Village study, tested serum then CT
Sigurdardóttir et al., 1997 BM Iceland EUR High 250,000 6.6 1975–1994 Retro Pop 4
Silva-Vergara et al., 1994 NCC Brazil AMR-L Middle 1,080 23.0 1992–1993 Cross Hosp 4
Solís-García del Pozo et al., SO-nonTB Spain EUR High 367,283 7.6 1990–2002 Retro Pop 4
2005
Soumaré et al., 2005 IA Senegal AFR Low 1,374 157.0 2001–2003 Retro Hosp 3 Tertiary only
Sur et al., 2015 SO-nonTB England EUR High 500,000 18.3 2008–2011 Retro Pop 4 Adult patients only
Takayanagui et al., 1996 NCC Brazil AMR-L Middle 484,483 269.6 1992–1995 Retro Pop 4
CONTINUED ON PAGE 7 »
Region; EUR = European Region; Hosp = hospital based; IA = intracranial abscess; NCC = neurocysticercosis; Pop = pop
AFR = African Region; AMR-L = Region of the Americas–Latin America; AMR-US/Can = Region of the Americas–United
F. C. Robertson et
al.
Tertiary only
HospMethod
4
nonTB = spinal osteomyelitis–non-tuberculosis; S. aureus = Staphylococcus aureus; TB-s/c = tuberculosis–spinal/cranial; WPR = Western Pacific Region.
diseases
separated by World Bank income level per 100,000 people
CNS Infection LIC MIC HIC
Retro Study
BM 85 42 6
NCC 401 256 0.4
4
Study
TABLE 1. Review of 71 studies included in the quantitative meta-analysis » CONTINUED FROM PAGE 6
* Meningitis/osteomyelitis.
12.2
6,100,000Incidence
Nontuberculous Osteomyelitis
Ten studies on spinal nontuberculous osteomyelitis
and discitis were suitable for inclusion (Supplemental
Sample
Tuberculous Meningitis/Osteomyelitis
Taiwan
osteomy-
elitis were suitable for inclusion (Supplemental Figs. 5
and
et al., 2004
one
study each originated from a MIC in Africa and
Southeast
Townes
studies
ranged from 0.51 cases/100,000 in a European HIC
(95%
Design Scale
Mean
was not a source of heterogeneity for intracranial
64,806
5,134
114,177
262,283
10,993
1,005,612
TB-Related Disease*
3,573
544,647
abscess
Year
(p = 0.53), nontuberculous osteomyelitis (p = 0.99), or
worldwide
tu-
berculous meningitis/osteomyelitis (p =
0.60).
Incidence
0.57
0.56
14‡
18‡
10
1
55
Publication Bias
Begg’s p value and Egger’s p value were
nonsignificant for each of the five CNS infection types,
except for NCC where the Egger’s test was significant
4,731
57,856
108,426
45,839
†
†
3
5
944,980
6,967
1,088,237
120,520
5,149
Discussion
This study represents the first comprehensive
estimate of the global burden of neurosurgically relevant
† No income data available for estimation of mean incidence or number affected per year. Value counted as zero for worldwide estimate.
0.15
0.52
8,636,606
24,743,893
1,249,602
6,436,739
436
974,194
55,007
2,907,146
95,147
643,674
Bacterial
55‡
11
6
15
Meningitis
Bacterial meningitis remains a significant cause of
CNS infection worldwide, particularly in the region of
1,928,530,522
916,775,857
648,060,427
357,270,594
1,873,450,273
990,267,592
7,348,671,249
634,315,984
SEAR
WPR
EMR
EUR
FIG. 2. Global incidence and burden of CNS infection. For the five CNS infection types studied, the combined incidence (A) and
global burden (B) of CNS infection are depicted, as are proportions of infection by pathology (C). Publications on cerebral malaria,
cryptococcal meningitis, unspecified CNS infections, and HIV-related CNS infections were not included since those are primar-
ily medically managed disease entities with less relevance for neurosurgical intervention. Map reproduced with permission from
OpenStreetMap Contributors, CC BY-SA 2.0 (http://ww w.openstreetmap.org/copyright). Figure is available in color online only.
FIG. 3. Forest plot demonstrating distribution of overall incidence of BM by WHO region. Twenty-two studies on BM were
included, and data were analyzed according to WHO region. Overall incidence was highest in Africa and lowest in AMR-US/Can.
Solid squares represent the point estimate of each study, and the diamonds represent the pooled estimate of the incidence for
each subgroup. The width of the diamond denotes 95% CIs. The size of the solid squares is proportional to the weight of the study.
ES = effect size. Figure is available in color online only.
F. C. Robertson et
al.
calculation of incidence in Southeast Asia using income peutic purposes, with aerobic, anaerobic, mycobacterial,
data estimates (see Methods) showed abscess rates of 49 and fungal cultures to guide medical treatment;13
cases/100,000 people. The etiology of brain abscess is however, LICs are often forced to rely on empirical
believed to relate directly to poor socioeconomic condi- medical man- agement because of limitations in both
tions,130 including both hematogenous and direct radiographic and surgical resources. For instance, in a
spread from pneumonia, poor dental hygiene and series of 112 cerebral abscesses in Burkina Faso, 47% of
associated cardiac valvular vegetations, previous patients were treated with antibiotics alone, while 53%
surgery, or other contiguous sites.29,192 Successful underwent surgery.85
management generally requires surgical drainage for This contrasts with higher-income countries, where
both diagnostic and thera- nearly
90% of cases undergo surgical treatment28,80,130 and
medi-
10 J Neurosurg June 15, 2018
F. C. Robertson et
al.
FIG. 4. Forest plot demonstrating distribution of overall incidence of BM by World Bank income level. Twenty-two studies on
BM were included, and data were analyzed according to LIC, MIC, and HIC World Bank indication. Figure is available in color
online only.
TABLE 4. Most common pathogens reported by each study for bacterial meningitis and intracranial abscess
all LICs and MICs, but rather that it is simply not known. While the five disease categories studied include
pa- Note, however, that the high incidence in HICs indicates thology that often requires surgical intervention,
this list that vertebral osteomyelitis may be a disease afflicting is not comprehensive and omits multiple
diseases that may the developed world. Known risk factors include injection indeed require neurosurgery, such as
HIV-related infec- drug use, diabetes, and a compromised immune system,7 tions. However, less common
diseases that were omitted, several of which are prevalent in more developed nations such as cerebral
schistosomiasis, prion disease, and neu- but are becoming increasingly common in the developing roborreliosis,
are unlikely to greatly affect the estimated world.131,149 Our data indicate that vertebral osteomyelitis is volume of
CNS infections.
not currently a major contributor to the global neurosurgi- Additionally, regions in which CNS infections are
sus-
cal infectious volume; however, the continuation of ongo- pected to occur with the greatest frequency are also
those
ing epidemiological trends may show a rise in vertebral regions with studies of the lowest methodological
quality. osteomyelitis in the near future. The exclusion of large regional and national
registries ex-
cludes a large body of data that could have greatly
impact- Study Limitations and Future Directions ed the power of our approximations. To
include data from The disease estimations presented in this study are the greatest possible number of regions
and achieve our based on the most wide-ranging and comprehensive stud- goal of describing the global CNS
infectious disease vol- ies available. Strengths of this study include the compre- ume, we used a lower
FIG. 5. Forest plot demonstrating distribution of overall incidence of NCC by WHO region. Neurocysticercosis was the most
reported individual disease in publications of CNS infections worldwide (27 of 71 included in the final statistical analysis). Overall
incidence was highest in AFR and lowest in EMR. Solid squares represent the point estimate of each study, and the diamonds
represent the pooled estimate of the incidence for each subgroup. The width of the diamond denotes 95% CIs. The size of the
solid squares is proportional to the weight of the study. Figure is available in color online only.
J Neurosurg June 15, 13
2018
F. C. Robertson et
al.
FIG. 6. Forest plot demonstrating distribution of overall incidence NCC by World Bank income level. Twenty-seven studies
regard- ing NCC were analyzed according to LIC, MIC, and HIC World Bank indication. Solid squares represent the point estimate
of each study, and the diamonds represent the pooled estimate of the incidence for each subgroup. The width of the diamond
denotes
95% CIs. The size of the solid squares is proportional to the weight of the study. Figure is available in color online only.
TABLE 5. Publication bias results for 5 disease outcomes 8. Al Ayed M, Al Jumaah S, AlShail E: Central nervous sys-
tem and spinal tuberculosis in children at a tertiary care
p Value, p Value, center in Saudi Arabia. Ann Saudi Med 33:6–9, 2013
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outcome of childhood meningitis in rural Yemen: a 2-year
BM Asymmetrical 0.48 0.68 hospital-based study. J Infect 53:228–234, 2006
NCC Asymmetrical 0.29 0.02 10. Alavi SM, Sharifi M: Tuberculous spondylitis: risk factors
IA Mildly asymmetrical 0.32 0.47 and clinical/paraclinical aspects in the south west of Iran. J
Infect Public Health 3:196–200, 2010
SO-nonTB Asymmetrical 0.79 0.11
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TB-related disease* Symmetrical† 1.00 0.89 Al-Sadoon S, Rahman MM, et al: Tuberculous spondylitis:
Boldface type indicates statistical significance.
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* Meningitis/osteomyelitis.
1976) 26:E565–E570, 2001
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Disclosures
The authors report no
conflict of interest
concerning the materi- als
or methods used in this
study or the findings
specified in this paper.
Author Contributions
Conception and design:
Robertson, Lepard, Rattani,
Dewan, Park. Acquisition of
data: Robertson, Lepard,
Davis. Analysis and inter-
pretation of data: Robertson,
Lepard, Mekary, Davis,
Yunusa, Bat- iculon, Rattani,
Dewan. Drafting the article:
Robertson, Lepard, Davis.
Critically revising the
article: Robertson, Lepard,
Mekary, Davis, Gormley,
Baticulon, Mahmud, Misra,
Rattani, Dewan,
Park. Reviewed submitted
version of manuscript: all
authors. Approved the final
version of the manuscript
on behalf of all authors:
Robertson. Statistical
analysis: Robertson,
Lepard, Mek- ary, Yunusa.
Administrative/technical/m
aterial support: Mekary,
Gormley, Rattani, Dewan,
Park. Study supervision:
Robertson, Lepard, Dewan,
Park. Cartography/figures:
Baticulon.
Supplemental Information
Online-Only Content
Supplemental material is
available with the online
version of the article.
Supplemental
Materials.
https://thejns.org/doi /su
ppl /10.3171/
2017.10. J NS17359.
Previous Presentations
This work was presented as
an abstract at the Congress
of Neuro- logical Surgeons
Annual Meeting held on
October 7–11, 2017, in
Boston, MA.
Correspondence
Faith Robertson: Harvard
Medical School, Boston, MA.
faith_
robertson@hms.har vard.edu.
J Neurosurg June 15, 31
2018