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LITERATURE REVIEW

Epidemiology of central nervous system infectious


diseases: a meta-analysis and systematic review
with implications for neurosurgeons worldwide
*Faith C. Robertson, BS, 1,2 Jacob R. Lepard, MD, 3 Rania A. Mekary, MSc, PhD, 2,4
Matthew C. Davis, MD, MPH, 3 Ismaeel Yunusa, PharmD, 2,4 William B. Gormley, MD, MPH,
MBA, 1,2,5
Ronnie E. Baticulon, MD, 6 Muhammad Raji Mahmud, MD, 7 Basant K. Misra, MD, 8
Abbas Rattani, MBe, 9,10 Michael C. Dewan, MD, MSCI, 10,11 and Kee B. Park, MD 10
1
Harvard Medical School; 2Computational Neuroscience Outcomes Center, Brigham and Women’s Hospital, Department of
Neurosurgery, Boston, Massachusetts; 3Department of Neurosurgery, University of Alabama, Birmingham, Alabama;
4
MCPHS University, Department of Pharmaceutical Business and Administrative Sciences, School of Pharmacy, Boston;
5
Department
of Neurological Surgery, Brigham and Women’s Hospital, Harvard Medical School, Boston, Massachusetts; 6University of the
Philippines College of Medicine, Philippine General Hospital, Manila, Philippines; 7Department of Surgery, National Hospital
Abuja, PMB 425, Federal Capital Territory, Nigeria; 8Department of Neurosurgery & Gamma Knife Radiosurgery, P. D.
Hinduja National Hospital, Mahim, Mumbai, India; 9Meharry Medical College, School of Medicine, Nashville, Tennessee;
10
Global Neurosurgery Initiative, Program in Global Surgery and Social Change, Department of Global Health and Social
Medicine, Harvard Medical School, Boston, Massachusetts; and 11Department of Neurological Surgery, Vanderbilt University
Medical Center, Nashville, Tennessee

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
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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

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entral nervous neurosurgeon workforce pooled the reported a


system (CNS) deficit.51 incidence of t
infections For instance, in many CNS infections in i
continue to cause Sub-Saharan African various countries to c
countries, the estimate the re-
significant
current workforce is gion-specific incidence
morbidity and R
approximately one via a meta-analysis. As
mortality world- e
neurosurgeon per a number
wide, despite the

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
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and Meta-Analyses reviewed a random were reported as


(PRISMA) guidelines.117 subset of articles at both proportions of a
A complete review of the the abstract review and population, including
literature was conducted full-text review stages to age (mean, median,
using PubMed, form a consensus on the range, and standard
EMBASE, and the application of selection deviation), sex, case
Cochrane Database of criteria. At this time, the fatality rate, and surgical
Systematic Reviews in refer- ences of all burden. Case fatality
November 2016 to included studies were was defined as the
capture studies published cross-examined for rel- number of deaths
between 1990 and 2016. evant cited articles, divided by the number of
The list of search terms, which were included if cases. Surgical volume
which aimed to capture they fulfilled the burden was defined as
region-specific selection criteria. the proportion (%) of
epidemiological data on A 6-point scale was reported cases that
CNS infectious diseases, used to grade the required surgical
can be found in the methodologi- cal quality intervention. To deliver
Supplemen- tal of each study. Articles a regional break- down
Appendix. In summary, were assigned points for of disease, results were
MeSH and title/abstract prospective data organized and presented
terms were used to collection, research in relation to the WHO
maximize the inclusion setting (institu- tional vs region from which each
of publications re- population), ideal study was
garding CNS infection population type, sample
epidemiology (incidence, size (> 50), and
preva- lence, burden, reporting of incidence.
mortality, etc.). Titles Studies were ranked
and abstracts of the accordingly from 0 to
yielded articles were 5.54 A minimal inclusion
screened separately by threshold was set to
two reviewers (F.C.R., select for high-quality
J.R.L.). Articles research; studies from
containing high-income countries
epidemiological data on (HICs) required a score
CNS infection volume of 4 or 5 for meta-
(i.e., incidence, analysis inclusion,
prevalence) and disease whereas scores of 2–5
burden were included. were accepted for studies
All case reports, case- based in LMICs to
con- trol studies, prevent publica- tion
comparison studies, bias secondary to a
randomized controlled paucity of high-quality
trials, historical articles, research in resource-
commentaries, and poor settings.
practice guidelines were
excluded. Inconsistencies D
between article a
inclusion/exclusion were t
resolved by joint re- a
evaluation (F.C.R.,
J.R.L.) by both R
investigators before a e
full-text re- view. p
Subsequently, a review
o
team (F.C.R., J.R.L.,
M.C. Davis) obtained the r
full-text articles and t
performed data i
extraction. To ensure n
selection accuracy, g
reviewers jointly Descriptive statistics
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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
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Results Supplemental Table 1.


Literature Incidence, Demographics, and
Yield Subtype
A detailed description of the inclusion/exclusion A total of 508,078 cases of CNS infections
process is noted in Fig. 1. The initial literature search of across all studies were included, with a total sample
the PubMed, EMBASE, and Cochrane databases yielded size of
10,906 arti- cles, which were screened according to the 130,681,681 individuals. There was a high degree of
aforementioned methods. A review of each article’s
het-
reference section added
erogeneity across all disease categories (not shown),
13 relevant articles, yielding a total of 154 articles for
with
this review. Of the 154 studies that met selection
I2 values ranging from 42.9% for toxoplasmosis to
criteria, 83 did not report incidence for the total
79.6%
population (for example, many NCC studies presented
incidence within an epilepsy population); therefore, for TB–spinal/cranial to 91.7% for NCC. The incidence
these studies were included in the qualitative analysis of
but excluded from the quantitative meta-analysis. These studied CNS infection was consistently highest in LICs,
excluded studies provide a valuable review of the fol-
literature regarding reported disease in the developing lowed by MICs and then HICs (Table 2). Regarding
world, containing information on demograph- ics and WHO
outcomes (age, sex, rates of infection requiring surgical regions, Africa had the highest rates of BM, NCC, and
intervention, and mortality rates); these are sum- TB-
marized in Supplemental Table 1.2,3,8,10,11,19–23,25– related disease, whereas Southeast Asia had the
27,33,37,38,40, highest
41,43,46,50,55,56,63,67,69,76–79,83– reported rates of intracranial abscess, and Europe had
85,88,89,82,91,93,96,97,100,104,106,108,113,115,121,123, the
125–128,137,139,141–
145,148,150,153,156,161,163,164,166,169,170,173,176,177,180,182,186,190,
highest reported rates of non-TB spinal osteomyelitis
(Ta-
The 71 papers that did report
192,193,195,196,198,199,201
ble 3). The global burden of these five CNS infections
incidence were included in the statistical meta-analysis by
(Table 1).4,5, WHO region and the proportion of infections by
7,9,12,15,18,24,32,34–36,42,44,47,48,53,57–62,65,66,70,71,73–75,80–
82,86,87,90,94,95,98,99, pathology
101–103,105,110,114,118,120,122,129,132,133,135,138,140,151,152,154,157– are depicted in Fig. 2. Case fatality was calculated from
160,165,172,174,178,
the
179,183,184,187–
189,194,200
included studies; however, because of the sporadic and
lim-
The final 71 studies included data from 42 ited reporting of mortality, the resultant calculations
individual countries, which were representative of the may
global com- munity and all seven WHO regions: 10 represent an over- or underestimation of the true
studies from Af- rica, 6 from the US/Canada, 16 from rates.
Latin America, 5 from Southeast Asia, 21 from Europe,
6 from the Eastern Mediterranean, and 7 from the Bacterial Meningitis
Western Pacific. Of the 71 full-text studies, 39
originated from HICs, 25 from MICs, and 7 from LICs. Twenty-two studies on BM were suitable for inclu-
Article details including individual con- siderations and sion. Nine studies were from Europe, four from
relative limitations are outlined further in Table 1 and Africa,

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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.

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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
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s
.

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TABLE 1. Review of 71 studies included in the quantitative meta-analysis
Disease Income Sample Incidence Study Study Study Method
Authors & Year Category Country WHO Region Level Size (Nʹ) (nʹ) Period Design Scale Score Limitations/Considerations
Adhikari et al., 2013 NCC Nepal SEAR Low 6,975 13.2 2007–2011 Retro Hosp 3
Adriani et al., 2007 BM Netherlands EUR High 28,333,333 232.0 1998–2002 Pros Pop 5
Akiyama et al., 2013 SO-nonTB Japan SEAR High 11,600,000 355.9 2007–2010 Retro Pop 4 Nationwide database–vertebral osteomyelitis
Al Khorasani & Banajeh, 2006 BM Yemen EMR Middle 103,484 28.0 1999–2001 Retro Hosp 3 Children aged <5 yrs only
Anwary et al., 2015 IA South Africa AFR Middle 3,000,000 15.5 1993–2011 Retro Hosp 2 CT diagnosis, sporadic data collection
Assane et al., 2017 NCC Mozambique AFR Low 1,723 6.4 2007 Cross Pop 4
Azad et al., 2003 NCC India SEAR Middle 863 60.2 1991–2002 Retro Hosp 4 Tertiary only; MRI reviewed
Beronius et al., 2001 SO-nonTB Sweden EUR High 438,503 11.6 1990–1995 Retro Hosp 4
Campagne et al., 1999 BM Niger AFR Low 547,743 471.9 1981–1996 Retro Pop 5
Chan et al., 2002 BM Singapore WPR High 8,000 24.4 1993–2000 Retro Hosp 3 Adults only; tertiary hospital only
Chapp-Jumbo, 2004 BM Nigeria AFR Low 9,254 18.7 1993–2003 Retro Hosp 3 Tertiary only; age > 14 yrs
Char et al., 2010 IA West Indies AMR-L Middle 12,724 2.4 1970–2008 Other Pop 5 Autopsy–patients who died w/ abscess
Cruz et al., 1999 NCC Ecuador AMR-L Middle 6,118 89.0 1994 Cross Pop 5
de Almeida et al., 2011 NCC Brazil AMR-L Middle 6,500 6.3 1977–1994 Pros Pop 5 Autopsy
Del Brutto, et al., 2005 NCC Brazil AMR-L Middle 2,548 8.0 2004 Cross Pop 5
del la Garza et al., 2005 NCC USA AMR-US/Can High 300,000 18.0 1994–1997 Retro Hosp 4
Ferreccio et al., 1990 BM Chile AMR-L High 550,000 80.6 1985–1987 Retro Pop 4 Study completed in pediatrics
Fleury et al., 2010 NCC Mexico AMR-L Middle 4,706 120.0 2004 Retro Hosp 2 Neurology/neurosurgery database
Fluegge et al., 2006 BM Germany EUR High 727,760 58.5 2001–2003 Pros Pop 5
Ford & Wright, 1994 BM Swaziland AFR Middle 750,000 67.3 1991–1992 Pros Pop 4
Frank-Briggs & Alikor, 2011 BM Nigeria AFR Middle 35,473 15.7 2004–2009 Retro Hosp 4 Pediatric neurology unit
Gallitelli et al., 2005 IA Italy EUR High 4,000,000 30.4 1996–2000 Retro Hosp 4 Tertiary only
Garcia-Lechuz et al., 2002 TB-s/c Spain EUR High 50,000 2.0 1993–1999 Retro Hosp 4 Tertiary only
Gómez Rodríguez et al., 2004 NCC Spain EUR High 127,000 1.8 1983–2003 Retro Hosp 4 Tertiary only
Granerod et al., 2013 SO-nonTB England EUR High 16,000,000 2,006.5 2005–2009 Other Pop 4 Prospective study w/ capture–recapture models
Grazziotin et al., 2010 NCC Brazil AMR-L Middle 1,009 109.2 1995–1996 Retro Hosp 3 Cranial CT patients in hospital
Hernández-Cossio et al., 1999 NCC Cuba AMR-L Middle 1,337 0.2 1964–1989 Retro Hosp 3 Tertiary only
Howitz & Homøe, 2014 BM Denmark EUR High 255,599 23.0 1996–2009 Retro Pop 3 Postop BM
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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
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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.

TABLE 2. Worldwide estimated totals for CNS infectious

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

IA 240 0.52 0.54


1995–2000 SO-nonTB UN UN 4
Hosp
TB-related disease* UN 0.57 0.56
Study

UN = data unavailable in literature.


1986–2002 Retro

* Meningitis/osteomyelitis.
12.2
6,100,000Incidence

Nontuberculous Osteomyelitis
Ten studies on spinal nontuberculous osteomyelitis
and discitis were suitable for inclusion (Supplemental
Sample

Figs. 3 and 4). Eight studies were performed in Europe,


10.5

and one each was performed in the Eastern


Mediterranean and Southeast Asia. The overall estimate
of the total popula- tion affected was 108,426 per annum
AMR-US/CanIncome
High
4,452

(Table 3). The re- ported incidence from individual


studies ranged from 0.27 cases/100,000 people (95% CI
0.16–0.45) to 39.7/100,000 (95% CI 34.5–45.8). All
included studies originated from HICs, and the overall
pooled estimate of incidence was 4 cases/100,000 people
High

(95% CI 1–9). Case fatality for non- TB osteomyelitis


was available in six studies,24,37,76,82,186,187 giving an overall
rate of 13.6% (95% CI 3.8%–23.5%), with the highest
report of 26.8% in an elderly population in New
USA

Zealand76 and the lowest (< 0.01%) in England.187


WPR

Study quality was not a source of heterogeneity in a


meta- regression analysis (p = 0.99).
Disease
NCC

Tuberculous Meningitis/Osteomyelitis
Taiwan

Four studies on tuberculous meningitis and/or


Limitations/Considerations

osteomy-
elitis were suitable for inclusion (Supplemental Figs. 5
and
et al., 2004

6). Two studies originated from HICs in Europe, and


IA

one
study each originated from a MIC in Africa and
Southeast
Townes

Asia. The overall estimate of the global population


affected
Xiao et al., 2005

by TB meningitis or osteomyelitis was 1,005,612 each


year
(Table 3). The reported incidence from individual
Score

studies
ranged from 0.51 cases/100,000 in a European HIC
(95%
Design Scale

CI 0.16–1.66) to 54.8/100,000 in an African MIC (95%


CI
11.4–263.8; Supplemental Figs. 5 and 6). Case fatality
for
TB osteomyelitis was only available in one Turkish
study,
Period

with a case fatality of 21.1%.78 All deaths were


associated
with stage III recrudescent
disease.
(nʹ)

J Neurosurg June 15, 2018 7


Size (Nʹ)
No. Affected
TABLE 3. Worldwide estimated inci
F. C. Robertson et
al.

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

† (p = 0.02; Table 5). The funnel plot was asymmetrical




for all of the different disease outcomes, which suggests


that studies showing a higher incidence could be
missing, and, consequently, our results could be an
underestimation. Because at least 10 studies are needed
0.73


to assess publication bias with a funnel plot, assessment



3
5

of bias could not be completed for tuber- culous


meningitis/osteomyelitis (4 studies).
3,144
2,810
4,666

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.

CNS in- fectious diseases. The results of this systematic


review and meta-analysis underscore the epidemiological
0.88
0.72
0.76

0.15
0.52

dispropor- tions of disease by region, income status, and


49‡
19

pathogen. Areas of lower income are particularly


vulnerable to the persistence and spread of infection due
to poverty, over- crowding, inadequate access to clean
1,894
8,408,393
1,491
9,168

8,636,606

24,743,893
1,249,602
6,436,739

water and proper sanitation systems, and insufficient


access to health care overall.72,119,171 In our study of the
five categories of CNS infection, LICs had an overall
incidence of 726 cas- es/100,000 people and MICs had
299/100,000, compared with approximately 11/100,000
in the high-income coun- terparts. Furthermore, LMICs
0.53
0.23

436

have the smallest neurosur- gical workforce, with many


461
1
197
650

LMICs in Sub-Saharan Africa having only one


neurosurgeon per 3–10 million constitu- ents, in contrast
to one per 20,000–60,000 in Europe and other
1,060,692
7,145
71,287

974,194
55,007

2,907,146
95,147
643,674

HICs.1,52,147,162 The limited workforce and resources in


LMICs compounded by the increased burden of CNS in-
fection highlight the importance of this public health
issue.

Bacterial
55‡
11
6

‡ Calculated based on income data for WHO region.


2
52
65

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

Sub- Saharan African known as the “meningitis belt.”6,116


Our study revealed an annual incidence of 65
cases/100,000 people for the AFR, corroborating
findings from the 2014
* Meningitis/osteomyelitis.

WHO Global Health Observatory database, which re-


ported an annual incidence ranging from 0.03/100,000 in
AMR-US/CAN

Mauritania to 227/100,000 in the Democratic Republic


Worldwide

of Congo (http://apps.who.int/gho/data). These similar


AMR-L

SEAR
WPR
EMR
EUR

con- clusions served as validation for our methodology.


AFR

More- over, the significant contrast between the


incidence in Af- rica and more Westernized regions such
8 J Neurosurg June 15, 2018
F. C. Robertson et
al.

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.

J Neurosurg June 15, 9


2018
F. C. Robertson et
al.

N survey within the Soutou cidence of NCC was I


e village in a historically noted in the Eastern n
u endemic region of Mediterranean at 0.23 t
Senegal, which showed cases/100,000 people.
r r
an incidence of One proposed
o 516 cases/100,000 a
c explanation is that c
people. In contrast, predominantly Muslim
y several studies fo- cused r
regions have a smaller
s only on symptomatic a
pork industry and
t disease by screening therefore a substantially n
i within epileptic i
populations, which may lower rate of cysti-
c cercosis and subsequent a
e have underestimated the
fecal-oral transmission l
total incidence of NCC
r infection. The lowest leading to NCC.114
c regional in- Neurocysticercosis can A
o require neurosurgical b
s interven- s
i tion for biopsy, c
s treatment of
e
Neurocysticercosis hydrocephalus, or
alleviation s
was the most reported s
individual disease in of mass effect.16,155
publications of CNS Furthermore, as the While our study
infections worldwide most common showed a globally low
(27 of 71 studies). The cause of acquired incidence of intracranial
burden of NCC was seizures worldwide, abscess (1 case/100,000
most prominent in NCC-related refrac- people), LICs had a
Africa and in LMICs, tory epilepsy often significantly higher
where neurosurgeons are necessitates surgery.36,181 burden of disease. Latin
few,51 with an incidence Overall, NCC America had the highest
of 650 and 401 provokes sequelae that incidence among the
cases/100,000 people, require surgical countries with available
respectively. Latin intervention and figures (19
American countries contributes to the burden cases/100,000 people),
contributed the greatest of neurosurgical disease, although this statis- tic
amount of high-quality particu- was based on a single
research on NCC, and l study in the West
WPR and SEAR had a Indies.36 The
substantial rates of
infection as well. Our r
results corroborate that l
NCC has been a known y
public health problem in
these four WHO regions i
and in indi- vidual n
LMICs because of poor
hygiene, methods of pig e
management and n
slaughter, and d
inadequate waste and e
wa- ter management.151 m
Importantly, our i
estimates may involve c
selection bias as many
population-based studies a
were con- ducted in r
villages and regions of e
known endemnicity. For a
instance, Secka et al. s
conducted a population- .
based radio- graphic
J Neurosurg June 15, 10
2018
F. C. Robertson et
al.

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.

J Neurosurg June 15, 11


2018
F. C. Robertson et
al.

cally managed patients cases/100,000 people tion, or spinal column t


are closely monitored based on the single study invasion and i
with serial imaging.61 in Cam- eroon by Lootie compressive myelopa- s
Overall, reduced et al.101 Interestingly, our thy. In a Danish study of
patients with spinal TB, In our study, the
mortality in this disease review demon- strated nontuberculous vertebral
pro- cess with the advent that much of the known 54/133 (40.6%) had
neurological deficits on spondylodis- citis was
of CT imaging and epidemiological data for the least prevalent of the
neurosurgical in- CNS TB is limited to admission and 17.3%
presented with cauda five diseases, affecting
tervention has been MICs and HICs, with no approximately 100,000
corroborated in other LIC in- cluded in the equina syndrome,
requiring surgi- cal people each year
studies,29,130,191 quantitative meta- worldwide. The surgical
emphasizing the analysis. intervention.84 In a
Filipino study of TB intervention rate ranged
importance of both These severe forms of from 9.2% described by
imaging and surgery as extrapulmonary TB can meningitis in children,
the mortality rate was Grammatico et al. in
standard care. cause significant France69 to 96.8% by
morbidity and mortality 16%, and 71% of
patients exhibited signs Menon et al. in Oman.111
T via the development of Of note, all 10 included
u hydrocephalus, of hydrocephalus.93
studies were reflec- tive
b encephalitis, vasculitis, Thus, neurosurgeons
thrombosis, infarc- have a role to intervene of
er in CNS TB for biopsy,
c HICs.17,24,62,66,69,75,101,110,157,1
spinal de- compression
ul and stabilization, and
60,185
This does not
o CSF diversion. Fur- imply that the incidence
si thermore, despite few of non-TB
s- publications on the spondylodiscitis is zero
R epidemiology of CNS for
el TB in LICs, it is
suspected that in these
at countries, the demand
e for CNS TB treatment is
d highest and should be
C investigated further.
N
S N
Di o
s n
e t
a u
s b
e e
Tuberculosis-related r
CNS disease includes c
TB menin- gitis and TB u
spondylitis. The WHO l
data repository reports o
an average annual
u
incidence of systemic
TB infection as s
244 cases/100,000
people over the last 5 O
years, of which s
spondylodiscitis and t
meningitis represent e
approximately o
2% and 3%, m
respectively.175,197 In our
study, the region with y
the highest noted e
incidence was Africa l
with a rate of 55 i
J Neurosurg June 15, 12
2018
F. C. Robertson et
al.

TABLE 4. Most common pathogens reported by each study for bacterial meningitis and intracranial abscess

Age Range Total Most Common Pathogen


Authors & Year Country WHO (yrs) Cases 1st 2nd 3rd
BM
Adriani et al., 2007 Netherlands EUR 17 to 83 34 S. pneumoniae H. influenzae N. meningitidis
Campagne et al., 1999 Niger AFR 0 to 40+ 7078 N. meningitidis S. pneumoniae H. influenzae
Ford & Wright, 1994 Swaziland AFR 0 to 15+ 85 S. pneumoniae N. meningitidis H. influenzae
Gebremariam, 1998 Ethiopia AFR <1 55 K. pneumoniae E. coli Enterobacter spp.
Soumaré et al., 2005 Senegal AFR 2 to 85 62 S. pneumoniae N. meningitidis Salmonella spp.
Ferreccio et al., 1990 Chile AMR-L 0 to 5 343 H. influenza only
Schuchat et al., 1997 USA AMR-US/Can 0 to 60+ 248 S. pneumoniae N. meningitidis Group B streptococcus
Al Khorasani & Banajeh, 2006 Yemen EMR 1 to 15 153 N. meningitidis S. pneumoniae H. influenzae
Mahmoud et al., 2002 UAE EMR 0 to 29 125 H. influenzae S. pneumoniae N. meningitidis
Fluegge et al., 2006 Germany EUR 0 to 3 mos 707 Group B streptococcus only
Kalliola et al., 1999 Finland EUR 0 to 3 mos 485 Group B streptococcus only
Klobassa et al., 2014 Austria EUR 0 to 5 74 S. pneumoniae only
Nørgaard et al., 2003 Denmark EUR 0.5 to 88 45 S. aureus only
Østergaard et al., 2005 Denmark EUR 22 to 69 187 S. pneumoniae only
Reinert et al., 1993 France EUR 0 to 5 277 H. influenzae only
Sigurdardóttir et al., 1997 Iceland EUR 16 to 45+ 132 N. meningitidis S. pneumoniae L. monocytogenes
Chan et al., 2002 Singapore WPR 14 to 72 15 S. pneumoniae N. meningitidis Group B streptococcus
Hui et al., 2005 China WPR 15 to 86 35 Unknown S. pneumoniae S. suis
Limcangco et al., 2000 Philippines WPR 0 to 5 118 H. influenza only
Lu et al., 2000 Taiwan WPR 18+ 202 K. pneumoniae P. aeruginosa S. pneumoniae
Sakata, 2007 Japan WPR 0 to 9 52 H. influenza only
IA
Char et al., 2010 West Indies AMR-L 0 to 76 93 S. pneumoniae Proteus spp. S. aureus
Jamjoom et al., 1994 Saudi Arabia EMR 0 to 80 22 S. aureus S. milleri Unknown
Lu et al., 2002 Taiwan WPR 1 mo to 80 123 S. viridans Unknown Mixed
Xiao et al., 2005 Taiwan WPR 2 mos to 84 178 S. viridans S. aureus Peptostreptococcus spp.
H. influenzae = Haemophilus influenzae; K. pneumoniae = Klebsiella pneumoniae; L. monocytogenes = Listeria monocytogenes; N. meningitidis = Neisseria meningiti-
des; P. aeruginosa = Pseudomonas aeruginosa; S. aureus = Staphylococcus aureus; S. milleri = Streptococcus milleri; S. pneumoniae = Streptococcus pneumoniae;
S. suis = Streptococcus suis; S. viridans = Stretococcus viridans.

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

12 J Neurosurg June 15, 2018


F. C. Robertson et
al.

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.

14 J Neurosurg June 15,


2018
F. C. Robertson et
al.

generalizability to entire by the availability of


regions. However, this resources. Finally,
strategy of using a lower heterogeneity remained
threshold for high in most categories
underrepresented regions despite stratifying by
fol- lows precedent.31 trial-level covariates;
Furthermore, gold- this could be attributable
standard diagnostic to residual confounding
testing is frequently or variance in true rates
unavailable in low- rather than sampling
resource settings. error. Study quality did
Unsurprisingly, included not appear to be a source
studies with a broader of hetero- geneity, likely
definition of infection because the studies that
(such as seropositivity provided incidence and
for cysticercosis and
were consequently
history of seizure) had a
entered in the meta-
higher rate of infection
than those studies with a analysis were generally
stricter definition of of moderate to high
infection. While we re- quality.
port the volume of CNS While these
infections that are most limitations are
likely to require surgery, substantial, they
our estimates for true highlight the difficulty in
neurosurgical de- mand obtaining high-quality
were restricted because epidemiological data on
few publications infectious diseases
specifically indicated the affecting the CNS,
proportion of patients particularly in low-
requiring surgery in their resource settings.
investigation. It would Further research should
have been ideal to show specifically ad- dress the
this proportion of limitations of this study,
surgical cases for each with particular emphasis
disease category, as well on population-based
as to describe and epidemiological studies
quantify the in LMICs.
neurosurgical proce-
dures performed in C
patients with
neurosurgical infections o
on a global scale. This n
would allow comparison
of neuro- surgical c
treatment of CNS l
infections across WHO u
regions, which could
have differing s
management options i
dictated
o
n
s
Here, we performed a
systematic review and
meta- analysis of more
than 10,000 titles and
ultimately included

J Neurosurg June 15, 15


2018
F. C. Robertson et
al.

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
CNS Infection Funnel Plot Begg’s Test Egger’s Test 9. Al Khorasani A, Banajeh S: Bacterial profile and clinical
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
11. Alothman A, Memish ZA, Awada A, Al-Mahmood S,
TB-related disease* Symmetrical† 1.00 0.89 Al-Sadoon S, Rahman MM, et al: Tuberculous spondylitis:
Boldface type indicates statistical significance.
analysis of 69 cases from Saudi Arabia. Spine (Phila Pa
* Meningitis/osteomyelitis.
1976) 26:E565–E570, 2001
† Need at least 10 studies to assess publication bias.
12. Anwary MA: Intracranial suppuration: Review of an 8-year
experience at Umtata General Hospital and Nelson Mandela
Academic Hospital, Eastern Cape, South Africa. S Afr Med
154 articles to estimate the global volume of CNS in- J 105:584–588, 2015
13. Arlotti M, Grossi P, Pea F, Tomei G, Vullo V, De Rosa FG,
fections that may require neurosurgical intervention. To et al: Consensus document on controversial issues for the
our knowledge, this is the first study of its kind. In treatment of infections of the central nervous system: bacte-
total, these studies included over 130,681,681 patients rial brain abscesses. Int J Infect Dis 14 (Suppl 4):S79–
across 44 countries. While our study provides an S92, 2010
approximation, our results can be used as a benchmark 14. Assana E, Lightowlers MW, Zoli AP, Geerts S: Taenia
against which lo- cal disease incidence can be solium taeniosis/cysticercosis in Africa: risk factors, epide-
compared. Overall, we have described the estimated miology and prospects for control using vaccination. Vet
global and regional incidence of five CNS infectious Parasitol 195:14–23, 2013
15. Assane YA, Trevisan C, Schutte CM, Noormahomed EV,
diseases of neurosurgical relevance. The strength and Johansen MV, Magnussen P: Neurocysticercosis in a rural
quality of epidemiological information regarding population with extensive pig production in Angónia dis-
neurosurgical disease in the developing world is trict, Tete Province, Mozambique. Acta Trop 165:155–160,
certainly lacking, yet those populations are the ones 2017
most afflicted by the burden of infectious CNS disease. 16. Association of American Medical Colleges: Number and
The data in this study provide the neurosurgical percentage of active physicians by sex and specialty,
community with an inclusive estimate of the global in 2014 Physician Specialty Data Book. Washington,
incidence of CNS infectious disease. DC: AAMC, 2014, p 12 (https://www.aamc.org/
download/473260/data/2014physicianspecialtydatabook.pdf)
[Accessed January 26, 2018]
Acknowledgments 17. Attili SVS, Gulati AK, Singh VP, Varma DV, Rai M,
We acknowledge the Vanderbilt Medical Scholars Program Sundar S: Neurological manifestations Hiv-infected patients
for providing Abbas Rattani with support on this project and the around Varanasi, India. Afr J Neurol Sci 25:33–40, 2006
Wil- son Family Clinical Scholars Program for providing Jacob 18. Azad R, Gupta RK, Kumar S, Pandey CM, Prasad KN,
Lepard with support on this project. Husain N, et al: Is neurocysticercosis a risk factor in coex-
istent intracranial disease? An MRI based study. J Neurol
Neurosurg Psychiatry 74:359–361, 2003
Reference 19. Baccouche K, Elamri N, Belghali S, Bouzaoueche M,
Zeglaoui H, Bouajina E: Epidemiological study of infec-
s tious spondylitis in a Tunisian center: about 118 cases. Ann
1. Aarli JA, Diop AG, Lochmüller H: Neurology in sub-Saha- Rheum Dis 75 (Suppl 2):850, 2016 (Abstract)
ran Africa: a challenge for World Federation of Neurology. 20. Ballard JL, Carlson G, Chen J, White J: Anterior thoraco-
Neurology 69:1715–1718, 2007 lumbar spine exposure: critical review and analysis. Ann
2. Abbasi F, Besharat M: Tubercolosis spondylitis (Pott’s dis- Vasc Surg 28:465–469, 2014
ease) in Iran, evaluation of 40 cases. Iran J Clin Infect Dis 21. Bamba S, Lortholary O, Sawadogo A, Millogo A,
6 Suppl:170–172, 2011 Guiguemdé RT, Bretagne S: Decreasing incidence of cryp-
3. Abdullah J: Clinical presentation and outcome of brain tococcal meningitis in West Africa in the era of highly
abscess over the last 6 years in community based neurologi- active antiretroviral therapy. AIDS 26:1039–1041, 2012
cal service. J Clin Neurosci 8:18–22, 2001 22. Benedeti MR, Falavigna DL, Falavigna-Guilherme AL,
4. Adhikari S, Sathian B, Koirala DP, Rao KS: Profile of Araújo SM: [Epidemiological and clinical profile of neuro-
children admitted with seizures in a tertiary care hospital of cysticercosis patients assisted by the Hospital Universitário
Western Nepal. BMC Pediatr 13:43, 2013 Regional de Maringá, Paraná, Brazil.] Arq Neuropsiquiatr
5. Adriani KS, van de Beek D, Brouwer MC, Spanjaard L, de 65:124–129, 2007 (Portuguese)
Gans J: Community-acquired recurrent bacterial meningitis 23. Bern C, Garcia HH, Evans C, Gonzalez AE, Verastegui
in adults. Clin Infect Dis 45:e46–e51, 2007 M, Tsang VC, et al: Magnitude of the disease burden from
6. Agier L, Martiny N, Thiongane O, Mueller JE, Paireau J, neurocysticercosis in a developing country. Clin Infect Dis
Watkins ER, et al: Towards understanding the epidemiology 29:1203–1209, 1999
of Neisseria meningitides in the African meningitis belt: a 24. Beronius M, Bergman B, Andersson R: Vertebral osteomy-
multi-disciplinary overview. Int J Infect Dis 54:103–112, elitis in Göteborg, Sweden: a retrospective study of patients
2017 during 1990–95. Scand J Infect Dis 33:527–532, 2001
7. Akiyama T, Chikuda H, Yasunaga H, Horiguchi H, Fushimi 25. Bhattarai R, Budke CM, Carabin H, Proaño JV, Flores-
K, Saita K: Incidence and risk factors for mortality of Rivera J, Corona T, et al: Estimating the non-monetary bur-
vertebral osteomyelitis: a retrospective analysis using the
16 J Neurosurg June 15,
2018
F. C. Robertson et
al.

J Neurosurg June 15, 17


2018
F. C. Robertson et
al.

den of Oncel E, epilepsy caused 45. Del Brutto OH:


neurocysticercosis in Camcioglu Y, Salman by intrahippocampal Neurocysticercosis in
Mexico. PLoS Negl N, et al: Bacterial calcified cysticercus: Western Europe:
agents causing a case report. J a re-emerging disease?
Trop Dis
meningitis during Korean Med Sci Acta Neurol Belg
6:e1521, 2012
2013-2014 in Turkey: 13:445–448, 1998 112:335–343,
26. Bhavan KP, Marschall
a multi-center 40. Corrêa-Lima ARM, 2012
J, Olsen MA, Fraser VJ,
hospital-based de Barros Miranda-Filho 46. Del Brutto OH,
Wright NM,
prospective D, Valença Salgado P, Lama J, Del
Warren DK: The
surveillance study. MM, Andrade- Brutto VJ, Campos
epidemiology of
Hum Vaccin Valença L: Risk X, Zambrano M, et al:
hematogenous
Immunother factors for acute Calcified
vertebral
12:2940–2945, 2016 symp- neurocysticercosis
osteomyelitis: a cohort
34. Chan YC, Wilder- tomatic seizure in associ-
study in a tertiary care
Smith A, Ong BK, bacterial meningitis in ates with hippocampal
hospital.
Kumarasinghe G, children. J Child atrophy: a population-
BMC Infect Dis
Wilder-Smith E: Neurol 30:1182– based study.
10:158, 2010
Adult community 1185, 2015 Am J Trop Med Hyg
27. Biaukula VL,
acquired bacterial 41. Cowppli-Bony P, 92:64–68, 2015
Tikoduadua L, Azzopardi
men- Sonan-Douayoua T, 47. Del Brutto OH,
K, Seduadua A,
ingitis in a Akani F, Datie AM, Santibáñez R, Idrovo L,
Temple B, Richmond
Singaporean teaching Assi B, Aka-Diarra E, Rodrìguez S,
P, et al: Meningitis in
hospital. A seven-year et al: Epidemiology Díaz-Calderón E, Navas
children in Fiji:
overview (1993– of hospitalized C, et al: Epilepsy and
etiology,
2000). Singapore patients in neurology: neurocysti-
epidemiology, and
Med J 43:632–636, experience of Cocody cercosis in Atahualpa: a
neurological sequelae.
2002 teaching hos- door-to-door survey in
Int J
35. Chapp-Jumbo EN: pital at Abidjan rural coastal
Infect Dis 16:e289–
Neurologic admissions in (Côte-d’Ivoire). Afr J Ecuador. Epilepsia
e295, 2012
the Niger delta Neurol Sci 23:7553, 46:583–587, 2005
28. Brouwer MC,
area of Nigeria - a ten 2004 48. del la Garza Y, Graviss
Coutinho JM, van de
year review. Afr J 42. Cruz ME, Preux PM, EA, Daver NG, Gambarin
Beek D: Clinical char-
Neurol Sci 23:77, Debrock C, Cruz I, KJ,
acteristics and
2004 Schantz PM, Shandera WX, Schantz
outcome of brain
36. Char G, West KA, Tsang VC, et al: PM, et al:
abscess: systematic
Jaggon JR: Intracranial [Epidemiology of Epidemiology of neu-
review
abscesses: cerebral cysticercosis rocysticercosis in
and meta-analysis.
Epidemiological trend in Houston, Texas. Am J
Neurology 82:806–
over a 39-year period an Andean Trop Med Hyg
813, 2014
at the univer- community in 73:766–770, 2005
29. Brouwer MC,
sity of the West Ecuador.] Bull Soc 49. DerSimonian R,
Tunkel AR, McKhann
Indies. Internet J Pathol Exot Laird N: Meta-analysis
GM II, van de Beek
Third World Med 92:38–41, 1999 (Fr) in clinical trials
D: Brain abscess. N
8:1, 43. Daniele B: revisited. Contemp
Engl J Med 371:447–
2010 Characteristics of central Clin Trials 45 (Pt
456, 2014
37. Chen CH, Sy HN, Lin nervous system tuber- A):139–145, 2015
30. Burki T: Meningitis
LJ, Yen HC, Wang SH, culosis in a low- 50. Domingo P, Suarez-
outbreak in Niger is an
Chen WL, et incidence country: a Lozano I, Torres F, Pomar
urgent warning.
al: Epidemiological series of 20 cases and V, Ribera E,
Lancet Infect Dis
characterization and a review of the Galindo MJ, et al:
15:1011, 2015
prognostic factors literature. Jpn J Bacterial meningitis in
31. Butler C, Hill H:
in patients with Infect Dis 67:50–53, HIV-1-infected
Chlormadinone acetate as
confirmed cerebral 2014 patients in the era of
oral contracep-
cryptococcosis in 44. de Almeida SMT, highly active
tive. A clinical trial.
central Torres LF: antiretroviral therapy. J
Lancet 1:1116–1119,
Taiwan. J Venom Neurocysticercosis— Acquir Immune Defic
1969
Anim Toxins Incl retro- Syndr 51:582–587,
32. Campagne G,
Trop Dis 21:12, 2015 spective study of 2009
Chippaux JP, Djibo S, Issa
38. Christensen ASH, autopsy reports, a 17- 51. Duron RM, Garcia
O, Garba A:
Andersen ÅB, Thomsen year experience. J HH, Kurdi A, Medina
[Epidemiology and
VO, Andersen Community Health MT, Rodriguez
control of bacterial
PH, Johansen IS: 36:698–702, 2011 LC: Chapter 3.5.
meningitis in chil-
dren less than 1 year in Tuberculous Neuroinfections, in
Niamey (Niger).] Bull meningitis in Neurological
Soc Pathol Denmark: a Disorders: Public
Exot 92:118–122, review of 50 cases. Health Challenges.
1999 (Fr) BMC Infect Dis Geneva: WHO
33. Ceyhan M, Ozsurekci 11:47, 2011 Press, 2006
Y, Gürler N, Karadag 39. Chung CK, Lee SK, 52. El Khamlichi A:
Chi JG: Temporal lobe
18 J Neurosurg June 15,
2018
F. C. Robertson et
al.

Neurosurgery in Africa. sentation of invasive


Clin Neurosurg neonatal group B
52:214–217, 2005 streptococcal infec-
53. Ferreccio C, Ortiz E, tions in Germany.
Astroza L, Rivera C, Clemens Pediatrics 117:e1139–
J, e1145, 2006
Levine MM: A 59. Ford H, Wright J:
population-based Bacterial meningitis in
retrospective assessment Swaziland: an
of the disease burden 18 month prospective
resulting from invasive study of its impact. J
Haemophilus Epidemiol
influenzae in infants and Community Health
young children in 48:276–280, 1994
Santiago, Chile. 60. Frank-Briggs AI,
Pediatr Infect Dis J Alikor EAD: Pattern of
9:488–494, 1990 paediatric neuro-
54. Fiegin VL, Forouzanfar logical disorders in Port
MH, Krishnamurthi R, Harcourt, Nigeria. Int J
Mensah Biomed
GA, Connor M, Bennett Sci 7:145–149, 2011
DA, et al: Global and 61. Gallitelli M, Lepore V,
regional bur- Pasculli G, Di Gennaro L,
den of stroke during Logroscino G, Carella
1990-2010: findings from A, et al: Brain abscess: a
the Global need
Burden of Disease Study to screen for pulmonary
2010. Lancet 383:245– arteriovenous
254, 2014 malformations.
(Erratum in Lancet Neuroepidemiology
383:218, 2014) 24:76–78, 2005
55. Fitzwater SP, 62. García-Lechuz JM,
Ramachandran P, Julve R, Alcalá L, Ruiz-
Nedunchelian K, Kahn G, Serrano MJ,
Santosham M, Chandran Muñoz P: [Tuberculous
A: Bacterial meningitis in spondylodiskitis (Pott’s
children disease):
<2 years of age in a experience in a general
tertiary care hospital in hospital.] Enferm Infecc
South India: Microbiol
an assessment of clinical Clin 20:5–9, 2002
and laboratory features. J (Span)
Pediatr 63. Gebremariam A:
163 (1 Suppl):S32–S37, Neonatal meningitis in
2013 Addis Ababa: a
56. Flecker R: Assessing the 10-year review. Ann
economic burden of Trop Paediatr 18:279–
neurocysticer- 283, 1998
cosis hospitalizations in
the United States, 2003–
2012. Am
J Trop Med Hyg 91 (5
Suppl 1):364, 2014
(Abstract)
57. Fleury A, Moreno García
J, Valdez Aguerrebere P, de
Sayve Durán M, Becerril
Rodríguez P, Larralde C,
et al:
Neurocysticercosis, a
persisting health problem
in Mexico.
PLoS Negl Trop Dis
4:e805, 2010
58. Fluegge K, Siedler A,
Heinrich B, Schulte-Moenting
J,
Moennig MJ, Bartels DB,
et al: Incidence and
clinical pre-
J Neurosurg June 15, 19
2018
F. C. Robertson et
al.

20 J Neurosurg June 15,


2018
F. C. Robertson et
al.

64. Gmeiner MA, Wagner SL: New estimates of in Qatar: a descriptive 82. Jensen AG, Espersen
H, Zacherl C, Polanski P, incidence of retrospective study from F, Skinhøj P, Rosdahl
Auer C, encephalitis in England. its referral VT, Frimodt- Møller
van Ouwerkerk WJ, et Emerg Infect Dis center. Eur Neurol N: Increasing
al: Long-term mortality 19:1455–1462, 2013 73:90–97, 2015 frequency of
rates in pedi- 71. Grazziotin ALF, 78. Inal AS, Kurtaran B, vertebral
atric hydrocephalus—a Fontalvo MC, Santos MB, Candevir A, Tasova Y, Aksu osteomyelitis
retrospective single- Monego F, HSZ: following
center study. Grazziotin AL, Kolinski Tuberculous meningitis Staphylococcus
Childs Nerv Syst VH, et al: in adults: evaluation of aureus bacteraemia in
33:101–109, 2017 Epidemiologic pattern 38 cases. Denmark
65. Goel D, Dhanai JS, of patients with Clin Microbiol Infect 1980–1990. J Infect
Agarwal A, Mehlotra V, neurocysticercosis 15 (Suppl 4):S129, 34:113–118, 1997
Saxena V: diagnosed by computed 2009 (Abstract) 83. Jeong SJ, Choi SW,
Neurocysticercosis and tomography in Curitiba, 79. Jaiswal SK, Murthy Youm JY, Kim HW, Ha HG,
its impact on crude Brazil. Arq JMK, Reddy PM, Sri Yi JS:
prevalence rate Neuropsiquiatr Krishna S: Microbiology and
of epilepsy in an Indian 68:269–272, 2010 Incidence of seizure epidemiology of
community. Neurol 72. Greener R, Sarkar S: disorder associated with infectious spinal disease.
India 59:37– Risk and vulnerability: do solitary cysti- J Korean Neurosurg
40, 2011 socioeco- cercus granuloma and Soc 56:21–27, 2014
66. Gómez Rodríguez N, nomic factors influence single calcific NCC: A 84. Johansen IS, Nielsen SL,
Penelas-Cortés Bellas Y, the risk of acquiring study among Hove M, Kehrer M, Shakar
Ibáñez Ruán HIV in Asia? children accessing S,
J, González Pérez M, AIDS 24 (Suppl 3):S3– government schools in Wøyen AV, et al:
Sánchez Lorenzo ML: S11, 2010 Hyderabad dis- Characteristics and
[Infectious 73. Hernández-Cossio O, trict. Ann Indian Acad clinical outcome of
spondylodiscitis in a Hernández-Fustes OJ: Neurol 18 (Suppl bone and joint
health area of Galicia [Neurocysticercosis and 2):S21, 2015 tuberculosis from 1994
(Spain) from epilepsy in Cuba.] Rev (Abstract) to 2011: a retro-
1983–2003.] Med Neurol 80. Jamjoom A, Jamjoom spective register-based
Interna 21:533–539, 29:1003–1006, 1999 ZA, Naim-Ur-Rahman, study in Denmark. Clin
2004 (Span) (Span) Tahan A, Infect Dis
67. Góngora-Rivera F, 74. Howitz MF, Homøe P: Malabarey T, Kambal 61:554–562, 2015
Santos-Zambrano J, The risk of acquiring A: Experience with 85. Kabré A, Zabsonré S,
Moreno-Andrade T, bacterial brain abscess Diallo O, Cissé R:
Calzada-López P, Soto- meningitis following in the central province [Management
Hernández JL: The surgery in Denmark, of Saudi Arabia. Trop of brain abscesses in era
clinical spectrum 1996–2009: a Geogr Med of computed tomography
of neurological nationwide 46:154–156, 1994 in sub-
manifestations in AIDS retrospective cohort 81. Jensen AG, Espersen F, Saharan Africa: a review
patients in Mexico. study with emphasis on Skinhøj P, Frimodt-Møller of 112 cases.]
Arch Med Res ear, N: Neurochirurgie
31:393–398, 2000 nose and throat (ENT) Bacteremic 60:249–253, 2014 (Fr)
68. Goodman-Meza D, and neurosurgery. Staphylococcus aureus 86. Kalliola S, Vuopio-
Ware JA, Anthony A, Epidemiol Infect spondylitis. Arch Varkila J, Takala AK, Eskola
Coyle CM, Nash 142:1300–1309, 2014 Intern J:
TE: Retrospective 75. Hui ACF, Ng KC, Med 158:509–517, Neonatal group B
review of cysticercosis Tong PY, Mok V, Chow 1998 streptococcal disease in
in returned United KM, Wu A, et Finland: a ten-
States travelers. Am J al: Bacterial meningitis year nationwide study.
Trop Med Hyg 91 (5 in Hong Kong: 10- Pediatr Infect Dis J
Suppl 1):364, years’ experi- 18:806–810,
2014 (Abstract) ence. Clin Neurol 1999
69. Grammatico L, Baron Neurosurg 107:366– 87. Kehrer M, Pedersen C,
S, Rusch E, Lepage B, 370, 2005 Jensen TG, Lassen AT:
Surer N, 76. Hutchinson C, Hanger Increasing
Desenclos JC, et al: C, Wilkinson T, Sainsbury incidence of pyogenic
Epidemiology of R, Pithie spondylodiscitis: a 14-
vertebral osteomyelitis A: Spontaneous spinal year popula-
(VO) in France: infections in older tion-based study. J
analysis of hospital- people. Intern Infect 68:313–320, 2014
discharge data 2002– Med J 39:845–848, 88. Kenyon PC, Chapman
2003. Epidemiol 2009 ALN: 10 years of experience
Infect 136:653–660, 77. Imam YZB, of
2008 Ahmedullah HS, Akhtar N, tuberculous vertebral
70. Granerod J, Cousens S, Chacko KC, osteomyelitis in
Davies NW, Crowcroft NS, Kamran S, Al Alousi F, Sheffield. J Infect
Thomas et al: Adult tuberculous 59:S435–S436, 2009
meningitis
J Neurosurg June 15, 21
2018
F. C. Robertson et
al.

89. Khalifa ABH, Mastouri Travel Med 18:191–


M, Abdallah HB, Noomen 197, 2011
S, 95. Leshem E, Kliers I,
Kheder M: [Acquired Bakon M, Zucker T,
bacterial meningitis in Potasman I,
Monastir Schwartz E:
region, Tunisia (1999– [Neurocysticercosis in
2006): bacteriological Israel.] Harefuah
aspects and 149:576–579, 620, 2010
susceptibility patterns.] (Hebrew)
Bull Soc Pathol Exot 96. Libanore M, Rossi
104:42–48, MR, Bicocchi R,
2011 (Fr) Antonioli P, Leclercq
90. Klobassa DS, Zoehrer A, Ghinelli F: High
B, Paulke-Korinek M, incidence of Listeria
Gruber- monocytogenes
Sedlmayr U, meningitis in a north-
Pfurtscheller K, eastern Italian area. Clin
Strenger V, et al: The Microbiol
burden Infect 15 (Suppl
of pneumococcal 4):S648, 2009
meningitis in Austrian (Abstract)
children between 97. Lildal TK, Korsholm
2001 and 2008. Eur J J, Ovesen T: Diagnostic
Pediatr 173:871–878, challenges in
2014 otogenic brain
91. Kono Y, Prevedello abscesses. Dan Med J
DM, Snyderman CH, 61:A4849, 2014
Gardner PA, 98. Limcangco MRT, Salole
Kassam AB, Carrau EG, Armour CL:
RL, et al: One thousand Epidemiology
endoscopic of Haemophilus
skull base surgical influenzae type b
procedures meningitis in Manila,
demystifying the Philippines, 1994 to
infection 1996. Pediatr Infect
potential: incidence and Dis J 19:7–11,
description of 2000
postoperative menin- 99. Lino RS Jr, Reis MA,
gitis and brain Teixeira VP: [Occurrence of
abscesses. Infect ence-
Control Hosp phalic and cardiac
Epidemiol cysticercosis
32:77–83, 2011 (Cysticercus cellulosae)
92. Kuti BP, Bello EO, in necropsy.] Rev
Jegede TO, Olubosede O: Saude Publica 33:495–
Epidemiological, 498, 1999
clinical and prognostic (Portuguese)
profile of child- 100. Liu CC, Cho YH, Ho
hood acute bacterial TS, Wang SM, Shen CF:
meningitis in a resource Childhood
poor setting. J
Neurosci Rural Pract
6:549–557, 2015
93. Lee LV:
Neurotuberculosis
among Filipino
children: an
11 years experience at
the Philippine
Children’s Medical
Center. Brain Dev
22:469–474, 2000
94. Leshem E, Kliers I,
Bakon M, Gomori M,
Karplus R,
Schwartz E:
Neurocysticercosis in
travelers: a nation-wide
study in Israel. J
22 J Neurosurg June 15,
2018
F. C. Robertson et
al.

J Neurosurg June 15, 23


2018
F. C. Robertson et
al.

tuberculosis in southern Jpn J review.] Rev Med 119. Morrow BH:


Taiwan—with Infect Dis 66:503– Chir Soc Med Identifying and mapping
emphasis on central 506, 2013 Nat Iasi 113:402–409, community vulner-
nervous system 107. Malekpour-Afshar R, 2009 (Romanian) ability. Disasters 23:1–
complications. Int J Karamoozian S, Shafei H: 114. Millogo A, Nitiéma P, 18, 1999
Antimicrob Agents 42 Post trau- Carabin H, Boncoeur-Martel 120. Moyano LM, O’Neal
Suppl:S138–S139, matic meningitis in MP, SE, Ayvar V, Diaz A,
2013 (Abstract) neurosurgery Rajshekhar V, Rodriguez S,
101. Looti AZL, Kengne department. Am J Tarnagda Z, et al: Tsang VC, et al: High
AP, Djientcheu VDP, Kuate Infect Prevalence of prevalence of silent
CT, Dis 5:21–25, 2009 neurocys- neurocysticer-
Njamnshi AK: Patterns 108. Medina MT, Aguilar- ticercosis among cosis in an endemic
of non-traumatic Estrada RL, Alvarez A, people with epilepsy in rural community in
myelopathies in Durón RM, rural areas of Peru. Am J Trop
Yaoundé (Cameroon): Martínez L, Dubón S, Burkina Faso. Med Hyg 87 (5 Suppl
a hospital based study. et al: Reduction in rate Epilepsia 53:2194– 1):328–329, 2012
J Neurol of epilepsy 2202, 2012 (Abstract)
Neurosurg Psychiatry from 115. Mitha A, Boutry N, 121. Moyano LM, Saito M,
81:768–770, 2010 neurocysticercosis by Nectoux E, Petyt C, Lagrée Montano S, Gonzalvez GE,
102. Lu CH, Chang WN, community M, Olaya S,
Chang HW: Adult bacterial interventions: the Happiette L, et al: Ayvar V, et al: Two
meningitis Salamá, Honduras Community-acquired large epilepsy surveys in
in Southern Taiwan: study. Epilepsia bone and joint a cysticerco-
epidemiologic trend 52:1177–1185, 2011 infections in children: sis-endemic region in
and prognostic 109. Medina MT, Rosas E, a 1-year prospective Tumbes, Peru. Am J
factors. J Neurol Sci Rubio-Donnadieu F, Sotelo epidemiological Trop Med Hyg
182:36–44, 2000 J: study. Arch Dis Child 87 (5 Suppl 1):133,
103. Lu CH, Chang WN, Neurocysticercosis as 100:126–129, 2015 2012 (Abstract)
Lin YC, Tsai NW, Liliang the main cause of late- 116. Mohammed I, Iliyasu 122. Moyano LM, Saito
PC, Su onset epilepsy G, Habib AG: Emergence M, Montano SM,
TM, et al: Bacterial in Mexico. Arch and con- Gonzalvez G, Olaya
brain abscess: Intern Med 150:325– trol of epidemic S, Ayvar V, et al:
microbiological 327, 1990 meningococcal Neurocysticercosis as a
features, 110. Menon KV, Sorour meningitis in sub- cause of epi-
epidemiological trends TM: Epidemiologic and Saharan lepsy and seizures in
and therapeutic demographic Africa. Pathog Glob two community-based
outcomes. QJM attributes of primary Health 111:1–6, 2017 studies in a
95:501–509, 2002 spondylodiscitis in a 117. Moher D, Shamseer L, cysticercosis-endemic
104. Madhugiri VS, Sastri Middle Eastern Clarke M, Ghersi D, region in Peru. PLoS
BV, Srikantha U, Banerjee population sample. Liberati A, Negl Trop Dis
AD, World Neurosurg Petticrew M, et al: 8:e2692, 2014
Somanna S, Devi BI, 95:31–39, 2016 Preferred reporting 123. Murillo O, Grau I, Lora-
et al: Focal intradural 111. Menon S, Bharadwaj items for systematic Tamayo J, Gomez-Junyent J,
brain infec- R, Chowdhary A, review and meta- Ribera A, Tubau F, et al:
tions in children: an Kaundinya DV, analysis protocols The changing
analysis of Palande DA: Current (PRISMA-P) 2015 epidemiology of
management and epidemiology of statement. Syst Rev bacteraemic
outcome. intracranial abscess- 4:1, 2015 osteoarticular infections
Pediatr Neurosurg es: a prospective 5 118. Montano SMV, in the early 21st cen-
47:113–124, 2011 year study. J Med Villaran MV, Ylquimiche L, tury. Clin Microbiol
105. Mahmoud R, Microbiol 57:1259– Figueroa JJ, Infect 21:254.e1–
Mahmoud M, Badrinath P, 1268, 2008 Rodriguez S, Bautista 254.e8, 2015
Sheek-Hussein M, 112. Meyding-Lamadé U, CT, et al: 124. Murphy V, Dunne
Alwash R, Nicol AG: Strank C: Herpesvirus Neurocysticercosis: A: Mixed effects versus
Pattern of meningitis infections of the asso- fixed effects
in Al-Ain medi- central nervous system ciation between modelling of binary data
cal district, United in seizures, serology, and with inter-subject
Arab Emirates—a immunocompromised brain CT in rural variability. J
decadal experience patients. Peru. Neurology Pharmacokinet
(1990–99). J Infect Ther Adv Neurol 65:229–233, 2005 Pharmacodyn 32:245–
44:22–25, 2002 Disorder 5:279–296, 260, 2005
106. Mahmoudi S, Zandi H, 2012 125. Mwang’ombe NJ:
Pourakbari B, Ashtiani MT, 113. Miftode E, Vâţă A, Brain abscess at the
Mamishi S: Acute Leca D, Hurmuzache M, Kenyatta Nationai,
bacterial meningitis Dorneanu Hospital, Nairobi. East
among children O, Manciuc C, et al: Afr Med J 77:323–325,
admitted into an [Community acquired 2000
Iranian referral acute bacterial 126. Mwang’onde BJ,
children’s hospital. meningitis—a 10 year Chacha M, Nkwengulila
24 J Neurosurg June 15,
2018
F. C. Robertson et
al.

G: The public rural


health and Bolivia: a population-
socioeconomic burden based survey. Epilepsia
of Taenia solium cysti- 46:1127–
cercosis in Northern 1132, 2005
Tanzania. Int J Infect 133. Nicolosi A, Hauser WA,
Dis 21 (Suppl Musicco M, Kurland LT:
1):227–228, 2014 Incidence and prognosis
127. Mwanjali G, of brain abscess in a
Kihamia C, Kakoko DVC, defined
Lekule F, Ngowi population: Olmsted
H, Johansen MV, et al: County, Minnesota,
Prevalence and risk 1935–1981.
factors associ- Neuroepidemiology
ated with human Taenia 10:122–131, 1991
solium infections in 134. Nishimura K, Hung T:
Mbozi District, Current views on
Mbeya Region, geographic distri-
Tanzania. PLoS Negl bution and modes of
Trop Dis 7:e2102, infection of
2013 neurohelminthic
128. Namani SA, Koci BM, diseases.
Milenković Z, Koci R, J Neurol Sci 145:5–14,
Qehaja-Buçaj 1997
E, Ajazaj L, et al: Early 135. Nørgaard M,
neurologic Gudmundsdottir G, Larsen
complications and long- CS, Schønheyder
term sequelae of HC: Staphylococcus
childhood bacterial aureus meningitis:
meningitis in a limited- experience with
resource country cefuroxime treatment
(Kosovo). Childs Nerv during a 16 year period
Syst 29:275–280, in a Danish
2013 region. Scand J Infect
129. Narata AP, Arruda Dis 35:311–314, 2003
WO, Uemura E, Yukita S, 136. Obaro SK, Habib AG:
Blume AG, Control of meningitis
Suguiura C, et al: outbreaks in the
[Neurocysticercosis. A African meningitis belt.
tomographic Lancet Infect Dis
diagnosis in neurological 16:400–402, 2016
patients.] Arq 137. O’Neal SE, Flecker RH:
Neuropsiquiatr Hospitalization frequency and
56:245–249, 1998 charges for
(Portuguese) neurocysticercosis,
130. Nathoo N, Nadvi United States, 2003–
SS, Narotam PK, van 2012.
Dellen JR: Brain Emerg Infect Dis
abscess: management 21:969–976, 2015
and outcome analysis of
a computed
tomography era
experience with 973
patients. World
Neurosurg 75:716–726,
612–617, 2011
131. Nguyen VT,
Scannapieco M: Drug abuse
in Vietnam: a
critical review of the
literature and
implications for future
research. Addiction
103:535–643, 2008
132. Nicoletti A, Bartoloni
A, Sofia V, Bartalesi F,
Chavez JR,
Osinaga R, et al:
Epilepsy and
neurocysticercosis in
J Neurosurg June 15, 25
2018
F. C. Robertson et
al.

26 J Neurosurg June 15,


2018
F. C. Robertson et
al.

138. Ong S, Talan DA, Sánchez neurocysticercosis in a 157. Rasit AH, Razak M,
Moran GJ, Mower JL, Noh J, et al: pig farming Ting FS: The pattern of
W, Newdow M, Neurocysticercosis in community in northern spinal tuber-
Tsang VC, et al: persons with epilepsy India. Trans R Soc culosis in Sarawak
Neurocysticercosis in Medellín, Colombia. Trop Med Hyg General Hospital. Med J
in radiographically Epilepsia 39:1334– 105:531–536, 2011 Malaysia
imaged seizure 1339, 1998 152. Ptaszynski AE, Hooten 56:143–150, 2001
patients in U.S. 145. Pandey S, Singhi P, WM, Huntoon MA: The 158. Reinert P, Liwartowski
emergency Bharti B: Prevalence and incidence A, Dabernat H, Guyot C,
departments. treatment gap of spontaneous Boucher J,
Emerg Infect Dis in childhood epilepsy epidural abscess in Carrere C:
8:608–613, 2002 in a north Indian city: Olmsted County from Epidemiology of
139. Oniankitan O, a community- 1990 through 2000: a Haemophilus influenzae
Bagayogo Y, Fianyo based study. J Trop rare cause of spinal type b
E, Koffi-Tessio V, Pediatr 60:118–123, pain. Pain Med disease in France.
Kakpovi K, Tagbor 2014 8:338–343, 2007 Vaccine 11 (Suppl
KC, et al: 146. Park KB, Hodaie M, 153. Pyrgos V, Seitz AE, 1):S38–S42, 1993
[Spondylodiscitis at Osorio-Fonseca E, Rubiano Steiner CA, Prevots DR, 159. Riise OR, Kirkhus E,
a hos- pital AM, Warf B, Dewan Williamson Handeland KS, Flatø B,
outpatient clinic in M, et al: Bogota PR: Epidemiology of Reiseter T,
Lome, Togo.] Med Declaration. cryptococcal Cvancarova M, et al:
Trop (Mars) GlobalNeurosurgery. meningitis in the US: Childhood
69:581–582, 2009 (Fr) org. 1997–2009. PLoS One osteomyelitis-incidence
140. Østergaard C, (https://globalneurosur 8:e56269, 2013 and
Konradsen HB, Samuelsson gery.org/ 154. Raina SK, Razdan S, differentiation from
S: Clinical bogota-declaration/) Pandita KK, Sharma R, other acute onset
presentation and [Accessed January 26, Gupta VP, musculoskeletal fea-
prognostic factors of 2018] Razdan S: Active tures in a population-
Streptococcus pneu- 147. Park KB, Johnson epilepsy as indicator of based study. BMC
moniae meningitis WD, Dempsey RJ: Global neurocysticercosis Pediatr 8:45, 2008
according to the focus neurosurgery: in rural Northwest 160. Rodriguez-Gomez M,
of infection. BMC the unmet need. World India. Epilepsy Res Willisch A, Fernandez-
Infect Dis 5:93, 2005 Neurosurg 88:32–35, Treat 2012:802747, Dominguez
141. Ouiminga HAK, 2016 2012 L, Lopez-Barros G,
Thiam AB, Ndoye N, 148. Pelkonen TI, Leite 155. Rajshekhar V: García-Porrúa C,
Fatigba H, Thioub Cruzeiro M, Monteiro L, Surgical management of Gonzalez-Gay MA:
M, Memou S, et al: Pitkäranta A, neurocysticercosis. Luberculous spondylitis:
[Intracranial Roine I, Peltola H: Int J Surg 8:100–104, epidemiologic and
empyemas: epide- Outcome of acute 2010 clinical study
miological, clinical, childhood bacterial 156. Rajshekhar V, Raghava in non-HIV patients
radiological and meningitis in Luanda, MV, Prabhakaran V, from northwest Spain.
therapeutic aspects. Angola. Clin Oommen A, Clin Exp
Retrospective study of Microbiol Infect 15 Muliyil J: Active Rheumatol 20:327–333,
100 observations.] (Suppl 4):S569, 2009 epilepsy as an index of 2002
Neurochirurgie (Abstract) burden of neuro- 161. Rodriguez-Levya I,
60:299–303, 2014 (Fr) 149. Poshyachinda V: cysticercosis in Vellore Juarez-Sanjuan A, Cuevas E:
142. Ozsürekci Y, Kara A, Drugs and AIDS in district, India. Neurocysticercosis in a
Cengiz AB, Celik M, southeast-Asia. Neurology 67:2135– general hospital in San
Ozkaya- Forensic Sci In 2139, 2006 Luis Potosí,
Parlakay A, Karadağ- 62:15–28, 1993 México. Revista
Oncel E, et al: Brain 150. Prasad KN, Prasad A, Ecuatoriana de
abscess in child- Gupta RK, Nath K, Pradhan Neurologia 9:33–35,
hood: a 28-year S, 2000
experience. Turk J Tripathi M, et al: 162. Rosman J, Slane S,
Pediatr 54:144–149, Neurocysticercosis in Dery B, Vogelbaum MA,
2012 patients with active Cohen-Gadol
143. Palacio G, Tobón ME, epilepsy from the pig AA, Couldwell WT: Is
Mora O, Sánchez JL, farming community of there a shortage of
Jiménez M, Lucknow neurosurgeons in
Muñoz A, et al: district, north India. the United States?
[Prevalence of Trans R Soc Trop Neurosurgery 73:354–
neurocysticercosis in Med Hyg 103:144– 366, 2013
indi- 150, 2009 163. Rosselli D, Rueda JD:
viduals affected by 151. Prasad KN, Verma A, Burden of pneumococcal
epilepsy.] Rev Neurol Srivastava S, Gupta RK, infection
25:1406–1410, Pandey CM, in adults in Colombia. J
1997 (Span) Paliwal VK: An Infect Public Health
144. Palacio LG, Jiménez I, epidemiological study 5:354–359,
Garcia HH, Jiménez ME, of asymptomatic 2012
J Neurosurg June 15, 27
2018
F. C. Robertson et
al.

164. Sahai S, Mahadevan S, in a neurosurgery and


Srinivasan S, Kanungo R: neurologi-
Childhood bacterial cal intensive care unit. J
meningitis in Neurol Neurosurg
Pondicherry, South Psychiatry
India. 80:1381–1385, 2009
Indian J Pediatr 171. Schiavo R, May
68:839–841, 2001 Leung M, Brown M:
165. Sakata H: Invasive Communicating risk
Haemophilus influenzae and promoting disease
infections in mitigation measures in
children in Kamikawa epidem-
subprefecture, ics and emerging disease
Hokkaido, Japan, settings. Pathog Glob
1996–2005, before the Health
introduction of H. 108:76–94, 2014
influenzae type b 172. Schuchat A, Robinson
vaccination. J Infect K, Wenger JD, Harrison
Chemother 13:30–34, LH, Farley
2007 M, Reingold AL, et al:
166. Sakho Y, Badiane Bacterial meningitis in
SB, N’Dao AK, N’Diaye the United
A, Gueye M, States in 1995. N Engl J
N’Diaye IP: Pott’s Med 337:970–976, 1997
disease in Senegal. Eur 173. Schuler M,
J Orthop Surg Zimmermann H, Altpeter E,
Traumatol 13:13–20, Heininger U:
2003 Epidemiology of tick-
167. Salekeen S, borne encephalitis in
Mahmood K, Naqvi IH, Switzerland,
Baig MY, Akhter ST, 2005 to 2011. Euro
Abbasi A: Clinical Surveill 19:20756, 2014
course, complications (Erratum in
and predictors of Euro Surveill 19:20765,
mortality in patients 2014)
with tuberculous 174. Secka A, Grimm F,
meningitis—an expe- Marcotty T, Geysen D, Niang
rience of fifty two cases AM,
at Civil Hospital Ngale V, et al: Old focus
Karachi, Pakistan. of cysticercosis in a
J Pak Med Assoc Senegalese
63:563–567, 2013 village revisited after
168. Sánchez AL, Lindbäck half a century. Acta
J, Schantz PM, Sone M, Sakai Trop 119:199–
H, 202, 2011
Medina MT, et al: A 175. Sharma SK, Mohan A:
population-based, case- Extrapulmonary tuberculosis.
control study Indian J Med Res
of Taenia solium 120:316–353, 2004
taeniasis and
cysticercosis. Ann Trop
Med Parasitol 93:247–
258, 1999
169. Sarfo FS, Akassi J, Badu
E, Okorozo A, Ovbiagele B,
Akpalu A: Profile of
neurological disorders in
an adult neu-
rology clinic in Kumasi,
Ghana.
eNeurologicalSci 3:69–
74,
2016
170. Scheithauer S, Bürgel U,
Ryang YM, Haase G, Schiefer
J,
Koch S, et al:
Prospective surveillance
of drain associated
meningitis/ventriculitis
28 J Neurosurg June 15,
2018
F. C. Robertson et
al.

J Neurosurg June 15, 29


2018
F. C. Robertson et
al.

176. Sheybani F, Arabikhan Suppl):P1.272, 2016 Brazil.] 194. Varma A, Gaur KJ: The
HR, Naderi HR: (Abstract) Arq Neuropsiquiatr clinical spectrum of
Herpes simplex 183. Solís-García del Pozo 54:557–564, 1996 neurocysticer-
encephalitis (HSE) and J, Vives-Soto M, Lizán- (Portuguese) cosis in the Uttaranchal
its outcome in the García M, 189. Townes JM, region. J Assoc
patients who were Martínez-Alfaro E, Hoffmann CJ, Kohn MA: Physicians India
admitted to a tertiary Segura-Luque JC, Neurocysticercosis 50:1398–1400, 2002
care hospital in Solera-Santos J: in Oregon, 1995–2000. 195. Villarán MV, Montano
Mashhad, Iran, over a [Incidence of Emerg Infect Dis SM, Gonzalvez G, Moyano
10-year period. J Clin infectious spondylitis 10:508–510, LM,
Diagn Res 7:1626– in the province of 2004 Chero JC, Rodriguez S,
1628, 2013 Albacete (Spain).] 190. Trevisol-Bittencourt et al: Epilepsy and
177. Shrestha SR, Awale P, Enferm Infecc PC, da Silva NC, Figueredo neurocysticer-
Neupane S, Adhikari N, Microbiol Clin R: cosis: an incidence study
Yadav BK: 23:545– [Prevalence of in a Peruvian rural
Japanese encephalitis in 550, 2005 (Span) neurocysticercosis population.
children admitted at 184. Soumaré M, Seydi M, among epileptic in- Neuroepidemiology
Patan Hospital. Ndour CT, Fall N, Dieng Y, patients in the west of 33:25–31, 2009
J Nepal Paediatr Soc Sow Santa Catarina– 196. Wang H, Li C, Wang J,
29:17–21, 2009 AI, et al: southern Brazil.] Arq Zhang Z, Zhou Y:
178. Sigurdardóttir B, [Epidemiological, Neuropsiquiatr Characteristics
Björnsson OM, Jónsdóttir clinical, etiological 56:53–58, 1998 of patients with spinal
KE, features of (Portuguese) tuberculosis: seven-year
Erlendsdóttir H, neuromeningeal 191. Tseng JH, Tseng MY: experience
Gudmundsson S: diseases at the Fann Brain abscess in 142 of a teaching hospital in
Acute bacterial men- Hospital Infectious patients: factors Southwest China. Int
ingitis in adults. A 20- Diseases Clinic, Dakar influencing outcome Orthop
year overview. Arch (Senegal).] Med Mal and mortality. Surg 36:1429–1434, 2012
Intern Med Infect Neurol 65:557– 197. Watts HG, Lifeso RM:
157:425–430, 1997 35:383–389, 2005 (Fr) 562, 2006 Tuberculosis of bones and
179. Silva-Vergara ML, 185. Srinivas D, Veena 192. Tsou TP, Lee PI, Lu joints. J
Vieira CdeO, Castro JH, Kumari HB, Somanna S, CY, Chang LY, Huang LM, Bone Joint Surg Am
Micheletti LG, Bhagavatula I, Chen JM, 78:288–298, 1996
Otaño AS, Franquini Anandappa CB: The et al: Microbiology 198. Wee LY, Tanugroho RR,
júnior J, et al: incidence of and epidemiology of Thoon KC, Chong CY,
[Neurologic and postoperative brain abscess and Choong
labora- meningitis subdural empyema in a CT, Krishnamoorthy S,
tory findings in a in neurosurgery: an medical center: a 10- et al: A 15-year
population of an institutional year experi- retrospective analy-
endemic area for experience. Neurol ence. J Microbiol sis of prognostic factors
taenia- India Immunol Infect in childhood bacterial
sis-cysticercosis, 59:195–198, 2011 42:405–412, 2009 meningitis.
Lagamar, MG, Brazil 186. Strauss I, Carmi-Oren 193. van Well GTJ, Paes Acta Paediatr 105:e22–
(1992–1993)]. Rev N, Hassner A, Shapiro M, BF, Terwee CB, Springer P, e29, 2016
Inst Med Trop São Giladi M, Roord JJ, 199. Winkler AS, Mosser P,
Paulo 36:335–342, Lidar Z: Spinal Donald PR, et al: Schmutzhard E: Neurological
1994 (Portuguese) epidural abscess: in Twenty years of dis-
180. Singh BB, Khatkar search of reasons for pediatric tuberculous orders in rural Africa: a
MS, Gill JP, Dhand NK: an meningitis: a systematic approach.
Estimation of increased incidence. retrospective cohort Trop Doct
the health and Isr Med Assoc J study in the western 39:102–104, 2009
economic burden of 15:493–496, 2013 cape 200. Xiao F, Tseng MY, Teng
neurocysticercosis in 187. Sur A, Tsang K, of South Africa. LJ, Tseng HM, Tsai JC: Brain
India. Acta Trop Brown M, Tzerakis N: Pediatrics 123:e1–e8, abscess: clinical
165:161–169, 2017 Management of 2009 experience and analysis
181. Singh G, Chowdhary adult spontaneous of prognostic fac-
AK: Epilepsy surgery in spondylodiscitis and tors. Surg Neurol
context of its rising incidence. 63:442–450, 2005
neurocysticercosis. Ann R Coll Surg 201. Zhang Z, Cai X, Li J,
Ann Indian Acad Engl 97:451–455, Kang X, Wang H, Zhang L, et
Neurol 17 (Suppl 2015 al:
1):S65–S68, 2014 188. Takayanagui OM, Retrospective analysis
182. Sokhi D, Diaz M, Castro e Silva AA, Santiago of 620 cases of brain
Ngugi A, Solomon T, Fevre RC, abscess in
E, Meyer Odashima NS, Terra Chinese patients in a
AC: Epilepsy VC, Takayanagui AM: single center over a 62-
prevalence, treatment [Compulsory year period.
gap, and stigma in notification of Acta Neurochir (Wien)
western Kenya. cysticercosis in 158:733–739, 2016
Neurology 86 (16 Ribeiräo Preto-SP,
30 J Neurosurg June 15,
2018
F. C. Robertson et
al.

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

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