Tropical Medicine and International Health doi:10.1111/tmi.

13059

volume 23 no 6 pp 589–595 june 2018

Systematic Review

Human immunodeficiency virus in patients with tuberculous

meningitis: systematic review and meta-analysis
Ali Pormohammad1, Mohammad Javad Nasiri2, Seyed Mohammad Riahi3 and Fatemeh Fallah2

1 Student Research Committee, Department of Microbiology, School of Medicine, Shahid Beheshti University of Medical Sciences,
Tehran, Iran
2 Department of Microbiology, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran
3 Department of Epidemiology, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran

Abstract introduction Human immunodeficiency virus (HIV)-infected individuals are at increased risk for
all forms of extrapulmonary tuberculosis (TB), including tuberculous meningitis (TBM). This study
aimed to investigate the frequency of HIV in patients with TBM.
methods PubMed, Embase, Web of Science and Cochrane Library were searched for articles
including relevant data. Stata version 14.0 (StataCorp, College Station, Texas, USA) was used to
analyse the data.
results Twenty studies were identified. The pooled frequency of HIV among adult patients with
TBM was 38.0% (95% CI: 21.0–57.0; I2 = 97%). In children (under the age of 15 years), 6.0%
(95% CI: 1.0–13.0; I2 = 0.0%) had HIV infection. In patients with bacterial meningitis other than
TBM, 36.0% (95% CI: 19.0–53.0; I2 = 100%) were HIV-infected.
conclusions A relatively high frequency of HIV in patients with TBM was indicated by our study.
Establishment of diagnostic criteria and effective treatment strategies for TBM/HIV co-infection are
recommended for better management of patients with TBM+HIV.

keywords tuberculous meningitis, human immunodeficiency virus, systematic review

frequency of HIV in TBM cases; however, there are

Introduction
Tuberculosis (TB) and human immunodeficiency virus
(HIV) are infectious causes of death globally. In 2016,
10.4 million people contracted TB, and 1.7 million died
from it [1]. TB meningitis (TBM) is the most severe form
of TB, with significant morbidity and mortality [2, 3].
Approximately 30% of patients with TBM die despite TB
treatment [4]. The clinical features of TBM are similar to
those other meningoencephalitides, making diagnosis dif-
ficult [3]. Consequently, delay in diagnosis and start of
treatment have a negative impact on patient outcome [3].
The human immunodeficiency virus (HIV) epidemic has
complicated all aspects of TBM management. Infection is
more likely to progress to TBM when patients are co-
infected with HIV [5]. The case fatality rate for TBM in
adults is higher among HIV-infected patients than among
uninfected patients [6, 7]. Although the magnitude of
HIV in TBM cases is well described, the frequency of
HIV in such high-risk patients has not been reported. So
far, several hospital-based studies have reported the
increasing discrepancies between the results. Thus, this
study was designed to determine the frequency of HIV in
patients with TBM by systematic review and meta-analy-
sis according to the Preferred Reporting Items for System-
atic Reviews and Meta-Analyses statement [8].
Methods
Search strategies
PubMed, Embase, Web of Science and Cochrane Library
were searched for articles published between January
1985 and March 2018. Search terms were ‘tuberculous
meningitis’, ‘TBM’, ‘acquired immunodeficiency syn-
drome’, ‘AIDS’, ‘HIV’ and ‘human immunodeficiency
virus’. Titles, abstracts and full texts of retrieved articles
were screened and assessed for eligibility independently
and in duplicate by two investigators. Reference lists of
selected articles were searched to identify further relevant
studies.

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A. Pormohammad et al. HIV in patients with tuberculous meningitis

Eligibility Quality assessment

Inclusion criteria. Studies were included if they met all
of the following criteria: (i) evaluating TBM; (ii) present-
ing the frequency of HIV in TBM cases; and (iii)
reporting standard laboratory-confirmed TBM. We used
the case definition by Marais et al. [9] for TBM.
Briefly, for definite TBM, patients should fulfil clinical
entry criteria plus one or more of the following:
acid-fast bacilli seen in the CSF; Mycobacterium
tuberculosis cultured from CSF; or CSF-positive
commercial nucleic acid amplification test. Patients
without microbiological confirmation were classified as
probable, possible or not TBM, depending on their total
diagnostic score.
Exclusion criteria. Studies were excluded if they focused
only on TBM or HIV, did not report confirmed TBM or
did not report the frequency of HIV in TBM.
Data extraction and data collection
Data were extracted by two reviewers independently and
inconsistencies checked by a third reviewer. We extracted
the following data from each article: name of the first
author, publication date, country, number of suspected
meningitis cases, number of confirmed TBM cases, and
number of HIV+TBM cases.
Quality assessment of the studies was performed accord-
ing to the Critical Appraisal Checklist recommended by
the Joanna Briggs Institute [10]. Studies with score >6
were included in the final analysis.
Meta-analysis
Analyses were performed using random-effects weights.
To estimate a pooled effect, we utilised the ‘metaprop’
command. We used ‘ftt cimethod’ (score) or Freeman–
Tukey transformation procedures for collecting binomial
data. The between-study heterogeneity was assessed using
Cochran’s Q, the I2 statistic and Galbraith graph. To
check for publication bias, we generated funnel plots and
used Egger’s and Begg’s tests (P < 0.05 was considered
indicative of statistically significant publication bias,
funnel plot asymmetry also suggest bias in the meta-
analysis). All the analyses were conducted using Stata
14.0 (StataCorp, College Station, Texas, USA).
Results
A total of 1099 articles were found in the initial search,
of which 485 records were screened by title and abstract,
and 20 studies were included in the final analysis [11–30]
(Figure 1). Table 1 summarises the main characteristics

Search in electronic data bases (n = 1099)

PubMed: 303
Embase: 397
Web of sciences: 379
Cochrane library: 20
Excluded duplicates
(n = 614)
Title and abstract screening
(n = 485)

Excluded irrelevant
(n = 446)

Full text assessed for eligibility

(n = 39) Excluded irrelevant (n = 19)

Reason for exclusion:

Studies included in quality
assessment and meta-analysis
(n = 20)
• Did not report HIV frequency in TBM cases
or not reported TBM (n = 11)
• Patients data not reported (1)
• Were case report or review articles (n = 3)
• Duplicate data (n = 4)
Figure 1 Flow diagram detailing review
process and study selection.

590 © 2018 John Wiley & Sons Ltd

 © 2018 John Wiley & Sons Ltd
Table 1 Characteristics of the included studies reporting the frequency of HIV among patients with TBM

No. of No. of
suspected patients HIV in
cases Total No. of with No. of patients suspected
Published Adult/ with patients with definite with probable/ cases with HIV in patients
Tropical Medicine and International Health

First author time Country Mean age Children meningitis TBM TBM possible TBM meningitis with TBM

Lang 1998 Dominican NA Children 84 24 5 19 1 0

Republic
Silbera 1999 South Africa 45 years Adult 60 9 6 3 38 9
Bonington 2000 South Africa 30 years Adult 69 33 8 25 22 12
Chaidir 2001 Indonesia 30 years Adult 230 207 105 102 51 37
Baker 2002 USA NA Adult 29 5 5 0 8 1
Chan 2003 China NA Adult NA 31 5 26 NA 1
Thwaites 2004 Vietnam NA Adult 330 132 107 25 NA 14
A. Pormohammad et al. HIV in patients with tuberculous meningitis

Cagatay 2004 Turkey 34 years Adult NA 35 10 25 NA 3

Juan 2006 Spain 34 years Adult 127 18 10 8 NA 14
Bhigjee 2007 South Africa 32 years Adult NA 36 NA NA NA 31
Caws 2007 Vietnam NA Adult 137 57 40 17 88 40
Sinha 2009 India 30 years Adult NA 101 29 72 NA 0
Sardella 2010 Brazil 48 years Adult 156 19 18 1 24 8
Kim 2010 South Korea 45 years Adult 89 31 10 21 2 0
Patel 2013 South Africa 33 years Adult 204 123 59 64 173 103
Solari 2013 Peru 35 years Adult 155 59 18 41 33 22
Nhu 2014 Vietnam NA Adult 379 182 151 31 79 66
Solomons 2015 South Africa 36 months Children 101 55 13 42 8 6
Ruiz 2015 Spain NA Adult 190 11 5 6 15 2
Love 2016 Zambia NA Adult 99 29 NA NA 80 27

591
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A. Pormohammad et al. HIV in patients with tuberculous meningitis

of the included studies. The target population in 18 of 20 HIV infection in patients with TBM
studies was adult patients with TBM; in the two remain-
The pooled frequency of HIV among adult patients with
ing studies, it was children. In all included studies, TBM
TBM was 38.0% (95% CI: 21.0–57.0; I2 = 97%) (Fig-
was investigated by standard criteria as described previ-
ure 2). Likewise, 6.0% (95% CI: 1.0–13.0; I2 = 0.0%)
ously [9]. All included studies reported the frequency of
of children (under the age of 15 years) with TBM had
HIV among patients with TBM. A total of 1197 patients
HIV infection. As presented in the Galbraith plot in Fig-
with TBM were included in the meta-analysis. These
ure 3, the studies outside the range between 2 and 2
reports came from 12 countries and were written
were seen as the outliers and the major source of het-
between 1998 and 2018.
erogeneity. On visual inspection, the funnel plot appears
asymmetric (Figure 4). However, as per Begg’s (P = 0.1)
Risk of bias assessment and Egger’s (tests) (P = 0.7), there was no evidence of
asymmetry.
Based on the quality assessment of the included studies,
all studies were identified as having a low risk of bias.

%
Author Country Year ES (95% CI) Weight

Silbera South Africa 1999 1.00 (0.70, 1.00) 4.99

Bonington South Africa 2000 0.36 (0.22, 0.53) 5.63
Chaidir Indonesia 2001 0.18 (0.13, 0.24) 5.88
Baker USA 2002 0.20 (0.04, 0.62) 4.47
Chan China 2003 0.03 (0.01, 0.16) 5.61
Thwaites Vietnam 2004 0.11 (0.06, 0.17) 5.85
Cagatay Turkey 2004 0.09 (0.03, 0.22) 5.65
Juan Spain 2006 0.78 (0.55, 0.91) 5.41
Bhigjee South Africa 2007 0.86 (0.71, 0.94) 5.66
Caws Vietnam 2007 0.70 (0.57, 0.80) 5.75
Sinha India 2009 0.00 (0.00, 0.04) 5.83
Sardella Brazil 2010 0.42 (0.23, 0.64) 5.43
Kim South Korea 2010 0.00 (0.00, 0.11) 5.61
Patel South Africa 2013 0.84 (0.76, 0.89) 5.85
Solari Peru 2013 0.37 (0.26, 0.50) 5.76
Nhu Vietnam 2014 0.36 (0.30, 0.43) 5.88
Ruiz Spain 2015 0.18 (0.05, 0.48) 5.13
Love Zambia 2016 0.93 (0.78, 0.98) 5.59
Overall (I^2 = 97.06%, p = 0.00) 0.38 (0.21, 0.57) 100.00

–.25 0 .5 1
Frequency (%)

Figure 2 Forest plots of studies, investigating the frequency of HIV among patients with TBM. (Forest plot for indicating 95% confi-
dence interval in each study. Estimation (ES) of variance for each study was carried out using ftt cimethod (score) or Freeman–Tukey
transformation procedures).

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Tropical Medicine and International Health volume 23 no 6 pp 589–595 june 2018

A. Pormohammad et al. HIV in patients with tuberculous meningitis

b/se(b) Fitted values and HIV have globally increased in recent years [1].
2 TBM is the most severe form of TB and carries a high
morbidity and mortality [31]. Infection with HIV is
0 Silbera Love
Juan Bhigjee among the powerful known risk factors predisposing
Baker
–2 Ruiz Sardella Caws
Patel for progression to active TBM [2]. According to our
study, 38.0% of TBM was HIV-associated TBM. The
b/se(b)

Chan Boningto
Cagatay Solari relatively high frequency of HIV in TBM may have
several negative effects on patient’s management. For
example, in terms of laboratory features, the diagnosis
Nhu
–8.68224
Thwaites of TBM can be masked by atypical CSF findings. Previ-
Chaidir
ous studies indicated a lower CSF leucocyte count and
a lower protein level in HIV-infected patients [32–34].
0 9.37532
1/se(b) Typically, in patients with TBM, there is lymphocytic
pleocytosis, with an elevated protein and low glucose
Figure 3 Galbraith plot of the frequency of HIV among patients levels [35, 36]. HIV could also alter the clinical presen-
with TBM (The study outside the range between 2 and 2 was
tation of TBM. In TBM patients with HIV, basal
seen as the outlier and the major source of heterogeneity).
meningeal enhancement and hydrocephalus on CT
might be less common and there could be more bacilli
in the meninges than in those who are HIV-uninfected
Funnel plot with pseudo 95% confidence limits
[36, 37]. In terms of treatment and outcome, a previ-
0
ous study reported more treatment failures in HIV-
infected patients with TBM than in HIV-uninfected
s.e. of logeventrate

patients, which suggests that HIV infection may influ-

.5
1 Resistance to TB drugs is among the most important
1.5
–4 –2
logeventrate
Figure 4 Funnel plot of the studies, investigating the publication
bias. (The Begg’s and Egger’s tests showed no evidence for publi-
cation bias (Begg’s P = 0.3, Eggers’s P = 0.2).
HIV infection in patients with other bacterial meningitis
The pooled frequency of HIV among patients with bacte-
rial meningitis other than TBM was 36.0% (95% CI:
19.0–53.0; I2 = 100%) (Figure S1). The funnel plot
shows some evidence of publication bias (P < 0.05 for
Begg’s rank correlation analysis and Egger’s weighted
regression analysis) (Figure S2).
Discussion
TB and HIV co-infection is the leading cause of mor-
tality among patients with TB and people living with
HIV/AIDS. The prevalence and incidence of both TB
ence responses to treatment and the likelihood of hav-
ing a relapse [32]. The case fatality rate is significantly
higher in HIV-infected than uninfected adults [37, 38].
factors that may have contributed to the high case
fatality rate in HIV-infected patients with TBM. A
higher proportion of M. tuberculosis isolates from HIV-
infected patients was resistant to more than one first-
0 2 line TB drug [2, 37]. Also, the optimal time to initiate
antiretroviral therapy (ART) in patients with HIV and
TB co-infection remains controversial. Early initiation
of ART with TB treatment may be associated with
drug toxicities, while delayed initiation may result in
HIV disease progression and death [39].
The current study has some limitations. First, it cannot
represent the global prevalence of HIV in TBM because
the magnitude of the issue is not yet investigated in many
countries. Second, heterogeneity exists among the
included studies. Although the random-effects model
allows for heterogeneity, controversy remains about com-
bining study estimates in its presence. Third, as with any
systematic review, limitations associated with potential
publication bias should be considered. Finally, the mor-
tality rate, treatment failures and CSF parameters in
TBM patients with and without HIV infection could not
be analysed because of the limited information obtained
from the studied articles.
In conclusion, our systematic review and meta-analysis
indicate a relatively high frequency of HIV in patients

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A. Pormohammad et al. HIV in patients with tuberculous meningitis

with TBM. Establishment of diagnostic criteria and effec- 12. Silber E, Sonnenberg P, Ho KC et al. Meningitis in a com-
tive treatment strategies for TBM/HIV co-infection are munity with a high prevalence of tuberculosis and HIV
recommended for better management of TBM/HIV co- infection. J Neurol Sci 1999: 162: 20–26.
infection. 13. Bonington A, Strang JI, Klapper PE et al. TB PCR in the
early diagnosis of tuberculous meningitis: evaluation of the
Roche semi-automated COBAS Amplicor MTB test with ref-
Acknowledgements erence to the manual Amplicor MTB PCR test. Tuberculosis
2000: 80: 191–196.
This study is related to the project NO. 1396/50181 14. Chaidir L, Ganiem AR, Vander Zanden A et al. Comparison
From Student Research Committee, Shahid Beheshti Uni- of real time IS6110-PCR, microscopy, and culture for diag-
versity of Medical Sciences, Tehran, Iran. We also nosis of tuberculous meningitis in a cohort of adult patients
appreciate the “Student Research Committee” and in Indonesia. PLoS ONE 2012: 7: e52001.
“Research & Technology Chancellor” in Shahid Beheshti 15. Baker CA, Cartwright CP, Williams DN, Nelson SM,
University of Medical Sciences for their financial support Peterson PK. Early detection of central nervous system
of this study. tuberculosis with the Gen-Probe nucleic acid amplification
assay: utility in an inner city hospital. Clin Infect Dis 2002:
35: 339–342.
References 16. Chan KH, Cheung RT, Fong CY, Tsang KL, Mak W, Ho
SL. Clinical relevance of hydrocephalus as a presenting fea-
1. World Health Organization (WHO). Global tuberculosis
ture of tuberculous meningitis. QJM 2003: 96: 643–648.
report 2017, in Global tuberculosis report 2017. 2017.
17. Thwaites GE, Chau TTH, Farrar JJ. Improving the bacterio-
2. Torok ME, Chau TT, Mai PP et al. Clinical and microbio-
logical diagnosis of tuberculous meningitis. J Clin Microbiol
logical features of HIV-associated tuberculous meningitis in
2004: 42: 378–379.
Vietnamese adults. PLoS ONE 2008: 3: e1772.
18. Cagatay AA, Ozsut H, Gulec L et al. Tuberculous meningi-
3. Thwaites GE, Chau TT, Stepniewska K et al. Diagnosis of
tis in adults–experience from Turkey. Int J Clin Pract 2004:
adult tuberculous meningitis by use of clinical and labora-
58: 469–473.
tory features. Lancet 2002: 360: 1287–1292.
19. Juan RS, S
anchez-Su
arez C, Rebollo MJ et al. Interferon c
4. Thwaites G, Chau TT, Mai NT, Drobniewski F, McAdam
quantification in cerebrospinal fluid compared with PCR for
K, Farrar J. Tuberculous meningitis. J Neurol Neurosurg
the diagnosis of tuberculous meningitis. J Neurol 2006: 253:
Psychiatry 2000: 68: 289–299.
1323–1330.
5. Berenguer J, Moreno S, Laguna F et al. Tuberculous menin-
20. Bhigjee AI, Padayachee R, Paruk H, Hallwirth-Pillay KD,
gitis in patients infected with the human immunodeficiency
Marais S, Connoly C. Diagnosis of tuberculous meningitis:
virus. N Engl J Med 1992: 326: 668–672.
clinical and laboratory parameters. Int J Infect Dis 2007:
6. Thwaites GE, Nguyen DB, Nguyen HD et al. Dexametha-
11: 348–354.
sone for the treatment of tuberculous meningitis in
21. Caws M, Dang TM, Torok E et al. Evaluation of the
adolescents and adults. N Engl J Med 2004: 351: 1741–
MODS culture technique for the diagnosis of tuberculous
1751.
meningitis. PLoS ONE 2007: 2: e1173.
7. Brancusi F, Farrar J, Heemskerk D. Tuberculous meningitis
22. Sinha MK, Garg RK, Anuradha HK et al. Vision impair-
in adults: a review of a decade of developments focusing on
ment in tuberculous meningitis: predictors and prognosis. J
prognostic factors for outcome. Future Microbiol 2012: 7:
Neurol Sci 2010: 290: 27–32.
1101–1116.
23. Sardella IG, Singh M, Kumpfer S, Heringer RR, Saad MH,
8. Moher D, Liberati A, Tetzlaff J, Altman DG; Prisma Group.
Sohler MP. Evaluation of Lionex TB kits and mycobacterial
Preferred reporting items for systematic reviews and meta-
antigens for IgG and IgA detection in cerebrospinal fluid
analyses: the PRISMA statement. PLoS Med 2009: 6:
from tuberculosis meningitis patients. Mem Inst Oswaldo
e1000097.
Cruz 2010: 105: 722–728.
9. Marais S, Thwaites G, Schoeman JF et al. Tuberculous
24. Kim SH, Cho OH, Park SJ et al. Rapid diagnosis of tubercu-
meningitis: a uniform case definition for use in clinical
lous meningitis by T Cell—based assays on peripheral blood
research. Lancet Infect Dis 2010: 10: 803–812.
and cerebrospinal fluid mononuclear cells. Clin Infect Dis
10. Munn Z, Moola S, Riitano D, Lisy K. The development of a
2010: 50: 1349–1358.
critical appraisal tool for use in systematic reviews: address-
25. Patel VB, Theron G, Lenders L et al. Diagnostic accuracy of
ing questions of prevalence. Int J Health Policy Manag
quantitative PCR (Xpert MTB/RIF) for tuberculous meningi-
2014: 3: 123.
tis in a high burden setting: a prospective study. PLoS Med
11. Lang AM, Feris-Iglesias J, Pena C et al. Clinical evaluation
2013: 10: e1001536.
of the gen-probe amplified direct test for detection of
26. Solari L, Soto A, Agapito JC et al. The validity of
mycobacterium tuberculosiscomplex organisms in cere-
cerebrospinal fluid parameters for the diagnosis of tubercu-
brospinal fluid. J Clin Microbiol 1998: 36: 2191–
lous meningitis. Int J Infect Dis 2013: 17: e1111–e1115.
2194.

594 © 2018 John Wiley & Sons Ltd


Tropical Medicine and International Health
A. Pormohammad et al. HIV in patients with tuberculous meningitis
27. Nhu NT, Heemskerk D, Thu do DA et al. Evaluation of
GeneXpert MTB/RIF for diagnosis of tuberculous meningi-
tis. J Clin Microbiol 2014: 52: 226–233.
28. Solomons RS, Visser DH, Friedrich SO et al. Improved diag-
nosis of childhood tuberculous meningitis using more than
one nucleic acid amplification test. Int J Tuberc Lung Dis
2015: 19: 74–80.
29. Parra-Ruiz J, Ramos V, Due~ nas C et al. Rational application
of adenosine deaminase activity in cerebrospinal fluid for the
diagnosis of tuberculous meningitis. Infection 2015: 43:
531–535.
30. Love S, Mubanga E, Munkondya S et al. Optimizing CSF
diagnostics of tuberculous meningitis in zambia (P1. 289).
Neurology 2016: 86(Suppl 16): P1. 289.
31. Garg RK. Tuberculosis of the central nervous system. Post-
grad Med J 1999: 75: 133–140.
32. Karstaedt AS, Valtchanova S, Barriere R, Crewe-Brown HH.
Tuberculous meningitis in South African urban adults. QJM
1998: 91: 743–747.
33. Vinnard C, Macgregor RR. Tuberculous meningitis in
HIV-infected individuals. Curr HIV/AIDS Rep 2009: 6:
139–145.
34. Thwaites GE, Chau TT, Caws M et al. Isoniazid resistance,
mycobacterial genotype and outcome in Vietnamese adults
with tuberculous meningitis. Int J Tuberc Lung Dis 2002: 6:
865–871.
35. Rock RB, Olin M, Baker CA, Molitor TW, Peterson PK.
Central nervous system tuberculosis: pathogenesis and clini-
cal aspects. Clin Microbiol Rev 2008: 21: 243–261.
Corresponding Author Mohammad Javad Nasiri, Department of Microbiology, School of Medicine, Shahid Beheshti University
of Medical Sciences, Koodakyar St., Tabnak Blv., Yaman Ave., Chamran highway, Tehran 19839-63113, Iran.
E-mail: Mj.nasiri@hotmail.com
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13653156, 2018, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/tmi.13059 by CAPES, Wiley Online Library on [18/01/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
volume 23 no 6 pp 589–595 june 2018
36. Thwaites GE, Hien TT. Tuberculous meningitis: many ques-
tions, too few answers. Lancet Neurol 2005: 4: 160–170.
37. Thwaites GE, Duc Bang N, Huy Dung N et al. The influ-
ence of HIV infection on clinical presentation, response to
treatment, and outcome in adults with tuberculous meningi-
tis. J Infect Dis 2005: 192: 2134–2141.
38. Katrak SM, Shembalkar PK, Bijwe SR, Bhandarkar LD. The
clinical, radiological and pathological profile of tuberculous
meningitis in patients with and without human
immunodeficiency virus infection. J Neurol Sci 2000: 181:
118–126.
39. T€or€ok ME, Yen NT, Chau TT et al. Timing of initiation of
antiretroviral therapy in human immunodeficiency virus
(HIV)–associated tuberculous meningitis. Clin Infect Dis
2011: 52: 1374–1383.
Supporting Information
Additional supplemental material may be found online in
the Supporting Information section at the end of the
article:
Figure S1. Forest plots of studies, investigating the fre-
quency of HIV with bacterial meningitis other than
TBM.
Figure S2. Funnel plot of the studies, investigating the
publication bias. (The Begg’s and Egger’s tests showed
some evidence for publication bias (P < 0.05).
595