Association between neuromyelitis optica and tuberculosis in a Chinese population
Association between neuromyelitis optica and tuberculosis in a Chinese population
Rui Li 0
Xiaonan Zhong 0
0 Equal contributors Multiple Sclerosis Center, Department of Neurology, The Third Affiliated Hospital of Sun Yat-Sen University , No. 600 Tianhe Road, Guangzhou, Guangdong Province 510630 , China
Background: A number of reports have described the presence of tuberculosis (TB) in neuromyelitis optica (NMO) patients. However, a definite association between the two conditions has not been conclusively demonstrated. Methods: To investigate the association between NMO and TB in a Chinese population, we performed a retrospective review of hospital records of NMO patients, control patients and tuberculosis meningitis (TBM) patients from January 1, 1995 to December 31, 2011. Results: The frequency of preceding/simultaneous active pulmonary TB (PTB) was not significantly different between NMO patients (1.1%) and control groups (2.3% in myasthenia gravis, 1.1% in polymyositis or dermatomyositis, zero in idiopathic facial palsy and viral meningitis/meningoencephalitis). NMO cases differed from TBM cases in terms of demographics, course (recurrent or monophasic), cerebrospinal fluid analysis and magnetic resonance images. Two TBM patients shared partial clinical features with NMO (one of the TBM patients had a longitudinal extensive spinal cord lesion involving the holocord, and the other had optic neuritis before anti-tuberculosis treatment). NMO antibodies were only detected in NMO patients and not in TBM patients with myelitis or optic neuritis. Conclusions: We could not confirm previous suggestions of the association between PTB and NMO. Direct infection of the central nervous system by TB may mimic NMO in some respects, but whether NMO-like symptoms that develop during the course of TB should be considered and diagnosed as NMO is open to discussion.
Neuromyelitis optica; Tuberculosis; NMO-IgG
Neuromyelitis optica (NMO) is a severe demyelinating
disease of the central nervous system (CNS) that
preferentially affects the optic nerve and spinal cord . The
disease is idiopathic and the discovery that patients are
seropositive for aquaporin-4-specific autoantibody
(AQP4Ab or NMO-IgG) suggested the existence of an underlying
immunopathogenic mechanism [1,2]. Although NMO
usually occurs in isolation, reports over the past century have
suggested an association between NMO and tuberculosis
(TB) [3-8]. A study by Hughes and colleagues described
three patients that developed acute necrotic myelopathy
during the course of active pulmonary TB (PTB) . A
report from the Western Cape of South Africa described
six patients with optic neuropathy and myelopathy with
associated active PTB but no evidence of TB infection in
the CNS . Another study, also carried out in South
Africa, suggested PTB-associated NMO developed in
patients with active infection because 79% (11/14) of NMO
patients had a preceding or simultaneous diagnosis of PTB
. Finally, Feng and colleagues described the benefits of
anti-tuberculosis treatment in steroid-refractory Chinese
NMO patients .
Although an association between NMO and TB has
been suggested in a number of reports from different
geographical regions, a definite association between the two
conditions has not been conclusively demonstrated.
Further investigation and clarification would be helpful in the
diagnosis and treatment of patients who develop
NMOlike symptoms (longitudinal extensive myelitis and optic
neuritis) during the course of TB. We therefore
performed a retrospective study to investigate whether
there is an association between NMO and TB in the
Ethical approval was given by the medical ethics
committee of the third affiliated hospital of Sun Yat-sen University
with the following reference number: 33. Written
informed consent was obtained from the patient for
publication of the clinical data and any accompanying images.
Patients and selection criteria
To study the prevalence of PTB in NMO patients
compared with controls, we performed a retrospective review
of hospital records of patients with a diagnosis of NMO
that were admitted to our hospital, The Third Affiliated
Hospital of Sun Yat-Sen University, from January 1, 1995
to December 31, 2011. All NMO patients fulfilled the
2006 Wingerchuk criteria  (the 1999 Wingerchuk
diagnostic criteria were used for several cases owing to a lack
of NMO-IgG data ). Patients with evidence of
sarcoidosis, vasculitis, clinically manifest systemic lupus
erythematosus, Sjogrens syndrome or another explanation for optic
neuritis or myelitis were excluded . The control groups
consisted of patients with myasthenia gravis, polymyositis
or dermatomyositis, idiopathic facial palsy, and viral
meningitis/meningoencephalitis (VM). To avoid any confusion
with aseptic meningitis/meningoencephalitis, patients were
considered to have VM when either a viral etiology was
confirmed or antiviral treatment was effective. VM was
only diagnosed after ruling out bacterial, fungal, and
noninfectious causes of meningitis (malignancy, autoimmune
disorders, neurosarcoidosis) . To ensure a similar
background exposure to TB, control and NMO cases were
matched for sex, age at time of admission (within 10 years),
and date of admission (within a range of 5 years). If more
than one matching control was identified per case,
the one with the closest age at admission was included.
These patients were used as controls because there is no
known causal association with the risk factor under
The following data were collected for all NMO and
control cases: sex, age at onset of neurological
symptoms, and the presence or absence of a diagnosis of
active PTB . Active PTB was defined either as a
diagnosis of PTB preceding the onset of NMO by fewer
than 6 months, or PTB that was not cured before
admission for neurological disease. Duration from diagnosis of
PTB to onset of neurological symptoms (if previously
diagnosed with PTB), cerebrospinal fluid (CSF) data
(if available), and NMO-IgG serum status (if available)
was also collected for all cases.
To investigate whether patients with tuberculosis
meningitis (TBM) shared partial clinical features to NMO
patients fulfilling the 2006 Wingerchuk criteria, we also
enrolled TBM patients admitted to our hospital during
the same period using TBM criteria according to Thwaites
. Detailed data on clinical presentation, CSF reports,
magnetic resonance imaging (MRI) reports, therapy, and
outcomes were collected for NMO and TBM cases. Using
MRI, spinal cord lesions extending over three or more
vertebral segments on the spinal cord were defined as
longitudinal extensive spinal cord lesions (LESCLs). Linear
lesions were defined on T2-weighted imaging on MRI
according to Misu et al.  as: (i) consecutive linear shape
lesions on the sagittal plane and (ii) symmetric, with a
preferential involvement in the central gray matter on the
Serum NMO-IgG antibodies were tested according to the
manufacturers instructions using aquaporin 4-transfected
cells from a commercial sampling kit (EUROIMMUN AG,
All statistical analyses were performed using Statistical
Program for Social Sciences (SPSS) statistical software
(version 16.0, San Francisco, CA, USA). P < 0.05 was
considered statistically significant. Comparisons of the presence
of PTB between NMO patients and controls were carried
out using the Chi-squared test.
We enrolled 88 patients with NMO (67 diagnosed using
the 2006 Wingerchuk diagnostic criteria and 21 using
the 1999 Wingerchuk diagnostic criteria) and 352
controls into our study. The data on the presence of PTB in
NMO and control groups are shown in Table 1. One
NMO patient among the total 88 (1.1%) had a preceding
diagnosis of PTB. The frequency of active PTB in NMO
patients was not significantly different from that in
patients with myasthenia gravis, polymyositis or
dermatomyositis, facial neuritis, and VM (P > 0.05).
The single NMO patient who had a previous history
of PTB showed no evidence (in either CSF or radiology
reports) indicative of TB infection in the CNS. She was a
26-year-old woman who experienced visual blurring
simultaneously in bilateral optic neuritis and hemiplegia
of her left limbs, 2 months prior to admission. She was
positive for NMO-IgG and the CSF protein
concentration was 0.67 g/L, while glucose concentration and cell
count were normal. Brain MRI showed non-specific
white matter lesions. Spinal MRI showed a LESCL from
C1 to T5 without evidence of meningeal enhancement
or tuberculoma (Figure 1). The patient was diagnosed
with NMO. She had consolidation in her chest X-ray
3 months prior to admission. During hospitalization she
had a cough and her sputum was positive for acid-fast
bacilli. Chest radiography revealed extensive bilateral
TB tuberculosis; PTB pulmonary tuberculosis; NMO neuromyelitis optica; VM
viral meningitis/meningoencephalitis; M male; F female; P: comparison for
active PTB presence between NMO and each control groups.
Figure 1 Spinal MRI of the NMO patient with active PTB. a: axial
T2-weighted image showing a cervical lesion predominantly involving
the central cord; b: T1-weighted contrast image revealing slight
enhancement of the lesion; c: T2-weighted image showing a
longitudinal extensive spinal cord lesion.
Myasthenia gravis 88 (17/71)
confluent consolidation, predominantly involving the upper
lobes. Ziehl-Neelsen microscopy showed no acid-fast bacilli
in her CSF. After anti-tuberculosis treatment combined
with methylprednisolone pulse therapy, her PTB recovered,
but she had recurrent myelitis during the 17-month
followup period. Special MRI procedures including diffusion and
magnetic resonance spectroscopy were not performed
because they were unavailable during that period. However,
taking MRI features, discussion with neurosurgeons, and
the later follow-up into consideration, intramedullary
tuberculoma could be excluded.
Table 2 shows the demographic and clinical features of
NMO and TBM patients. Out of 92 TBM patients, 10
had myelitis (spinal meningitis, n = 2; tuberculoma, n = 1;
meningitis combined with tuberculoma, n = 2; focal or
extensive spinal lesions with hydrocephalus, meningitis or
tuberculoma in brain MRI, n = 2; clinical manifestations
indicating myelitis, n = 3). Two TBM patients had optic
neuritis, of which one developed optic neuritis before
anti-tuberculosis treatment. Compared with TBM related
myelitis (TBM-MY), NMO patients had a higher female:
male ratio (71:7 vs. 3:7), higher relapse rate of myelitis
(75% vs. 0), higher seropositive rate of NMO-IgG (82.1%
vs. 0%), and a higher frequency of normal cell count,
protein, glucose and chloride concentration in the CSF. CSF
TB-antibody positivity was found in 30% (3/10) of patients
with TBM-MY, but not in NMO patients. Spinal MRI was
performed in all NMO patients and 7/10 TBM-MY
patients. There were no spinal MRI data for the three
remaining TBM-MY patients because MRI was not
available at the time. However, these patients presented with
typical clinical symptoms indicating myelitis. Spinal cord
lesions in NMO patients mostly extend over multiple cord
levels involving central gray matter (linear lesions, shown
in Figure 2) or holocord (LESCLs and spinal lesions with
central/holocord involvement were found in 73.9% of
patients). Compared with NMO patients, spinal image
features of TBM-MY patients were different. Meningeal
enhancement (57.1% of patients), or tuberculoma (42.9%
of patients), which is characterized by oval lesions with
low (or iso-) T1-weighted image signal, typical target sign
T2-weighted image signal, and nodular or rim
enhancement in spinal cord was common (Figures 3 and 4).
Although one TBM-MY patient had LESCLs, similar to
the characteristic spinal MRI finding in NMO, the
tuberculoma in his medulla suggested direct TB infection of
the CNS (Figure 5). Methylprednisolone pulse therapy was
administered to all NMO patients in the acute phase.
During remission, six patients received additional
immunosuppressants. All 92 TBM patients received anti-tuberculosis
therapy (isoniazid, rifampicin, ethambutol plus
pyrazinamide or streptomycin for 86 patients and isoniazid,
rifampicin, ethambutol plus second-line drugs for the remaining
Table 2 Demographic and clinical features of NMO and TBM patients
NMO n = 88
Age, mean SD, years
Relapse of myelitis, n(%)
Increased protein level, n(%)
Decreased glucose level, n(%)
TB-antibody positivity, n(%)
Mycobacterium tuberculosis, n(%)
Seropositive NMO-IgG, n(%)
Central or holocord involvement, n(%)
Meningeal enhancement, n(%)
Follow-up duration, median (range), months
NMO neuromyelitis optica; TBM tuberculosis meningitis; TBM-MY:TBM related-melitis; TBM-ON:TBM related-optic neuritis; F female; M: male; CSF cerebrospinal fluid;
MRI magnetic resonance imaging; LESCLs longitudinal extensive spinal cord lesions.
Several reports have suggested PTB-related NMO is
caused by an immune response to TB infection. Acute
necrotic myelopathy or NMO occurred in a few patients
with active PTB. A postmortem study found
demyelination in the spinal cord without any evidence of TB
involvement [3,4]. The study by Hughes and colleagues
suggested tubercle bacillus, the bacterium that causes
TB, shares antigens with myelin basic protein so that
lymphocytes sensitized against mycobacterium recognize
Figure 2 Spinal cord lesion in an NMO patient. The lesions are
shown by arrows. a: T2-weighted image showing a linear-shape
lesion; b: axial T2-weighted image showing a cervical lesion
predominantly involving the central gray matter in the spinal cord.
Figure 3 Spinal MRI of a CNS-TB patient with spinal cord
involvement. ab: meningeal and whole lesion enhancement on a
T1-weighted contrast image; c: T2-weighted image showing an
isolated lesion at the T5 level of the spinal cord.
Figure 4 Spinal MRI findings in a CNS-TB patient with spinal
cord involvement. a: tuberculoma with iso-intensity on sagittal
T1-weighted image; b: T1-weighted contrast image showing
enhancement of the whole lesion and meninges; c: tuberculoma
with iso-intensity on a sagittal T2-weighted image.
and attack myelin . Recently, a report from South
Africa described a higher proportion of active PTB in
NMO patients compared with controls (79% vs. 14%,
P = 0.0013 < 0.05) . CNS-TB was excluded in all
cases. In contrast to this previous report, we could
not confirm an association of NMO with PTB. Only
one (1.1%) of the 88 patients in the NMO group was
previously diagnosed with PTB and this was similar
to the percentage observed in the control group (P > 0.05).
Western Cape Province in South Africa had an annual TB
incidence of 517 per 100 000 in 2007 , while the
estimated national incidence for China was considerably
lower than that in South Africa (approximately 154 per
100 000 in 2006 according to World Health Organization
reports , and even as low as 70 per 100 000 in some
areas of China ). It is therefore likely that the
prevalence of NMO in regions with a high incidence of TB is
different from the idiopathic autoimmune form seen in
areas of relatively low TB incidence.
Another possible explanation for TB-related NMO
relates to a nonspecific adjuvant effect of TB that
amplifies the immune response. It is relatively easy to induce
an autoimmune disease in genetically susceptible
animals via immunization with complete Freunds adjuvant
(containing inactivated M. tuberculosis) and an
autoantigen [19-21]. Although we do not know to what extent
the adjuvant effect of M. tuberculosis contributes to the
pathogenesis of the experimental autoimmune
encephalitis (EAE) model, a myelin-specific antigen in incomplete
Freunds adjuvant lacking M. tuberculosis can also
induce EAE in marmosets , suggesting that, at least in
Figure 5 Spinal MRI of a CNS-TB patient with spinal cord
involvement. a: axial T2-weighted image showing central gray
matter involvement of the spinal cord. b: T1-weighted contrast
image revealing tuberculoma enhancement in the medulla but no
enhancement of the spinal cord lesion; c: T2-weighted image
showing a longitudinal extensive spinal cord lesion without a
some species, this agent is not necessary for induction
It has also been proposed that some NMO cases are
caused by a direct CNS infection with tuberculosis. In a
small controlled study carried out by Feng and colleagues
from China, positivity for M. tuberculosis DNA in the CSF
of 2 out of 12 steroid-refractory NMO patients (confirmed
using nested polymerase chain reaction and the long-term
clinical efficacy of anti-tuberculosis treatment in these
patients) suggested pathogenesis involves direct CNS
infection . However, it is possible that Feng et al.s study
may have been subjected to selection bias because the
authors used the original criteria for NMO diagnosis
(Wingerchuck 1999), which did not require NMO-IgG
data, and their patients showed a high rate of CSF
abnormalities (CSF protein levels were increased in 53.9% of
patients and 50% had elevated CSF leukocyte counts) .
The present study used the newer, revised criteria that are
more specific for NMO diagnosis than the original criteria
. Contrary to the findings in Feng et al.s study,
elevated protein level (15.9% of patients) and pleocytosis
(18.2% of patients) in CSF were not common in our NMO
patients (Table 2). Although these relatively low
frequencies contrast with some reports from Western countries
(which found abnormal CSF cell counts in the majority of
patients in the acute phase [11,23]), our data are
consistent with some previous studies carried out in Asia (27.3%
of NMO patients had CSF pleocytosis in southern China
, 25% in Japan , and 0 in Iran ).
Although our data show that TBM patients may
develop myelitis or optic neuritis, many of these TBM
patients can be differentiated from NMO patients on the
basis of demographics, course (recurrent or
monophasic), CSF, and neuroimaging features. However, it is
worthwhile to note that two TBM patients shared partial
clinical features with NMO; one of the TBM patients
had LESCLs involving holocord, similar to the
characteristic spinal MRI finding in NMO, and the other had
optic neuritis before anti-tuberculosis treatment. This
finding supports the notion that direct TB infection of
the CNS may incidentally mimic NMO in some aspects.
The presence of NMO-IgG has rarely been tested in
TB-related NMO cases in older studies because
NMOIgG was not discovered until 2004 . Only one report
has described two patients who developed NMO-like
symptoms during the course of TB, but both patients
showed seronegativity for NMO-IgG . Consistent with
this previous report, the two patients who shared partial
clinical features with NMO in our study were also
negative for NMO-IgG. We presume that these NMO-like
symptoms with NMO-IgG negativity may differ from
NMO with NMO-IgG positivity. In fact, reports have
shown that NMO-IgG negative NMO differs clinically
and epidemiologically from NMO-IgG positive disease
and may even have a distinct pathogenesis . Despite
the high specificity of NMO-IgG for diagnosis of NMO
[1,2,10], NMO-IgG negativity cannot rule out its
diagnosis absolutely. This is because NMO-IgG levels and even
serostatus can vary during follow-up . Thus, diseases
that mimic NMO, including CNS infections with a focus
on the spinal cord and optic nerves, still have the
potential to be diagnosed as NMO with NMO-IgG negativity.
Recently, Miller and co-workers suggested that patients
showing evidence of another explanation for NMO-like
symptoms should be excluded from NMO diagnosis
. Therefore, it is still debatable whether NMO-like
symptoms that develop during the course of TB should
be considered and diagnosed as NMO.
The nature of NMO and its association with TB in the
Chinese population may differ from populations from
other regions. We could not confirm previous
suggestions of an association between PTB and NMO. Direct
TB infection of CNS may incidentally mimic NMO in
some respects, but whether NMO-like symptoms that
develop during the course of TB are diagnosed and
treated as NMO is open to discussion. Although our
findings argue against a causal association of NMO and
TB, this study is limited by its retrospective design. We
only focused on the relationship between NMO and active
PTB and TBM because of limited datasets. A broader
association of TB (for instance, distant or treated TB) and
NMO should also be explored. Moreover, TB (the risk
factor) does not occur at a sufficiently high frequency in
either NMO patients or controls in our study to draw a
definitive conclusion; therefore, a possible association
between NMO and TB may be missed because of the small
sample size. A larger prospective investigation with a
long-term follow-up will be helpful in answering this
CNS: Central nervous system; CSF: Cerebrospinal fluid; LESCL: Longitudinal
extensive spinal cord lesions; MRI: Magnetic resonance imaging;
NMO: Neuromyelitis optica; PTB: Active pulmonary tuberculosis;
TB: Tuberculosis; TBM: Tuberculosis meningitis; TBM-MY: Tuberculosis
meningitis-related myelitis; VM: Viral meningitis/meningoencephalitis.
The authors declare no conflicts of interest.
All authors have made substantial contributions to the intellectual content of
the paper. RL and XZ contributed to the conception, design, and drafting of
the manuscript. AW and YD contributed to the acquisition, analysis, and
interpretation of data. WQ, ZL, and XH revised the manuscript critically for
intellectual content. All authors read and approved the final manuscript.
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