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Clinical Neurology and Neurosurgery 163 (2017) 76–80
Contents lists available at ScienceDirect
Clinical Neurology and Neurosurgery
journal homepage: www.elsevier.com/locate/clineuro
Full Length Article
Differential diagnosis of scrub typhus meningitis from tuberculous
meningitis using clinical and laboratory features
MARK
⁎
Ashraf V. Valappila, , Sohanlal Thiruvothb, Jabir M. Peedikayilc, Praveenkumar Raghunatha,
Manojan Thekkedathc
a
b
c
Department of Neurology, Malabar Institute of Medical Sciences, Calicut, Kerala, India
Department of Microbiology, Malabar Institute of Medical Sciences, Calicut, Kerala, India
Department of Internal Medicine, Malabar Institute of Medical Sciences, Calicut, Kerala, India
A R T I C L E I N F O
A B S T R A C T
Keywords:
Lymphocytic meningitis
Scrub typhus
Tuberculosis
Differential diagnosis
Objectives: The involvement of the central nervous system in the form of meningitis or meningoencephalitis is
common in scrub typhus and is an important differential diagnosis of other lymphocytic meningitis like tuberculous meningitis (TBM). The aim of this study was to identify the clinical and laboratory parameters that
may be helpful in differentiating scrub typhus meningitis from TBM.
Patients and methods: We compared of the clinical and laboratory features of 57 patients admitted with scrub
typhus meningitis or TBM during a 3-year period. Patients who had abnormal cerebrospinal fluid (CSF) and
positive scrub typhus enzyme-linked immunosorbent assay serology (n = 28) were included in the scrub typhus
meningitis group, while the TBM group included those who satisfied the consensus diagnostic criteria of TBM
(n = 29).
Results: Compared with the TBM group, the mean duration of symptoms was less in patients with scrub typhus
meningitis, who also had a lower magnitude of neurological deficits, such as altered mental status and cranial
nerve and motor deficits. Patients with scrub typhus meningitis had a lower CSF white blood-cell count (WBC)
than the TBM group (130.8 ± 213 195 ± 175 cells/mm3, P = 0.002), lower CSF protein elevation
(125 ± 120 vs. 195.2 ± 108.2 mg/dl, P = 0.002), and higher CSF sugar (70.1 ± 32.4 vs. 48.7 ± 23.4 mg/
dl, P = 0.006). Features predictive of the diagnosis of scrub typhus meningitis included the absence of neurological impairment at presentation, blood serum glutamic-oxaloacetic transaminase > 40 international units
(IU)/L, serum glutamic-pyruvic transaminase > 60 IU/L, total blood leukocyte count > 10,000/mm3, CSF
protein < 100 mg/dl, CSF sugar > 50 mg/dl, CSF WBC < 100 cells/mm3. All patients with scrub typhus
meningitis recovered completely following doxycycline therapy
Conclusions: This study suggests that, clinical features, including duration of fever, neurological deficits at
presentation and laboratory parameters such as CSF pleocytosis,CSF protein elevation, CSF sugar levels and liver
enzyme values are helpful in differentiating scrub typhus meningitis from tuberculous meningits. These features
with scrub IgM serology may be helpful in identifying patients with scrub meningitis and in avoiding prolonged
empirical antituberculous therapy in cases of lymphocytic meningitis.
1. Introduction
Scrub typhus is a vector borne rickettsial infection caused by
Orientia tsutsugamushi and is commonly observed in terrains of the
tsutsugamushi triangle, a geographical region of South and East Asia,
including the Indian sub-continent and the Southwest Pacific. [1–3] The
unique propensity of O. tsutsugamushi involving vascular endothelial
cells results in multiple organ dysfunctions in scrub typhus. Scrub typhus involves both the central (CNS) and peripheral nervous systems.
⁎
The CNS complications include meningitis, encephalitis, infarction,
cerebellitis, hemorrhages, and demyelination. [4–6] The complications
of the peripheral nervous system include mononeuritis multiplex, brachial plexus neuropathy, polyneuropathy, and Guillain Barre syndrome.
[7–9] The CNS involvement is often a prominent clinical manifestation,
and meningitis or meningoencephalitis occurs in 12–26% of the affected patients. [4,10] Scrub typhus meningitis is an important cause of
meningitis in endemic areas. [11] However, it remains an unclear entity, and clinical features differentiating meningitis due to scrub typhus
Corresponding author at: Department of Neurology,Malabar Institute of Medical Sciences,Govindapuram PO Calicut-673016, Kerala, India.
E-mail addresses: [email protected], [email protected] (A.V. Valappil).
http://dx.doi.org/10.1016/j.clineuro.2017.10.022
Received 31 May 2017; Received in revised form 13 October 2017; Accepted 21 October 2017
Available online 23 October 2017
0303-8467/ © 2017 Elsevier B.V. All rights reserved.
Clinical Neurology and Neurosurgery 163 (2017) 76–80
A.V. Valappil et al.
from other forms of meningitis are still lacking. In areas where both
scrub typhus and tuberculosis are endemic, tuberculous meningitis
(TBM) forms the closest and the most important differential diagnosis
because both cause lymphocytic meningitis. The aim of this study was
thus to identify the clinical and laboratory parameters that may be
helpful in differentiating scrub typhus meningitis from common TBM.
Table 1
patient characteristics, laboratory features and CSF analysis.
2. Materials and methods
All patients aged 15 years or above who were hospitalized with a
diagnosis of scrub typhus meningitis and TBM over a 3-year period
were included in the study. The diagnosis of scrub typhus was confirmed by serum IgM enzyme-linked immunosorbent assay (ELISA;
Scrub typhus Detect IgM ELISA, InBios India, detecting IgM antibodies
to O. tsutsugamushi derived recombinant antigen). Meningitis was suspected and cerebrospinal fluid (CSF) analysis was performed if a patient
had one or more of the following clinical features: Headache, nausea/
vomiting, seizures, altered sensorium, or neck rigidity. In addition to
CSF protein, sugar, and cell counts, the centrifuged deposit was subjected to the Grams, Ziehl-Neilsen, and India ink staining techniques to
identify cell wall characteristics of bacteria and help identify
Mycobacteria and Cryptococcus species. Patients who were IgM ELISA
positive for O. tsutsugamushi and had features suggesting meningitis on
CSF analysis, and in whom other causative organisms were not found
on stains, were defined as scrub typhus meningitis cases. Patients
hospitalized during the same period with a diagnosis of TBM were included as controls. We used the TBM consensus diagnostic criteria as
previously reported by Marais et al. [12] Both definite and probable
patients with TBM were included. The clinical and laboratory features
of patients with scrub typhus meningitis and TBM were compared.
Statistical analysis was performed using the SPSS software for
windows. Descriptive data were represented by the mean (standard
deviation [SD]) or median (range). The chi-square test was used to
compare dichotomous variables and Mann-Whitney test was used for
continuous variables. Logistic regression analysis was performed after a
univariate and multivariate analysis to predict the diagnosis of scrub
typhus meningitis. A p-value < 0.05 was considered statistically significant.
Parameter
Scrub typhus meningitis
n = 28 (%)
Tuberculous
meningitis N = 29 (%)
P value
Age
Duration of
fever
Headache
Seizure
Altered mental
status
Neck stiffness
CSF-TC(cells/
cumm)
CSF-Protein
(mg/dl)
CSF Sugar (mg/
dl)
Hb (gm/dl)
ESR(mm/hr)
WBC count
(cells/
cumm)
SGOT (IU/L)
SGPT (IU/L)
ALP (IU/L)
Total bilirubin
(mg/dl)
40.2 ± 17.6
8.8 ± 3.4
47.1 ± 18
15 ± 9.7
0.145
0.04
23 (82)
9(32)
8(28.6)
19 (65.5)
14(48.3)
18(62)
0.15
0.21
0.01
14(50)
130.8 ± 213
21(72)
195 ± 175
0.08
0.002
125 ± 120
195.2 ± 108.2
0.002
70.1 ± 32.4
48.7 ± 23.4
0.006
12.8 ± 1.72
32.6 ± 15.7
13260.7 ± 4626.5
12.3 ± 1.8
39.6 ± 25.1
9220 ± 4014.3
0.194
0.227
0.002
135 ± 97.7
150 +112.7
204.7 ± 95.7
1.64 ± 2.45
39.6 ± 50.8
46.5 ± 27.4
140.7 ± 136.2
1.16 ± 1.69
< 0.001
< 0.001
0.012
0.89
meningitis, respectively. Leukocytosis was significantly higher in the
scrub
typhus
meningitis
group
(13,260 ± 4,626.5
vs.
9220 ± 4,014.3; p = 0.002). The blood hemoglobin level and erythrocyte sedimentation rate (ESR) did not differ significantly between
the two groups.
In contrast, the CSF findings were markedly different between the
two groups. The scrub typhus group had a lower CSF pleocytosis and a
lesser degree of protein elevation. More than the 2/3rd of the scrub
typhus cases had a CSF cell count up to 100 cells/mm3, while only
14.3% of the patients had counts exceeding 200 cells/mm3. In the TBM
group, nearly half of the patients had cell counts between 100 and 200
cells/mm3 (Fig. 1). Both groups had CSF lymphocytic pleocytosis, with
a mean lymphocytic level of 99% in the scrub typhus group and 96% in
the TBM group. The mean CSF cell count was significantly higher in the
TBM group. Approximately 50% of the scrub typhus cases had a CSF
protein level below 100 mg/dl, whereas 61% of the TBM group had CSF
protein between 100–200 mg/dl (Fig. 2). The mean CSF protein level
was significantly higher in the TBM group. A CSF sugar level below
50 mg/dl was observed in 48% of the patients with TBM and 14% of the
patients with scrub typhus (Fig. 3).
A comparison of clinical and laboratory features including 3 groups,
3. Results
During the study period, there were 28 cases of scrub typhus meningitis. Of those, 14 were male patients and 14 were female patients.
The most common presenting complaints were fever (100%), headache
(82%), vomiting (71%) and seizures (32%). Pathognomonic eschar was
found only in seven patients (25%). Three patients had papilledema,
and one of those also had lateral rectus palsy.
The control group consisted of 29 patients (13 males and 16 females) diagnosed with TBM. Of those, 13 had definite TBM (positive
CSF polymerase chain reaction [PCR] for tuberculosis) and 16 had
probable TBM. Most common presenting complaints were fever (90%),
headache (65%), seizures (48%) and altered mental status (62%). Five
patients had papilledema, three had other cranial nerve deficits, and
two had hemiparesis. The clinical and laboratory features of the cases
and controls are presented in Table 1.
The duration of the fever prior to the presentation was longer in the
TBM group than in the scrub typhus group (14.9 ± 19.6 days vs.
8.8 ± 3.4 days, p = 0.11). The patients with scrub typhus were less
likely to present with seizures and altered mental status compared with
patients with TBM. Focal deficits were more common in the TBM group.
The most notable laboratory findings on admission were a higher
degree of elevation of liver enzymes in the scrub typhus meningitis
group, while most of the TBM group had near normal values. Serum
glutamic pyruvic transaminase (SGPT) levels > 65 international units
(IU) and serum glutamic oxaloacetic transaminase (SGOT) > 40 IU/L
were observed in 79% and 89% of patients with scrub typhus
Fig. 1. Distribution of CSF WBC count.
Comparison of CSF WBC count in patients with scrub typhus meningitis and tuberculous
meningitis (p value 0.002)
77
Clinical Neurology and Neurosurgery 163 (2017) 76–80
A.V. Valappil et al.
Table 3
Logistic regression analysis indicating predictors differentiating scrub typhus meningitis
from TBM.
Variable
SGOT (> 40IU/L)
SGPT (> 60 IU/L)
WBC (> 10000/
mm3)
CSF WBC (> 100/
mm3)
CSF Protein
(> 100mg/dl)
CSF Sugar
(> 50mg/dl)
Neurological
impairment
Fig. 2. Distribution of CSF Protein levels.
Comparison of CSF Protein levels in patients with scrub typhus meningitis and tuberculous meningitis (p value 0.002)
Odds ratio
p value
Cox & Snell R
Square
Nagelkerke R
Square
21.875
26.19
5.7
< 0.001
< 0.001
0.003
0.348
0.378
0.157
0.464
0.504
0.209
0.151
0.001
0.181
0.241
0.036
0.002
0.273
0.364
5.6
0.009
0.13
0.174
0.325
0.045
0.07
0.09
Note: Table 3
Odds ratio for the variables SGOT, SGPT, WBC and CSF sugar are more than one indicating higher than their respective cut of value are indicator of scrub typhus and as the
odds ratio for the variables CSF WBC and CSF Protein are less than one indicating values
less than their respective cut of are indicator of Scrub typhus. Neurological impairment is
associated with TBM.
count > 10,000 mm3, CSF protein < 100 mg, CSF sugar > 50 mg/
dl, and CSF white blood cell (WBC) count < 100 cells/mm3. The odds
ratios and their predictability (Cox & Snell and Nagelkerke R Square)
are given in Table 3. A multiple logistic regression with these factors
and the duration of fever (in days) was also performed. Strongest predictor was CSF protein followed by SGOT level and Total WBC count.
The full model containing these factors was statistically significant and
enabled the distinguishing between scrub typhus and TBM in 88% of
the cases (50 out of 57).
All patients with scrub typhus meningitis recovered well and became asymptomatic by 2–5 days following the treatment. The average
hospital stay was 5 days. Neuroimaging by either computed tomography or magnetic resonance imaging was performed in all patients.
Only three patients revealed abnormalities, with one bearing a gyral
edema and two showing a mild ventriculomegaly. The average hospitalstay for the patients with TBM was 12 days. Five patients with TBM had
residual neurological deficits at the time of discharge and four patients
succumbed to illness.
Fig. 3. Distribution of CSF Sugar levels.
Comparison of CSF Sugar levels in patients with scrub typhus meningitis and TBM (p
value 0.013)
scrub meningitis, probable TBM and Definite TBM was also done as
shown in Table 2. Findings were almost similar to the two group
comparison (Table 1), except for non significant association of peripheral blood WBC count and alkaline phosphatase between scrub
meningitis and definite TBM. There was no statistically significant
difference between definite and probable TBM.
Logistic regression analysis was performed after a uni- and multivariate analysis. The univariate logistic regression analysis revealed a
statistically significant association between scrub typhus and the following variables: absence of neurological impairment at presentation,
blood SGOT > 40 IU, SGPT > 60 IU, total blood leukocyte
Table 2
Comparison of Clinical characteristics, laboratory findings and outcome- Scrub meningitis versus definite and probable TBM.
Scrub meningitis (SM) (n = 28)
Probable TBM (PT) (n = 16)
Definite TBM (DT) (n = 13)
P value
Intergroup comparison P value
Duration of fever(mean) in days
8.8 ± 3.4
17.1 ± 22.5
12.3 ± 16.04
0.55
SM vs PT
SM vs DT
0.85
0.28
Seizures
Altered mental status
WBC count (cells/mm [3])
9
8
13260 ± 4626.5
8
8
8193.8 ± 3293.7
7
10
10484.6 ± 4572
0.45
0.049
0.001
SGOT (IU/L)
135 ± 97.7
29.8 ± 39
51.7 ± 62
< 0.001
SGPT (IU/L)
150 ± 112.7
44.3 ± 35.4
49.2 ± 17
< 0.001
SAP (IU/L)
204.7 ± 95.7
186 ± 187
103.4 ± 56.2
0.001
CSF TC (cells/mm [3])
130.8 ± 213
210.4 ± 167.3
176 ± 188.7
0.007
CSF protein (mg/dl)
125 ± 120.5
204 ± 134
184.5 ± 68.1
0.001
CSF Sugar (mg/dl)
70.1 ± 32.4
49.5 ± 26.5
47.6 ± 19.9
0.22
SM
SM
SM
SM
SM
SM
SM
SM
SM
SM
SM
SM
SM
SM
0.001
0.14
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
0.13
0.004
0.031
0.002
0.002
0.06
0.05
Outcome – Death or sequelae
0
5
4
0.033
78
vs
vs
vs
vs
vs
vs
vs
vs
vs
vs
vs
vs
vs
vs
PT
DT
PT
DT
PT
DT
PT
DT
PT
DT
PT
DT
PT
DT
Clinical Neurology and Neurosurgery 163 (2017) 76–80
A.V. Valappil et al.
4. Discussion
count and CSF protein level than patients with scrub typhus (Figs. 1 and
2). The CSF sugar level was also significantly lower in patients with
TBM than in the scrub typhus group (Fig. 3). In the logistic regression
analysis, a CSF protein < 100 mg/dl, CSF WBC count < 100 cells/
mm3, and CSF sugar > 50 mg/dl were found to be predictive for the
diagnosis of scrub typhus meningitis.
Doxycycline remains the drug of choice in scrub typhus meningitis.
In Thailand, rifampicin has been shown to be more effective than
doxycycline in managing scrub typhus infections. [26] However, the
use of rifampicin for scrub typhus in areas where tuberculosis is also
endemic raises a larger concern for the resistant tuberculosis, and is
thus not recommended. All patients with scrub typhus meningitis in our
study recovered within 2–5 days of doxycycline therapy. The case
fatality rate in the earlier studies was up to 30%,[27] but recent studies
reported a lower mortality rate of 5–6%.[13,25] This difference in the
course and outcome may represent a difference in the time to diagnosis
and treatment or a variation in the strain of the organism causing the
infection. Four patients in the TBM group succumbed to illness in the
present study.
In conclusion, scrub typhus is a re-emerging cause of acute and subacute lymphocytic predominant meningitis, which can be difficult to
differentiate from other lymphocytic meningitis like TBM. The eschar, a
pathognomonic clinical sign, is often not present, and, since the larval
bite is painless, a history of insect bite is usually not elicited by the
patients. Several laboratory features such as the elevated liver enzymes,
blood leukocytosis, normal CSF sugar, lower of CSF WBC count, and
CSF protein elevation can be helpful features to differentiate scrub typhus meningitis from TBM. Scrub typhus meningitis is a milder complication of scrub typhus and generally resolves completely with doxycycline therapy. Rifampicin-based antitubercular therapy can mask
the diagnosis of scrub typhus and sometimes results in patients enduring long-term TBM therapy. Since India is endemic to tuberculosis
and scrub typhus, the awareness of simple methods to treat scrub typhus with access to specific tests like scrub typhus IgM ELISA may go a
long way in avoiding unwarranted treatment in patients with lymphocytic meningitis. Our study, however, is limited by its sample size,
and further studies on a larger scale are still warranted.
Scrub typhus meningitis is a lymphocytic predominant meningitis.
TBM possesses a diagnostic challenge in patients presenting with a subacute onset of meningitis, because both TBM and scrub typhus meningitis cause lymphocytic meningitis. India is one country among five
that have the highest prevalence of TBM. [13] The purpose of this study
was to characterize scrub typhus meningitis and meningoencephalitis in
an endemic area and to identify clinical and basic laboratory features
that enable the differentiation of scrub typhus meningitis from TBM. To
the best of our knowledge, this is the first study that compared directly
the clinical and laboratory features of scrub typhus meningitis and
TBM.
A high index of suspicion is needed for diagnosing scrub typhus
meningitis because it presents with acute undifferentiated febrile illness
with features of meningitis. This is further confounded by the nonavailability of specific tests to diagnose scrub typhus in most centers.
We used the IgM ELISA test to confirm scrub typhus, which has both
high specificity (90%) and sensitivity (90%) when compared to the
indirect immunofluorescence and complement fixation tests. [14–16]
The diagnosis of TBM usually relies on clinical evidence, which combines supportive clinical, laboratory, and radiological findings. The
standard diagnostic criteria for the diagnosis of TBM have not been
established, and most reports have used different case definitions.
[17–19] In the present study, we used the consensus diagnostic criteria
previously proposed by Marais et al. [12]
The present results indicated several potentially useful distinguishing features. The majority of the typically presenting symptoms,
such as headache and vomiting, were not significantly different between the two groups. In contrast, the duration of fever prior to the
presentation of the condition was significantly longer in the TBM group.
The mean duration of fever in the scrub typhus group was similar to
that reported in a previous study. [20] The neurological impairments
(altered consciousness, seizures, mild focal signs, multiple cranial nerve
palsies, dense hemiplegia, or paraparesis) were less common in the
patients with scrub typhus compared with the TBM group. This was a
predictive factor in the differential diagnosis between these two conditions in the regression analysis. Papilledema was noted in three patients (10%) with scrub typhus, which is not in agreement with a previous report suggesting the occurrence of papilledema in up to a fifth of
patients with scrub typhus. [20]
Many of the standard blood laboratory findings were not significantly different between the two groups. The blood hemoglobin
levels and ESR did not differ between the two groups. In contrast, the
blood leukocytosis level was significantly higher in patients with scrub
typhus. A total blood leukocyte count of more than 10,000 per mm3 was
a significant feature of scrub typhus meningitis in the logistic regression
analysis. A mild rise of liver enzymes (from 67 to over 90%) was reported in the majority of patients with scrub typhus in various studies.
[21–23] Elevated SGPT (79%), SGOT (89%), and alkaline phosphatase
levels (61%) were found in patients with scrub typhus meningitis in our
study. The elevated SGOT and SGPT levels were the strongest predictors
of scrub typhus meningitis in the logistic regression analysis.
The mean CSF WBC count in the scrub typhus group was 130.8
cells/mm3 and the median was 60 cells/mm3. We observed a wider
range of CSF cell count of 1–840 cells/mm3. Previous Indian series by
Abhilash et al. [24] reported a slightly lower mean CSF cell count (80
cells/mm3), but the range was similar to our series. The mean CSF
protein in the scrub typhus group was 124.9 mg/dl and range was
30–669 mg/dl. Abhilash et al. [24] reported a slightly lower mean CSF
protein level (105 ± 80 mg/dl) and an almost similar range of CSF
protein (13–640 mg/dl). Unlike in bacterial or tuberculous meningitis,
hypoglychorrhachia, which is characterized by a low CSF glucose level,
is not common in scrub typhus meningitis. In the present study, hypoglychorrhachia was observed in 14% of patients with scrub typhus
meningitis. Patients with TBM had a significantly higher CSF WBC
Funding
None.
Conflict of interest
No conflicts of interest.
Acknowledgement
We are grateful to Mr. Sadjith Kuyyattil of MIMS Academy for statistical analysis.
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