Electroencephalography and clinical Neurophysiology, 84 (1992) 549-552

549

© 1992 Elsevier Scientific Publishers Ireland, Ltd. 0168-5597/92/$05.00

E V O P O T 91548

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Diagnostic role of brain-stem auditory evoked potentials in neurobrucellosis Basim A. Yaqub, Mohammad M.U. Kabiraj, Abrulrahman Shamena, Munira A1-Bunyan, Abdulkader Daif and Abdulrahman Tahan Dit,ision of Neurology and Neurophysiology, King Khalid Unil'ersity Hospital, Riyadh (Saudi Arabia) (Accepted for publication: 27 July 1992)

Summary

Evoked potential audiometry and brain-stem auditory evoked potentials were evaluated in 15 patients with systemic brucellosis in whom brucella meningitis was suspected clinically. In 8 patients cerebrospinal fluid (CSF) was abnormal with high brucella titre, and evoked potentials were abnormal in all of them. In 7 patients the CSF was normal and evoked potentials were also normal. Brain-stem auditory evoked potential abnormalities were categorised into 4 types: (1) abnormal wave I, (2) abnormal wave V, both irreversible, (3) prolonged I - I l l interpeak latencies, and (4) prolonged 1-V interpeak latencies, both reversible. These findings are of important diagnostic value and correlate well with the clinical features, aetiopathogenesis and final outcome. Key words: Neurobrucellosis; Brain-stem auditory evoked potentials; Evoked potential audiometry

Brucellosis is a common infectious disease in many parts of the world, especially in the Mediterranean countries and the Middle East (Kambal et al. 1983; Shakir et al. 1987; Lulu et al. 1988; AI-Deeb et al. 1989). Neurobrucellosis is due to direct involvement of the nervous system and constitutes 5% of the cases (Shakir et al. 1987: AI-Deeb et al. 1989). Meningitis involvement with lymphocytic pleocytosis in the cerebrospinal fluid (CSF) is found in all cases (Bashir et al. 1985; AI-Deeb et al. 1988). Meningitis may be isolated or assocated with various symptoms due to central a n d / o r peripheral nervous system involvement (Shakir et al. 1987; AI-Deeb et al. 1988). Diagnosis is not easy since the brucella can be cultured from the CSF in less than 50% of cases (AI-Deeb et al. 1988, 1989) while CSF findings are unspecific and similar to those seen in tuberculous or viral meningitis. The aim of this study is to evaluate the changes in evoked potential audiometry (EPA) and brain-stem auditory evoked potentials (BAEPs) and their diagnostic and prognostic role in brucellosis.

Methods and materials Evoked potentials were prospectively evaluated in 15 patients, 5 men and 10 women aged 8-55 years. All had systemic manifestations of brucellosis and high lgG serology for brucellosis with a titre of 1/320 or more. All patients were suspected of meningitis. Cerebrospinal fluid (CSF) protein, glucose, cell count and differential, and IgG brucella titres were determined in all patients. Diagnosis of neurobrucellosis (NB) was made if the CSF showed lymphocytic pleocytosis with abnormally high protein level and brucella titre of 1/128 or more. Diagnosis of systemic brucellosis (SB) was made if CSF was normal and CSF titre for brucellosis was not detected.

Correspondence to: Dr. B.A. Yaqub, Associate Professor in Neurology, King Khalid University Hospital, P.O. Box 7805 (38), Riyadh 11472 (Saudi Arabia). Tel.: 467 1939/1532; Fax: 476 2558/418 1853.

EPA and BAEPs were done in all patients before starting the treatment. Patients with previous hearing problems or audiological disorders were excluded. A Medelec ST10 sensor was used and evoked potentials were done using alternating monoaural clicks of 100/zsec duration with a stimulation rate of 10 Hz, and contralateral masking noise. Filter settings were at 100 Hz and a 3 kHz. The signals were recorded from A2-C z or A t - C z surface electrodes at vertex and both earlobes. 1024 responses were averaged in each run, 2 runs were performed for each ear and compared for reproducibility. E P A was performed by recording wave V at 20, 40, 60, and 80 d B / N H L (normal hearing level). Absence of wave V at 20 d B / N H L was considered to be abnormal. BAEPs were done using monaural click stimulation at 60 dB above hearing threshold, and the peaks of waves I. III and V were identified. If the BAEPs were not well defined using ipsilateral ear reference, a recording was made with contralateral ear reference. In all patients we documented the amplitude, latency and interpeak latencies (1PL) of waves I, III and V. Wave I, lI1 and V latencies and IPL were abnormal if their values exceeded the mean + 3 S.D. of the controls. The amplitude of waves 1 and V was considered abnormal if it was less than the minimal amplitude of any of the controls. Wave V was also considered abnormal if the I / V amplitude ratio was more than the mean + 3 S.D. in controls. Latencies, amplitude and IPL of BAEPs of the controls are given in the legend of Table I. On the basis of CSF data, the patients were divided into 2 groups: group l with normal CSF, considered to have systemic brucellosis without nervous system involvement (SB), and group I1 with abnormal CSF considered to have neurobrucellosis (NB). EPA and BAEPs were evaluated in the two groups. In patients with abnormal E P A and BAEPs, they were repeated after completion of treatment with antibiotics.

Results Group I consisted of 7 patients (3 men, 4 women). The mean age was 33 years (19-52 years). The neurological presentation in this

B.A. Y A Q U B ET AL.

550 TABLE I Clinical and evoked potential abnormalities in patients with neurobrucellosis (group II). Patient

Right

Left

Additional clinical signs

EPA/HT "

BAEP b abnormalities

EPA/HT

BAEP abnormalities

> 60

Wave I latency c, 2.24 msec

> 90

Wave l absent

Bilateral hearing impairment Lt > Rt

2

> q0

Wave 1 latency, 2.21 msec ~

> 90

Wave I absent

Bilateral hearing impairment

3

> 40

Wave V of small amplitude d, 0.15 #V; and delayed latency, 6.92 msec

> 40

Normal

Rt: 3rd N palsy Lt: pyramidal signs

4

> 40

Wave V absent

> 40

I - V IPL delayed, 4.69 msec

None

5

< 20 Normal

Wave V of small amplitude, 0.12/~V; and delayed latency, 6.52 msec

> 40

I - l l I IPL delayed, 2.76 msec

Papilloedema Lt > Rt

6

> 40

I - V IPL delayed, 4.80 msec

> 90

Wave I absent and also the subsequent waves

Bilateral pyramidal signs. Lt. ear deafness

7

> 40

l - I l l IPL delayed, 2.92 msec

< 20 Normal

I - V IPL delayed, 4.96 msec

None

8

< 2(1 Normal

l - I l l IPL delayed, 2.86 msec

> 40

I - V IPL delayed, 4.85 msec

None

" E P A / H T = evoked

potential audiometry hearing threshold. b BAEPs = brain-stem auditory evoked potentials. c Latencies were measured to wave peaks. a Amplitudes were measured from the wave peak to the following trough. Normal values of controls (65 subjects, 32 females and 33 males, age (15-55 years). Latencies and Wave I, Wave IlL Wave V, l - I l I IPL, I I I - V IPL, I - V IPL,

IPL in msec 1.7-+0.15 3.8_+0.20 5.7-+0.25 2.1 +0.19 1.9+0.20 4.0_+ 0.21

Amplitude in ~V Wave !, (/.35_+0.21 (range 0.11-0.92) Wave III, 0.30-+0.10 (range 0.07-0.62) Wave V, 0.50_+0.20 (range 0.18-0.92) I / V amplitude ratio 76% _+44%

group consisted of fever, headache, myalgia, dizziness and suspicions of meningitis, signs of neck stiffness or Kernig's sign. EPA and BAEPs were normal in all patients. Group II consisted of 8 patients (3 men, 5 women). The m e a n age was 32 years ( [7-55 years). The clinical picture of this group was as in group I, with or without mild pyramidal signs a n d / o r swelling of the optic discs. Hearing impairment was clinically evident in only 3

patients, but BAEPs were abnormal in the 8 patients. BAEP abnormalities were bilateral in 7 patients. The E P A hearing threshold, clinical data and evoked potential findings in the 8 patients with NB are summarized (Table I). BAEP abnormalites were classified into 2 types: type I - abnormal waves (Fig. 1): abnormal wave I, in 5 out of 16 (31%) records and abnormal wave V in 3 out of 16 records (19%), and type II -

0.15.uVI

.5o uV

1.72

i

2,24

80ad

B

B.88

~

"IV

"~

5.76

1 msec

1 m sec

80dB

b

Fig. l. a: BAEPs of right ear (patient no. l). Delayed wave I. A 21-year-old male with progressive hearing impairment. The record showed delayed wave 1 at a latency of 2.24 msec (normal: 1.7_+0.15). b: BAEPs of right ear (patient no. 3). Abnormal wave V. A 17-year-old female with right 3rd nerve palsy and left pyramidal signs. Wave V is of small amplitude, 0.15 ~V (normal range 0.18-0.92) and delayed at a latency of 6.92 msec (normal: 5.7 + 0.25), I / V ratio - 255% (N: 76% + 44%).

EPs IN N E U R O B R U C E L L O S 1 S

T

551

1.72

]/~

0.30 3.48

4.48

5.92

uV I msec • ^^

~'~

80dB

3;[ 6 . 8 8

~,

"~

30uV[ " I lrnsec

Fig. 2. a: BAEPs of left ear (patient no. 5). Prolonged I 111 IPL in a 27-year-old female with bilateral papilloedema. The record showed prolonged l - I l l 1PL of 2.76 msec (normah 2.1 ±0.19). b: BAEPs of left ear (patient no. 7). Prolonged I - V IPL. A 32-year-old female with meningeal signs. The record showed prolonged I - V IPL latency of 4.96 msec (normal: 4.0 ± 0.21 ).

prolonged IPL (Fig. 2), prolonged I - I l l IPL, in 4 o u t o f 16 records (25%) and prolonged I - V IPL, in 3 out of 16 records (19%). Only 1 out of 16 (6%) records was normal.

Type 1, abnormal wat:es la. Abnormal wave l (31%) - wave I was either absent, delayed in latency (N: 1.7+0.15) or of small amplitude of less than 0.11 /~V (N: 11.3+0.21, range 0.11-0.92). The subsequent waves were either normal or absent. These abnormalities were seen in 5 records, bilaterally in 2 (patients 1, 2) and unilaterally in 1 patient (patient 6) (Fig. la). lb. Abnormal wave V (19%) - wave V was either absent or of small amplitude of less than 0.18 p,V (N: (1.5 + 0.12, range 0.18-0.92). Other waves were normal. This was seen in 3 records of patients 3, 4 and 5. The abnormality was unilateral in those patients (Fig. lb). Type I1, prohmged IPL Ila. Prolonged I - I I I IPL (25%) - this was seen in 4 records, unilaterally in 2 (patients 5 and 7) and bilaterally in 1 (patient 8) (Fig. 2a). lib. Prolonged I - V IPL (19%) - the configuration and amplitude of the waves were normal, but I - V IPL was prolonged (Fig. 2b). This abnormality was unilateral in 3 records of patients 4, 6 and 7. In all patients with abnormal records, the test was repeated 3 - 6 months after completion of antibiotic therapy. Type I p a t i e n t s w i t h abnormal waves showed no change while those of type It with prolonged IPL normalised.

Discussion

This study shows the high incidence of B A E P abnormalities in neurobrucellosis which were observed in all patients and for 15 out of 16 ears. Clinically, however, only 3 out of 8 patients had hearing problems while the remaining 5 had no detectable clinical hearing problems. Other patients with normal BAEPs had no evidence of nervous system involvement. These findings are consistent with a recent report by Kuraibet et al. (19881 in which BAEPs were abnormal in all patients with neurobrucellosis. Thus evoked potentials can be considered as a simple non-invasive method to indicate nervous system involvement in patients with brucellosis. The various BAEP abnormalities that we observed probably reflect the different types of auditory pathway d a m a g e s . d o c u m e n t e d in the literature (AI-Deeb et al. 1988, 1989). In patients with prolonged 1-11I IPL, the meningitis may cause a reversible compression of the proximal part of the cochlear nerve which can be released by treatment. In patients with prolonged I - V IPL the reversible abnormalities of BAEPs may reflect neurobrucella panencephalitis affecting the brain-stem. Abnormal wave V indicates involvement of the upper brain-stem with symptomatic or silent lesions. As it is irreversible on treatment, this abnormality could reflect ischaemic damage due to vasculitis or

demyelinating lesions. Both types of lesion have been reported in neurobrucellosis (Nelson-Jones 195l; Fincham et al. 1963; Sahs 19781. Abnormal wave I indicates cochlear nerve damage or necrosis which might be due to direct invasion of the cochlear nerve by the brucella or its endotoxins, or to long-standing compression of the cochlear nerve caused by the meningitis (Fincham et al. 19631. Lack of improvement of some BAEP abnormalities is of bad prognosis for the cochlear nerve function (wave I abnormalities) and neurological symptomatology (wave V abnormalities), Patients with wave V abnormalities did not fully recover. This supports the clinical observation that patients with vasculitis or demyelination are usually left with sequelae (AI-Deeb et al. 1988, 19891. The high incidence of BAEP abnormalities in brucella meningitis has not been described in other types of meningitis such as tuberculous or aseptic meningitis both of which have similar clinical and CSF features, so these findings are of diagnostic value in pointing to brucella meningitis. In conclusion, BAEPs are a useful non-invasive diagnostic tool to indicate nervous system involvement in patients with systemic brucellosis. They are important in predicting outcome after therapy. Also they might be of some help to differentiate brucella meningitis from other types of aseptic and tuberculous meningitis when the culture and CSF parameters are inconclusive or not yet available. We thank Dr. Saleh AI-Deeb, Head of Neurology, Department of Neuroscience at Riyadh A r m e d Forces Hospital, for critical comment and advice in preparing the manuscript. And we also thank Ms Miguela de la Fuente for performing the evoked potentials and Ms Lydia Gallardo and Ms Clarina de Venancio for excellent secretarial assistance.

References

AI-Deeb, S.M., Yaqub, B.A., Sharif, H,S. and AI-Rajeh, S.M. Neurobrucellosis. In: P.J. Vinken, G.W. Bruyn and H.L. Klawans (Eds.), Handbook of Clinical Neurology, Vol. 8(52). Elsevier/North-Holland, Amsterdam, 1988: 581-601. AI-Deeb, S.M., Yaqub, B.A., Sharif, H.S. and Phadke, J.G. Neurobrucellosis: clinical characteristics, diagnosis, and outcome. Neurology, 1989, 39: 498-501. Bashir, R., AI-Kawi, M.Z., Harder, E.Z. et al. Nervous system brucellosis: diagnosis and treatment. Neurology, 1985, 35: 15761581. Fincham, R.W., Sahs, A . L and Joynt, P.J. Protein manifestation of nervous system brucellosis. J. Am. Med. Ass., 1963, 184: 269-276. Kambal, A.M., Mahgoub, E.S., Jamjoom, G.A. and Choudry, M.H. Brucellosis in Riyadh, Saudi Arabia: a microbiological and clinical study. Trans. Roy. Soc. Trop. Med. Hyg., 1983, 7: 820-824. Kuraibet, A., Shakir, R., Trontely, J., Butinar, D. and AI-Dim A. Brainstem auditory evoked potential (BAEP) abnormalities in brucellosis. J. Neurol. Sci., 1988, 87: 307-313.

552 Lulu, A.R., Araj, G.G., Khateeb, M.I., Mustafa, M.Y., Yusuf, A.R. and Fenech, F.F. Human brucellosis in Kuwait: a prospective study of 400 cases. Quart. J. Med., 1988, 249: 39-54. Nelson-Jones, A. Neurological complications of undulant fever - the clinical picture. Lancet, 1951, i: 495-498.

B.A. YAQUB ET AL. Sahs, A.L. Malta fever, undulant fever. In: P.J. Vinken and G.W. Bruyn (Eds.), Handbook of Clinical Neurology. Elsevier/NorthHolland, Amsterdam, 1978: 305-326. Shakir, R.A., AI-Din, A.S. and Arajetal, G.F. Clinical categories of neurobrucellosis. Brain, 1987, 110: 213-223.

Diagnostic role of brain-stem auditory evoked potentials in neurobrucellosis.

Evoked potential audiometry and brain-stem auditory evoked potentials were evaluated in 15 patients with systemic brucellosis in whom brucella meningi...
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