The authors have declared that no competing interests exist.
Conceived and designed the experiments: JFdMC DUG JRL. Performed the experiments: JFdMC LL PHDC MSFM. Analyzed the data: JFdMC LL LDdO. Contributed reagents/materials/analysis tools: DUG JRL. Wrote the paper: JFdMC DUG LL LDO GVdMT TdAP PHDC JRL.
‡ DUG and JRL are joint senior authors.
Schistosomal myeloradiculopathy (SMR), the most severe and disabling ectopic form of
A cross-sectional comparative study enrolled 22 patients with definite SMR and 22 healthy controls that were submitted to clinical, neurological examination and GVS. Galvanic stimulus was applied in the mastoid bones in a transcranial configuration for testing VEMP, which was recorded by electromyography (EMG) in the gastrocnemii muscles. The VEMP variables of interest were blindly measured by two independent examiners. They were the short-latency (SL) and the medium-latency (ML) components of the biphasic EMG wave.
VEMP showed the components SL (p = 0.001) and ML (p<0.001) delayed in SMR compared to controls. The delay of SL (p = 0.010) and of ML (p = 0.020) was associated with gait dysfunction.
VEMP triggered by GVS identified alterations in patients with SMR and provided additional functional information that justifies its use as a supplementary test in motor myelopathies.
Schistosomal myeloradiculopathy is a rare and severe form of schistosomiasis caused by
Schistosomal myeloradiculopathy (SMR) is the most severe and disabling ectopic form of
In the acute phase of SMR, the patients present with lumbar and/or lower limbs pain, generally associated with sensitive and motor alterations of lower limbs as well as bladder, intestinal and sexual dysfunctions. If not promptly and adequately diagnosed and treated, the patients remain with serious spinal cord injury sequelae, commonly handicapped, and eventually die because of infectious complications [
There is no consensus about the recommended doses and duration of steroid therapy [
Galvanic vestibular stimulation (GVS) is a simple, safe, low-cost and easily reproducible technique used to trigger the vestibular evoked myogenic potential (VEMP) [
VEMP recorded in the soleus or gastrocnemius muscle produces a biphasic EMG wave, with the short-latency (SL) component initiating at approximately 60ms after stimulus onset, followed by the medium-latency (ML) component, which initiates at around 100ms after stimulus onset and is in the opposite polarity of the SL [
The aim of this study was to investigate the spinal cord function of patients with SMR using VEMP with GVS. The results were compared to those of a healthy control group and were crossed with data from neurological examination.
The Ethics Committee of Federal University of Minas Gerais, Brazil, approved this study (protocol n° 11895813.1.00005149) and it was conducted according to the principles expressed in the Declaration of Helsinki. All subjects gave their informed and written consent.
This was a comparative cross-sectional study that enrolled 22 patients with SMR and 22 healthy controls. It was performed between September 2013 and August 2014 at the infectious diseases outpatient clinic of Federal University of Minas Gerais, in Belo Horizonte, Brazil.
The group with SMR consisted of 22 patients with definite diagnosis following these criteria: clinical manifestations of myelopathy or myeloradiculopathy; evidence of exposure to
The 22 included patients were under follow-up at the infectious diseases outpatient clinic of Universidade Federal de Minas Gerais. They had been treated in the acute phase of SMR with praziquantel 50mg/kg and with prednisone 1mg/kg/day for 6 months [
The control group consisted of 22 healthy adults, asymptomatic and with no diagnosis of either acute or chronic diseases that could bring physical or psychological limitations. In addition, they had no history of admission to inpatient care facilities for the previous 6 months. Exclusion criteria were vertigo complaints and/or abnormal neurological examination.
All participants (n = 44) were submitted to anamnesis, clinical and neurological examination. Patients with urinary dysfunction were submitted to urodynamics to confirm neurogenic bladder. Neurogenic bowel was clinically diagnosed if patients presented fecal incontinence and/or fecal constipation with regular need for laxatives, enema or manual maneuvers. Erectile dysfunction was defined according to the Sexual Health Inventory for Men (SHIM) [
GVS was characterized by a direct monophasic and rectangular 2mA current with pulses of 400ms (model EvP4/ATCPlus, Contronic Ltd., BR). A bipolar current was applied on mastoid bone processes using self-adhesives surface electrodes, with a diameter of 3cm (model CF3200, Valutrode, Axelgaard, Fallbrook, CA, USA). For transmastoid binaural stimulation, both polarities of current were used: cathode right, anode left (CRAL) and cathode left, anode right (CLAR). One trial consisted of 15 CRAL stimuli and then 15 CLAR stimuli, being the inter-stimuli interval randomized between 4 and 5 seconds. Each participant underwent two trials for the right leg and two trials for the left leg [
GVS trigged VEMP and the EMG responses were recorded in the gastrocnemius muscle using self-adhesive surface electrodes (model 2223BRQ, 3M, Saint Paul, MN, USA) and one recording channel. The two recording electrodes were vertically placed approximately 5 cm below the popliteal fossa, at a distance of approximately 5 cm between their centers. The reference electrode was placed in the back of the thigh, approximately 5 cm above the recording electrodes. Gastrocnemius was chosen over soleus muscle because of the grater amplitude of the EMG waves [
During the GVS procedures, subjects remained standing barefoot on a flat surface, with their eyes closed, feet close together and their bodies leaning forward. This position induces the gastrocnemii muscles to keep the contraction and engagement in balance control, which is essential for better evoked responses [
An EMG response with onset between 40 and 90ms that inverted with reversal of the stimulus was identified as the SL component. The ML component was subsequent to SL, opposite in polarity and with greater amplitude and duration, occurring at least 90ms after stimulus onset. With the superimposition of the traces with inverted polarity, the point where traces diverged from the EMG baseline marked the onsets of SL and ML, judged visually and measured by the cursor. The first traces-divergence was marked as the onset of SL component. In sequence, traces returned to baseline and diverged again. The second traces-divergence marked the onset of ML component (
(A) Normal responses: superimposed traces of two polarities (cathode right anode left and then cathode left and anode right) reveal inversion of waves and define short-latency (SL) and medium-latency (ML) onsets points. The continuous vertical thick line indicates the galvanic vestibular stimulus onset. (B) Abnormal responses: no identification of SL or ML waves.
Sample size was calculated
EpiData (EpiData Data Entry, Data Management and basic Statistical Analysis System. Odense Denmark, EpiData Association, 2000–2008) was used to build the data bank and SPSS version 15.0 (SPSS, Inc., Chicago, IL, USA) was used for all statistical analyses. Double entered data had asymmetric distribution for all continuous variables, but height (Shapiro-Wilk test). Therefore, non-parametric tests were used for all analyses (Mann-Whitney test for independent samples, Wilcoxson test for dependent samples, Spearman for correlation), with the exception of Student T test for comparison of height between groups. ROC curve was done to analyze the diagnostic performance of SL and ML. The confounders were controlled by linear regression. The level of significance was 5%.
The potential confounders age [
Among the 22 patients with SMR, 17 were male (77%) and the ages varied between 20 and 70 years (median: 42, interquartile range: 28–52). The control group consisted of 22 healthy individuals, 12 male (55%), with ages between 19 to 70 years (median: 30, interquartile range: 26–44). Clinical characteristics of both groups are described and compared in
Variable | Patients with SMR (n = 22) | Controls (n = 22) | P value |
---|---|---|---|
Age (years) | 41.5 [28.0/ 51.5] | 30.0 [25.8/ 43.8] | 0.162 |
Men | 17 (77) | 12 (55) | 0.203 |
Women | 5 (23) | 10 (46) | 0.203 |
Weight (kg) | 70.75 [61.13/ 86.50] | 71.00 [59.75/ 84.25] | 0.707 |
Height (m) | 1.69 ± 0.10 | 1.71 ± 0.08 | 0.432 |
Body mass index | 25.3 [22.3/ 27.7] | 24.5 [21.4/ 28.0] | 0.534 |
Data are expressed in median [interquartile range], mean value ±standard deviation or absolute numbers (percentage).
Time of SMR diagnosis ranged from one month to 16 years (median: 61 months, interquartile range: 27–144). Manifestations/sequelae of each patient with SMR are described in
Clinical manifestations of SMR | N° of patients (%) |
---|---|
2 (9) | |
9 (41) | |
11 (50) | |
12 (55) | |
13 (59) | |
14 (64) | |
10 (59) | |
15 (68) | |
15 (68) | |
16 (73) |
Affected spinal cord segments |
N° of patients (%) | |||
---|---|---|---|---|
Yes | No | No available data | Total | |
T1-T6 | 3 (13.6) | 12 (54.5) | 7 (31.8) | 22 (100.0) |
T7-T12 | 8 (36.4) | 7 (31.8) | 7 (31.8) | 22 (100.0) |
Conus | 11 (50) | 5 (22.7) | 6 (27.3) | 22 (100.0) |
Cauda equine | 4 (18.2) | 10 (45.5) | 8 (36.4) | 22 (100.0) |
*According to sensitive level and MRI done in the acute phase
SL and ML responses were delayed in patients with SMR compared to controls (
VEMP | Examiner | Healthy controls (n = 22) | Patients with SMR (n = 22) | p value |
---|---|---|---|---|
median and quartiles (milliseconds) | ||||
SL | A | 58.73 [55.57/ 60.94] | 63.77 [59.68/ 74.18] | 0.001 |
B | 52.35 [49.20/ 56.80] | 58.10 [54.30/ 61.80] | 0.003 | |
ML | A | 108.57 [105.72 / 121.44] | 137.57 [122.43/ 152.71] | <0.001 |
B | 121.55 [101.23/ 133.70] | 130.35 [123.60/ 164.00] | 0.012 |
The SL (p = 0.010) and ML (p = 0.024) were more delayed in patients with gait disturbance in the SMR group. No other alteration in the neurological examination was associated with delay in VEMP response.
Neurophysiology techniques are usually used for assessing spinal cord injury, including motor evoked potential with transcranial magnetic stimulation, somatosensory evoked potentials, electroneuromyography, nerve-conduction studies, and motor-evoked potentials as the VEMP [
VEMP using acoustic stimulation was shown to be altered in 10 out of 29 (34%) patients with definite SMR [
The alteration of VEMP in the lower limbs that was triggered by GVS indicates dysfunction in the reticulospinal and the vestibulospinal tracts, which are located in the anterior and lateral spinal cord [
The patients with SMR that could not stand were not included, because EMG responses were recorded in the muscles engaged in the maintenance of standing posture. It is possible to record EMG responses from erectors spinae muscles following GVS in sitting patients. In fact, this study was already done to define the level of spinal cord injury [
The diagnosis of acute SMR is based on clinical signs and symptoms, parasitological confirmation and MRI [
In conclusion, the SL and ML components of VEMP triggered by GVS and recorded in the lower limbs were delayed or absent in patients with SMR, especially in those with gait disturbance. The component ML was more accurate than the SL component. These results showed that VEMP triggered by GVS identified vestibulospinal deficit in patients with SMR. The use of this exam may improve prediction and monitoring of functional outcome during the treatment of SMR by providing additional information on the spinal cord of these patients.
CE: cauda equina *neurogenic bladder clinically diagnosed (patients refused to do urodynamics). #SHIM: Sexual Health Inventory for Men [1–7: severe erectile dysfunction (ED); 8–11: moderate ED; 12–16: mild to moderate ED; 17–21: mild ED; 22–25: no ED] [
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We would like to thank Dr. Sílvio Roberto de Sousa Pereira and Dr. Luciana Cristina dos Santos Silva for their support and advice.