Osmangazi Tıp Dergisi
Osmangazi Journal of Medicine 2022;
Hemorajik ve İskemik Serebrovasküler Hastalık
Tanısı Alan Hastalarda Kan Laktat Düzeyinin Prognoz
Evaluation
of Neuromuscular Functions in Hashimoto’s
Üzerine Etkisi
Thyroiditis
Research Article / Araştırma Makalesi
The Effect of Blood Lactate Level on Prognosis in Patients with
Hemorrhagic
Ischemic
Cerebrovascular
Hashimoto
Tiroiditindeand
Nöromusküler
Fonksiyonların
DeğerlendirilmesiDisease
Halil Güllüoğlu, Hasan Armağan Uysal
İD
Izmir University of Economics,
Medicalpoint Hospital Neurology
Department, Izmir, Turkey
İD
Abstract
Hashimoto’s thyroiditis is the most prevalent autoimmune thyroid disease with an increasing incidence. Although the exact causes
and pathogenesis of Hashimoto’s thyroiditis are not yet fully understood, the literature indicates complex interactions of immunologic, genetic, environmental, and epigenetic factors. It generally leads to hypothyroidism which can cause neuromuscular
problems including neuropathy and myopathy. Data on neuromuscular functions of Hashimoto’s thyroiditis patients are relatively
underreported and not up to date. The current observational study aimed to evaluate neuromuscular functions and sympathetic
skin responses (SSR) in patients with Hashimoto’s thyroiditis and compare them with healthy participants. In total, 50 patients
(25 females, 25 males; mean age, 31.6±4.9 years; range: 25-40 years) including 33 euthyroid, 10 with subclinical hypothyroidism,
and 7 with hypothyroidism were included. The control group consisted of 50 healthy individuals (25 females, 25 males; mean
age: 31.5±5.1 years; range, 25-40 years). Nerve conduction studies, repetitive nerve stimulation, SSRs and F wave recordings were
performed in all participants. There were significant differences in the mean SSR latency and amplitude both in the upper extremities (p<0.001 and p=0.013, respectively) and in the lower extremities (p=0.008 and p=0.002, respectively) in the comparison
groups. There was a significant difference in comparison groups regarding needle electroneuromyography (EMG) tests (p=0.012)
and 14% of the patients showed myogenic EMG findings. In addition, a significant correlation was found between EMG findings
and anti-TPO levels in the Hashimoto’s thyroiditis patients (r=0.453; p=0.001). No significant differences were found in the nerve
conduction studies, routine EMG tests, repetitive nerve stimulations or F wave recordings between patients and control groups.
Hashimoto’s thyroiditis, can cause negative influences on the proper functioning of neuromuscular systems. SSR, and electrophysiological tests may be beneficial for early detection and investigation of neuromuscular abnormalities in these patients.
Keywords: Hashimoto’s thyroiditis, neuromuscular problems, electromyography, autoimmune thyroid disease
Özet
Correspondence:
Halil GÜLLÜOĞLU
Izmir University of Economics,
Medicalpoint Hospital Neurology
Department, Izmir, Turkey
e-mail: gulluoglu35@yahoo.com
Hashimoto tiroiditi, görülme sıklığı artan en sık görülen otoimmün tiroid hastalığıdır. Hashimoto tiroiditinin kesin nedenleri ve
patogenezi henüz tam olarak anlaşılamamasına rağmen, literatür immünolojik, genetik, çevresel ve epigenetik faktörlerin karmaşık etkileşimlerini göstermektedir. Genellikle nöropati ve miyopati gibi nöromüsküler sorunlara neden olabilen hipotiroidizme
yol açar. Hashimoto tiroiditi hastalarının nöromüsküler fonksiyonlarına ilişkin veriler nispeten az rapor edilmiştir ve güncel değildir. Bu gözlemsel çalışma Hashimoto tiroiditi olan hastalarda nöromüsküler fonksiyonları ve sempatik deri yanıtlarını (SSR)
değerlendirmeyi ve sağlıklı katılımcılarla karşılaştırmayı amaçlamıştır. Çalışmaya 33 ötiroid, 10'u subklinik hipotiroidizmli, 7'si
hipotiroidizmli olmak üzere toplam 50 hasta (25 kadın, 25 erkek; yaş ortalaması 31.6±4.9 yıl; dağılım: 25-40 yıl) dahil edildi.
Kontrol grubu 50 sağlıklı bireyden (25 kadın, 25 erkek; yaş ortalaması: 31.5±5.1 yıl; dağılım: 25-40 yıl) oluşuyordu. Tüm katılımcılarda sinir iletim çalışmaları, tekrarlayan sinir stimülasyonu, SSRs ve F dalga kayıtları yapıldı. Karşılaştırma gruplarında hem üst
ekstremitelerde (sırasıyla p<0.001 ve p=0.013) hem de alt ekstremitelerde (sırasıyla p=0.008 ve p=0.002) ortalama SSR gecikmesi
ve genliğinde anlamlı farklılıklar vardı. Karşılaştırma gruplarında iğne elektronöromiyografi (EMG) testleri açısından anlamlı fark
vardı (p=0.012) ve hastaların %14'ünde miyojenik EMG bulguları saptandı. Ayrıca Hashimoto tiroiditli hastalarda EMG bulguları
ile anti-TPO düzeyleri arasında anlamlı korelasyon saptandı (r=0.453; p=0.001). Hastalar ve kontrol grupları arasında sinir iletim
çalışmalarında, rutin EMG testlerinde, tekrarlayan sinir stimülasyonlarında veya F dalgası kayıtlarında anlamlı fark saptanmadı.
Hashimoto tiroiditi, nöromüsküler sistemlerin düzgün çalışması üzerinde olumsuz etkilere neden olabilir. SSR ve elektrofizyolojik
testler, bu hastalarda nöromüsküler anormalliklerin erken tespiti ve araştırılması için faydalı olabilir.
Anahtar Kelimeler: Hashimoto tiroiditi, nöromüsküler problemler, elektromiyografi, otoimmün tiroid hastalığı
Caglayan T, Ozakin E, Ozdemir AO, Acar N, Canakci ME, Arslan E,Dolgun H, Kaya Baloglu F, The Effect of Blood Lactate Level
on Prognosis in
Patients with
Hemorrhagic and
Ischemic Cerebrovascular
Journal
of Medicine, 2021
Received
10.07.2022
Accepted
14.08.2022 Disease,
OnlineOsmangazi
published
16.08.2022
Doi: 10.20515/otd.796303
Gulluoglu H, Uysal HA Evaluation of Neuromuscular Functions in Hashimoto’s Thyroiditis, Osmangazi Journal of Medicine, 2022;44(6): 761-772 Doi: 10.20515/otd.1142946
761
Electrophysiology of Hashimoto's Thyroiditis
Electrophysiology of Hashimoto's Thyroiditis
1. Introduction
Hashimoto’s thyroiditis, also known as
chronic
lymphocytic
thyroiditis
or
autoimmune thyroiditis is the most prevalent
autoimmune thyroid disease with an
increasing incidence. Hashimoto’s thyroiditis
is characterized by enhanced thyroid volume,
lymphocyte infiltration of parenchyma, and
the presence of specific autoantibodies against
thyroid antigens, namely, thyroid peroxidase
(TPO) and thyroglobulin (TG) (1, 2).
Hashimoto’s thyroiditis is estimated to affect
about 10% of the general population, is
diagnosed in females up to ten times more
often than males; the frequency of disease
increases with age and it can also be seen in
children and even in infants (3, 4). Although
the exact causes and pathogenesis of
Hashimoto’s thyroiditis are not yet fully
understood, the literature indicates complex
interactions of immunologic, genetic,
environmental, and epigenetic factors.
Hashimoto’s thyroiditis can also coexist with
various other autoimmune disorders such as
type 1 diabetes, rheumatologic syndromes,
celiac disease, and multiple sclerosis (4, 5).
Hashimoto’s thyroiditis symptoms may
include weight gain, paresthesia, fatigue,
constipation, muscle weakness, cramps, hair
loss, infertility, and several psychological
problems and it generally leads to
hypothyroidism (4, 5). Among these, the role
of Hashimoto’s thyroiditis on the impairment
of neural and muscular functions of patients is
relatively underreported and not up to date,
therefore, further research is required to
address the issue. Neuromuscular problems
including neuropathy and myopathy are
common in patients with hypothyroidism with
up to 80% of patients complaining of
associated symptoms (6, 7). It has been
reported that almost one-third of patients with
hypothyroidism develop muscle weakness,
myalgia, fatigue, and muscle cramps (8) and
most of them may have mononeuropathy or
polyneuropathy because of axonal damage or
myelin involvement (9). The current study
aimed to evaluate neuromuscular functions
and sympathetic skin responses (SSR) in
patients with Hashimoto’s thyroiditis and
compare them with healthy participants.
2. Material and Methods
The present observational study was
conducted at Neurology Department of İzmir
University of Economics Medicalpoint
Hospital between January 2014 and December
2021. Patients with a diagnosis of
Hashimoto’s thyroiditis were included in the
study. All patients were examined for
systemic disorders such as diabetes mellitus,
vasculitis, rheumatic disease, malignancy, and
hematologic disorders and only the ones who
had not any of these concurrent systemic
problems were included. In total, 50 patients
(25 females, 25 males; mean age, 31.6±4.9;
range:25-40) including 33 euthyroid, 10 with
subclinical hypothyroidism, and 7 with
hypothyroidism were included in the study.
The control group consisted of 50 healthy
individuals (25 females, 25 males; mean age:
31.5±5.1 years; range, 25-40 years) with
similar age and sex profile to the patient group
and with no previous thyroid disorder any
current neurological disorder. The study was
approved by the Local Clinical Research
Ethics Committee. All participants included in
the study provided written informed consent.
Electrophysiological studies
Electrophysiological studies were conducted
using
the
Nihon
Kohden
(Japan)
Electromyograph measuring system (Model:
MEB-9400K).
All
study
participants
underwent electroneuromyography (EMG)
performed by a single physiatrist who was
blind to the patient groups. Distal motor
latencies and motor nerve conduction
velocities were calculated using disc surface
cup (Ag/AgCl) recording electrodes which
were 5 mm in diameter. Sensory conduction
velocity, sensory nerve action potential
amplitudes, and distal sensory latencies were
recorded using ring electrodes. Motor and
sensory conduction recordings of ulnar nerve;
motor and sensory conduction recordings of
median nerve; motor conduction recordings of
peroneal and tibial nerve, and sensory
conduction recordings of sural nerve were
performed. Needle EMG recordings were
performed with the left deltoid muscles and
rectus femoris muscles. Electrophysiological
parameters were assessed according to the
normal values of the laboratory. A minimum
762
Osmangazi Tıp Dergisi, 2022
Osmangazi Tıp Dergisi, 2022
ambient temperature of 25°C and distal
extremity skin temperature of >32°C were
conserved during all electrophysiological
studies.
Repetitive nerve stimulation
Repetitive nerve stimulations were recorded
from the orbicularis oris muscles. Ten stimuli
at 5 Hz stimulation frequency and 10 Hz
stimulation frequency were applied to the
facial nerve at the tragus, during rest and
every minute for 4 minutes after 30 seconds
exercise with maximal isometric muscle
contraction of the recording muscle. A
decrement of more than 10% between the first
and fourth motor response was considered as
positive. The decrement ratios between the
first and fourth (dec1-4) motor response were
calculated.
F wave recordings
F wave parameters including minimum f
latency, maximum f latency, f latency
chronodispersion, and f wave persistency
were studied in median, ulnar, peroneal, and
tibial nerves of all participants. Recording
electrodes placed on the belly tendon
montage, wave recording done from a relaxed
muscle. The stimulating cathode was proximal
to the anodal electrode to prevent anodal
block
Sympathetic Skin Responses
SSRs were recorded via the active electrodes
placed in the left palm and sole and the
reference electrodes on the dorsum of the left
hand and foot, by placing the participants in
the reclining position. A two-channel
recording from foot and hand as lower and
upper
extremities
were
obtained
simultaneously
by
stimulating
the
contralateral median nerve at the level of the
wrist. The stimulus was increased to just
above the threshold level and applied not
regularly to minimize habituation. Five
potentials were recorded and the mean values
were used for the analyses.
Statistical Analysis
Statistical analysis was performed using the
PASW Statistics for Windows, Version 18.0.
(SPSS Inc., Chicago, IL, USA). The
descriptive statistical data were expressed as
numbers and percentiles for categorical
variables and as mean, standard deviation,
median, and minimum-maximum (range) for
numerical variables. The normal distributions
of variables were tested by visual (histograms
and probability graphics) and analytical
(Kolmogorov-Smirnov/Shapiro-Wilk)
test
methods. For categorical variables, in two
group comparisons, the Chi-Square test was
used when appropriate. For numerical
variables, in two group comparisons, the
Mann-Whitney U test was used when data
were not normally distributed. The Student’s
T-test was used when numerical variables are
normally distributed. For the analysis of the
correlation between needle EMG findings and
free T3, free-T4, thyroid stimulating hormone
(TSH), anti-thyroid peroxidase (anti-TPO),
and anti-thyroglobulin (anti-TG) levels,
Spearman’s
correlation
analysis
was
performed for non-normally distributed
variables. A p value of <0.05 was set as
statistically significant.
3. Results
The study included a total of 100 participants,
of whom 50 had Hashimoto’s thyroiditis (33
patients with euthyroid, 10 patients with
subclinical hypothyroid, and 7 patients with
hypothyroid; mean age, 31.6±4.9 years) and
50 were healthy controls (mean age, 31.5±5.1
years). In the patient group, mean time since
the diagnosis of hypothyroidism was 5.1±3.0
years (minimum 1 year and maximum 10
years) and of the patients, 42% were using
levothyroxine, 30% have previous history of
levothyroxine, and 28% were not using
levothyroxine. The demographic and clinical
data and the comparison of these parameters
between patient and control groups are
summarized in Table 1. Accordingly, there
were no significant differences between
patient and control groups regarding sex
(p=1.000), age (p=0.937), height (p=0.894)
and
weight
(p=0.358).
Biochemistry
laboratory test results regarding Hashimoto’s
thyroiditis namely creatine kinase levels, free
T3 and T4 levels, TSH levels, anti-TPO
763
Electrophysiology of Hashimoto's Thyroiditis
Electrophysiology of Hashimoto's Thyroiditis
levels, anti-TG levels were compared between
patient and control groups. There were
elevated TSH levels (p=0.009), elevated antiTPO levels (p<0.001), and elevated anti-TG
levels (p<0.001) in the patient group as
compared with the control group with respect
to the normal laboratory range. The
differences in creatine kinase levels
(p=0.035), and free T3 (p=0.249) and T4
levels (p=0.354) between the patient and
control group were not significant.
Facial nerve decrement ratios of the
participants were compared between patient
and control groups. There was no significant
difference between the patient and control
groups in facial nerve decrement ratios (%)
between responses 1-4 for repetitive
stimulations both at 5 Hz (both patient and
control mean values were 5, p=0.579) and at
10 Hz (mean values were 8 and 6 for patient
and control groups, respectively; p=0.097)
frequencies.
F-wave recordings including minimum and
maximum
f-latency,
f-latency
chronodispersion and f-wave persistence in
median, ulnar, peroneal, and tibial nerves of
all participants were performed and are shown
in Table 2. F wave recordings of these nerves
were similar between the patient and control
groups (p>0.05 for all).
SSR and motor and sensory functions of
median nerve were measured in all
participants and the results are demonstrated
in Table 3. According to the collected data,
there were significant differences in the mean
SSR latency and amplitude both in the upper
extremities
(p<0.001
and
p=0.013,
respectively) and in the lower extremities
(p=0.008 and p=0.002, respectively) in the
comparison groups. For both upper and lower
extremities, mean SSR latency was higher and
mean SSR amplitude was lower in the patient
group than those of the control group. There
was no significant difference between the
patient and control groups in motor latency
(p=0.942), motor distal amplitude (p=0.874),
and motor velocity (p=0.485) values of the
median nerve. In addition, no significant
difference was found between the patient and
control groups in the sensory data of the
median nerve recorded for both thumb
(p=0.208, p=0.684, p=0.402 for latency,
764
amplitude and velocity values, respectively)
and index fingers (p=0.296, p=0.496, p=0.289
for latency, amplitude and velocity values,
respectively).
Motor and sensory functions of the ulnar
nerve were tested in all participants and the
findings are shown in Table 4. There was no
significant difference between the patient and
control groups in ring finger median-ulnar
sensory latency difference (p=0.447), motor
distal latency (p=0.772), motor amplitude of
below sulcus segment (p=0.981), motor
amplitude of above sulcus segment (p=0.970),
motor velocity of below sulcus segment
(p=0.740), motor velocity of above sulcus
segment (p=0.539), and sensory data
(p=0.972, p=0.959, p=0.505 as latency,
amplitude, and velocity, respectively) of the
ulnar nerve.
Nerve conduction studies of peroneal, tibial,
and sural nerves were performed in all
participants and the results are shown in Table
5. There was no significant difference
between the patient and control groups in
distal motor latency (p=0.948), and motor
amplitude (p=0.992; p=0.961) and motor
velocity (p=0.883; p=0.581) in the caput
fibula 2 cm distal and 9 cm proximal of the
peroneal nerve, respectively. Similarly, no
significant difference was found between the
patient and control groups in motor latency
(p=0.830), motor amplitude (p=0.841) and
motor velocity (p=0.567) parameters of the
tibial nerve, and in sensory latency (p=0.749),
sensory amplitude (p=0.646), and sensory
velocity (p=0.890) parameters of the sural
nerve. There was no significant difference
between the patient and control groups in
routine EMG tests (p=0.242), whereas there
was a significant difference in comparison
groups regarding needle EMG tests (p=0.012)
and 7% of the patients showed myogenic
EMG findings. Further, the correlation
analysis between the needle EMG findings
and free T3; free-T4; TSH; anti-TPO, and
anti-TG levels was performed in the patients
with Hashimoto’s thyroiditis (Table 6) and a
significant correlation was found between
EMG findings and anti-TPO levels (r=0.453;
p=0.001). No significant correlation was
found for the following parameters: free T3,
free-T4, TSH, and anti-TG levels.
25 (50.0)
25 (50.0)
31.5 ± 5.1
165.2 ± 3.6
64.2 ± 4.8
50 (100.0)
-
25 (50.0)
25 (50.0)
31.6 ± 4.9
165.3 ± 3.8
65.1 ± 4.7
33 (66.0)
10 (20.0)
Female
Male
Age, years, Mean±SD
Height, cm, Mean±SD
Weight, kg Mean±SD
Euthyroid, n (%)
Subclinical hypothyroidism, n (%)
102.5 (39-167)
2.7 (1.5-4.5)
1.3 (0.7-1.7)
3.515 (0.68-4.94)
3.4 (0.3-5.3)
3.1 (0.9-4.1)
125 (49-1588)
1.9 (1.1-4.5)
1.3 (0.2-1.7)
4.305 (0.68-11.2)
258.75 (4.3-1349)
78.55 (1.8-283.9)
Creatine kinase level, u/L (29-168), Mean (min-max)
Free T3, pg/mL (1.5-4.6), Mean (min-max)
Free T4, ng/dL (0.7-1.7), Mean (min-max)
TSH, miu/mL (0.35-4.94), Mean (min-max)
Anti-TPO, iu/mL (0-5.6), Mean (min-max)
Anti-TG, iu/mL (0-4.11), Mean (min-max)
765
<0.001***
<0.001***
0.009***
0.354***
0.249***
0.035***
N/A
N/A
N/A
0.358**
0.894**
0.937**
1.000*
p
SD: Standard deviation; N/A: Not applicable; *Chi-Square test; **Student’s T-test. ***Mann Whitney U test. T3: triiodothyronine; T4: thyroxine; TSH: thyroid stimulating hormone;
anti-TPO: anti-thyroid peroxidase; anti-TG: anti-thyroglobulin.
Hypothyroidism, n (%)
7 (14.0)
Sex, n (%)
Controls
N=50
Patients
N=50
Table 1. Demographic and clinical data of the patient and control groups
Osmangazi Tıp Dergisi, 2022
Osmangazi Tıp Dergisi, 2022
766
54.9 (49.9-58.9)
5.2 (4-6.4)
68 (50-81)
54.9 (49.9-61.7)
5.25 (4-7,4)
62 (43-81)
Tibial nerve maximum f latency, ms, should be maximum 51-59
Tibial nerve f latency chronodispersion (ms), should be maximum 6 ms
Tibial nerve f wave persistence, %
ms: milliseconds; *Mann Whitney U test; The descriptive statistical data are shown as median (minimum-maximum).
49.9 (45.5-52.5)
Peroneal nerve maximum f latency, ms, upper limit 52-58
50.2 (45.5-55.5)
54.2 (49.9-56.9)
54.85 (49.7-60.1)
Peroneal nerve minimum f latency, ms, upper limit 46-52
Tibial nerve minimum f latency, ms, should be maximum 45-53
49.1 (45.5-51.8)
49.6 (43.9-54.8)
Ulnar nerve f wave persistence, should be >50%
5 (3-6.3)
68 (50-81)
62 (50-81)
Ulnar nerve f latency chronodispersion, ms, should be maximum 4 ms
68 (50-81)
3.5 (2-4.1)
3.5 (2-5.9)
Ulnar nerve maximum f latency, ms, upper limit 31-33
62 (37-81)
30.6 (26.9-32.9)
30.9 (26.9-35.4)
Ulnar nerve minimum f latency, ms, upper limit 27-29
5.3 (3-8.7)
26.9 (23.8-28.9)
27.65 (23.8-31.1)
Median nerve f wave persistency, should be >50%
Peroneal nerve f wave persistence, %
68 (50-81)
65 (43-81)
Median nerve f latency chronodispersion, ms, should be <4 ms
Peroneal nerve f latency chronodispersion, ms, should be maximum 6 ms
3.1 (2-4)
Median nerve maximum f latency, ms, upper limit 30-34
27.5 (24.1-31.1)
24.1 (21.3-27.9)
25 (21.3-30.1)
Median nerve minimum f latency, ms, upper limit 26-28
3.35 (2-7)
N=50
N=50
28,8 (24.1-36.1)
Controls
Patients
Table 2. F-wave recordings of median, ulnar, peroneal and tibial nerves in patient and control groups
Electrophysiology of Hashimoto's Thyroiditis
0.480
0.340
0.204
0.209
0.498
0.062
0.066
0.103
0.543
0.152
0.069
0.082
0.474
0.132
0.058
0.052
p*
Electrophysiology of Hashimoto's Thyroiditis
767
2.2 (1.5-3.1)
1.415 (1.22-1.59)
1.6 (1.1-2.5)
3.61 (3.1-3.95)
18.7 (12.2-25.1)
55.6 (50.1-61.3)
3.1 (2.7-3.5)
20.7 (16.8-29.1)
53.55 (50.2-60.1)
3.2 (2.7-3.4)
20.15 (14.7-29.1)
53.5 (50.7-59.8)
2.025 (1.5-3.1)
1.5 (1.15-2.2)
1.3 (0.8-2.5)
3.61 (3.1-3.95)
18.7 (12.1-25.1)
54.4 (50.1-61.3)
3.2 (2.7-4.5)
20.5 (10.5-29.1)
52.9 (38.9-60.1)
3.25 (2.7-4.3)
19.4 (11.9-29.1)
53.4 (39.4-59.8)
Upper extremities sympathetic skin response (5 responses) mean latency, s (1.46±0.04)
Upper extremities sympathetic skin response (5 responses) mean amplitude, mV (2.5±0.3)
Lower extremities sympathetic skin response (5 responses) mean latency, s (1.4±0.07)
Lower extremities sympathetic skin response (5 responses) mean amplitude, mV (1.6±0.2)
Median nerve motor latency, ms
Median nerve motor distal amplitude, mV
Median nerve motor velocity, m/s
Median nerve sensory amplitude, mV, thumb
Median nerve sensory velocity, m/s, thumb
Median nerve sensory latency, ms, index finger
Median nerve sensory amplitude, mV, index finger
Median nerve sensory velocity, m/s, index finger
SSR: Sympathetic skin response; ms: milliseconds; mV: millivolt; *Mann Whitney U test; The descriptive statistical data are shown as median (minimum-maximum).
Median nerve sensory latency, ms, thumb
Controls
N=50
1.39 (1.18-1.55)
Patients
N=50
1.495 (1.18-2.5)
Table 3. Sympathetic skin responses, and motor and sensory conduction recordings of median nerve in patient and control groups
0.289
0.496
0.296
0.402
0.684
0.208
0.485
0.874
0.942
0.002
0.008
0.013
<0.001
p*
Osmangazi Tıp Dergisi, 2022
Osmangazi Tıp Dergisi, 2022
0.2 (0.1-0.3)
3.1 (2.8-3.6)
19.4 (14.3-27.8)
19.9 (15.1-26.8)
57.5 (50.3-62.5)
0.2 (0.1-0.5)
3.1 (2.8-3.6)
19.45 (12.3-27.8)
19.9 (14.1-27.5)
57.5 (50.3-62.5)
Ring finger median ulnar sensory latency difference (>0.3 is pathological)
Ulnar nerve motor distal latency, ms
Ulnar nerve motor amplitude, mV, below sulcus segment (5 cm distal)
Ulnar nerve motor amplitude, mV, above sulcus segment (5 cm proximal)
Ulnar nerve motor velocity, m/s, below sulcus segment
768
3.2 (2.7-3.8)
20.5 (14.9-30.3)
58.2 (51.6-67.4)
3.2 (2.7-3.8)
20.7 (14.9-30.3)
57.35 (50.1-67.4)
Ulnar nerve sensory amplitude, mV
Ulnar nerve sensory velocity, m/s
ms: milliseconds; mV: millivolt; *Mann Whitney U test; The descriptive statistical data are shown as median (minimum-maximum).
Ulnar nerve sensory latency, ms
65.7 (57.1-69.9)
65.1 (57.1-69.9)
Ulnar nerve motor velocity, m/s, above sulcus segment
Controls
N=50
Patients
N=50
Table 4. Motor and sensory conduction recordings of ulnar nerve in patient and control groups
Electrophysiology of Hashimoto's Thyroiditis
0.505
0.959
0.972
0.539
0.740
0.970
0.981
0.772
0.447
p*
Electrophysiology of Hashimoto's Thyroiditis
4.5 (3.9-5.2)
9.9 (6.7-15.2)
49.3 (45.4-55.4)
11.3 (7.3-17.3)
58.1 (54.3-62.4)
4.7 (3.7-5.2)
4.63 (3.8-5.2)
9.85 (4.7-15.2)
49.25 (45.4-55.4)
11.3 (5.3-17.3)
58.1 (54.1-62.4)
4.7 (3.7-5.2)
Peroneal nerve distal motor latency, ms
Peroneal nerve motor amplitude, mV, caput fibula 2 cm distal
Peroneal nerve motor amplitude, mV, caput fibula 9 cm proximal
Peroneal nerve motor velocity, m/s, caput fibula 9 cm proximal
769
50 (45.9-55.1)
4.1 (2.9-4.8)
18.6 (11.3-25.3)
49.65 (44.3-57.2)
49.7 (43.9-55.1)
4.15 (3.1-4.9)
18.6 (11.3-25.3)
49.65 (42.8-57.2)
Tibial nerve motor velocity, m/s
Sural nerve sensory latency, ms
Sural nerve sensory amplitude, mV
Sural nerve sensory velocity, m/s
ms: milliseconds; mV: millivolt; *Mann Whitney U test; The descriptive statistical data are shown as median (minimum-maximum).
11.05 (7.6-18.4)
10.9 (7.6-18.4)
Tibial nerve motor amplitude, mV
Tibial nerve motor latency, ms
Peroneal nerve motor velocity, m/s, caput fibula 2 cm distal
Controls
Patients
Table 5. Motor conduction recordings of peroneal and tibial nerve, and sensory conduction recordings of sural nerve in patient and control groups
0.890
0.646
0.749
0.567
0.841
0.830
0.581
0.961
0.833
0.992
0.948
p*
Osmangazi Tıp Dergisi, 2022
Osmangazi Tıp Dergisi, 2022
0.048
0.740
0.054
0.708
r
p*
Free T4
0.912
-0.016
TSH
In the present study, it was found that there was a significant difference in
SSRs between the patient and control groups. For both upper and lower
extremities, the mean SSR latencies were prolonged, and the mean SSR
amplitudes were decreased in the patient group than those of the healthy
control group implying the impairment of the sympathetic system function
in the patients compared to the controls. Consistently with the current
study, in a previous research, Merello et al. (10) reported that patients
with autoimmune hypothyroidism showed sudomotor dysfunctions
revealed by the abnormal SSR results likely be resulted from a destructed
autoimmune reaction. On the other hand, there are some other studies
found contrary results regarding SSR measurements. Gautam et al. (11)
and Ümit Yemişci et al. (7) found no significant alterations in SSRs
between hypothyroid patients and healthy controls in their research. SSR
is one of the most frequently used non-invasive techniques for the
evaluation of sympathetic fibers dysfunction in neuropathies and
sympathetic system disorders in other diseases. It is simple, fast, and easy
to apply; however, it has its methodical limitations similar to other
electrophysiological procedures (12, 13). In addition to these limitations,
variations in the characteristics of the patient groups, sample size, and the
stages of the disease may result in controversial SSR measurements.
4. Discussion
0.001
0.453
anti-TPO
0.160
0.202
anti-TG
770
Apart from SSR measurements, various electrophysiological tests
including repetitive stimulations of facial nerve; F-wave recordings of the
median, ulnar, peroneal, and tibial nerves; motor and sensory conduction
recordings of the median and ulnar nerve; motor conduction recordings of
the peroneal and tibial nerve, and sensory conduction recordings of the
sural nerve were performed to investigate any abnormalities in the patients
with Hashimoto’s thyroiditis. In all of these detailed tests, no significant
differences were found in the electrophysiological parameters between
patients and control groups. In a previous study, Ozata et al. (9) studied
the distal latency, nerve conduction velocity, and F responses in the
median and peroneal nerves, and they recorded sensory nerve conduction
Nevertheless, the literature lacks adequate data in terms of SSR in
immunologically mediated disorders which suggest the need for further
investigations of SSR in Hashimoto’s thyroiditis to have more comparable
and insightful clinical data (14). Although SSR alone cannot be used as a
diagnostic tool for autonomic dysfunction, it may be utilized in
combination with some other methods such as cardiovascular reflexes for
the evaluation of autonomic nervous system functions and before the
therapeutic interventions, as suggested previously (7, 10).
*Spearman’s correlation analysis. TSH: thyroid stimulating hormone; anti-TPO: anti-thyroid peroxidase; anti-TG: anti-thyroglobulin.
Needle EMG
Free T3
Table 6. Results of the correlation analysis between the needle electroneuromyography (EMG) findings and biochemistry laboratory test results in the patients with
Hashimoto’s thyroiditis
Electrophysiology of Hashimoto's Thyroiditis
Electrophysiology of Hashimoto's Thyroiditis
Osmangazi Tıp Dergisi, 2022
Osmangazi Tıp Dergisi, 2022
velocities and sensory potential amplitudes in
the sural and median nerves. As consistent
with the current study, they could not find any
significant
difference
in
the
electrophysiological data between patients
with subclinical hypothyroidism and controls
and they speculated that the results may be
associated with the early stage of the disease
in these patients. In another study, oppose to
these results, researchers measured some
extent of electromyographic variations, even
in the early stages of subclinical
hypothyroidism where they found motor
parameters were more affected in the longer
nerves and a higher proportion as compared to
the sensory nerves and the progression of
thyroid insufficiency was correlated with the
decline of the motor and sensory amplitudes
in all of the studied nerves (15). In two other
studies, the hypothyroidism patients displayed
a significant tendency of nerve conduction
slowness as compared with controls (16, 17).
Khedr
et
al.
(18)
recorded
electrophysiological measurements showing
that half of the hypothyroid patients had
peripheral nervous system involvement, and a
few of them had axonal neuropathy (9%) and
myopathy (9%). Similarly, in the current
study, 7 of the patients with Hashimoto’s
thyroiditis (14%) showed myogenic EMG
findings.
Furthermore,
a
significant
correlation was found between EMG findings
and anti-TPO levels in the patients, which
supports the association between Hashimoto’s
thyroiditis and neuromuscular disorders. In
addition, despite no statistical significance
between the groups, early phase carpal tunnel
syndrome was observed in three patients (6%
of the patients). It revealed the importance of
performing electrophysiological tests in
hypothyroid patients, even in the very early
stage of disease to detect the nervous system
involvement. Eslamian et al. (8) measured
similar electrophysiological abnormalities in
patients
with
untreated
spontaneous
hypothyroidism and suggested early treatment
to slow down the progression rate of the
neuromuscular complications or minimize
their formation.
As expected, there were elevated TSH levels,
anti-TPO, and anti-TG levels in the patient
group than those in the control group as the
indicators of Hashimoto’s thyroiditis and may
have possible effects on the functioning of the
neuromuscular system and thus on the
recordings. The differences in creatine kinase
levels and free T3 and T4 levels between the
patient and control group were not significant
and they may not interfere with the test
results.
The homogeneity of the comparison groups in
the current study was high with no significant
difference according to the demographic
features. Further, patients with no concurrent
disease were recruited in the study which
otherwise
may
interfere
recorded
neuromuscular data. This matching data
between patient and control groups and
specific selection of the patients enhances the
reliability of the data comparison and the
strength of the study. On the other hand,
coexisting systemic disorder free selection of
the study participants restricted the population
of the study and low number of participants in
both groups may be insufficient to record and
address all of the neuromuscular effects of
Hashimoto’s thyroiditis.
Even though the current study results did not
establish any significant difference in the
electrophysiological data of the patient and
healthy samples with the exception of SSRs
data, it seems that electrophysiological studies
may be useful as a tool in the case of early
detection of neuromuscular issues in
particular individuals with Hashimoto’s
thyroiditis.
In conclusion, it is well known that thyroid
hormones are the main regulators of human
metabolism and they are involved in many
processes and biological activities of the
neuromuscular
systems.
Hashimoto’s
thyroiditis, which results from impaired or
abnormal thyroid hormones, can cause
negative influences on the proper functioning
of
these
systems.
SSR
and
electrophysiological tests may be beneficial
for early detection and investigation of
neuromuscular abnormalities in patients with
Hashimoto’s thyroiditis.
771
Electrophysiology of Hashimoto's Thyroiditis
Electrophysiology of Hashimoto's Thyroiditis
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