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| ORIGINAL ARTICLE |
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| Year : 2023 | Volume
: 40
| Issue : 1 | Page : 20-26 |
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Impact of the coronavirus disease 2019 pandemic on the patient profile evaluated in the electromyography laboratory
Irem Ilgezdi Kaya, Meltem Inci, Nermin Gorkem Sirin, Mehmet Baris Baslo, Elif Kocasoy Orhan
Department of Neurology and Clinical Neurophysiology, Istanbul Faculty of Medicine, Istanbul University, Istanbul, Turkey
| Date of Submission | 24-Jul-2022 |
| Date of Decision | 10-Jan-2023 |
| Date of Acceptance | 20-Jan-2023 |
| Date of Web Publication | 29-Mar-2023 |
Correspondence Address:
Irem Ilgezdi Kaya
Department of Neurology and Clinical Neurophysiology, Istanbul Faculty of Medicine, Istanbul University, Istanbul
Turkey
 Source of Support: None, Conflict of Interest: None
DOI: 10.4103/nsn.nsn_135_22
Objective: The objective of this study was to evaluate how the coronavirus disease 2019 pandemic affected the profile of patients admitted to the electromyography (EMG) laboratory and the types of neurophysiologic evaluations.
Methods: We included patients who were admitted to our EMG laboratory in the first 6 months of the pandemic period (Period 1) and the same 6 months of the previous year (Period 2). In view of changes in health-care strategies, lockdown, and disease awareness during the pandemic, each group was divided into 3-month periods (early and late). Demographic and clinical characteristics and electrophysiologic data were evaluated retrospectively and compared between the groups.
Results: In Period 1, there were 1872 studies of 1829 patients, and in Period 2, there were 625 studies of 607 patients. Electrodiagnoses for cranial neuropathies were more frequent during the pandemic when compared with before the pandemic (P = 0.018). The subgroup analysis revealed that the ratio of segmental anterior horn involvement decreased in the early pandemic period (P = 0.003), myopathies decreased in the late pandemic period (P = 0.001), and cranial neuropathies increased in the late pandemic period (P = 0.005) compared with the same periods in the previous year.
Conclusion: During the pandemic, there have been changes in clinical practice approaches in the electrophysiology laboratory. More cranial neuropathies seemed to be diagnosed in the EMG laboratory during the pandemic, including new-onset facial neuropathies, which was the most significant finding of our study.
Keywords: Coronavirus disease 2019, electromyography, electrophysiology laboratory, pandemic, peripheral neurologic diseases
How to cite this article:
Kaya II, Inci M, Sirin NG, Baslo MB, Orhan EK. Impact of the coronavirus disease 2019 pandemic on the patient profile evaluated in the electromyography laboratory. Neurol Sci Neurophysiol 2023;40:20-6 |
How to cite this URL:
Kaya II, Inci M, Sirin NG, Baslo MB, Orhan EK. Impact of the coronavirus disease 2019 pandemic on the patient profile evaluated in the electromyography laboratory. Neurol Sci Neurophysiol [serial online] 2023 [cited 2023 Jun 10];40:20-6. Available from: http://www.nsnjournal.org/text.asp?2023/40/1/20/372780 |
| Introduction | |  |
Coronavirus disease 2019 (COVID-19) is an infectious disease caused by severe acute respiratory syndrome virus 2. The first case was detected in Wuhan, China, in December 2019. The disease quickly spread in a short time and caused a pandemic. The first patient infected with COVID-19 was announced in Turkey on March 11, 2020.
In parallel with the changes in the social, psychological, and economic fields caused by the pandemic, various strategies have been developed for the health-care system in many countries. In Turkey, following the first case, the use of diagnostic tests quickly became widespread and the health-care system was revised in short intervals with the increase in the number of patients. A constitution of guidelines on rules for health-care providers and patients, triaging of outpatients, limiting outpatient services due to COVID-19, reorganized services for patients with COVID-19 in hospitals, lockdowns, travel restrictions, and finally, vaccination programs were among these strategies.
In addition to the factors previously described, neurologic involvement due to COVID-19 also had an impact on the number and the profile of patients evaluated in neurology wards, as well as practical approaches in electrophysiology laboratories. This study aimed to provide information about the profile of the patients admitted to the electromyography (EMG) laboratory of our clinical neurophysiology department before and during the pandemic and evaluate how the pandemic affected the neurophysiologic approaches of our laboratory.
Methods
Patients who were admitted to our EMG laboratory in the first 6 months of the pandemic and the same 6 months of the previous year were included in the study. All electrophysiologic studies of each patient performed on different days and the same period were included. Patients who were admitted between March and August 2019 were determined as being in the period before the pandemic (Period 1), and those admitted between March and August 2020 were during the pandemic (Period 2). In view of changes in health-care strategy, lockdowns, and disease awareness during the pandemic, each group was divided into 3-month periods, “Subgroup 1” for March–May 2019, “Subgroup 2” for June–August 2019, “Subgroup 3–early pandemic” for March–May 2020, and “Subgroup 4–late pandemic” for June–August 2020 [Figure 1]. Demographic and clinical characteristics of patients such as age, sex, presentation date to the laboratory, symptoms, the types and results of electrophysiologic examinations, and the number of pathologies detected were obtained from the medical records and evaluated retrospectively. | Figure 1: Timeline of the study. Prepandemic and pandemic groups are marked in the figure
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Period 1
Patients were evaluated with three EMG devices in three different rooms. A single companion was allowed in the laboratory. After taking a careful history and performing a detailed neurologic examination, an electrodiagnostic study was planned and performed in the presence of one technician and one physician. In the period before the pandemic, approximately 300–350 patients/month, aged between 1 month and 90 years, who were admitted from the outpatient clinic, inpatient wards, and emergency wards were evaluated in the EMG laboratory.
Period 2
Laboratory conditions were arranged according to the guide named “Rules to be observed/followed in EMG investigations during the COVID-19 outbreak” published on the web page of the Turkish Clinical Neurophysiology Electroencephalogram-EMG Association on April 10, 2020.[1] During the pandemic, patients with urgent and acute conditions were prioritized, and appointments for elective cases were postponed. Patients were checked for COVID-19 symptoms using a questionnaire before being admitted to the laboratory. Electrophysiologic examinations were not performed for those with symptoms of infection, but COVID-19 tests could not be performed either because testing was not common at that time. Permission and informed consent forms were obtained from all patients.
Wearing masks was mandatory for the patients and companions, and hand hygiene was recommended. All patients except children and patients with disabilities were admitted to the laboratory unaccompanied. Two EMG devices were used during the pandemic. EMG equipment was wrapped with cling film daily. EMG rooms were regularly ventilated. As much as possible, different devices were used for outpatients and inpatients. Health-care workers were questioned daily in terms of COVID-19 symptoms. Personal protective equipment such as disposable aprons, bonnets, goggles, face shields, masks, and gloves was provided for the physicians and technicians before taking patients into the laboratory. Electrodiagnostic studies were planned as quickly as possible to provide sufficient information for the differential diagnosis.
Electrophysiology evaluations
The electrophysiologic studies of patients were planned according to the prediagnosis and neurological evaluation before and during the pandemic. These studies included nerve conduction studies (NCS), needle EMG, autonomic tests, tests for the evaluation of neuromuscular junction disorders such as repetitive nerve stimulation and single-fiber EMG, evoked potential tests, reflex studies, surface EMG recordings for movement disorders, and sphincter EMG.
Electrophysiologic diagnoses were classified by experienced clinic neurophysiologists as polyneuropathies (acute or chronic), peripheral neuropathies (traumatic or nontraumatic), motor neuron diseases (segmental or diffuse involvement), radiculopathies (cervical or lumbar), plexopathies (brachial or lumbosacral), myopathies, neuromuscular junction diseases, movement disorders, cranial neuropathies (optic, trigeminal, facial, and accessory nerve), and abnormalities in somatosensorial or motor evoked potential tests.
Statistical analysis
Statistical analysis was performed using the SPSS program version 21.0 (IBM, Armonk, New York, USA). Results are given as means, standard deviations, ranges for continuous variables, and percentages and counts for categorical variables. Between-group comparisons for continuous variables were performed using Student's t-test for the before-pandemic and pandemic groups. The Chi-square test was used for categorical variables. P < 0.05 was considered statistically significant.
An informed consent form was obtained from each patient. The local ethics committee and the Turkish Ministry of Health approved the study (April 17, 2020, number 2020/517).
| Results | | |
Before-pandemic versus pandemic period
One thousand eight hundred seventy-two studies of 1829 patients in Period 1 and 625 studies of 607 patients in Period 2 were evaluated. There were 1341 (55%) female patients. In Period 1, 1015 (55.5%) patients were female, and in Period 2, 326 (53.7%) patients were female. There was no significant sex difference in the subgroups (P > 0.05). The demographic data of the patients are summarized in [Table 1]. The electrophysiologic studies in Period 1 consisted of 1714 NCS, 1015 needle EMG, 28 autonomic tests, 72 repetitive nerve stimulations, 124 single-fiber EMGs, 36 evoked potential tests, 6 reflex studies, 1 surface EMG recording, and 2 sphincter EMGs. In Period 2, the studies comprised 553 NCS, 359 needle EMGs, 15 autonomic tests, 19 repetitive nerve stimulations, 39 single-fiber EMGs, 27 evoked potential tests, 2 reflex studies, and 1 sphincter EMG; no surface EMG recordings were performed. Electrodiagnoses for cranial neuropathies were higher during the pandemic when compared with before the pandemic (29/625, 4.6% and 50/1872, 2.7%, respectively, P = 0.018).
Subgroup analysis of the before-pandemic period and the early and late pandemic periods
The number of patients, types of neurophysiologic studies, and electrodiagnoses according to the predetermined subgroups are presented in [Table 2]. The number of normal examinations was higher in Subgroup 2 compared with the late pandemic period (Subgroup 4) (P = 0.015). The ratio of segmental anterior horn involvement, lumbosacral radiculopathies, myopathies, and cranial neuropathies was found to be statistically significant between subgroups (P = 0.003, P = 0.002, P = 0.001, and P = 0.005, respectively). The analysis revealed that the ratio of segmental anterior horn involvement decreased in the early pandemic period (Subgroup 3) compared with Subgroup 1 (P = 0.003), myopathies decreased in the late pandemic period (Subgroup 4) compared with Subgroup 2 (P = 0.001), cranial neuropathies increased in the late pandemic period (Subgroup 4) compared with Subgroup 2 (P = 0.005), and there were fewer lumbosacral radiculopathies before the pandemic (Subgroup 2) compared with Subgroup 4 (P = 0.002). | Table 2: Three months analysis of demographic and laboratory data before and during the pandemic
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Cranial neuropathies during the pandemic
Because of the increased number of studies with cranial neuropathies during the pandemic, we evaluated the clinical characteristics of the patients. In the pandemic, a total of 17 patients had 20 EMG studies for facial neuropathies due to recurrent studies in 2 patients (1 patient with 2 studies and the other 1 with 3 studies). Among the patients with facial neuropathies, all had acute or subacute symptoms, except one with congenital facial paralysis and two with symptoms that they had had for a year. The remaining nine studies for cranial neuropathy were visual evoked potentials performed in nine patients. The electrodiagnosis of optic neuropathy was performed to diagnose chronic symptomatic or asymptomatic demyelinating lesions in seven of nine patients.
| Discussion | | |
In this study, we aimed to evaluate the effect of the COVID-19 pandemic on the electrodiagnoses in our neurophysiology laboratory. As expected, the number of patients and electrophysiologic studies during the pandemic were significantly decreased when compared with the prepandemic period. The decrease in these parameters during the pandemic can be explained by the regulations on the electrophysiology laboratory conditions and recommendations on conservative approaches that reduced the hospital admissions of the patients. The number of abnormal examinations was higher during the pandemic compared with the same periods in the previous year, especially in the late pandemic period, which was statistically significant. This result may be because patients did not admit to the hospital unnecessarily during the pandemic, unlike those with severe symptoms. We also demonstrated that some electrophysiologic diagnoses increased and some decreased in the before-pandemic and pandemic periods. The electrophysiologic diagnoses of cranial neuropathies increased and myopathies decreased in the late pandemic period, and segmental anterior horn involvement decreased in the early pandemic period compared with the same months of the previous year.
We found a decrease in the number of studies in the first 3 months of the pandemic, which includes the lockdown, compared with before the pandemic and the second 3 months of the pandemic. In Turkey, after March 22, 2020, people aged over 65 years and those with various chronic diseases were restricted from leaving their homes. After April 3, 2020, this restriction was expanded to apply to those aged under 20 years. Lockdown was applied to all citizens after April 11, 2020. With the decrease in the number of cases, the restrictions were gradually relaxed and a “controlled social life” began after May 4, 2020. In our study, we examined the months of March–May and June–August for comparison with the previous year, taking into account the factors such as the high increase in the number of cases, the high level of uncertainty about the disease and lockdown, especially in the first 3 months of the pandemic. Considering the number of patients in our laboratory, a significant decrease was observed after March 17, 2020, even though there were no patient admissions between March 24 and April 3, 2020. After May 28, 2020, a gradual increase in inpatient admissions was observed.
In previous studies, the patients admitted to hospitals were younger during the pandemic compared with a year before.[2],[3] They suggested that social isolation, especially among the elderly due to the high risk of severe infection, might have caused this result. In our study, we observed that patients who were admitted to our laboratory in the late pandemic period were older than in the same period of the previous year. This could be related to the end of lockdown for people aged ≤ 20 and ≥65 years in the late pandemic period in our country.
COVID-19-associated neurologic manifestations began to be reported such as gustatory and olfactory disorders, myalgia, headache, impaired consciousness, encephalitis, toxic-metabolic encephalopathy, posterior reversible encephalopathy syndrome, epilepsy and seizures, cerebrovascular diseases, Guillain–Barre syndrome (GBS), myelitis, myositis, and peripheral nerve involvement.[4],[5],[6] Varatharaj et al. investigated the neurologic and neuropsychiatric complications associated with COVID-19 in the United Kingdom (UK) and they found peripheral nervous system complications in 5% of patients.[7] Most patients with peripheral nervous system involvement had gustatory and olfactory disorders and GBS.[4]
Olfactory and taste disorders are considered early manifestations of COVID-19 infections. Patients with isolated oculomotor, trochlear, and facial nerve damage have also been described.[8] Cranial neuropathies, including facial and optic neuropathy, increased in the late pandemic period compared with the previous year in our study. Codeluppi et al. compared patients who were diagnosed as having facial palsy in the first phase of the COVID-19 pandemic in Italy with the same period of the previous year and they found that the number of patients admitted to the emergency ward due to facial palsy during the pandemic was higher than before the pandemic; the rate of patients associated with infection was 9% in the prepandemic period and was 21% during the pandemic.[9] Lima et al. described eight patients who developed facial paralysis associated with COVID-19 infections.[10] In line with these studies, we observed an increase in cranial neuropathies, mainly with new-onset peripheral facial paralysis, examined during the pandemic compared with the previous year.
Although infections are known to be triggers for GBS, there is no consensus on the change in the incidence of GBS during the pandemic. Keddie et al. retrospectively investigated hospitalized patients with GBS from the UK National Immunoglobulin Database from January 1 to May 31, 2020, and compared them with patients with GBS from January 1 to May 31 from the NHS England immunoglobulin database between 2016 and 2019. In England, the first case was reported on January 31, there was no significant increase in the number of cases until March, and the highest number of cases before this study was reported on May 1. Therefore, they found that, contrary to expectations, between March and May 2020, the incidence of GBS decreased compared with the same months between 2016 and 2019.[11] In the international prospective cohort study of Luijiten et al., which investigated GBS after COVID-19 infections, 49 patients with GBS were included within the first 4 months of the pandemic, and of these, 8 (16%) were confirmed and 3 (6%) were possible COVID-19 infections. The authors suggested that it was not known whether this 22% prevalence might be due to the high prevalence of COVID-19 infection or COVID-19 increased risk for GBS. According to their ongoing International GBS Outcome Study, they observed no increase in the recruitment of patients with GBS compared with previous years.[12] Gigli et al. examined the frequency of GBS cases between March and April 2017–2019 and compared them with the same months in 2020. Contrary to the previous study, they found that there was a 5.41-fold increase in the number of cases in 2020 compared with the previous 3 years.[13] In our study, similar to many previous studies, we observed no increase in the number of examinations for GBS in the first 6 months of 2020 compared with the previous year. Even considering that the incidence of GBS typically decreases during the summer, the number of cases was not different between June and August 2020 compared with the previous year.
In our study, we found that the number of electrophysiologic examinations with myogenic changes decreased in the late pandemic period. It is known that coronavirus infections may be associated with myopathies. In two different COVID-19 studies from China, researchers found myalgia or fatigue in 44%–70% of hospitalized patients and creatinine kinase elevation in some of these patients.[14],[15] Agergaard et al. also demonstrated fatigue among patients with mild or moderate COVID-19 infections during long-term follow-up, all of whom showed myopathic changes on quantitative EMG. Therefore, they suggested that myopathy might be an important cause of fatigue in the long-term follow-up of COVID-19, even in nonhospitalized patients.[16] In addition, critical illness myopathy may develop in severe cases of COVID-19, especially in patients requiring long-term mechanical ventilation.[17] Although we expected to find that myopathies increased during the pandemic when compared with the previous year, we found the opposite in the 3–6 months after the beginning of the pandemic. At that time, the relationship between myopathy and fatigue after COVID-19 had not been recognized. The follow-up of patients after severe disease also lacked because of the high number of cases of severe COVID-19.
Although autoimmune diseases are expected to exacerbate with infection, the number of new-onset myasthenia gravis (MG) cases associated with COVID-19 is very limited. Huber et al. recently reported a case of a woman with post-COVID-19 MG with mild respiratory symptoms and anosmia/ageusia.[18] One study found that the risk of COVID-19 in patients with MG was not higher than in the general population, regardless of immunosuppressive treatments.[19] There are a small number of reports about exacerbation of preexisting MG due to COVID-19 infections.[8] We also observed no significant change in the number of electrophysiologic examinations for neuromuscular junction involvement.
In our study, we found that the number of studies for segmental anterior horn involvement decreased in the early pandemic period. We thought that this decrease was most likely due to the significant reorganization of the health system to cope with patients with COVID-19 in the early pandemic period and the fear of transmission of COVID-19 with hospital admissions.
Our study had several limitations. First, we did not include data such as medical histories and clinical features except electrophysiologic and demographic data. Second, the duration of electrophysiologic examinations in the laboratory was not examined. Third, we examined the patient profile in a dynamic process because the decisions taken for the health-care system during the pandemic were frequently updated, so it may not be appropriate to generalize our results. The fact that our electrophysiology laboratory is a reference center, the high number of patients evaluated before and during the pandemic, and the variety of examinations performed can be counted among the strengths of our study. For these reasons, we suggest that our data may accurately reflect the investigations of peripheral nervous system involvement during the pandemic.
| Conclusion | | |
The number of patients examined in our laboratory in the first 6 months of the COVID-19 pandemic decreased significantly compared with the same period of the previous year. Although COVID-19-related peripheral neurologic diseases have been reported in the literature, we did not detect a significant increase in most of the peripheral neurologic diseases examined in our laboratory during the pandemic compared with the previous year, except cranial neuropathies including facial and optic neuropathies.
Acknowledgments
The authors thank specially to Dr. Ayse Deniz Elmalı for her contribution in the programming of the study during the pandemic period.
Financial support and sponsorship
This study was funded by Scientific Research Projects Coordination Unit of Istanbul University. Project number: GAP-36802.
Conflicts of interest
There are no conflicts of interest.
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[Figure 1]
[Table 1], [Table 2]
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