key: cord-0788835-wthjgk1z authors: Lallana, Sofía; Fonseca, Elena; Restrepo, Juan Luis; Quintana, Manuel; Seijo‐Raposo, Iván; Abraira, Laura; Santamarina, Estevo; Álvarez‐Sabín, José; Toledo, Manuel title: Medium‐term effects of COVID‐19 pandemic on epilepsy: A follow‐up study date: 2021-04-27 journal: Acta Neurol Scand DOI: 10.1111/ane.13439 sha: 2a310cbb1a90730de71b0c05a40a84545a7f25e3 doc_id: 788835 cord_uid: wthjgk1z OBJECTIVE: To analyze the medium‐term impact of the COVID‐19 pandemic on epilepsy patients, focusing on psychological effects and seizure control. METHODS: Prospective follow‐up study to evaluate the medium‐term effects of the COVID‐19 pandemic on a cohort of epilepsy patients from a tertiary hospital previously surveyed during the first peak of the pandemic. Between July 1, 2020, and August 30, 2020, the patients answered an online 19‐item questionnaire, HADS, and PSIQ scales. Short‐ and medium‐term effects of the pandemic confinement and the perception of telemedicine were compared. RESULTS: 153 patients completed the questionnaire, mean ± SD age, 47.6 ± 19.3 years; 49.7% women. Depression was reported by 43 patients, significantly more prevalent than in the short‐term analysis (29.2% vs. 19.7%; p = .038). Anxiety (38.1% vs. 36.1%; p = 0.749) and insomnia (28.9% vs. 30.9%, p = .761) remained highly prevalent. Seventeen patients reported an increase in seizure frequency (11.1% vs. 9.1%, p = .515). The three factors independently associated with an increase in seizure frequency in the medium term were drug‐resistant epilepsy (odds ratio [OR] = 8.2, 95% CI 2.06–32.52), depression (OR = 6.46, 95% CI 1.80–23.11), and a reduction in income (OR = 5.47, 95% CI 1.51–19.88). A higher proportion of patients found telemedicine unsatisfactory (11.2% vs. 2.4%), and a lower percentage (44.8% vs. 56.8%) found it very satisfactory (p = .005). CONCLUSIONS: Depression rates increased significantly after the first wave. Depression, drug‐resistant epilepsy, and a reduction in family income were independent risk factors for an increased seizure frequency. Perception of telemedicine worsened, indicating need for re‐adaptation. Coronavirus disease 2019 (COVID- 19) , which is caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), has caused more than 2 million deaths worldwide since the first cases were reported in December 2019. 1, 2 This pandemic has presented the medical community and society with unprecedented challenges. To control the spread of the COVID-19 pandemic in Spain, the government imposed a nationwide lockdown that lasted from March 13, 2020, to June 20, 2020 . After this period, restrictions were gradually eased, giving way to a "new normal" characterized by curtailment of a wide range of everyday activities and new social distancing measures. 3 In August 2020, the cumulative 7-day incidence of COVID-19 in Spain was 78.2 cases per 100,000 inhabitants, with nearly 400,000 total cases and 30,000 deaths. 4 The healthcare system was striving to adapt to the new situation, while preparing for a probable second wave. The collapse of the emergency services in March and April 2020 had a major effect on urgent medical conditions such as heart attacks and stroke, causing treatment delays and increased morbidity and mortality rates. 5 Once a certain normalcy had been restored, studies on the medical and psychological effects of lockdown on patients with chronic illnesses began to emerge. 6, 7 The medical community has made enormous efforts to enable and promote the use of telemedicine as a safe way of monitoring patients with stable illness, 8 including those with chronic epilepsy, for whom an array of suitable new technologies exists. 9, 10 Although telemedicine still has a long way to go, it will certainly provide an essential alternative to traditional in-person visits for some time, and efforts must be made to ensure continued quality of care. Tertiary hospitals in Spain have adapted care protocols and procedures in many areas and prioritized the use of remote monitoring for patients with chronic disease. 11 Spanish studies of the impact of the pandemic and lockdown measures in the setting of epilepsy have mainly identified collateral effects, 12,13 although one recent study described a higher incidence of COVID-19 in patients with epilepsy than in those without, probably because of the higher proportion of dependent and institutionalized patients in this population. 14 A previous cross-sectional survey-based study by our group analyzing the short-term effects of the COVID-19 pandemic on epilepsy patients from a tertiary hospital in Barcelona, Spain, showed emerging lockdown-related symptoms such as anxiety and depression in addition to sleep disturbances and reduced family income. 15 Almost 10% of the patients reported an increase in seizure frequency, found to be independently associated with tumor-related epilepsy, drug-resistant epilepsy, insomnia, and reduced income. The general perception of telemedicine among the patients surveyed was positive. In this follow-up study, we analyzed the medium-term effects of the COVID-19 pandemic in the same cohort of patients, 15 with a focus on the psychological impact of the pandemic and lockdown and their possible association with seizure control. We also re-evaluated perceptions of telemedicine, which has since been incorporated into routine practice at our epilepsy unit. In a previous study, we evaluated the short-term effects of the COVID-19 pandemic in a cross-sectional survey of all patients from the epilepsy unit at Hospital Vall d'Hebron in Barcelona, Spain, who had received a telephone consultation during the first month of lockdown (March 16, 2020, to April 17, 2020) . Their in-person appointment had been canceled following the Spanish Government's declaration of a national state of emergency on March 14. 16 The full details of the study are described elsewhere. 15 In brief, patients aged 17 years or older with a definitive diagnosis of epilepsy according to the International League Against Epilepsy (ILAE) criteria 17 were consecutively included. Patients consulting for neurological symptoms other than seizure and patients/caregivers unable to answer the questionnaire were excluded. All epilepsies were classified according to the current ILAE classification. 18 Information on antiepileptic drug (AED) treatment, mean baseline seizure frequency, and drug resistance was obtained from medical records. A note was also made of modified Rankin scale score, intellectual disability, dysphagia, and demographic data, including current living and employment situation. All the consultations were performed by an epileptologist by telephone. The patients or their caregivers were then administered a 19-item telephone survey by a neurologist. The follow-up study to assess the medium-term effects of the pandemic on the same cohort of patients was performed between July 1, 2020, and August 30, 2020. Patients who had died were excluded from the analysis and cause of death recorded. Those who could not be contacted, were unwilling to participate, or did not complete the follow-up survey were also excluded. A link to access the online survey was sent by email following telephone contact with a neurologist to obtain consent. When contact by email was not possible (because of personal limitations or Internet access problems), the survey was administered directly to the patient or caregiver by telephone by a neurologist. The online survey consisted of three questionnaires: the 19-item questionnaire used in the first study, the Hospital Anxiety and The statistical analyses were performed in the IBM SPSS Statistics We analyzed data for 153 of the 255 epilepsy patients who participated in the initial study on the short-term effects of the COVID-19 panedmic. 15 The details of the selection process are summarized in Table 1 . No significant differences in seizure control were observed on comparing the short-and medium-term effects of the COVID-19 pandemic on our cohort of patients with epilepsy. In the second study, conducted in July and August 2020, 17 patients (11.1%) reported an increase in seizure frequency, 125 (81.6%) reported no change, and five (3.3%) reported a decrease. Six patients (3.6%) did not know. The short-and medium-term effects are compared in Table 2 . Demand for emergency services increased following the easing of restrictions (11.1% vs. 3.3%; p = .008). Eight patients (5.3%) visited an emergency department because of seizures in the summer and three (2%) considered doing so but did not because they were afraid of becoming infected with SARS-CoV-2. Three (2%) called the emergency phone line and were told to stay at home, and another three (2%) tried to call but could not get through because the lines were overwhelmed. No significant differences in the number of patients reporting delays in epilepsy-related tests were observed between the first and second study (14 vs. 15 ). Four of the 15 patient who reported delays during the new normal also reported an increase in seizure frequency. Just four patients (2.6% vs. 2% in the first study) reported difficulties obtaining their AEDs from the pharmacy, and in all cases, the reason was that their prescription had expired. Perceptions of telemedicine worsened significantly between the first and follow-up study (p = .005), with a higher proportion of patients stating that they were dissatisfied ( The sample was drawn from the "Epilepsy in time of COVID-19" cohort, 15 a real-life cohort from an epilepsy unit at a tertiary hospital comprising a wide range of patients, including those with intellectual disability and/or dependency for activities of daily living. The percentage of patients with drug-resistant epilepsy was similar to that expected for the general epilepsy population. 21 The online survey was designed by a trained epileptologist, and to minimize variations, the follow-up telephone interviews were conducted by the same epileptologists who took part in the first wave of the study. In this second study, self-reported psychiatric comorbidities (depression, anxiety, and sleep disturbances) were compared with scores on the HADS and PSIQ, which have both been validated in patients with epilepsy. 22, 23 The main finding of this follow-up study of the medium-term effects of the COVID-19 pandemic on patients with epilepsy was a significant increase in depression rates. Almost a third of the patients reported feeling depressed, and 24.3% had borderline or pathologic scores on the HADS-D. This represents a 33% increase in self-reported depression compared with the first survey, which had already detected a rise in emerging psychiatric symptoms such as anxiety and depression during the first month of lockdown. While Emergency consultation a n (%) .008 Delays in epilepsy-related tests b n (%) 28 (11) The socioeconomic effects of the pandemic have also had a significant effect on psychological distress and mental health, 31 being the socioeconomic status a known determinant of psychological distress and health outcomes among epilepsy patients. 32, 33 In our cohort, 27% of patients were still affected by a reduction in income several months after the easing of restrictions, and this factor was the second strongest predictor of an increase in seizure frequency. Our findings also show a major shift in perceptions of telemedicine, with the proportion of patients reporting dissatisfaction with remote visits increasing from 2% during lockdown to around 11% in the summer. In a survey conducted during the first peak of the pandemic, 88% of Spanish epileptologists reported dealing with their patients by telephone and stated that it was difficult to handle complex issues via this channel. 11 In a US study of telehealth perceptions during the pandemic, 34 66% of epilepsy patients reported being very satisfied with teleconsultations. In our study, the proportion of patients reporting high satisfaction levels fell from 57% during lockdown to 45% in the summer. In the US study, 66% of patients were optimistic about the future role of telemedicine, compared with just 41.5% and 36.7% of patients in the first and second waves of our survey. The more favorable opinions observed in the United States may partly be due to the younger age of the patients and the fact that the survey was conducted at a time when the pandemic had not yet affected the whole country. 35 The positive perceptions of telemedicine observed in our population in the first study may be biased by the fact that the survey was conducted by telephone. Nevertheless, the significant change observed over the months should lead to reflection that several adjustments need to be made to adapt telemedicine to daily practice and strengthen patients' confidence in this valuable tool. On a more optimistic note, 67% of the patients surveyed in the United States suggested the possibility of a hybrid model combining telehealth, with telephone or video consultations, and traditional visits; this option was also spontaneously proposed by our patients and could be a good direction to pursue. We also detected an increase in emergency consultations (from 3.3% in March/April to 11% in July/August). Some of these visits may correspond to visits that patients postponed during the early days of the pandemic because of fear of becoming infected with SARS-CoV-2 at the hospital. The proportion of patients reporting delays in testing remained similar, at around 10%, indicating that there was still a backlog to clear. Delays in the performance of epilepsy-related tests were associated with an increase in seizure frequency, and we believe that this relationship may be bidirectional, since a higher proportion of tests are ordered for patients with drug-resistant epilepsy. Nevertheless, a sooner performance of these tests could have provided important information and therefore allow treatment adjustment and a more accurate assessment in these patients. Our study has several limitations. The pre-pandemic baseline scores for anxiety and depression were not collected in our sample, even though prior studies performed in our population area portrayed TA B L E 3 Clinical factors associated with seizure control during and after lockdown in the first wave of the coronavirus disease 2019 pandemic lower rates of psychiatric pathologies before the COVID-19 pandemic. 29 Besides psychological comorbidities and sleep disturbances were measured using validated tests, changes in seizure frequency were based on self-reported data. Our findings may also be affected by selection bias as just 50% of the patients from the initial study completed the follow-up survey. This low response rate was partly related to technical difficulties encountered with the online questionnaire (such as difficulties to access it or receiving it). We think that the introduction of telemedicine in our day to day will require a progressive learning process in our population, both in patients and in healthcare professionals. This study has provided new evidence on the mediumterm effects of the COVID-19 pandemic on patients with epilepsy, and effects we believe are likely to endure beyond the pandemic. Further longitudinal and multicenter studies of larger international populations are needed to confirm our observations and clarify uncertainties surrounding the future consequences of the COVID-19 pandemic. We detected a significant increase in the proportion of epilepsy patients experiencing depressive symptoms after the first peak of the COVID-19 pandemic. The main risk factors for an increase in seizure frequency were depression, reduced income, and drug-resistant epilepsy. Anxiety and insomnia rates remained high, and perceptions of telemedicine worsened significantly. The full consequences of the COVID-19 pandemic and social distancing measures have yet to be determined in the setting of epilepsy, although as our results suggest, they are likely to be lasting and will call for adjustments to daily practice. We confirm that we have read the journal's position on issues concerning ethical publication and that this report is consistent with these guidelines. This research did not receive a grant from funding agencies in the public, commercial, or not-for-profit sector. 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