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A Systematic Review of the Validity and Reliability of the Patient-Determined Disease Steps Scale

Telemedicine provides a gateway to specialty care that, otherwise, patients with multiple sclerosis (MS) could have difficulty accessing. Studies have shown that telemedicine provides a valid alternative to in-person visits. There are limited data on the strengths and limitations of telemedicine from the perspective of MS providers.

After reviewing the literature and pilot testing questions about telemedicine in provider focus groups, a 34-question survey was created on the Qualtrics web platform. A stratified sample of MS providers throughout the United States was recruited to participate. The survey initiated in November 2019 and closed in November 2020.

Survey participants (N = 94) included neurologists (43.0%), advanced practice providers (28.0%), nurses (14.0%), mental health providers (7.0%), social workers (3.0%), rehabilitation providers (4.0%), and pharmacists (1.0%). Clinical video telemedicine (CVT) was the most commonly used platform, and 76.6% of respondents indicated that they used telemedicine to care for patients with MS. As a result of the COVID-19 pandemic, the rate of telemedicine use increased from 44.4% to 84.2%. Most health care providers (93.0%) were “very satisfied” or “somewhat satisfied” with their most recent telemedicine visit, and 94.4% of providers reported a desire to continue using telemedicine, although 84.6% found it difficult to perform a full examination.

There was a large uptick in the use of telemedicine when the COVID-19 pandemic forced clinics to cease in-person visits. Providers predominantly used CVT; store-and-forward telemedicine and remote patient monitoring have fewer technical issues than CVT and seem to be underused.

From the Department of Neurology, Johns Hopkins University, Baltimore, MD, USA (PK); Veteran's Administration Multiple Sclerosis Center of Excellence-East, Baltimore, MD, and Washington, DC, USA (HM, ZM, SJ, MW); Department of Neurology, George Washington University, Washington, DC, USA (MW). 

 Peter Keszler, DO, 7315 Wisconsin Ave, Ste 700, Bethesda, MD 20814, USA; 

Thanks to the health care providers who participated in the surveys and responded to the promises and challenges of telemedicine.

The authors declare no conflicts of interest.

 This study was supported by the National Multiple Sclerosis Society (HC-1610-25978) and the US Department of Veterans Affairs Multiple Sclerosis Center of Excellence.

 Preliminary data from this study were presented as part of an abstract poster at the Americas Committee on Treatment and Research in MS Forum 2021 Virtual Conference; February 25-27, 2021.

It is often difficult for patients with multiple sclerosis (MS) to access specialty care; major barriers include geographic distance from providers, traveling restrictions due to neurologic disability, and limited or partial health insurance coverage.

 Access is further impaired by inclement weather and health-related concerns (eg, COVID-19, MS flare). One study showed that 30% of patients with MS do not see a neurologic specialist for their care.

 Patients who are seen by a neurologist are more likely to be prescribed a disease-modifying treatment and receive multidisciplinary services,

Telemedicine, the use of technology to provide access to clinical care when distance separates patients and providers,

 could allow for broader and more convenient access to MS specialty care. There are several types of telemedicine: (1) clinical video telemedicine (CVT), in which a provider and patient communicate through an audiovisual platform (eg, Zoom [Zoom Video Communications, Inc]); (2) pure audio real-time interface (eg, performing telephone surveys); (3) store-and-forward telemedicine, in which patient test results (eg, cognitive tests, optical coherence tomography) are stored and then reviewed by a remote clinician; and (4) remote monitoring, which includes wearing a device or using an app that sends real-time data to a remote provider.

The COVID-19 pandemic forced a shift in how practitioners provided care due to the need for social distancing to decrease potential exposures for a patient population that is at higher risk

 than the general population. Providers and the National Multiple Sclerosis Society issued guidance for using telemedicine to help reduce this risk.

 This was made possible by health insurance providers relaxing restrictions on reimbursement for telemedicine services, which had resulted in limited use.

 Centers for MS quickly made plans to transition to telemedicine platforms.

 As a result, there was a massive rise in the use of teleneurology, with virtual visits skyrocketing and in-person visits plummeting.

Most studies looking at the use of telemedicine in MS care have been single-center studies with small sample sizes. There are limited data on the strengths and limitations of telemedicine from the perspective of MS providers. Designed and begun before the rise of COVID-19, this study aimed to examine the views of a large, diverse group of MS care providers on telemedicine. We were fortunate to capture the pre–COVID-19 pandemic period as well as the pandemic period in the survey.

The survey questions were developed by evaluating the current telemedicine literature

 and previous surveys of telemedicine in MS care.

 Questions were pilot tested for readability, relevance, and completion time with a group of 10 MS care providers in the Washington, DC, region. Once finalized, the questions were uploaded to the Qualtrics web platform (Qualtrics). The survey consent, platform, and distribution were approved by the Washington, DC, Veterans Affairs Medical Center institutional review board.

The study team sampled providers from the 4 US Census regions by targeting major MS programs in these regions along with MS provider groups (eg, the International Organization of Multiple Sclerosis Nurses). Major MS programs were tertiary referral centers and part of the Consortium of Multiple Sclerosis Centers. The MS provider groups were composed of the core subspecialists that care for patients with MS. We sampled several different types of MS programs (eg, academic, private practice, government) in different geographic areas of the United States. The MS health care provider sample included (1) specialty and general neurologists, (2) rehabilitation specialists (eg, physiatrists, physical and occupational therapists), (3) advanced practice providers (APPs), (4) nurse specialists, and (5) other specialty providers (eg, psychologists, psychiatrists, social workers). The goal was to assess a broad national sample of MS health care providers to determine use patterns and views of telehealth.

The survey was composed of 34 questions and was distributed using a secure Qualtrics platform weblink to individual email addresses (

, all supplemental materials are in a PDF at the end of the online article). Original emails were sent to the practice as a whole, and then follow-up emails targeted individual providers; 2 or 3 reminder emails were sent, which increased participation 25% on average. The actual response rate is unclear because the number of people who received the initial group email is unknown; depending on the practice, it seems to have ranged from approximately 50% to 100%. The MS health care providers completed the web-based survey between November 20, 2019, and November 15, 2020. Responses were then stratified based on those who completed the survey before March 2020 (pre–COVID-19 pandemic) and during and after March 2020 (peri–COVID-19 pandemic).

The web-based survey data contained no unique identifiers. Survey responses were analyzed using Qualtrics software and SAS version 15.2 (SAS Institute Inc). Participants were not offered compensation or incentives to participate in the survey.

The survey was opened by 105 people; 94 completed the full survey, representing a diverse group of provider types (

). The respondents’ specialty areas were as follows: neurologist (n = 40; 42.6%); APPs (n = 26; 27.7%); nurse (n = 13;13.8%); psychologist, neuropsychologist, or psychiatrist (n = 7; 7.4%); social worker (n = 3; 3.2%); physiatrist (n = 2; 2.1%); physical therapist or occupational therapist (n = 2; 2.1%); and pharmacist (n = 1; 1.1%). The breakdown by US Census region was balanced. The providers had been in practice for a mean ± SD of 17.5 ± 12.1 years (range, 1–49 years).

In terms of use, 72 (76.6%) of the 94 respondents indicated that they had used telemedicine to evaluate patients with MS. Of those who had used telemedicine, a mean of 65.5% of their practice was dedicated to telemedicine. The most common platform for telemedicine was CVT (87.5%); 70.8% had used pure audio (ie, telephone counseling or surveys), 9.7% had used store-and-forward telemedicine, and 1.4% had used remote patient monitoring. Most providers used CVT in nonclinical settings (ie, from home) (82%) vs in clinical settings (ie, remote clinic room) (7.9%), with 11.1% of providers seeing patients in both settings. All providers had telehealth encounters in their same state, with a large portion also seeing patients across state lines (75.0%). A small proportion of MS providers even saw patients internationally (4.2%).

Overall, 93.0% of respondents were “very satisfied” or “somewhat satisfied” with their most recent telemedicine visit, 4.2% were “neither satisfied nor dissatisfied,” and 2.8% were “somewhat dissatisfied.” Respondents stated that they would “definitely” (73.2%) or “probably” (21.1%) like to continue using telemedicine, with 1.4% “not being sure” and 4.2% “probably not wanting” to use telemedicine again (

Providers reported that the benefits of telemedicine were improved access to services or specialists for patients (88.2%), greater convenience for providers (57.0%), lower costs for providers (29.0%), and better interactions with patients (28.0%) (

). Among the write-in advantages for telemedicine, the most common answer was greater convenience for patients (28.0%). Alternatively, 3.2% of providers responded, “Telemedicine would not provide any advantages for me,” and 2.1% were not sure what advantages there were.

Among the challenges with telemedicine, 84.6% of providers felt that it was difficult to perform a full examination using a remote platform (Figure 1). Other disadvantages reported were difficulties communicating with patients due to technological issues (60.4%), concerns about privacy and security (26.4%), the high cost of telemedicine equipment and support or lack of health insurance coverage (22.0%), and the inability to view laboratory test results (8.8%). A small group of providers felt that telemedicine would not provide any disadvantages for their practice (2.2%).

Pre–COVID-19 and Peri–COVID-19 Pandemic Differences in Telemedicine 

No surveys were completed between December 24, 2019, and March 17, 2020, providing a clear divide between respondents before the COVID-19 pandemic in the United States and those during the COVID-19 pandemic. The first case of COVID-19 was diagnosed in the United States in February 2020, but the response to the pandemic did not begin until March 2020.

 The last survey response was completed in November 2020. There were 18 survey responses before the start of the pandemic and 77 during the pandemic.

Looking at the data collected before vs during the COVID-19 pandemic, there was a dramatic rise in provider use of telemedicine, from 44.4% to 84.2% (Figure S3). During the peripandemic period, providers also dedicated more of their practice to telemedicine: 72.4% vs 14.4% before the pandemic (

). During the peripandemic period, providers were more likely to be unsatisfied with their most recent telemedicine visit (3.1% vs 0%) and to experience technical difficulties (89.3% vs 57.1%) and were less likely to be confident in their findings via telemedicine (21.9% vs 62.5%), to have telemedicine training (78.1% vs 87.5%), and to want to continue using telemedicine (93.8% vs 100%).

Provider Similarities and Differences in Telemedicine

There do not seem to be differences in satisfaction with the most recent telemedicine visit or desire to continue using telemedicine in the future among different provider types. There are differences in use of telemedicine and percentage of practice dedicated to telemedicine: neurologists, APPs, and nurses had similar use (75%–80%) and practice dedication (65%–70%); psychiatrists/psychologists had notably lower telemedicine use (57.1%) and practice dedication (43.8%). Neurologists were less confident in their evaluations via CVT compared with their in-person evaluations, with 24.2% reporting that they are not as confident; 9.5% of APPs were less confident as well, but no other provider type cited less confidence.

Practitioners who did not use telemedicine were more likely to be from the South. The low rate of telemedicine use persisted during the pandemic: in the South, telemedicine use was 70.8%, compared with 89.5% in the Northeast and the West and 92.9% in the Midwest. When prepandemic numbers are included, the south’s telemedicine use drops to 59.5%. The South also had the lowest percentage of practice dedicated to telemedicine, 42.7%, compared with the Northeast’s 70.9%, the Midwest’s 84.3%, and the West’s 82.4%.

There did not seem to be a strong correlation between the number of years in practice and the use of telemedicine or percentage of practice dedicated to telemedicine. In fact, the highest percentage of telemedicine use was among those with more than 30 years practicing medicine (90.9%), slightly above those who had been in practice 5 years or less (89.5%). The lowest use of telemedicine was among providers who had been in practice 6 to 10 years (61.5%); those practicing 21 to 30 years (70%) and 11 to 20 years (74.2%) were closer to the average.

This survey of 94 MS providers from around the United States gives a glimpse into their telemedicine use and their opinions regarding its benefits and limitations. Overall, most MS providers are comfortable using CVT and other types of telemedicine to evaluate patients. Telemedicine’s strengths included improved access and convenience and lower costs. Challenges were interpreting remote examinations, communicating with patients, and technical difficulties. This survey assessed MS providers before and during the COVID-19 pandemic; given the exponential growth in the use of telemedicine, provider views on its benefits and disadvantages are even more important.

Previous surveys of all physician types showed that telemedicine was vastly underused, with a 2016 study showing that only 15.4% of providers had used this option. Neurologists showed slightly better than average use compared with other physicians at 17.4%.

 Similar to the present study, CVT was the preferred mode of telemedicine, with store-and-forward telehealth and remote patient monitoring rarely used.

A recent article showed most MS providers (95.1%) using telemedicine in mid-2020, with almost half dedicating more than 50% of their practice to remote encounters.

 The overall higher percentage of telemedicine use but lower percentage of time dedicated to telemedicine compared with the present study may be accounted for by our longer period of data collection, which included earlier parts of the pandemic. This report did not capture data on prepandemic use of telemedicine.

Patients have expressed enthusiasm about using mobile and wearable devices to track clinical outcomes,

 and, as this study shows, this type of telemedicine tends to have fewer technical difficulties than CVT. Despite these advantages, there is limited clinical use of these types of telemedicine.

Among practitioners who said they were not sure whether they would like to continue using telemedicine or would probably not want to continue using telemedicine, 3 were neurologists and 1 was an APP. They had been in practice for a mean ± SD of 25.3 ± 13.9 years (range, 14.0–49.0 years). All 4 practitioners indicated that they had received training in telemedicine and felt very comfortable with computers, and 3 stated they that were not as confident in their evaluations. They were either “somewhat satisfied” or “neither satisfied nor dissatisfied” with their most recent telemedicine visit. Two were from the South, 1 was from the Midwest, and 1 was from the West.

Of interest, satisfaction with the most recent telemedicine visit did not seem to correlate with the desire to continue using telemedicine. Of the 6 providers who said that they were “somewhat disappointed” or “neither disappointed nor satisfied” with their most recent visit, 2 said that they would definitely want to continue using telemedicine, 2 said that they would probably want to continue, and 2 said that they would probably not want to continue.

Regional differences may be explained by differing loca government levels of pandemic restriction on travel and social distancing. Although other regions imposed strict lockdowns, the South did not completely restrict movement between states and within businesses. This may account for the reduced use of telemedicine in the South. In addition, telehealth policies vary between states. Many states in the south did not pass as many comprehensive laws to expand telemedicine coverage.

 This is consistent with the idea that the increase in telemedicine was due to necessity during the COVID-19 pandemic.

There are several differences in the pre–COVID-19 pandemic and the peripandemic responders. First, the peripandemic responders spent much more of their practice performing telemedicine, reported a higher percentage of technical difficulties, were less confident in their ability to assess and treat patients compared with in-person interactions, and had less telemedicine resources/support. The most likely explanation for these differences between the prepandemic group and the peripandemic group is that those already using telemedicine before the onset of the pandemic had chosen to make this a part of their practice and were comfortable with the technology. These clinics had the support, contingency plans, and tools necessary to run their operations smoothly, whereas the peri–COVID-19 pandemic group included providers who were forced into telemedicine by default. In addition, the surge of telemedicine use likely taxed the information technology infrastructure, and peripandemic providers were spending a far greater proportion of their practice using telemedicine. Teleconferencing fatigue is an often-experienced phenomenon that could explain some practitioners’ negative attitudes toward telemedicine.

 Finally, the pre–COVID-19 pandemic group skewed younger with less years of experience in practice compared with the peripandemic group. This age gap may have played a part in why those in the prepandemic group were earlier adopters of telemedicine and felt more comfortable with its implementation.

There are several recent studies demonstrating how telehealth has been successfully used in various aspects of MS care, including fatigue management

 The use of CVT has been shown to be feasible and cost-effective, and it had high satisfaction ratings from both patients and providers.

 Studies have shown little to no difference between telemedicine and in-person interventions

 and have demonstrated that the Expanded Disability Status Scale evaluation can be successfully and reliably completed via telemedicine.

 In addition, telemedicine has been shown to reduce patient travel burden, lower the indirect costs of missed work, and lower caregiver burden.

The strengths of this study include reaching a diverse pool of providers, not only in scope of practice, but also in geography. We acquired responses from all corners of the United States, representing 24 states and the District of Columbia. We also received input from a multidisciplinary range of MS care providers. Finally, the timing of the start of the study allowed us to collect data before and after the pandemic.

A limitation of this study is the limited scope of health care providers. Although the study sampled a wide range of providers, most were neurologists, APPs, or nurses, with only a few responders from other provider types. As a result, it is hard to compare these other provider types and may account for some of the intergroup differences noted. Moreover, the sample size of the pre–COVID-19 pandemic group is significantly smaller than that of the peripandemic group; a larger sample may have yielded more representative results. The study was designed before the COVID-19 pandemic, but the start date resulted in a limited recruitment period and a small sample before the pandemic onset. Ideally, a larger prepandemic sample coupled with the opportunity to retake the survey after the near universal adoption of telemedicine during the pandemic would have illustrated how provider views on telemedicine changed after increased exposure.

Overall, telemedicine provides a pathway to improve access to high-quality, cost-effective care for patients with MS and their providers. Most providers using CVT were satisfied, and the less technically challenging options of store-and-forward telemedicine and remote patient monitoring can be better used. Except for select clinical situations (eg, neurologic procedures), technological and reimbursement problems can be resolved if the practices and policies instituted during the pandemic are preserved. There is federal and state legislation to continue the current insurance reimbursements and policy allowances for telemedicine.

 Further studies are needed to see how the levels of training and support for telemedicine change as the use of telemedicine increases. To improve patient care and outcomes, the MS community, patients and providers of all types, should work toward nationwide telemedicine funding and interoperability.

Telemedicine and Multiple Sclerosis: A Survey of Health Care Providers Before and During the COVID-19 Pandemic

Although the COVID-19 quarantine required everyone to make lifestyle changes, it may have had especially profound implications for individuals who experience multiple sclerosis (MS)–related fatigue. Individuals with MS who suffer from fatigue are at risk of worsening symptoms and already predisposed to inactivity and social isolation. The objective of this study was to examine the impact of the COVID-19 national quarantine and related restrictions on mental, emotional, and physical fatigue in persons with MS in the United States.

We conducted a survey open to all adults (>18 years) with MS within the United States. The survey gathered demographic information and asked how the COVID-19 pandemic impacted their physical, mental, and emotional fatigue.

The survey was completed by 600 individuals, 478 with relapsing MS and 122 with progressive MS. There was a significant 2-way interaction of time by fatigue type; both physical and emotional fatigue significantly increased during the pandemic (

 <.01) and remained significantly higher after the pandemic than prior to the pandemic (

 <.01). Mental fatigue increased significantly during the pandemic (

 <.01) and although it remained higher, on average, after the pandemic, it was not significantly different from the level before the pandemic.

Individuals with MS experienced increases in physical, mental, and emotional fatigue over the course of the COVID-19 quarantine. Even after the lifting of quarantine restrictions, these levels have not returned to baseline. To adequately address fatigue, it is critical that health care professionals inquire about all types of fatigue in persons with MS.

From the Neuroimaging and Neurorehabilitation Laboratory, Wayne State University, Detroit, MI (ZAR,JF,NEF); the Department of Health Care Sciences, Wayne State University, Detroit, MI (JF, NEF); the Department of Physical Therapy, MGH Institute of Health Professions, Boston, MA (PP,NEF); and the Department of Neurology, Wayne State University, Detroit, MI (NEF). 

Nora E. Fritz, 259 Mack Ave #2324, Detroit, MI, 48201; 

Fatigue is one of the most common and debilitating symptoms of multiple sclerosis (MS)

; it is present in 64% to 81% of people with MS.

 Fatigue is commonly reported across disease subtypes and at all stages of the disease. It may arise both from central nervous system damage (primary fatigue) or as a result of accumulation of disease burden (secondary fatigue).

 Regardless of cause, fatigue contributes to a downward spiral of inactivity and social isolation

 and is the primary reason for job loss in persons with MS.

To limit the spread of COVID-19, a national emergency was declared in the United States on March 13, 2020, prompting a national quarantine. Although the quarantine forced all residents to make lifestyle changes, it may have had especially profound implications for individuals who experience MS-related fatigue. People with MS who have fatigue are at risk for symptom worsening and are predisposed to inactivity and social isolation. Thus, it is possible that prolonged isolation due to the pandemic may have further diminished physical activity and exacerbated symptoms of MS–related fatigue among people with MS. Indeed, in Turkey, people with MS reported greater fatigue, anxiety, and depression during quarantine than adults without MS

; however, a critical limitation of this study was the cross-sectional assessment of fatigue, anxiety, and depression during the pandemic without directly assessing the impact of COVID-19 on these symptoms. Whether the pandemic affected self-reported fatigue in people with MS is unclear.

In Italy, when compared with the 12 months prior, the 3-month lockdown resulted in perceived worsening of fatigue and overall disability in 32.4% of individuals with progressive MS, worsening depressive symptoms in 30.4%, and a shift to a more sedentary lifestyle, with 47.1% completely stopping exercise.

 Although this study describes COVID-19–related changes in fatigue in people with progressive MS, the study fails to report data on the severity and type of fatigue before or after lockdown. Despite these findings from recent European studies, the impact of the COVID-19 quarantine and the subsequent lifting of quarantine restrictions on fatigue in people with MS in the United States has not been examined. Thus, the objective of this study was to examine the impact of the COVID-19 national quarantine and its related restrictions on the mental, emotional, and physical fatigue experienced by people with MS in the United States.

We conducted a nationwide survey using REDCap (Vanderbilt University), a secure, Health Insurance Portability and Accountability Act–compliant, browser-based database and survey platform. Part of a larger cross-sectional study evaluating fatigue in people with MS, the survey was distributed through the National Multiple Sclerosis Society monthly newsletter and was available from November 1, 2021 through January 30, 2022. The Impact of COVID-19 survey was open to all adults (>18 years) with MS within the United States and took approximately 20 minutes to complete. All study procedures were approved by the Wayne State University Institutional Review Board.

The survey gathered demographic information and asked questions regarding fatigue severity, fatigue impact on daily activities, other MS symptoms, and how the COVID-19 pandemic impacted physical, mental, and emotional fatigue. Physical fatigue was defined as a lack of energy, weakness, or feeling “drained”; mental fatigue was defined as a lack of energy to think, brain fog, or feeling mentally tired; emotional fatigue was defined as feeling emotionally overwhelmed, burned out, or defeated.

 Each type of fatigue was rated using a scale ranging from 0 (no fatigue) to 10 (extreme fatigue). The survey asked for ratings of fatigue in 3 periods: (1) prior to March 2020; (2) March 2020 through May 2021; and (3) June 2021 to the present (ie, the day the survey was submitted), representing before the quarantine, during the quarantine, and the period after the easing of quarantine restrictions. Demographic information included age, sex, race, living situation, and employment status. Additionally, we collected information about current disease-modifying therapy, fatigue medication use, ambulatory status, assistive device use, and comorbidities. Disease severity was characterized with the self-reported Patient Determined Disease Steps (PDDS). The PDDS is a valid and reliable measure of disease disability in MS.

Descriptive data were examined for all variables. Participants who identified as having primary progressive MS or secondary progressive MS were pooled for analysis into a single progressive MS group. This is consistent with the most recent revisions of the MS phenotype descriptions, which consider primary and secondary progressive MS to fall under the umbrella of “progressive MS.”

 To determine whether fatigue levels and fatigue types were significantly different among the 3 time periods, a 2-way analysis of variance (ANOVA) was applied. We explored differences in fatigue across disease subtypes using ANOVA. Tukey post hoc comparisons were used to examine significant interaction effects.

Six hundred individuals living in the United States completed the survey, 478 with relapsing-remitting MS (RRMS) and 122 with progressive MS. Respondents had an average age of 50.9 ±12.5 years. The sample was largely female (82.8%), White (88.1%), living alone (83%), working full- or part-time (53.3%), ambulatory (96%) with relatively low disability (PDDS ≤ 3) (71%), and taking disease-modifying therapies (83.3%). In this sample, only 31.3% reported current use of medications to manage fatigue (

When asked to rate their physical, mental, and emotional fatigue levels, individuals reported greater fatigue (0-10 scale) during lockdown than before lockdown, and although the level of physical, mental, and emotional fatigue declined following the lifting of quarantine restrictions, fatigue levels did not return to previous levels. Physical fatigue was 0.6 points higher, mental fatigue 1.0 point higher, and emotional fatigue 0.8 points higher (

) than before the pandemic. There was a significant 2-way interaction of time by fatigue type; physical fatigue significantly increased during the pandemic (P <.01) and it remained significantly higher after the pandemic than before it (P <.01). Emotional fatigue also significantly increased during the pandemic (P <. 01) and it remained significantly higher after the pandemic than before it (P <.01). Mental fatigue increased significantly during the pandemic (P <.01), and although it remained higher, on average, after the pandemic, it was not significantly different after the pandemic than before it. Before the pandemic, physical fatigue was significantly greater than emotional (P <.01) and mental fatigue (P <.01), which did not differ from each other. During the pandemic, there was no difference between severity of physical and emotional fatigue, and both were significantly greater than mental fatigue. After the pandemic, physical fatigue was again significantly greater than both emotional (P <.01) and mental fatigue (P <.01), which did not differ from each other (

Differences in Fatigue Across Disease Subtypes 

There was a significant 2-way interaction of disease subtype by fatigue type; within progressive MS, there was a main effect of fatigue, such that physical fatigue was greater than mental (P <.01) or emotional (P <.01) fatigue, which did not differ from each other. There were no significant differences in the severity of fatigue subtypes in RRMS. Physical fatigue in individuals with progressive MS was also significantly greater than all types of fatigue in individuals with RRMS (

Impact of COVID-19 on Work and Self-Reported Exercise 

Of those individuals with MS who were employed (53.3%), 78.7% reported that their working arrangement (remote/in-person, hybrid) remained stable from before quarantine through quarantine. Only 20.7% reported some shift from remote back to in-person or to hybrid after quarantine (Table S1). A greater number of persons with RRMS (60.9%) reported working than did the participants with progressive MS (23.8%) (Table 1). Regardless of MS subtype, approximately 50% of individuals with MS reported that the pandemic impacted the amount they exercised; 82.7% reported that the pandemic affected the amount of social interaction they experienced weekly, but only 39.5% endorsed that the pandemic had negatively impacted their relationships (

The main finding of this study was that physical, mental, and emotional fatigue levels of people with MS in the United States increased during the COVID-19 lockdown, and although they declined slightly with the lifting of lockdown restrictions, these levels did not return to previous levels, which represents an overall worsening of fatigue for people with MS during this time period. Compared with the general population of adults aged 45 to 86 years, people with MS report 43% to 60% greater fatigue.

 Although all adults may have experienced a change in fatigue levels as a result of pandemic-related lockdowns, it is possible that the impact on people with MS was even greater. Indeed, 46% of nonhospitalized adults reported fatigue 6 months after having COVID-19. In comparison, all participants in this study reported at least some level of fatigue in the physical, mental, and emotional domains. Current evidence indicates that although fatigue is common in chronic diseases, the prevalence of severe and chronic fatigue is remarkably similar across chronic diseases, except for MS, Parkinson disease, and liver disease, in which the prevalence of severe and chronic fatigue was significantly higher.

A possible explanation for the increased mental and emotional fatigue levels may be changes in routine and responsibilities. The average age of our sample was 50.9 years and 83% lived with another person, so they may have been responsible for caring for young children who were suddenly home from school while also trying to work (53% of the sample was working). The intermingling of tasks and demands on time may contribute to the perception of greater fatigue. A possible explanation for a rise in physical fatigue levels may be related to an increase in sedentary behavior. In this study, individuals reported that the pandemic changed their level of exercise (52%) and social interactions (83%), which may have contributed to leaving the house less and sitting more. In addition, a prior study showed an association between higher self-reported fatigue levels and low activity levels, as well as an increased fall risk and lower quality of life in people with MS.

 Reports of exercising less during the pandemic suggest that before the pandemic, home-based exercise was not the regular mode of most participants. Thirty-three percent of physical therapists reported that aerobic training was reduced or unavailable during the pandemic and, despite 15% of physical therapists reporting increased use of relaxation/mind-body techniques or fatigue management techniques during the pandemic,

 fatigue in our sample still rose. There is an ongoing need for exercise services and skilled therapies at major medical centers; thus, clinicians should provide resources to wellness and exercise programming that can be successfully completed at home.

There was some discrepancy in how pandemic periods were defined. We defined 3 periods: before quarantine, prior to March 2020; quarantine, March 2020 through May 2021; and easing of quarantine restrictions, June 2021 to the present (ie, the day the survey was completed). Other studies either did not define the lockdown or quarantine periods,

 defined a single year (ie, 2020) for consideration,

 or defined only the lockdown period (March 2020 to May 2020) but allowed for tests within 3 (August 2020) and 6 (November 2020) months of lockdown to be considered in the dataset.

 Our results build on these studies by extending the focus beyond the immediate lockdown period to determine changes in the perception of fatigue over time.

While our sample was large, findings cannot be extrapolated to the general population of individuals with MS due to both survey bias (median PDDS score of 2 with an average age of 50.9) and participant recall bias; recall of fatigue levels over time would be more accurate with a longitudinal study design. Of course, in 2020, we did not anticipate that quarantine and restrictions would persist for such a long period of time. A longitudinal design of periodic surveys and the inclusion of a follow-up survey would potentially better capture fatigue and further our understanding of how long elevated perceptions of fatigue persist. Our data overcome some of these limitations by capturing different types of fatigue (physical, mental, emotional), albeit with simple survey questions created for this study that rank fatigue on a 0 to 10 scale. We did not differentiate whether fatigue was due to the pandemic or the worsening of disease and/or symptoms due to reduced activity levels, or whether it might be due to a combination of these factors. Finally, we did not ask participants whether they had a positive COVID-19 test, so we are unable to determine whether elevated fatigue levels may have been, in part, due to post–COVID-19 condition.

Fatigue is a common and debilitating symptom that can negatively impact quality of life. People with MS experienced increases in physical, mental, and emotional fatigue over the course of the COVID-19 quarantine and levels of fatigue did not return to baseline levels even after quarantine restrictions were lifted. Interestingly, prior work suggests that fatigue ratings tend to remain relatively stable over an 18-month period,

 which suggests that changes reported during COVID-19 lockdown may exceed natural disease progression. Persons with progressive MS reported higher levels of fatigue than those with RRMS. Providers who are attuned to the impact of fatigue can intervene with timely management strategies, but to adequately address fatigue, it is critical that health care professionals ask people with MS about all fatigue domains, which aligns with recent best-practice recommendations to use the Modified Fatigue Impact Scale to assess multiple domains of fatigue for comprehensive fatigue management in people with MS.

 This work was presented at the Wayne State University Eugene Applebaum College of Pharmacy and Health Sciences College Research Day in 2022.

The Impact of COVID-19 on Fatigue in Multiple Sclerosis

 Apathy, a neuropsychiatric symptom characterized by a lack of motivation and affecting cognitive, emotional, and behavioral domains, is being increasingly recognized in multiple sclerosis (MS), with an estimated prevalence of 19% to 43%. However, apathy remains underinvestigated in early MS. In this study, we aim to evaluate apathy in people with relapsing-remitting MS (RRMS) whose disease duration has been less than 5 years.

 The study included 38 people with RRMS with a disease duration of less than 5 years and 38 matched controls. Clinical and comprehensive neuropsychological evaluations were performed. Apathy was evaluated using the Apathy Evaluation Scale, Clinician Version (AES-C).
Depressive symptoms, anxiety, fatigue, and quality of life were also assessed.

 Apathy prevalence was 42.1%. Apathy scores correlated with depressive symptoms, anxiety, fatigue, lower quality of life, younger age, and worse performance in frontal lobe tests (Trail Making Test-A [TMT-A] and Symbol Digit Modalities Test). Independent apathy predictors were depressive symptoms (OR, 4.05; 95% CI, 1.22-13.5; 

 = .023), global quality of life (OR, 1.7; 95% CI, 1.08-2.64; 

 = .021), and TMT-A score (OR, 1.14; 95% CI, 1.02-1.27; 

 Apathy is a disabling symptom that is present in a significant percentage of people in the first years after they have been diagnosed with RRMS. Thus, people with MS should should be routinely screened for apathy, and symptoms should be managed when it occurs. We identified depressive symptoms, low quality of life, and executive dysfunction as predictors of apathy in this population.

From the Department of Neurology, Hospital da Luz Lisboa, Lisbon, Portugal. 

 Inês Brás Marques, MD, Hospital da Luz Lisboa, Avenida Lusíada 100, 1500-650 Lisbon, Portugal; 

 The authors acknowledge Renato Oliveira for his assistance in the initial setup of this study.

The author(s) declare no potential conflicts of interest.

This project (Reference LH.INV.F2019013) was partially financed by Hospital da Luz Lisboa under the initiative “Luz investigação—Bolsas Luz Saúde.” Hospital da Luz Lisboa was not involved in the scientific aspects of the study or the publication.

The content of this work was presented as an e-poster at the 10th Congress of the European Academy of Neurology; June 29-July 2, 2024; Helsinki, Finland.

Apathy is a behavioral and psychological syndrome characterized by a lack of motivation that impacts cognitive, emotional, or behavioral domains.

 Apathy is defined as a quantitative reduction of goal-directed activity compared with previous functioning that persists for a minimum of 4 weeks and affects at least 2 of the dimensions of behavior, cognition, emotionality, and social interaction.

This decline in initiative or interest in usual activities and emotional expression or responsiveness may cause clinically significant functional impairments that cannot be fully explained by other factors, such as physical disability, diminished consciousness, substance effects, and major changes in the patients’ environment.

Apathy is recognized as a neuropsychiatric manifestation of many neurological disorders, including Parkinson disease, Alzheimer disease, frontotemporal dementia, Huntington disease, cerebrovascular disease, and mild cognitive impairment.

 This disabling symptom is also being increasingly recognized in patients with multiple sclerosis (MS), with an estimated prevalence of 19% to 43%.

 Some studies in MS have also identified a correlation between apathy and cognitive dysfunction, particularly in executive functions, with apathy severity being a predictor of cognitive dysfunction at follow-up.

Despite these findings, apathy is still not part of the routine clinical assessment of people with MS, and its impact on patients’ lives is probably being underestimated. Additionally, studies evaluating apathy in the early stages of MS are lacking in the literature, and its prevalence in these initial phases is still underinvestigated. Thus, this study aims to evaluate the prevalence of apathy in people in the early phase of relapsing-remitting MS (RRMS). The association between apathy and clinical characteristics, cognitive functions, neuropsychiatric symptoms, and quality of life will also be assessed.

This study included a group of people aged 18 to 49 years with RRMS, as defined by the 2017 McDonald Criteria,

 with a disease duration of less than 5 years, who were followed in a neuroimmunology outpatient clinic of a tertiary center. Exclusion criteria included a diagnosis of progressive forms of MS, individuals under 18 or over 50 years of age, steroid treatment in the 4 weeks before the evaluation, a history of severe mental disorder (eg, major depression, psychosis, or schizoaffective disorder), other neurological conditions adversely affecting cognitive functions (eg, dementia, severe traumatic brain injury, stroke), and a history of substance abuse. Healthy controls (HCs) matched to patient demographics, including age, sex, and years of education, were also recruited. The protocol of the research project was approved by the ethics committee of our institution (Comissão de Ética do Hospital da Luz), and it conforms to the provisions of the Declaration of Helsinki. Written informed consent was obtained from all participants prior to assessments.

All participants underwent a clinical evaluation, including a full medical history and a complete neurological examination. Data collection included demographic variables such as age, sex, and years of education, as well as disease-specific information, including duration of MS, age at MS diagnosis, history of MS relapses, and current pharmacological treatment. Physical disability was assessed using the Expanded Disability Status Scale (EDSS).

Apathy was assessed through a clinical interview using the Apathy Evaluation Scale, Clinician Version (AES-C).

 This 18-item clinician-administered scale assesses various aspects of affective, behavioral, and cognitive apathy during the preceding 4 weeks. Each item has 4 possible answers rated from 0, 

, with a total score ranging from 18 to 72. Higher scores indicate more severe apathetic symptoms. Scoring guidelines provided by the original author are based on a clinician’s best judgment of the subject’s thoughts, feelings, and actions, evaluating both verbal and nonverbal data. The AES-C has been validated for the Portuguese population with defined cutoff points.

 In this study, participants with AES-C scores higher than the cutoff scores adjusted for educational level were categorized as apathetic.

A comprehensive formal neuropsychological assessment was performed by 2 trained neuropsychologists (CC and DS) with the following battery of tests: Montreal Cognitive Assessment,

a screening tool for global cognitive functioning; California Verbal Learning test

 for verbal learning and memory; Controlled Oral Word Association Test

 for verbal fluency; Digit Span Test Forward and Digit Span Test Backward

for immediate attention and working memory; Rey-Osterrieth complex Figure Test

 for visuo-constructional ability, planning, and spatial orientation; Stroop Color-Word Interference test

 for flexibility and inhibitory control; Symbol Digit Modalities Test (SDMT)

 for information processing speed and attention; Trail Making test Parts A (TMT-A) and B (TMT-B)

 for attention, information processing speed, and set-shifting ability; Wisconsin Card Sorting Test (WCST)

 for abstract reasoning, monitoring, and cognitive flexibility; and Judgment of Line Orientation test

Depression, Anxiety, Fatigue, and Quality-of-Life Assessment

Severity of depressive symptoms and anxiety were evaluated by the Patient Health Questionnaire (PHQ-9)

 and the General Anxiety Disorder Assessment (GAD-7),

 respectively. Fatigue was evaluated using the Modified Fatigue Impact Scale (MFIS)

 and quality of life was assessed with the 12-Item Short Form Survey (SF-12).

Descriptive statistics were utilized to present absolute and relative frequencies for categorical variables, while continuous variables were summarized using mean with SD or medians, as appropriate. Group comparisons were conducted using an independent-samples 

 test, depending on the variable type. Correlational analysis was performed using Spearman correlation and 2-tailed Pearson correlation to examine the relationship between apathy and clinical characteristics, cognition, mood disorders, fatigue, or quality of life. Variables found to be significant in the univariate analysis were selected for inclusion in a multivariate logistic regression model to identify predictors of apathy. All reported 

 values were 2-sided, and statistical significance was considered for values less than .05.

In total, 38 people with MS and 38 matched HCs were included in the study. 

 presents participant demographic and clinical data. People with MS had a mean disease duration of 1.9±1.3 years and a median EDSS score of 1.8.

We found a prevalence of apathy in people with MS of 42.1% (n = 16); they had a statistically significant higher score on the AES-C than controls (30 ± 9.69 vs 25.13 ± 5.43; 

 = .009). Apathy with no significant depressive symptoms associated, or 

, was present in 43.8% (n = 7) of patients with apathy.

shows the correlations between AES-C scores and disease characteristics, neuropsychiatric symptoms, and cognitive functions of people with MS.

In the correlation analysis, AES-C scores exhibited negative correlations with SF-12 scores (

 = .003). Positive correlations were observed between AES-C scores and PHQ-9 scores (

 = .008). No significant correlations were found between apathy and years of education, disease duration, or physical disability.

For cognitive functions, a correlation was found between apathy and performance on the TMT-A (

In the multivariate analysis, PHQ-9 scores (OR, 4.05; 95% CI, 1.22-13.5; 

 = .023), SF-12 total scores (OR, 1.7; 95% CI, 1.08-2.64; 

 = .021), SF-12-mental scores (OR, 0.603; 95% CI, 0.39-0.93; 

 = .022), and TMT-A scores (OR, 1.139; 95% CI, 1.02-1.27; 

 = .020) were independent predictors of apathy.

In this study, we assessed the prevalence of apathy and the correlational and predictive relationship with clinical, neuropsychiatric, and cognitive measures in people with early RRMS. We found the overall prevalence of apathy was 42.1%, consistent with reported prevalence rates in other studies focusing on apathy in MS.

 To the best of our knowledge, this is the first study evaluating apathy prevalence in early RRMS, suggesting that it occurs early in the disease course in a substantial proportion of patients.

This study revealed a negative correlation between apathy and quality of life, with higher apathy scores associated with lower global and mental quality of life, as also reported in another study in MS.

 Additionally, we identified lower quality of life as an independent predictor of the presence of apathy, which underscores the impact apathy may exert on the lives of people with MS from the earlier stages of the disease.

We also identified a correlation between apathy and depressive symptoms, consistent with other studies,

 and depressive symptoms were an independent predictor of apathy.

Although apathy and depression symptoms may overlap, many patients present with pure apathy, as did 43.8% of our population. This supports the findings that apathy can manifest independently of depression, as previously reported.

While symptoms such as loss of interest, lack of initiative, and social withdrawal may be present in both apathy and depression, distinctions exist. In depression, the loss of motivation is usually linked to feelings of hopelessness, sadness, and pessimism.

Caitlin McFadyen, MPH

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