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Impact of Fingolimod Discontinuation Strategy on Recurrence of Disease Activity in Individuals With Multiple Sclerosis

In multiple sclerosis (MS), telemedicine improves access to specialized medical care; however, barriers remain, including universal access and effective implementation. Focusing on telerehabilitation, ie, remotely delivered physical therapy, our goal was to identify barriers to telerehabilitation implementation and factors associated with patients completing telerehabilitation physical therapy treatment.

Quantitative data included a review of electronic health records of patients with MS treated at the University of California San Francisco Physical Therapy Faculty Practice. We extracted demographic, clinical, and transit-related factors. For patients who scheduled an initial evaluation, we recorded the number of follow-ups, cancellations, completed physical therapy goals, and discharges. Qualitative data included interviews with 3 board-certified neurologic physical therapists and patients’ perspectives recorded in the subjective portion of physical therapy notes.

We identified 111 patients with at least 1 visit (in-person or telerehabilitation) to physical therapy (82 women; mean ± SD age, 54.2 ± 12.7 years). Patients with no disability (Expanded Disability Status Scale [EDSS] score, 0) were 73% less likely to schedule a follow-up appointment (in-person or telerehabilitation) than those with some disability (EDSS score, >0) (odds ratio, 0.27; 95% CI, 0.09–0.75; 

 = .012). Neurologic physical therapists identified reduced travel burden and scheduling flexibility as benefits of telerehabilitation vs in-person visits. Barriers to telerehabilitation included low technological literacy, cognitive impairment, and fall risk. Patients described scheduling conflicts and pain/illness as barriers to telerehabilitation.

Patients with no disability were least likely to complete physical therapy treatment via telerehabilitation. Although both benefits and barriers to completing physical therapy via telerehabilitation are present, the neurologic physical therapists were supportive of a hybrid model for physical therapy.

From the Department of Neurology, MS and Neuroinflammation Clinic, UCSF Weill Institute for Neurosciences (AG, VJB, RMB), and the Department of Physical Therapy and Rehabilitation Science (VJB), University of California San Francisco, San Francisco, CA, USA; and the Multiple Sclerosis Center Sant’Andrea Hospital, University La Sapienza, Rome, Italy (VB). 

Arpita Gopal, PT, DPT, UCSF Weill Institute for Neurosciences, 1651 4th St, Room 622A, San Francisco, CA 94143 USA; 

The authors would like to thank Monika Patel, E.J. Gann, and Alexander Dien for their contribution to this work.

 This work was accepted for presentation as an abstract at the 2022 Combined Sections Meeting, San Antonio, Texas.

 Dr Bove is funded by the NMSS Harry Weaver Award. She has received consulting and advisory board fees from Alexion, Biogen, EMD-Serono, Genzyme-Sanofi, Novartis, and Roche-Genentech and research support from Akili Therapeutics, Biogen, and Roche Genentech. Dr Gopal, Ms Bonanno, and Dr Block declare no conflicts of interest.

Neurologic physical therapy can address symptomatic concerns and improve overall quality of life for people with multiple sclerosis (MS).

 Despite these benefits, at least 36% of people with MS in the United States are not able to access necessary physical therapy evaluation and treatment.

 Among the many barriers in accessing specialized care (eg, driving distance to specialty clinics, numerous appointments, inadequate health insurance), the marked variability in MS-related functional impairments (eg, balance, gait, vision, fatigue) can make it even more challenging to attend traditional in-person medical visits.

With high-speed internet and videoconferencing readily available, remotely delivered care via telerehabilitation has shown promise in bridging the gap between physical therapists and people with MS who have limited access to specialty care.

 Telerehabilitation is defined as the use of technology to provide access to rehabilitative care when distance separates patients and clinicians.

 Although telerehabilitation services were available before the SARS-CoV-2 pandemic, since March 2020, health care practitioners and patients have had to adapt to new models of care, and the adoption of telerehabilitation has greatly increased.

 Physical therapists have used videoconferencing, virtual communication software, and telephone visits to provide quality care while maintaining social distancing.

Several studies have pointed to the advantages of telemedicine-based care for people with MS more broadly, including the potential to permanently alter the known health care model.

 For example, telemedicine can decrease the time before people with MS can access specialized heath care services (eg, neurologic rehabilitation experts) compared with standard in-person care.

 Televideo-enabled neurologic care for patients with MS decreases travel time,

 and improves access to care in rural areas.

 Telerehabilitation, more specifically, could allow for clinicians to more conveniently monitor patient progress

 and for better communication between physical therapists and people with MS.

However, although offering possible benefits in terms of improved access, telerehabilitation also faces a variety of obstacles that must be called out and addressed to support its expanded and sustained adoption. In fact, a systematic review of obstacles to adoption of telemedicine worldwide identified limitations in the technological literacy of staff, resistance to change, and cost of technology.

 Infrastructure barriers (eg, limited internet connection, lack of access to technology) also represent systemic barriers.

 Despite expanded use of technologies to deliver telerehabilitation, limited work has been conducted to consider its feasibility, acceptance, and usability among users (both people with MS and physical therapists).

This study of a physical therapy practice has 2 aims: (1) to identify barriers to implementing telerehabilitation and in-person visits from the perspectives of people with MS and MS physical therapists and (2) to identify the demographic and clinical predictors for people with MS who successfully complete neurologic physical therapy treatment either in-person or via telerehabilitation.

With the approval of the University of California San Francisco (UCSF) institutional review board, we conducted an ambidirectional study

 with both retrospective and prospective elements. Electronic health record (EHR) data were collected from patients treated at the UCSF Physical Therapy Faculty Practice (PTFP), Mount Zion and Mission Bay centers, between April 1, 2020, and May 1, 2021. Patients were treated via telerehabilitation (using the UCSF information technology department–approved Zoom platform), in-person care, or a combination of in-person and telerehabilitation care. Physical therapists’ schedules included a mix of in-person and telerehabilitation visits each day. Of note, under expanded benefits from the Centers for Medicare & Medicaid Services, telerehabilitation is reimbursed at the same rate as in-person visits.

 Patients were adults with a neuroimmunology diagnosis: MS, neuromyelits optica spectrum disorder, or clinically isolated syndrome.

The following variables were extracted from the EHR: demographic variables (age, sex, employment status); clinical variables (Expanded Disability Status Scale [EDSS] score,

 disease-modifying therapies, comorbidities using the Charlson Comorbidity Index [CCI]); physical therapy-related variables (presenting symptom, symptom duration); and transit-related data (driving distance and time from home zip code, home zip code bike and transit score [calculated via Walk Score Research

] to reflect the quality of the cycling and public transit infrastructure).

Adoption of telerehabilitation was calculated by the number of physical therapy referrals issued during routine care at the UCSF Center for MS and Neuroinflammation and, subsequently, the number of initial physical therapy appointments scheduled from these referrals. We recorded the number of follow-up physical therapy appointments (visits after initial evaluation) scheduled and attended, as well as no-show visits.

Completion of physical therapy treatment was defined as the number of patients who met the physical therapy goals set at their initial appointment and were formally discharged from care (as opposed to not returning to physical therapy). We aimed to identify factors (demographic, disease-related, physical therapy treatment, transit-related) predictive of completing physical therapy treatment.

Qualitative Analysis of Barriers and Facilitators to Telerehabilitation Implementation

From the EHR review, we recorded patients’ reported barriers to attending appointments and completing physical therapy treatment from the subjective portion of the physical therapy notes as well as from patient messages to their physical therapist, when available.

Two of us (A.G. [DPT, PhDc; female; graduate student] and V.B. [MS physical therapy; female; research assistant]) conducted semistructured interviews with 3 of the 5 board-certified neurologic physical therapists who treated people with MS at the UCSF PTFP during the defined study period. These physical therapists were selected via convenience sampling (available for interview and experience treating people with neurological disorders) and were interviewed via Zoom. All 3 therapists provided informed consent to participate in this study. Before the interviews, the authors and physical therapists had working professional relationships, and the therapists were familiar with this study team’s long-term research interests. The semistructured interviews included general professional perspectives on telerehabilitation and the perceived barriers to patients and physical therapists. There were 5 key subject areas: (1) overall experience with the shift from in-person visits to telerehabilitation after SARS-CoV-2 shelter-in-place guidance, (2) barriers to using telerehabilitation technology, (3) characteristics of patients that could support completion of physical therapy treatment, (4) perceived benefits of telerehabilitation compared with in-person rehabilitation, and (5) the anticipated future of telerehabilitation. Interviews were recorded and transcribed using Zoom software. Two of us (A.G. and V.B.) made notes during and after the interviews; they independently developed code lists for salient themes after 1 interview and then discussed and agreed on a consolidated list. This code was then applied to the remaining interviews. These data were then reviewed with the senior author (R.M.B.). The coded data were grouped into the 5 salient themes and described qualitatively due to the low overall number of observations. The Consolidated Criteria for Reporting Qualitative Research checklist

 was used to minimize bias in the qualitative analysis.

In the quantitative analyses of telerehabilitation adoption and completion of physical therapy treatment in the present patient population, we analyzed possible demographic, disease-related, and transit-related predictors for completing physical therapy treatment using multiple linear regression and the LogWorth statistic to determine the contribution of each variable to the outcomes of interest.

 Odds ratios were used to identify relative odds of completing physical therapy treatment with respect to disability status (EDSS score, 0 vs >0) and comorbidity (CCI, 0 vs >0). Statistical analysis of the results and figure generation were conducted using JMP version 15 (SAS Institute Inc).

During the selected period (April 1, 2020, to May 1, 2021), 111 patients with demyelinating disease (109 with MS and 1 each with neuromyelits optica spectrum disorder and clinically isolated syndrome) were referred to the UCSF PTFP and scheduled for an initial visit: 82 (74%) were women; mean ± SD age was 54.2 ± 12.7 years, and median EDSS score was 4.0 (interquartile range, 2.5–6.5) (

). The 3 most common primary symptoms were impaired static/dynamic balance, decreased strength, and impaired gait/mobility. The initial evaluation was in-person (n = 20) or via telerehabilitation (n = 91). After the initial evaluation, 100 patients (90%) scheduled a follow-up appointment. Of the total follow-up appointments scheduled, 31% were canceled, and 60 visits were attended (15 in-person, 45 telerehabilitation). A total of 26 patients (23%) were discharged from physical therapy, of whom 20 (17%) met all their physical therapy goals, completing treatment. Patients who did not meet physical therapy goals (n = 10 [16%]) and did not schedule follow-up appointments were not formally discharged from physical therapy care. Twenty-four patients (20.8%) were still being treated at the time of data collection.

Completion of physical therapy treatment was not found to be associated with demographic, disease-related, or transit-related factors (

). However, patients with no disability (EDSS score, 0) were 73% less likely to schedule a follow-up appointment (in-person or telerehabilitation) than those with some disability (EDSS score, >0) (odds ratio, 0.27; 95% CI, 0.09–0.75; 

Communication between patients and the PTFP was available for 30 of 111 patients (27%). Most patients sent 1 message to the PTFP (n = 14), with 8 patients sending 2 or more messages. Patients cited the following barriers to attending telerehabilitation appointments: conflicts with other medical appointments (n = 11), illness and pain (n = 10), personal conflicts (eg, sick child, work conflict, vacation) (n = 9), preference to see a local physical therapist (n = 4), difficulties with the telerehabilitation platform/technological concerns (n = 4), and preference to wait until vaccinated against COVID-19 to attend an in-person visit (n = 3).

Interviews with neurologic physical therapists revealed several major themes (

, available in a PDF at the end of the online article). For the therapists, the shift from in-person to telerehabilitation during shelter-in-place guidelines occurred with relatively few administrative or financial obstacles. Both patients and physical therapists were flexible because of the emerging public health guidelines, and the transition to telerehabilitation did not result in major lapses in care. One physical therapist noted, “Once patients had their primary care and other appointments over Zoom, it was pretty easy to convince them that virtual physical therapy [was] also really valuable.” Having provided televideo visits using the approved Zoom technology for several years, UCSF was able to rapidly expand this capability to accommodate larger patient volumes. Telerehabilitation could be administered using instruments (eg, computers, tablets, personal smartphones) that are relatively easy to deploy with little burden to either patients or providers.

The 3 physical therapists all reported that the format of the telerehabilitation sessions was the same as the in-person format: sessions consisted of a subjective interview, assessment of range of motion and functional movement, and exercise demonstration and practice.

Two of the physical therapists noted patient barriers to using telerehabilitation technology, and these included poor internet connection, inexperience with video call platforms, limited technological literacy, and the need for an interpreter. One physical therapist mentioned, “Simply being able to access the Zoom platform and position the camera can be a limitation to treating someone.”With respect to the features that supported patients’ ability to receive telerehabilitation care, the therapists cited several patient-, home-, and disease-related factors. First, technological literacy was relevant because substantial time could be wasted troubleshooting rather than engaging in care. “So much time can be wasted figuring out the Wi-Fi network and pointing the camera in the right direction,” a physical therapist mentioned. In addition, a flexible schedule was cited as a positive factor, although this was not clearly relevant to receiving televideo vs in-person care. “It tends to be retired patients and those who work from home who like [telerehabilitation] and attend the most appointments,” a physical therapist noted. The primary home factor noted was enough space to move safely. For patients with more severe physical or cognitive limitations, the presence and support of a caregiver in the home were also noted. Importantly, “The caregiver has to be someone who is comfortable providing support and who is familiar with the patient’s needs. Not all are.”

With respect to functional status, lack of severe balance or mobility impairments that would preclude patients from moving without specialized attention or support (eg, unsafe assistive device use resulting in high fall risk) was noted as a situation in which care could be comparably delivered via telerehabilitation. Of note, a physical therapist mentioned, “Though fall risk might limit the scope of our session, there is still plenty we can do seated and it’s a great time to provide patient education.” The primary symptom for physical therapy referral was also a factor influencing the success of telerehabilitation. For example, physical the therapists felt that vestibular symptoms or facial paralysis are readily treatable via telerehabilitation, partially due to the fact that they require less specialized equipment or tactile input. Conversely, patients with balance and gait impairments, or who are otherwise at risk for falls, can be safety concerns and may not be appropriate for telerehabilitation. “Depending on the level of impairment, I might be able to work on balance from a seated position, but what they really need is to practice standing,” a physical therapist said in reference to modifications for telerehabilitation. These patients may also not experience as much benefit from telerehabilitation compared with in-person access to specialized equipment (eg, a patient who requires use of a ceiling harness for mobility training).

Although not related to telerehabilitation in particular, in contrast to more vague goals (eg, “I want to walk better”), the creation of attainable goals (eg, “I would like to be able to walk my dog for 1 mile”) was identified as a key factor in enhancing patient motivation. This factor was more common in patients who completed their physical therapy goals and were discharged from care because they would be more likely to adhere to a plan of care provided exclusively via telerehabilitation. Explicit and shared goal-setting may be particularly important in nurturing patient motivation from a distance.

Conversely, some factors were identified as representing specific barriers to telerehabilitation visits, leading to at least some, perhaps initial, in-clinic physical therapy treatment. Specifically, the need for human contact and tactile cues was noted for patients with either cognitive impairments or those who spoke languages other than English. For these patients, auditory cues alone via telerehabilitation might be insufficient to provide high-quality physical therapy: “Sometimes I find that verbal cues [aren’t] enough; we need to do tactile demonstration and external feedback and sometimes that is really hard to do over telerehabilitation,” a physical therapist said.

Cognitive impairment was noted as a barrier for 2 reasons. First, it can preclude use of telerehabilitation technology. Second, people with MS with cognitive impairments often have difficulties with concentration or are unable to attend to a task; video conference makes redirection challenging. Therefore, patients without substantial cognitive impairments were identified as more likely to benefit from telerehabilitation. However, a physical therapist mentioned, “If someone who is cognitively impaired has a really awesome caregiver, you can still have a great session. A caregiver who is really engaged and is comfortable making sure the patient is safe can make it possible to treat someone with cognitive impairment over Zoom.”

The perceived benefits of telerehabilitation vs in-person visits included reduced patient travel burden and improved scheduling flexibility. The reduction of travel time was noted by the 3 physical therapists as especially beneficial for patients who are unable to drive or travel independently, as well as for those who have full-time jobs and/or dependents. Telerehabilitation allowed patients to practice exercises in their homes, supervised by physical therapists. It also gave the therapists an understanding of the patients’ general home layouts and circumstances, as well as potential safety concerns present in their environments. One physical therapist endorsed the benefits of examining home environments, stating, “One really nice thing about [telerehabilitation] is getting a glimpse into a patient’s home which you normally wouldn’t get. You can provide suggestions for their bed or stairs set-up to help them reach their goals.” In addition, physical therapists noted that whereas in-person visits are focused on movement quality and analysis, telerehabilitation allows more time for explanation and education, the foundations of successful rehabilitation, particularly for those with neurologic conditions.

Finally, with respect to the future of telerehabilitation, the physical therapists interviewed indicated that a hybrid in-person/telerehabilitation model would be ideal for care, supporting an in-clinic to in-home continuum of care. One physical therapist said, “I think having [telerehabilitation] as an option is great to provide patient education and [for] patients who need some help tailoring their home program,” and another mentioned, “In between in-person sessions, [telerehabilitation] visits can be helpful so patients don’t have to come in as often.” Telerehabilitation allows for more flexible scheduling, is beneficial for providing education and counseling, and can improve access for those with higher disability and in areas geographically distant to specialized MS physical therapy care; however, some objective measures (eg, Berg Balance Scale) need to be completed in person and are critical for measuring patient progress toward goals, supporting a hybrid model of care. In addition, for patients with cognitive and visual impairments, verbal cues provided via telerehabilitation may be insufficient, and tactile support in-person may be beneficial.

This study, leveraging data on the adoption and completion of MS physical therapy treatment via telerehabilitation in the initial response to the COVID-19 pandemic at a large, urban medical center, contributes insights into telerehabilitation barriers and facilitators for people with MS. These include both patient-related factors (eg, disability level, employment) and therapist perspectives on designing safer, more effective, and more accessbile hybrid models for physical therapy care.

Interestingly, only 17% of insured people with MS completed all recommended sessions and met their treatment goals. Although we explored a variety of patient-, disease-, and transit-related factors, only increasing EDSS status was associated with meeting physical therapy goals. For patients with no disability (EDSS score, 0), scheduling and attending any type of physical therapy appointment may have represented less of a priority in the face of other personal and professional obligations, if the value of prophylactic rehabilitation care was not well established or appreciated. Other additional and nonexclusive barriers to treatment completion likely include systemic barriers, such as limited insurance coverage and low insurance reimbursement for physical therapists.

The practicing physical therapists’ preferences were for a hybrid MS rehabilitation model, with the optimal balance of in-person and telerehabilitation-enabled care determined based on a variety of patient-specific factors. The physical therapists suggested that an initial in-person visit may be warranted in persons with cognitive impairments to help provide nonverbal feedback and tactile cues, but other strategies to support home-based delivery may be used. A stepwise set of measures before beginning exercises was suggested to optimize safety during telerehabilitation for patients at greater risk for falls or with cognitive impairment: (1) obtaining an emergency telephone number for someone who can rapidly assist the patient if needed, (2) restricting the patient’s space with physical supports, (3) teaching the patient and/or caregiver fall prevention strategies (eg, using external supports such walls and chairs), and (4) asking the patient and/or caregiver to perform a home safety evaluation (eg, checking for loose rugs, uneven ground). Finally, physical therapists should learn redirection strategies that help people with cognitive impairments to return their attention to the rehabilitation activities.

Other areas that need to be addressed include patient technological literacy (eg, asking patients to attend an educational webinar on the use of the communication platform) and instructional clarity (ie, to support patient comprehension at all cognitive levels, perhaps with the assistance of a caregiver). Some of the barriers identified may also be relevant to reducing the risk and improving the effectiveness of the interventions.

The major limitation of this study was the retrospective data collection. In the future, quantitative and qualitative studies should investigate patient-, clinician-, and organization-level implementation barriers, especially for selected (eg, advanced disability) and underrepresented (eg, minority, rural) patient populations. Patient reports were collected from the subjective portion of physical therapy clinical notes, which may not have been exhaustive. Nonetheless, we believe that these pragmatic findings can inform the approach to MS telerehabilitation in other centers.

Although inclusion of qualitative data augments this analysis by providing exploratory insights regarding barriers and facilitators to telerehabilitation, the study design was not rooted in a specific qualitative method; the study would likely have been strengthened by discussion of data saturation, returning transcripts to physical therapists for comment, and obtaining feedback from physical therapists on the findings.

These results support the expanded use of telerehabilitation for MS care. A recent study from our institution suggests that implementation of telerehabilitation to orthopedic populations during shelter-in-place guidelines was feasible, and both patients and physical therapists were highly satisfied.

 Telerehabilitation is a burgeoning and valuable alternative method of delivering physical therapy services to people with MS

; it offers personalized interventions conducted by neurologic physical therapists, adapting the treatments based on the patient’s needs, expediting access to specialized physical therapy care, and saving time and opportunity costs.

 It is, however, important to acknowledge previous work that identifies the shortcomings of the rapid adoption of technology in other health populations (eg, veterans,

). This work seeks to expand on an existing framework

 to identify limitations, specifically as it relates to the delivery of physical therapy care, to inform future directions of more inclusive telerehabilitation models. Telerehabilitation extends delivery of care to more people with MS at all stages of the disease.

 This includes both younger patients with lower disability who are in the workforce, as well as more disabled or more remote patients for whom access is a major issue. The present study extends these observations by highlighting the qualitative factors that could be used as predictive factors in future efficacy trials and to optimize the delivery of MS telerehabilitation care.

Telerehabilitation can reduce barriers to care access for people with demyelinating disease. Although no demographic or transit-related factors were found to be predictors of completing physical therapy treatment, patients with minimal disability were less likely to complete treatment through a combination of telerehabilitation and in-person visits.

Physical therapists treating people with MS identified reduced travel burden and scheduling flexibility as benefits of telerehabilitation, and low technological literacy, cognitive impairment, and high fall risk as barriers. A hybrid model for physical therapy could include telerehabilitation, which is conducive to providing patient education, whereas in-person visits would enable collection of objective data (eg, reactive balance) and may be preferred for patients with cognitive and visual impairments.

Accessibility to Telerehabilitation Services for People With Multiple Sclerosis: Analysis of Barriers and Limitations

Multiple sclerosis (MS) is an inflammatory central nervous system demyelinating disorder resulting in neurologic decline. Patients predominantly have a relapsing and remitting disease course requiring multiple hospitalizations and, occasionally, rehospitalizations. Hospitalization readmission rates are important metrics that have direct financial implications for hospitals and serve as an indicator of disease burden on patients and society. We sought to analyze hospital readmissions of patients with MS and identify the subsequent predictive characteristics/comorbidities for readmission.

All hospital admissions due to MS were queried using the 2017 Nationwide Readmissions Database. All patients with nonelective rehospitalization within 30 days of discharge were examined.

The 30-day readmission rate for MS is 10.6% (range, 10.4%–10.8%). Female sex has a protective role in readmission rates, and age has no effect. Comorbidities, including heart failure, acute kidney injury, chronic obstructive pulmonary disease, chronic kidney disease, respiratory failure, substance abuse, diabetes, hypertension, peripheral artery disease, liver failure, anemia, coagulation disorders, cancer, depression, and infections, are predictive of readmissions, whereas sleep apnea is protective. No effect is seen with neurologic blindness, plasma exchange, or intravenous immunoglobulin treatment.

Several medical comorbidities are predictive of hospital readmission of patients with MS. Most rehospitalizations are due to infectious and neurologic etiologies; thus, targeted interventions may lead to lower readmission rates.

From the Department of Neurology (AP, WK) and Department of Internal Medicine (AA), University of South Alabama College of Medicine, Mobile, AL, USA. 

 Akhil Padarti, MD, Department of Neurology, University of South Alabama College of Medicine, 2451 USA Medical Center Dr, Mobile, AL 36617, USA; 

 Dr Kilgo is on the speakers’ bureaus of Biogen and Genentech; serves as a consultant for Genentech, Biogen, and Alexion Pharmaceuticals; and is a principal investigator for industry-sponsored clinical trials in association with Genentech; EMD Serono, Inc; and Bristol Meyers Squibb. The other authors have disclosed no relevant financial relationships.

Multiple sclerosis (MS) is an inflammatory demyelinating disease of the central nervous system.

 In most patients with MS, the disease follows a relapsing and remitting course resulting in neurologic disability. The prevalence of MS has increased in both developed and developing countries in part due to improvements in diagnosis and the development of novel disease-modifying agents.

 Multiple sclerosis is the leading cause of nontraumatic neurologic disability in younger adults.

 Medical costs of MS rank second only to those of congestive heart failure,

 and hospitalizations remain a significant portion of these costs: patients with MS are 3.5 times more likely to be hospitalized relative to the general population.

 With the growing prevalence of MS, it is imperative to decrease unnecessary readmissions to alleviate the health care system burden.

Hospital readmissions are also associated with negative patient outcomes, including hospital-acquired infections, deconditioning, and negative psychological effects.

 Therefore, readmission rates are an important quality measure, and understanding these rates will lead to identification of preventable adverse outcomes. The 30-day readmission rate is widely used as the indicator for hospital performance associated with financial implications.

 The identification of patients at high risk for readmission is the initial step to decrease readmissions and improve overall disease control.

Many studies have been published on hospital readmission rates,

 but there is minimal readmission data regarding MS. One current study is analyzing the trends in a European cohort.

 The only US study, published by Patel et al,

 analyzed MS readmissions stratified by age and sex. To date, the present study is the largest to analyze MS readmission rates in the general US population and the first study of MS readmission rates to use 

International Classification of Diseases, Tenth Revision (ICD-10)

 codes. Compared with previous versions, the 

 provides more specific diagnosis and procedural codes and minimizes misclassification of patients and procedures.

 The purpose of this study was to identify patients with MS at high risk for readmission within 30 days of their initial discharge.

This study examined MS hospital readmissions using 2017 discharge data from the Nationwide Readmissions Database (NRD) of the Healthcare Cost and Utilization Project (HCUP) developed by the Agency for Healthcare Research and Quality (AHRQ). The data provided a national representative sample of all-age, all-payer discharges from US nonfederal hospitals across 28 states.

 This was 18 million discharges (weighted estimate ~36 million discharges). All hospitalizations and rehospitalizations were determined using a deidentified unique patient linkage number. The data used represented 58.2% of all 2017 US hospitalizations.

The MS definition was determined by codes from Clinical Classifications Software Refined (CCSR) for the 

; all supplemental material is available in a PDF at the end of the online article). The primary outcome was the first unplanned readmission, defined as a nonelective rehospitalization within 30 days of discharge from the patient’s index hospitalization. If a patient had multiple such readmissions, only the first encounter was used for analysis. Exclusion criteria included admission in December, death during the initial hospitalization, and missing discharge data. The study was approved for exempt status by the University of South Alabama’s institutional review board. Similar methods have been used in previous studies.

 codes were used to define pertinent clinical variables. Data on teaching status, metropolitan/non-metropolitan location, control/ownership, and bed size were collected for each hospital (

). A cost analysis covered index admission length of stay, index admission cost, discharge destination, primary expected payer, and quartile of median household income (Table S2). We multiplied the hospital charges with the AHRQ’s all-payer cost-to-charge ratios to determine total cost. Severity of MS at the index hospitalization was measured by risk of mortality and loss of function subclasses (Table S2). Baseline patient comorbidities and procedures during the index hospitalization were determined (Table S2). The first CCSR diagnosis code determined the cause of readmission (

). All CCSR codes used in this study are presented (Table S1).

Statistical analysis was performed using IBM SPSS Statistics for Windows, version 1.0.0.118 (IBM Corp). To reduce bias, the data were weighted as recommended by the NRD. Two-sided 

 tests with a significance level of .05 were used for statistical analysis. Statistical differences in participants’ baseline characteristics were determined using the Pearson χ

 test for categorical variables and the Mann-Whitney 

 test for continuous variables; the reference group was participants with no readmissions. Multivariable logistic regression analysis was performed to determine the predictors of readmission, with adjustments for age group, sex, hospital status, and comorbidities (

Of 95,537 weighted admissions in the 2017 NRD with MS as the primary diagnosis, 10,102 patients were readmitted within 30 days of discharge. Patients with a primary diagnosis of MS were defined as those admitted for MS flare-ups and those admitted for MS workups and subsequently diagnosed as having MS. The 30-day readmission rate for the general population of patients with MS was 10.6% (range, 10.4%–10.8%) (

). The readmission frequency is highest in the first days after discharge, with decreasing frequency over the course of 30 days. Half of all readmissions occurred within 12 days of discharge from the index hospitalization.

The baseline characteristics for the index hospitalization are shown in Table S2. Most of the patients in the study were women aged 46 to 67 years, consistent with the epidemiology of MS. Readmission was less frequent for women than for men (10.2% vs 11.7%; 

 < .001). Patients with a weekend admission (

 = .002), a longer index hospitalization (

 < .001) were statistically significantly more likely to be readmitted. Patients with private insurance were less likely to be readmitted than were patients with Medicare. Patients in the top or bottom quartile of household income were more likely to be readmitted than those in the middle 2 quartiles. Patients with a higher risk of mortality and a loss of function were more likely to be readmitted in a severity-dependent manner. Interestingly, patients discharged to their homes with no services were less likely to be readmitted than those discharged with home health care or those transferred to a short- or long-term care facility.

Patient Comorbidities and Procedures During Index Hospitalization

Table S2 shows the effects of patient comorbidities and intravenous immunoglobulin (IVIg) and plasma exchange (PLEX) treatments on readmission rates. Higher readmission rates were seen in patients with the comorbidities analyzed except for alcohol abuse, hypertension, and obesity. Statistically significantly lower readmission rates were seen with neurologic blindness. There was no significant difference in readmission rates after PLEX or IVIg treatment.

Readmission diagnoses are shown in Table 1. The 3 most common causes of readmission were infectious complications (24.8%), neurologic complications (14.5%), and respiratory complications (6.9%), which correspond to 46.2% of all readmissions. Septicemia was the most frequent diagnosis for readmission (15.4%). The most frequent neurologic diagnosis of readmission was MS (9.0%). Other infrequent causes of readmission include complication of the genitourinary device (5.7%), urinary tract infection (4.1%), acute respiratory failure (2.2%), acute renal failure (2.1%), heart failure (2.1%), and pneumonia (2.0%).

Multivariable logistic regression analysis was preformed to identify the characteristics of patients at high risk for 30-day readmission (Table 2). Age was not predictive of readmission; all age groups studied had similar readmission rates. Relative to the Medicaid population, patients with private insurance (odds ratio [OR] = 0.679; 

 < .001), self-pay patients (OR = 0.776; 

 = .008), no-charge patients (OR = 0.537; 

 = .022), and other (insurance options, eg, workers’ compensation and other government programs) (OR = 0.651; 

 < .001) were protective against readmission (Table 2). Nonmetropolitan hospitals had decreased odds of readmission relative to nonteaching metropolitan hospitals (OR = 0.811, 

 < .001) (Table 2). There was no significance between metropolitan teaching hospitals and metropolitan non-teaching hospitals (OR = 0.999, 

 = .970). Several comorbidities, including heart failure (

 < .001), chronic obstructive pulmonary disease (

 < .001), are predictive of readmissions, whereas sleep apnea (

 = .241) treatment during the index hospitalization affected the odds of readmission.

This retrospective study analyzed 30-day readmission rates in patients hospitalized with a primary diagnosis of MS. Approximately 1 in 10 of these patients (10.6%) had a readmission within 30 days of discharge. This rate is relatively better than the overall readmission rates in the general population (13.9%) and in patients with nervous system diseases (14.0%).

 This finding is likely multifactorial and may be due to the broadening treatment landscape for MS, including more efficacious disease-modifying therapies. The readmission rate in this study is comparable with those in the previous European

Relapsing-remitting MS predominantly affects women, with a prevalence ratio of approximately 3:1.

 A similar sex ratio was seen in MS index hospitalizations, with women being 73.7% of all hospitalizations. However, this study found that female sex protected against readmission (Table 2). Previous studies have found that MS disease activity is more aggressive in men, specifically with earlier disability accumulation. This may be in part due to delays in seeking care, hormonal differences, or the increased percentage of men with primary progressive MS.

 Neither of the previous studies found a statistically significant sex difference for readmission.

 It is possible that the sex difference was discovered only because of the larger sample size in this study. In the general population, age is a factor in readmission rates, with readmission rates increasing as age increases.

 However, although readmitted patients tended to be older (Table S2), age was not predictive of readmissions after accounting for comorbidities (Table 2). This finding suggests that the comorbidities associated with older age play a larger role than age itself, as supported by the findings in earlier studies.

 Patients with Medicaid and patients with Medicare had similar odds of readmission, and all other types of insurance were protective (

). A similar trend was also identified in a previous study

 and is seen in the general population, as private insurance is obtained through employment and employed people have a higher baseline functional status.

 Only a small proportion (8.6%) of patients in this study were admitted to nonmetropolitan hospitals, perhaps because patients with severe MS relapses go to or are transferred to a metropolitan hospital with an affiliated MS specialist. Therefore, the disease severity is likely higher at metropolitan hospitals vs nonmetropolitan hospitals, accounting for the increased readmissions. This difference was not observed in the earlier study, possibly due to the smaller sample size.

Several studies have shown an increase in MS disease burden and hospitalizations over time,

 thought to be due to the progressive nature of the disease leading to higher disease burden in older patients. However, our data showed that, accounting for comorbidities, age is not a factor in hospital readmissions for patients with MS. Therefore, the increased comorbidities associated with aging are the likely cause of hospital readmissions rather than the progressive nature of MS. This is also shown by the stepwise increase in hospitalizations, the loss of function, and likelihood of dying in the All Patient Refined Diagnosis Related Groups (Table S2). These scales represent disease severity and preexisting conditions. Therefore, the higher the number of comorbidities, the higher the risk of loss of function or the likelihood of dying. Other studies reached the same conclusion.

The comorbidities that increased the odds of readmission are shown in 

. Many of these comorbidities have been previously identified as factors in MS rehospitalization, including heart failure,

 Several comorbidities, including hypertension, diabetes, and peripheral artery disease, lead to vascular damage due to oxidative radicals. The increased oxidative stress in the brain parenchyma has been shown to be a mediator of demyelination.

 However, in another study, hyperlipidemia, also a contributor to vessel damage and plaque buildup, was not shown to be predictive of readmission, although hypertension, diabetes, and obstructive lung disease were shown to worsen functional status in MS.

 The reproducibility of this effect may suggest that the oxidative damage of hyperlipidemia has less of an impact in MS than do diabetes and hypertension. In our study, optic neuritis did not affect readmission rates, likely as it is commonly seen in younger females with milder forms of the disease. In a previous study, optic neuritis was found to be protective of readmission.

 An unexpected finding was smoking’s lack of effect on readmission. Smoking has been shown to be a risk factor for MS and is associated with a poorer prognosis.

 However, the present data showed that smoking did not increase readmission odds. Sleep apnea was the only comorbidity protective against readmission in the present study. Further research is needed to determine whether this is an incidental finding or whether sleep apnea has a protective effect in MS.

Two treatment options for acute MS relapses are PLEX and IVIg, which circulate antibodies to decrease the host immune response. However, these treatments are generally reserved for persistent flare-ups that do not improve with intravenous corticosteroid use.

 Previous studies have suggested better outcomes with PLEX

 Treatment with neither PLEX nor IVIg was seen to affect readmission rates (Table 2). Because IVIg and PLEX treatments are reserved for resistant relapses, these patients may already have a higher likelihood of readmission. These second-line treatments may decrease readmissions such that no measurable effect can be identified on statistical analysis. Furthermore, few patients (approximately 0.5%) received PLEX or IVIg during their index hospitalization. These results are in accordance with the previous study in which no association was seen between PLEX/IVIg treatment and readmission in most of the subgroups analyzed, and in the few subgroups that showed statistical significance, PLEX/IVIg treatment increased readmission rates.

Analysis of readmission etiologies showed that the most common were infections (24.8%), predominantly nonspecific septicemia (15.4%) (Table 1). Patients with MS are at increased risk for infections: diaphragmatic weakness can lead to pneumonia, and neurogenic bladder can lead to urinary tract infections. Immunosuppressive drug use also contributes to the overall risk of infection. The second most common readmission cause was neurologic diagnoses (14.5%). This contrast with the previous analysis, which showed that half of all readmissions were due to neurologic complications.

 This difference may be explained by the improved treatment modalities developed for MS during the past several years. Other etiologies of readmissions are respiratory complications (6.9%), surgical device complications (6.7%), and cardiac complications (5.3%). Future research could use artificial intelligence and machine learning to develop algorithms to predict the patients at high risk for rehospitalization, and this could help physicians improve patient care and health care outcomes.

This study successfully used the 2017 NRD to identify characteristics of patients with MS with an increased likelihood of hospital readmission within 30 days and the specific etiologies of those readmissions. Many other studies have been conducted using the same methods.

 This study’s limitations follow. The NRD stores 

 codes for every encounter. Patients admitted through the emergency department and patients admitted for observation are not included in the database. Another constraint is the elements captured by the database. Race and ethnicity data are not available, limiting insight. Geographic information also is not captured by the database,

 although MS has a strong geographic distribution pattern. Importantly, no information is provided about a patient’s current medications or discharge medications, precluding the ability to distinguish patients who are taking disease-modifying agents that help control the disease. These factors likely play a role in readmission rates.

Misclassification bias is also present in this study. Although 

 coding is designed to improve accuracy and decrease coding errors, inaccuracies are likely still present. These are expected drawbacks when using a large database containing approximately 60% of inpatient admissions in the United States. Finally, because this is a retrospective, observational study, no statement about causation can be made from the data. The strength of the study as the largest readmission analysis of patients with MS to date remains.

During the past several decades, significant progress has been made in the management of MS. The disease burden, both financial and patient quality of life, has decreased due to a better understanding of the disease and increased treatment options. Hospital readmissions are a significant portion of the remaining disease burden of MS. This study identified several characteristics of patients at high risk for readmission. The most common causes of readmission are sepsis, MS, and respiratory failure. Future efforts to equip these patients with additional resources for better outpatient transitions might lead to decreased readmission rates, lessening the disease burden on patients with MS and on society at large.

Readmission Rates in Patients With Multiple Sclerosis: A Nationwide Cohort Study

Patients with multiple sclerosis (MS) were vulnerable to the effects of physical inactivity during the COVID-19 pandemic. As patients returned to in-person visits, providers reported seeing increased weakness, balance issues, falls, worsening pain, and spasticity. Social isolation also contributed to increased stress, depression, and anxiety. This study explored whether attending virtual wellness programs was associated with improvements in standard quality of life questionnaire scores for patients with MS.

The purposive convenience sample consisted of 43 patients in the treatment group and 28 in the control group. Patients in the treatment group attended 2 monthly programs for 6 months and completed a demographic questionnaire, the 36-Item Short Form Health Survey (SF-36), the Modified Fatigue Impact Scale, and the Medical Outcomes Study Pain Effects Scale (PES). Patients requested additional topics, resulting in 5 additional programs. The control group consisted of patients who chose not to attend the programs but agreed to complete the questionnaires.

In comparing questionnaire responses (6 months minus baseline) among the participants in the treatment group, an association was found between higher meeting attendance and improvements in emotional well-being (

 = .011), mindfulness on the SF-36 pain scale (

The results of this study suggest that a virtual wellness program may provide beneficial emotional support, physical exercise, and health promotion activities resulting in improved quality of life in people with MS. In addition, mindfulness and exercise programs may be beneficial in pain management.

From the Department of Neurology, University of Pennsylvania, Philadelphia, PA, USA (DJ, NG, VZ); the Department of Biostatistics, Epidemiology, and Informatics, University of Pennsylvania, Perelman School of Medicine, Philadelphia, PA, USA (SMW); and Philadelphia, PA, USA (ER). 

 Vanessa Zimmerman, MSN, Department of Neurology, University of Pennsylvania, 3400 Civic Center Blvd, Philadelphia, PA 19104, USA; 

: vanessa.zimmerman@pennmedicine.upenn.edu.

 The authors declare no conflicts of interest.

 Ms Weinstein provided statistical support and is funded by the National Science Foundation Graduate Research Fellowship Program. External speakers were paid honoraria supported by a grant from the Board of Women Visitors of the Hospital of the University of Pennsylvania and funding earned through successful completion of annual projects with the Neuroscience Service Line of Penn Medicine.

 Aspects of this study were presented in poster form at the Consortium of Multiple Sclerosis Centers Annual Meeting; October 25-28, 2021; Orlando, Florida.

Multiple sclerosis (MS) is a common, chronic, lifelong, unpredictable, and potentially highly debilitating neurologic condition that occurs more commonly in women than in men. It strikes most often in young adulthood but can even start in childhood and adolescence. There are nearly 1 million people living with MS in the United States.

The COVID-19 pandemic affected every activity of the Penn MS and Related Disorders Center at the Hospital of the University of Pennsylvania. Clinic visits were initially halted and then switched to a virtual format. Many patients were isolated by stay-at-home orders. As some patients began to return to in-patient clinic visits, providers found that deconditioning related to limited activity had resulted in increased weakness, spasticity, and balance issues, as well as increased pain. Patients also reported increased stress, depression, and anxiety.

For many, the pandemic created a wide range of long-term challenges, which are correlated with worsening neurologic symptoms in patients with MS.

 Although patients were encouraged to self-isolate for protection from the virus, for some it posed a threat to their physical and mental well-being

 and resulted in reduced quality of life.

 In 1 online survey, researchers found that 50% of patients with MS either reduced or ceased their physical activity during the pandemic and 32% reported that their fitness level had decreased.

To help patients with MS during the pandemic, Penn Center providers decided to offer virtual wellness programs. People with MS are becoming more interested in the concept of wellness,

 and there is evidence to suggest that in addition to disease-modifying therapies, lifestyle strategies that support wellness can help mitigate disease-related complications and comorbidities.

Abdel-Rahman Abdel-Aal, MSc

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