The unprecedented COVID-19 pandemic has required the use of social distancing and shelter-in-place orders to mitigate the spread of infection, which have created a need to rapidly adapt to the use of telemedicine in lieu of in-person visits in clinical practice. There are advantages and challenges of virtual visits. Advantages include continuity of care during the pandemic, travel convenience, access to specialists in underserved areas, and reduced microbial exposure for patients, providers, and staff alike.1 Challenges include the potential loss of face-to-face communication and observation of body language, diagnostic issues, potential technology failures, limited physical examination capabilities, and reimbursement challenges. The recent pandemic-related exemption for nonreimbursement of telemedicine by the Centers for Medicare and Medicaid Services (CMS) has mitigated the last of the challenges listed, for the time being.2

Teleneurology—the use of technology to provide remote neurologic care—has been utilized most in acute stroke management in rural areas because of the need for timely interventions.3 Across multiple neurologic subspecialties, including stroke, pain management, nonacute headache consultation, Parkinson disease, and epilepsy, teleneurology has shown noninferiority for efficacy and patient and caregiver satisfaction compared with in-person evaluations.4-8 Teleneurology has also had a role in routine follow-up visits and end-of-life care for individuals with amyotrophic lateral sclerosis (ALS), in which in-person visits sometimes are not possible because of the disease course.9 The current goals of teleneurology are to provide a high standard of care, offer the best treatment options possible, and avoid visits to urgent and emergent care settings to decrease exposure to and spread of COVID-19.

Practical Considerations for Teleneurology

With the rapid surge in COVID-19 incidence in the US beginning in early March 2020, many institutions rapidly implemented telehealth visits. Between March 13 and April 20, 2020 our neurology department at Wake Forest Baptist Medical Center comprised of 53 faculty clinicians conducted 1,113 video and 1,195 phone televisits, 73 and 102 of which, respectively, were for the neuromuscular clinic. During this time, we have worked through the logistics of a large-scale shift in the clinical workflow to meet the still growing volume of teleneurology visits; process charts for this workflow are available at the end of the online version of this article ( eFigure).

In our experience thus far, teleneurology visits have been well received by patients and clinicians alike. Patients appreciate the convenience, decreased microbial exposure, and the care expressed by their neurologist, with whom there is often a long-standing relationship. Certain patients may be more amenable to this type of visit than others. For example, a patient or their family must have access to technology for the video visit. The clinic also must have a team of dedicated clinical staff to help guide patients through the process of connecting virtually. Some evaluations may be more challenging over video, such as a new patient visit, especially if the diagnosis is challenging or components of the physical examination are essential for diagnosis. Asking the patient to have another person present during a visit is helpful in case assistance is needed (eg, having someone else hold the device so the patient’s gait or a specific muscle area can be examined).

From the clinician’s perspective, our team in the neuromuscular clinic has found the flexibility of video visits and the ability to continue treating our patients as a marker of enhanced job satisfaction. Logistically, we find it most effective to use a mobile device to connect with the patient via video while using a desktop or laptop computer for chart review and documentation. The visit must start with verbal consent that can be created as a smart phrase for easy use. The patient can participate in the history and complete many pertinent parts of the physical examination, although there are limitations. Procedures and certain select visits will still require in-person care, and teleneurology can augment that. We are also able to include trainees (ie, residents and fellows) by allowing the trainee to initiate the virtual visit and then discussing the case individually over the phone or setting up a web-based group meeting or conference call.

Teleneurology in Neuromuscular Medicine

Teleneurology has been used, to varying degrees, in neuromuscular medicine for decades.10 Individuals with neuromuscular disease are vulnerable to struggles with weakness, imbalance, pain, and, in many cases, chronic immunosuppression. These struggles create barriers to accessing care, making people with neuromuscular disease good candidates to reap the benefits of teleneurology check-ups (Table 1). Myasthenia gravis (MG) is among the most frequent reasons for a consultation in the neuromuscular clinic. We review a modified approach to the virtual evaluation of patients with MG and touch on teleneurology in other neuromuscular diseases.

Myasthenia Gravis

Although rigorous studies of teleneurology for treatment MG are lacking, MG is an area of neuromuscular medicine for which improved access to care and reliable management are needed. The chronic nature of MG and the use of steroids and immunosuppressants create a need for frequent medication monitoring, symptom evaluation, and repeated education to avoid myasthenic crisis and other associated complications.11 Pertinent parts of the physical examination relevant to MG—the cranial nerves—can be observed by the physician during teleneurology visits.

As an autoimmune disease, MG is characterized by fluctuating weakness and fatigue of ocular, limb, and/or bulbar muscles. Among people with MG, 80% are immunosuppressed at some point in their life12 and are at higher risk for infections, including COVID-19. Virtual visits are thus specifically beneficial to people with MG taking immunosuppressants and those with driving difficulties caused by ocular and limb muscle weakness. Compared with other neuromuscular conditions, a physical examination with audiovisual input is feasible for MG because the sensory and deep tendon reflexes are typically unaffected.

There are reliable and valid clinical measures for MG that can be used in the clinic or research setting. These measures include the quantitative MG (QMG) test, manual muscle test (MMT), and MG composite scale (MGC).13,14 The QMG and MMT are physician-reported tests whereas the MG composite is a hybrid of physician and patient-reported test items. Our neuromuscular medicine team modified these established scales into the teleMG scale by adjusting the existing validated screening instruments that can be used in the clinical assessment of MG (Table 2) during a teleneurology visit. Although it has yet to be validated, the teleMG scale can be especially helpful for monitoring changes in follow-up visits (Figure). A telehealth appointment with video is ideal for use of the teleMG scale, but it can be modified for a telephone visit if needed. The telephone version may include measures of breathing (single breath count) and speech or patient-reported scales (MG-quality of life [QOL] or MG activities of daily living [ADL]).15,16

<p>Figure: Woman with generalized seropositive myasthenia gravis being examined during a telehealth visit. Ptosis with frontalis contraction is apparent. After standing with arms outstretched at baseline (A), there is arm weakness after sustained abduction for 10 seconds (B). While sitting with shoulders abducted, elbow flexed, and wrists and fingers extended, mild wrist and finger extension weakness is apparent at baseline (C). Prominent finger extension weakness occurs after 10 seconds of sustained wrist and finger extension.</p>

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Figure: Woman with generalized seropositive myasthenia gravis being examined during a telehealth visit. Ptosis with frontalis contraction is apparent. After standing with arms outstretched at baseline (A), there is arm weakness after sustained abduction for 10 seconds (B). While sitting with shoulders abducted, elbow flexed, and wrists and fingers extended, mild wrist and finger extension weakness is apparent at baseline (C). Prominent finger extension weakness occurs after 10 seconds of sustained wrist and finger extension.

Amyotrophic Lateral Sclerosis

Because of progressive neurodegenerative loss of motor neurons, individuals with ALS require frequent monitoring and benefit from a multidisciplinary approach. The ALS Functional Rating Scale (ALSFRS) is validated and can be successfully administered with the help of caregivers during a telephone or video visit. The use of the ALSFRS allows for monitoring disease progression and effects of some interventions.17 Simple pulse-oximetry monitoring by patients can be used to assess respiratory status.18 In a 2017 study of ALS health care providers conducting video visits, the most commonly addressed issues were medication management, goals of care, and research, with a change in the patient’s medication regimen being the most common medical action taken as a result of a telehealth visit. The average telehealth visit in this study lasted 32 minutes (SD±12; range, 7-69 min). Technical problems occurred in 14% (8/56) of visits related to audio and/or video; however, no visits were canceled because of these technical difficulties.9

Neuropathy

Teleneurology visits for people with neuropathy address symptom management, medication modification, and treatment adherence. Physical examination maneuvers are limited, but simple muscle strength assessment and gait assessment can be informative. Telepresenters (medical personnel who participate in the visit and are trained in abbreviated neurologic examinations) allow for further assessment of necessary components such as further strength, sensory, and deep tendon reflex testing.19 In patients with chronic inflammatory demyelinating polyneuropathy (CIDP), using the Inflammatory Neuropathy Cause and Treatment (INCAT) score may help with monitoring disease progression and allow immunotherapy modification.

Myopathy

When evaluating a patient with myopathy, the neurologist must ensure accurate diagnosis and monitor for complications such as cardio-pulmonary dysfunction. A few studies evaluating the role of teleneurology for individuals with myopathy have been conducted in participants with facioscapulohumeral muscular dystrophy (FSHD) and Duchenne muscular dystrophy (DMD).18 Individuals with severe physical disabilities and chronic respiratory failure benefited from home telemonitoring for cardiorespiratory parameters, namely oxygen saturation, heart rate, and blood pressure, which were measured using a pulse-oximeter and a blood pressure machine. The use of teleneurology facilitated the detection of subclinical deterioration and timely neurology consultation to reduce hospital admission.20 Cardiorespiratory monitoring, psychosocial support, nutritional consultation regarding diet and body mass index (BMI), and other specialist consultations are some important interventions that can be provided via teleneurology for people with chronic myopathy.

Future Directions and Postpandemic Teleneurology

The way we practice neurology will continue to shift and new capabilities will arise in the field of teleneurology. Fluid work models for physicians may provide increased job flexibility and satisfaction. Teleneurology may play a larger role in education as we incorporate learners as some pilot programs have already investigated.21 Teleneurology may prove more cost efficient.19 Patients may benefit from access to care during nontraditional office hours. Teleneurology for neuromuscular medicine will require more investigation, such as validation of the teleMG scale that is underway, and the global COVID19 pandemic has fast-forwarded this initiative. For now, our obligation remains in the safety and well-being of our patients and teleneurology is a way to fulfill this obligation.

Summary

Despite the limitations of a teleneurology visit, effective assessment for a number of neuromuscular disorders can be accomplished as discussed. In most cases, patient and provider satisfaction for telehealth visits has been equivalent, and efficacy has shown noninferiority when compared to in-person visits across multiple neurologic subspecialties. Teleneurology remains an important strategy to mitigate the extensive repercussions of the COVID-19 pandemic.

ONLINE-ONLY SUPPLEMENTARY MATERIALS

<p>eFigure. Clinical workflow for telehealth visits via video (A) or phone (B) in the neurology department. Abbreviations: LOS, level of service; pt, patient.</p>

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eFigure. Clinical workflow for telehealth visits via video (A) or phone (B) in the neurology department. Abbreviations: LOS, level of service; pt, patient.

<p>eFigure. Clinical workflow for telehealth visits via video (A) or phone (B) in the neurology department. Abbreviations: LOS, level of service; pt, patient.</p>

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eFigure. Clinical workflow for telehealth visits via video (A) or phone (B) in the neurology department. Abbreviations: LOS, level of service; pt, patient.

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2. Centers for Medicare & Medicaid Services. Trump Administration Issues Second Round of Sweeping Changes to Support U.S. Healthcare System During COVID-19 Pandemic CMS.gov Newsroom. Published April 30, 2020. Accessed May 14, 2020. https://www.cms.gov/newsroom/press-releases/trump-administration-issues-second-round-sweeping-changes-support-us-healthcare-system-during-covid?fbclid=IwAR1E4jZjF-EyTuSwvc_LFZDtRcJ2XKPnqTbiPwSsJNnbZButulJPvIdjrrY

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RGM has participated on a medical advisory board with Alnylam Pharmaceutical