Background

Traditional medical practice is not always the most efficient or convenient way to provide care to our neurology patients. With an increasing demand for neurologic services in a growing population, technology can be one way to extend our reach to our patients. As technologies develop, it is paramount that practitioners maintain high-quality care, equivalent to traditional in-person visits. Information and communication technologies (ICTs) have great potential to address some of the challenges both developed and developing countries face in providing accessible, cost-effective, and high-quality health care services. Telemedicine uses ICTs to overcome geographical barriers and increase access to health care services, and is particularly beneficial for rural and underserved communities, groups that traditionally suffer from lack of access to health care. In this chapter, we will first discuss the rationale behind using teleneurology in different parts of the world including the different aspects of telemedicine such as tele-expertise (seeking the second opinion of one or more medical professionals regarding elements of the patient’s medical file), teleconsultation (remote consultations with a patient), and tele-education; and secondly, we will include the most representative international examples of teleneurology initiatives.

The burden of neurological disorders

According to the World Health Organization (WHO) in collaboration with the World Federation of Neurology, there are inadequate resources for patients with neurological disorders in most parts of the world, highlighting inequalities in the access to neurological care across different populations, and in particular in those living in low-income countries and underserved regions of the world. Neurological disorders are increasingly recognized as major causes of death and disability worldwide. Although age-standardized incidence, mortality, and prevalence rates of many neurological disorders declined for many countries from 1990 to 2015, the absolute number of people affected by, dying from, or remaining disabled from neurological disorders over the past 25 years has been increasing globally. In the last report of the Global Burden of Diseases (GBD), Injuries, and Risk Factors Study (GBD) 2016, globally, neurological disorders were the leading cause of Disability Adjusted Life Year (DALYs) (276 million [95% UI 247–308]) and the second leading cause of deaths (9.0 million [8.8–9.4]). The four largest contributors of neurological DALYs were stroke (42.2% [38.6–46.1]), migraine (16.3% [11.7–20.8]), Alzheimer’s and other dementias (10.4% [9.0–12.1]), and meningitis (7.9% [6.6–10.4]). As populations are growing and aging, and the prevalence of major disabling and neurodegenerative neurological disorders steeply increases with age, governments will face increasing demand for treatment, rehabilitation, and support services for neurological disorders. The scarcity of established modifiable risks for most of the neurological burden and the shortage of neurological services demonstrate that new knowledge is required to develop effective prevention and treatment strategies, to ensure equitable access. In this regard, teleneurology can be considered as an efficient and feasible alternative tool.

Clinical care

Other medical specialties

Telemedicine programs increase access to care in all clinical disciplines everywhere. Telemedicine is particularly suited to evaluating patients with Parkinson’s disease (PD) and other movement disorders, primarily because much of the physical exam findings are visual. Telemedicine offers the opportunity for enhanced access to specialty care, thus potentially reducing the lack of diagnosis, delay in treatments, and subsequent morbidity and mortality, and improving quality of life for patients with PD and other movement disorders. In the US, the Department of Veterans Affairs (VA) Office of Connected Care leverages robust telemedicine infrastructure and advanced information technologies, including telehealth and mobile applications, to provide alternatives to in-person clinic visits. These teleconsultations include not only synchronous encounters for patients at remote VA clinics, but home telehealth, and e-consultations as well. Kaiser Permanente, an integrated managed care consortium, has widely adopted a telehealth model accounting for more than half of all health encounters in the system in 2016. Medicare, the United States’ universal health care system for older (> 65 years of age) and disabled adults, currently reimburses telemedicine in only a subset of rural areas. Canada is also home to one of the most established telemedicine programs. This program offers telehealth visits from home as part of the armamentarium for caring for PD patients. Deep brain stimulation (DBS) makers are also examining ways to remotely perform DBS programming for PD patients without requiring patients to leave their homes. With regards to other movement disorders such as Huntington’s disease (HD), in a survey conducted to analyze the organization of clinical services for HD at 231 sites surveyed in Europe, North America, Latin America, and Oceania, multidisciplinary case reviews were offered in 54.5% of sites, and only videoconferencing and telemedicine were used by only 23.6% of sites.

Epilepsy remains an undertreated condition around the world, though efforts to improve epilepsy care have been promising in Western countries. There are more than 50 million epilepsy patients in the world, with 85% living in developing countries, according to the WHO. The WHO has suggested that nonphysician health workers should be empowered to diagnose and manage epilepsy; to do this, they will need considerable medical support, which might be provided by telemedicine through the telephone, smartphone applications, or a combination. The application of store-and-forward technology for electroencephalography (EEG) interpretation is a reasonable alternative in some countries where neurophysiologists are not readily available. The feasibility of an EEG service between a community hospital and a tertiary hospital has been tested in Spain. Most of the patients (98%) were satisfied with the tele-EEG system in a 116-patient study, and 75% preferred it to the conventional consult, due to reduced traveling expenses and the total invested time in the EEG test.

Similarly, tele-EEG has been a timely and effective method of providing EEG services in the United Kingdom, especially for hospitals that cannot recruit neurophysiologists. In Canada, the feasibility of epilepsy care follow-up through teleneurology was tested in a study conducted by the University of Alberta hospital epilepsy clinic. About 90% of patients in both groups were satisfied with the quality of the service. A Canadian survey reported that a large number of neurologists (79.5%) had access to videoconferencing equipment.

Teleneurology toward a preventive medicine and interdisciplinary approach

Telemedicine has shown efficacy in the treatment of chronic diseases such as heart failure and high blood pressure. Telemonitoring, for example, cardiovascular risk factors for stroke, or motor deterioration in PD, would facilitate early interventions and reduce the morbidity-mortality rate and the number of re-hospitalizations that directly correlate with social costs, and promoting a better quality of life. In Latin America, given the large and increasing burden of stroke, the GBD, Injuries, and Risk Factors 2017 study estimated that the prevention of attributable risk factors of stroke could reduce the stroke burden by 85.3% (95% uncertainty interval 82.6–87.8). The representative of ministries of 13 countries from Latin America participated in a meeting in Gramado, Brazil, in 2018 covering public stroke awareness, prevention strategies, delivery and organization of care, clinical practice gaps, and unmet needs. The meeting culminated with the adoption of the unique Gramado Declaration, signed by all ministerial officials who attended the meeting. The Gramado Declaration established priorities for stroke prevention and treatments to reduce the global and regional burden of stroke. In this declaration, the use of telemedicine was encouraged.

Several other projects have been developed in this field as well. In France, there are several telemedicine projects expanding and centered on the elderly designed to prevent mortality, morbidity, and the number of hospitalizations. One of these projects is called “Telegeria,” offering teleconsultations for elderly patients in geriatric hospitals and nursing homes based on the observation of polipathology and the occurrence of geriatric risks among the elderly, which requires multidisciplinary specialists including neurologists. As an example, a 15-month activity study identified 700 telemedicine sessions from retirement homes with hospital specialists involving different areas, ranging from orthopedics (35%) and cardiology (32%) to neurology (4%).

One of the most successful and established models of regional care in PD is the ParkinsonNet model in the Netherlands, where medical and allied health interventions are delivered within integrated regional community networks dispersed throughout the country by PD-specific therapists with specialized training who manage high caseloads. Better quality of care, fewer PD-related complications, lower mortality risk, and lower total health care costs have been achieved compared to usual care. The use of specialized occupational therapy delivered in the community setting has resulted in an improvement in self-perceived daily functioning. While ParkinsonNet has been introduced to other European countries such as Chzequia, its applicability has limited generalization across other health care systems. Singapore has also been working toward an interdisciplinary approach for community care of PD patients that allows health care professionals to participate actively in the clinical care of these patients.

Telemedicine programs in underserved areas

In low-income countries and other underserved areas, there are often large disparities in health care access between the rich and the poor, indicating that telemedicine could be open to most patients, regardless of wealth or status. Thus, in theory, telemedicine programs should represent an inexpensive and efficient way of extending medical care to remote and difficult-to-reach communities. Unfortunately, in practice, telemedicine, including neurology programs, faces limitations, such as the high initial cost of setting up a scheme and the lack of local expertise required for the maintenance and repair of core equipment. Key advantages of regional programs are the convenience for real-time teleconsultations (shared time zone and language) and the rapid patient referral to hub centers for further evaluation/treatment. There are several international programs designed to promote the use of teleneurology in underserved areas and developing countries. In this regard, a successful program developed in Albania and Cabo Verde was built by the Initiate-Build-Operate-Transfer (IBOT) strategy formulated by the International Virtual e-Hospital Foundation (IVeH) and with support from US government agencies such as the US Agency for International Development (USAID), Department of State, and United States European Command (EUCOM), and the Slovenian government (Ministry of Foreign Affairs), among other partners. Ratifi et al. reviewed the similarities and differences between telemedicine programs in two different countries. Out of 2442 teleconsultations in Cabo Verde and 2724 teleconsultations in Albania between 2014 and 2018, radiology, neurotrauma, stroke, and general neurology, followed by cardiology and orthopedics, were the champion clinical disciplines in both countries. This program, which was run progressively, reduced unnecessary and costly transfers, resulting in saved resources. According to the authors, the number of consultations reflects the lack of local specialty expertise to provide health care service, and it thus can be used as a model for establishing future planning and investment.

In another review of teleconsultations performed by Gowda et al. for neurology services in rural and semiurban parts of India between 2010 and 2017, 189 teleneurology outpatient consultations were provided through the Tele-Medicine Centre, located at a tertiary hospital-based research center in southern India. The most common diagnosis in these outpatient teleconsultations was a seizure disorder (17.5%), followed by cerebrovascular accident/stroke (14.8%). Interestingly, 87.3% were found to benefit from teleneurology consultations using interventions such as a change of medications (30.1%), referral to a specialist for review (15.8%), and further evaluation of illness and inpatient care (7.93%). Another study by Patterson et al., designed to compare referral patterns to the Swinfen Charitable Trust from the Middle East with those received from the rest of the developing world, found that simple emails connecting doctors in the Middle East with specialists elsewhere in the world were feasible and sustainable over time, even in war-torn countries. For neurological cases, radiological images were attached to the referring email for 10 patients and eight patients’ clinical images. The neurologist requested video clips for a further three patients. These consultations helped to diagnose brain tumors, demyelinating disease, conversion disorders, and, upon some other cases, referred to neuroradiology and neurosurgery opinions too.

In terms of movement disorders, over the last 7 years, the International Parkinson’s Disease and Movement Disorder Society has been sponsoring several teleneurology programs in underserved areas, including South America, Africa, and China. The Asynchronous Consultation in Movement Disorders (ACMD) is a specialized program conducted in Africa. This store-and-forward technology has enabled referring sites with slower internet speeds and variable electrical power to participate in ACMD. In addition, the referring sites in Africa can access the simple equipment required (laptop, digital camera, or smartphone) to request a consultation, eliminating the challenges of scheduling virtual clinic visits in different time zones. The ACMD program is structured so that the consultant solely provides advice to the local provider, who continues to be the treating physician. The consultant’s report may include differential diagnosis, a list of follow-up questions for consideration, and/or an empiric plan of care. The consultant can also attach other documents, such as relevant academic literature. The feedback from consultants and referrers has been overwhelmingly positive. In particular, the referrers have identified that the program has been especially useful as a professional development tool. In 2018, 12 out of 51 clinical cases (43%) presented using the ACMD platform were related to dystonia, myoclonus, and dyskinesias, and none contained queries regarding PD, likely the most commonly discussed movement disorder elsewhere. These observations highlight the difficulties of diagnosing hyperkinetic movement disorders in underserved areas. A different project conducted in China was designed to provide care to PD patients through a network of neighborhood clinics and train primary care neurologists in neighborhood clinics to diagnose and manage PD with specialist support. The community neurologists were satisfied with the use of telemedicine to obtain expert advice. Although it was not statistically significant, a reduction in fractures, emergency visits, and hospitalizations was observed in the intervention group. The use of telemedicine facilitated consultations between community neurologists and movement disorders experts, providing a step forward in access to high-quality care in remote provinces of China.

Humanitarian crisis

Humanitarian emergencies defined by armed conflict, political strife, famine, or natural disaster can devastate populations rapidly. Neurologic disorders accompany these complex humanitarian emergencies but often go unheeded, exacerbated by a scarcity of neurologists. Teleneurology offers the promise of neurologic care remotely in the face of this inadequate local clinician supply. An international program conducted teleneurology consultations with Médecins Sans Frontières, a medical humanitarian emergency nonprofit organization with several projects in different countries across the world, in addition to their search and rescue operations. In 2017, more than 150 consults were provided by > 10 neurologists with active medical license living in six countries, including three pediatric neurologists. Based on the Médecins Sans Frontières experience, the need for improved resource availability for neurologic disorders in resource-limited settings, and the importance of follow-up and feedback represent the potential areas of growth for future teleneurology projects in humanitarian crises.

On March 11, 2020, the WHO declared the coronavirus disease 2019 (COVID-19) outbreak as a pandemic. The response strategy included early diagnosis, patient isolation, symptomatic monitoring of contacts, suspected and confirmed cases, and public health quarantine. The COVID-19 pandemic has resulted in millions of infections and hundreds of thousands of deaths worldwide, despite community mitigation strategies to slow the transmission of disease and protect vulnerable populations. As hospitals became overrun with COVID-19 patients, the risk of visits for care of other disorders began to outweigh the risk of deferred care or alternative approaches. In many centers, other inpatient admissions or surgeries have been limited to life-threatening conditions.

Telemedicine can also be used to address the ongoing health care needs of patients with chronic illnesses, including neurological disorders, to reduce in-person clinic visits. Such uses of telemedicine reduce human exposures (among health care workers and patients) to a range of infectious diseases and ensure that medical supplies are reserved for patients who need them. Many European Union and Asian countries and the US have expanded laws and regulations to permit greater adoption of telemedicine systems, providing increased guidance on digital health technologies and cybersecurity expectations and expanded reimbursement options. In this regard, many organizations, including the American Academy of Neurology and the International Parkinson and Movement Disorder Society, have issued telemedicine guidelines.

In an international survey developed by the Telemedicine Study Group of the International Parkinson’s disease and movement disorder society, four domains of telemedicine—legal regulations, reimbursement, clinical usage, and barriers—were compared prior to and during the COVID-19 pandemic. Data were obtained from 43 countries within Pan-America, Europe, Middle East, Africa, and Asia-Oceania. Overall, there was a vast global increase in all forms of telemedicine for movement disorders, across low-to-high income countries, as an immediate response to the COVID-19 pandemic. This increase in teleneurology uses was aided by the widespread availability of technology and changes in government regulations. However, issues of privacy concerns, variable internet connections, lack of reimbursement, and a desire for training in telemedicine visits were highlighted worldwide.

Questions remain about the longevity of changes in regulations and reimbursement practices as the world moves past the COVID-19 pandemic. The need for “social distancing” during the COVID-19 pandemic has created a significant surge in the number of teleneurology visits, which will probably continue for the next few months. It may have initiated a more permanent transition to virtual technology incorporated medical care. Teleneurology, a solution for outpatient care during the COVID-19 pandemic, has been proposed for different neurological disorders. Different examples include: in Italy for dementia, amyotrophic lateral sclerosis, multiple sclerosis, frontotemporal lobar degeneration, and parkinsonism; in the US and India, for general neurology including urgent and nonurgent visits ; in Asia for central nervous system inflammatory diseases ; in Spain for neuromuscular disorders and epilepsy ; and in Saudi Arabia and Malaysia for stroke. In terms of neuropediatric disorders, a survey from different international epilepsy associations evaluated the effect of the COVID-19 pandemic on international access to care and practice patterns for children with epilepsy. This study concluded that in response to COVID-19, pediatric epilepsy programs have implemented crisis standards of care that include increased telemedicine, decreased EEG use, changes in treatments of infantile spasms, and cessation of epilepsy surgery, causing profound changes to the care of children with epilepsy.

Education

Successful integration of teleneurology training into general practitioner and allied health professional programs is vital to expand access to neurologic care around the world as the societal demand for these services increases. International examples include the development of the outpatient teleneurology curriculum for residents in the US. Afshari et al. reported the utility, challenges, and benefits of teleneurology training in 11 neurology residents after 2–4 weeks of rotation. After completing this course, residents’ performance on quizzes improved from 53% to 88% (p = 0.002), showing a statistically significant improvement in medical knowledge. The International Parkinson’s Disease and Movement Disorder Society has sponsored several international tele-education programs in movement disorders. The first one, in 2014, using a teleneurology approach, including a tele-education PD program for health providers, was conducted at Hospital Laquintinie in Douala (Cameroon). Twenty lectures over the course of a year connected participants with movement disorder experts using live, synchronous video conferences, and teaching materials. Thirty-three health professionals (52.4% women), including 16 doctors and 17 allied health professionals, and 18 speakers, participated. Videoconferences were successfully completed in 80%, participation ranged from 20% to 70%, and satisfaction was at least above average in 70% of participants. Whereas medical knowledge was dramatically improved, postcourse patient access was not changed in the short term.

The second project was conducted in 2016, using a different audience target: a movement disorders tele-education project for medical students was conducted in a low-middle-income country (Cameroon) and a middle-high-income country (Argentina) lacking access to movement disorders education. Six real-time videoconferences covering hyperkinetic and hypokinetic movement disorders were included. This study included 151 undergraduate medical students (79.4% from Argentina, 20.6% from Cameroon). Feasibility was acceptable with 100% and 85.7% of the videoconferences completed in Argentina and Cameroon, respectively, and medical knowledge improved similarly in both countries. Attendance was higher in Argentina compared to Cameroon (75% vs. 33.1%). The third program was started in 2018, and the results have not been published yet. In this program, called the Center to Center Movement Disorders Training Program, one academic center will partner up to two centers in underserved regions to develop movement disorders expertise in an underserved region.

Conclusion

Setting up any telemedicine program requires complex, multilevel partnerships between organizations from different sectors. Collaborating with the government allows the program to reach a massive scale and secure subsidies in costs to keep the end-user price low and provide health care at reduced rates for the poorest. Teleneurology is expanding across the world, facilitating the access of low-income countries and other underserved areas to neurological services. Several telemedicine studies for clinical care and education have been conducted, showing feasibility and high satisfaction in different neurology specialties and during a humanitarian crisis. With advances in the development of mobile communications in the future, there is no doubt that teleneurology will have a more significant impact on the delivery of health care around the world.