Neuroethics in the Era of Teleneurology

Abstract

The accelerating integration of telehealth technologies in neurology practice has transformed traditional interactions between neurologists and patients, allied clinicians and society. Despite the immense promise of these technologies to improve systems of neurological care, the infusion of telehealth technologies into neurology practice introduces a host of unique ethical challenges. Proactive consideration of the ethical dimensions of teleneurology and of the impact of these innovations on the field of neurology more generally can help to ensure responsible development and deployment across stages of implementation. Toward these ends, this article explores key ethical dimensions of teleneurology practice and policy, presents a normative framework for their consideration, and calls attention to underexplored questions ripe for further study at this evolving nexus of teleneurology and neuroethics. To promote successful and ethically-resilient development of teleneurology across diverse contexts, clinicians, organizational leaders and information technology specialists should work closely with neuroethicists with the common goal of identifying and rigorously assessing the trajectories and potential limits of teleneurology systems.

“Concern for people and their fate must always form the chief interest of all technical endeavors…”

– Albert Einstein

Introduction

The integration of telehealth technologies in neurology practice over the past decade, which was further catalyzed by the COVID-19 pandemic, has transformed traditional interactions between neurologists and patients, allied clinicians, and society. Despite the immense promise of these technologies to improve systems of neurological care, the introduction of these innovations in clinical neurology practice generates a host of novel ethical challenges. Might the contours of neurologists’ professional obligations and doctor-patient relationship be altered in virtual contexts? How can clinicians appropriately instill trust and convey empathy to patients and families beyond the traditional cubits of the clinic, synchronously or asynchronously?^{1, 2} What are the limits of teleneurology, and how ought clinicians, patients and surrogates be optimally counseled around these limitations? How should uniquely sensitive neurologic healthcare data be ethically stored, processed and shared while protecting privacy and confidentiality, guarding against cybersecurity threats and avoiding maleficence? Are teleneurology services accessible and equitable across diverse contexts? What are the ethical, legal and social implication of teleneurology-assisted diagnosis of disorders of consciousness or brain death? How do the principles of biomedical ethics shed light on these and other issues raised by virtual neurology practice? These are just some of the important questions that emerge at the intersection of neuroethics and teleneurology.

Careful and proactive consideration of the ethical dimensions of teleneurology is instrumental to ensuring responsible development and deployment across all stages of implementation. Toward these ends, this article explores key ethical aspects of teleneurology, presents a normative framework for their consideration, and calls attention to underexplored questions ripe for further study at this evolving nexus of neuroethics and teleneurology. To promote successful and ethically-resilient development of teleneurology systems of care across diverse contexts, clinicians, organizational leaders and information technology specialists should work closely with neuroethicists with the common goal of identifying and rigorously assessing the trajectories and potential limits of teleneurology.

Neuroethics in Teleneurology: Historical and Conceptual Context

Before delving into particular ethical issues raised by teleneurology, a brief overview of the evolving field of neuroethics, its history, and conceptual foundations, is in order. What is neuroethics, and how is it relevant to teleneurology? Neuroethics is the ethics of neuroscience, and as a discipline seeks to identify, analyze and clarify solutions to normative issues that arise in the evaluation or manipulation of the nervous system when conducting research or providing clinical care in the fields of the neurosciences.^3–11 Neuroethics may be considered a branch of biomedical ethics that deals specifically with the ethical and philosophical issues raised by neuroscience research and clinical practice.^12–17 Insofar as neurologists are responsible for evaluating and managing conditions that could impact foundational capacities subserving human identity, experience and interaction, the practice of neurology and allied fields is suffused with a particularly high concentration of sensitive philosophical and ethical issues.^18–20

Prior to the birth of neuroethics, bioethics more generally as a distinct academic field began in the United States in the 1960s in the shadow of the Nuremberg Trial, the Tuskegee syphilis experiment and other historical events that highlighted the need for greater ethical guidance and governance in medical practice and research.^21–23 The early principles of bioethics were subsequently articulated in the Belmont Report and later refined in a classic book by Beauchamp and Childress, Principles of Biomedical Ethics.^{24, 25} They include the principles of non-maleficence and beneficence, which underscore the importance of weighing harms and goods to patients or research subjects; the principle of autonomy, which emphasizes respect for patients’ rights to self-determination and dignity; and the principle of justice, which requires fairness and caring for the most vulnerable persons on a population level.²⁶ In addition to these principles, contemporary bioethical inquiry is informed by analysis of prior instructive cases (casuistry), projected utility calculations (consequentialism or utilitarianism), evaluation of obligations and rights (deontology), consideration of social relationships (ethics of care), social order (communitarianism), or mutual agreements (contractarianism), assessment of consideration of policies and practices that enrich medicine as a moral enterprise (virtue ethics), and by more pragmatic approaches such as clinical pragmatism (Figure 1).^27–29 Varied approaches to ethical inquiry and problem-solving may be encountered across different cultures and philosophical traditions. Through inclusive moral deliberation and reflective equilibrium, neuroethicists aim to identify and resolve complex disputes and achieve harmonious approaches to normative issues in clinical neurology, neuroscience, and allied fields.^30–32 A range of normative theories and philosophical approaches inform the foundations of neuroethics and provide means of generating practical guidance for those who encounter normative issues as they may arise in teleneurology practice or policy.^33–35

Figure 1.

Theoretical Foundations of Neuroethics.

In 2002, the Dana Foundation organized a meeting of over 200 neuroscientists, bioethicists, legal scholars and philosophers; this gave rise to the first definitions of neuroethics as the “study of the ethical, legal, and social questions that arise when scientific findings about the brain are carried into medical practice, legal interpretations, and health and social policy.”³⁶ Although it is beyond the present scope to fully survey the range of questions neuroethics has thus far contemplated, one may consider the discipline as dividing primarily into these domains: the ethics of neuroscience (including clinical neuroethics and research neuroethics) and the neuroscience of ethics. Clinical neuroethics deals with the issues raised by evolving practices in neurology, psychiatry and neurosurgery, improving understanding of the brain and consequent abilities to monitor and influence brain function with greater impact and precision.³⁷ Research neuroethics describes the challenges relating to the responsible conduct of neuroscience research, and develops guidance for the ethical conduct and translation of research.³⁸ The neuroscience of ethics deals with how biological insights inform the inquiry of how our brains give rise to the people that we are and the social structures and norms that we inhabit and create.³⁹ In 2019, members of the NIH BRAIN initiative published guiding principles of neuroethics, identifying this area as a high-priority research domain within the BRAIN Initiative.⁷ The NIH BRAIN Initiative Neuroethics Working Group subsequently disseminated a set of Neuroethics Guiding Principles that encourage teams involved in neuroscience research and advanced clinical care to undertake robust safety assessments; to consider issues “related to capacity, autonomy and agency;” to “protect the privacy and confidentiality of neural data;” to “attend to possible malign uses of neuroscience tools and neurotechnologies;” to emphasize caution in clinical translation; to “identify and address specific concerns of the public about the brain;” to “encourage public education and dialogue;” and to “behave justly and share the benefits of neuroscience research and resulting technologies.”^{7, 40} Clinicians and practice leaders should be familiar with these guiding principles and allow them to proactively inform trajectories of teleneurology development and deployment.

The forgoing conceptual and historical context can prove helpful in identifying and evaluating neuroethics issues as they arise in teleneurology policy and practice. By analyzing teleneurology through the unique lens of the canonical principles of bioethics, for instance, one begins to identify a range of distinctive issues, which will now be turned to.

Enhancing Autonomy through Teleneurology

The principle of autonomy prompts inquiry into how to promote patient self-determination, informed consent and meaningful participation in the context of virtual neurology encounters. On the basis of this principle, implementation of teleneurology services might be viewed as ethically imperative insofar as teleneurology could enhance patient autonomy through enabling access to comprehensive evaluations for patients who might not have otherwise been able to receive neurological assessment in traditional office settings due to geographic barriers, resource constraints, or disability.^41–43

Championing the potential of teleneurology to enhance the autonomy of patients and caregivers, a 2021 American Academy of Neurology (AAN) Position Statement on Telehealth highlights the potential autonomy-promoting effects of teleneurology including “improving convenience and democratizing access to subspecialists throughout the nation…enhanced comfort, convenience and safety, particularly for patients with limited mobility due to their medical condition or need for home medical support equipment…reduced caregiver stress… decreased time away from work or other essential activities for patients and care partners; increased care partner and provider participation…better assessment of social determinants of health, including the patient’s home environment…early intervention prior to a scheduled office visit, based on continuous assessment of neurological disease progression and treatment efficacy… [and] protection of patient and providers from infectious disease exposure and reducing use of personal protective equipment.”⁴³

However, the AAN Position Statement also describes limitations of telehealth technologies. These include potential challenges in appropriately triaging new patients (in contrast to follow-up patients with whom clinicians might have established sufficient familiarity), caring for patients in areas where local resources are unfamiliar to the remote clinician, barriers to effective use among patients with limited technological resources, impaired hearing, vision or language, and cybersecurity concerns.⁴³ If not appropriately anticipated and addressed, these limitations could potentially reduce the autonomy of some patients or caregivers in teleneurology interactions, posing ethical challenges and equity concerns. Rubeis and colleagues have emphasized the dual potential of telemedicine technologies to strengthen autonomy by giving “patients the opportunity to take charge of their own health by using self-tracking devices and allows health professionals to treat patients from a distance” while also carrying countervailing “dangers of depersonalization of medicine and the pathologization of daily life” that might ensue if technologies are not well aligned to patients’ needs and vital goals.⁴⁴ Some ethicists have accordingly described a reconfiguration of the concept of autonomy occasioned by telemedicine, marked by a “shift from patient autonomy to user or consumer autonomy, the vision of empowered autonomy in participatory, democratic care and medicine” thus calling for an expanded construal of patient autonomy in the era of telemedicine.⁴⁵

Justice and Equity in Teleneurology

The principle of justice motivates related considerations surrounding equitable access to teleneurology services across diverse geographic and social contexts. Especially in the context of the COVID-19 pandemic, virtual neurology encounters have been widely used to help facilitate equitable, safe and reliable access to medical evaluation across a variety of geographic and clinical settings.^46–62 Teleneurology enabled hub-and-spoke model system design may also be used to democratize access to neurology expertise and to aid in appropriate triage of neurologically complex patients, including those with stroke and disorders of consciousness.^63–65 Statements and resources made available by the American Medical Association (AMA), American Academy of Neurology (AAN), American Psychiatric Association (APA), Centers for Medicare & Medicaid Services (CMS), American Academy of Physical Medicine and Rehabilitation (AAPMR), and other organizations have supported implementation of, and access to, telemedicine services, emphasizing themes of justice in their respective guidance and resources. Capturing these ethical themes, the term ‘TechQuity’ (i.e., tech equity) has recently been advanced and defined as “the strategic development and deployment of technology to advance health equity,” along with modernized formulations of the “five A’s of access” originally conceived by Penchansky & Thomas — affordability, availability, accessibility, accommodation, and acceptability.^66–68 In the realm of post-graduate neurology training, analogous motifs of maximizing inclusiveness and diversity through virtual application and interview processes have been explored, and underscore how the impact of technology on the field of neurology spans beyond clinical interactions and into systems of recruitment and training of the next generation of neruologists.^69–72

Although the advent of teleneurology carries immense potential to promote the ethical ideals of justice and equity, disparities have been described in access to telehealth technologies and in digital literacy. If not proactively addressed, these disparities may preclude equitable access to teleneurology services across diverse populations and potentially exacerbate pre-existing healthcare inequalities, particularly among underserved minority populations, elderly patients, and patients with low health literacy or digital literacy.^73–93 It is estimated that over 1 in 4 Americans lack access to requisite technologies or digital literacy to engage in telemedicine visits, raising concerns that patients who are most vulnerable and in need of enhanced healthcare access may be the ones who are least likely to benefit from the advent of telemedicine technologies.⁹⁴ These issues are further magnified in considering access to teleneurology in less developed countries.

Responding to these concerns, Nouri et al. (2020) have formulated key recommendations for clinicians and health systems to establish equitable access, including proactively identifying access disparities through improved data collection and monitoring; mitigating barriers to digital literacy and technological resources (including the development of educational/training programs and helping connect patients with reduced-cost access solutions); addressing health-system barriers through advanced screening, providing interpreter access, and increasing awareness among leadership of barriers to telemedicine access; and advocating for expanding availability of low-cost technological resources (including broadband internet), pay parity for virtual visits, and funding for telemedicine expansion in under-resourced settings.⁹⁴ Proactive capacity building, policy innovation, and advocacy leadership can thus help to ensure that the potential to improve equity and promote justice through teleneurology is captured and sustained.

Beneficence, Non-Maleficence and the Therapeutic Relationship in Teleneurology Settings

The principles of beneficence and non-maleficence prompt associated considerations of how to maximize benefits and minimize unintended harms to patients through teleneurology. Appropriate implementation of teleneurology services may improve quality of care and permit superior longitudinal follow-up, especially for those with chronic neurologic disorders requiring frequent follow-up visits and for patients who are located in rural areas.^95–99 The utilization of hospital-based teleneurology programs may also be associated with shorter length of hospital stay and reduced time to consultation completion, enabling earlier neurological diagnosis and timelier treatment.^{100, 101} Telemedicine services permitting e-consultations between primary care providers and specialists have additionally been found to reduce vulnerability to medical error among internal medicine patients.¹⁰² However, limitations and potential pitfalls of teleneurology must also be considered. Some have raised concerns that replacing face-to-face interactions with virtual interactions may occasion an erosion of the doctor-patient relationship, with potential downstream effects on trust, empathy and adherence.¹⁰³ These elements are important not only by virtue of their foundational role in the doctor-patient relationship, but also due to their potential impact on health outcomes.^104–106 While some aspects of doctor-patient communication may be maintained through virtual encounters, other aspects, including non-verbal behaviors and touch, may be lacking and potentially impact communication quality.¹⁰⁷

Despite these theoretical concerns and potential tradeoffs, recent research has suggested that empathy can be effectively communicated and therapeutic rapport well established¹⁰⁸ in virtual contexts. In one prospective cohort study of patients who received acute stroke consultation, no differences were found in patient perceptions of physician empathy between virtual and in-person visits.¹⁰⁹ The authors concluded that “empathy can be conveyed by facial expression, voice and attentiveness in a telemedicine encounter and, in the setting of acute stroke care, does not require physical touch or proximity.”¹⁰⁹ These findings suggest that despite theoretical concerns, with appropriate communication strategies, the integrity of the doctor-patient relationship can be maintained, and even strengthened, through virtual encounters.

In light of these opportunities, Modic et al. have developed strategies and a communication tip-sheet to enhance “webside manner” through the framework of relationship-centered care.¹¹⁰ Others have championed the use of technologies to augment and expand the therapeutic relationship,¹¹¹ suggesting that appropriately deployed teleneurology services could be a positive, constructive force in the longitudinal neurologist-patient alliance. To harness this potential, training curricula to educate and prepare clinicians for this new paradigm of neurological care might be considered, and development is already underway.^{70, 112–114}

In asynchronous teleneurology evaluations or “second-opinion” e-consults, how to appropriately implement the forgoing strategies is less clear, due to the limited nature of interactions which are often confined to text or separated from the patient or family through an intermediary.^115–118 Further investigation is needed to clarify best practices for optimal communication and relationship-building in asynchronous environments. Studies examining patient and surrogate perception of information received through asynchronous teleneurology consultations, as well as the clinical effectiveness of these technologies and the information exchange they enable, can help refine present practice and inform clinical teleneurology practice guidelines. Clinicians who perform asynchronous teleneurology consultations should, in advance, seek to clarify the intended recipient(s) of the consultation report, and tailor background content, explanatory language and framing of recommendations accordingly. These elements could vary considerably depending on whether the recipient is a patient, family member, primary care physician, or a specialist with pre-existing domain-specific background knowledge. When possible, feedback to the clinician who performed the asynchronous teleneurology consultation on the reception and effectiveness of the information furnished may help promote clinician engagement and identify strategies for improvement. If patient outcomes are left opaque following the provision of e-consultative input, important opportunities for iterative learning and quality improvement may be missed, and perceived accountability for outcomes potentially unduly lessened.¹¹⁹ When bad news or a poor prognosis must be delivered, it should be conveyed with utmost sensitivity and empathy, and with transparent recognition of the potential limitations of teleneurology assessment, especially when performed asynchronously.

Apart from the potential impact of teleneurology on the therapeutic relationship, a separate category of ethical concerns relating to the theme of non-maleficence involves risks of misdiagnosis or medical error through teleneurology. Such concerns might arise due to the comparatively limited neurological examination capabilities in the virtual environment, especially in audio-only visits. Appropriate training and familiarity with telemedicine technologies and their limitations may help ameliorate perceived risks of medical error.¹²⁰ Limitations in remote neurological examination may also be mitigated through the use of self-examination techniques that patients or local proxies can perform themselves with instructions.^121–123 Patients and caregivers should be empowered to securely share recordings of notable episodes or physical/behavioral findings. For example, caregivers of a patient with a seizure disorder who is experiencing a new spell semiology might benefit from the ability to share a video recording capturing the spell type in question; caregivers of a patient with a disorder of consciousness (DoC) should be similarly empowered to securely share recordings of notable, intermittently observed purposeful behaviors that could shift the diagnostic impression from unresponsive wakefulness syndrome (UWS) / vegetative state (VS) to the minimally conscious state.^{63, 124} Opportunities to educate patients and families around methods of capturing and sharing potentially impactful findings should be recognized and strengthened. Leveraging teleneurology capacities in this way to increase patient or caregiver involvement in the diagnostic process could foreseeably augment diagnostic rigor and accuracy.

Teleneurology-Assisted Brain Death Determination: An Emerging Frontier in Neuroethics

In perhaps the most consequential area of neurologic diagnosis, access to teleneurology services has been found to facilitate more timely diagnosis of death by neurological criteria / brain death and earlier determination of suitability for organ donation.^125–127 While preliminary results have been promising, further regulatory and ethical guidance is needed to inform appropriate, consistent and guideline-congruent utilization of teleneurology in the remote diagnosis of brain death.

Presently, neither AAN consensus criteria for the diagnosis of brain death nor the Uniform Determination of Death Act (UDDA) explicitly address the role of teleneurology in brain death determination in settings where local expertise may be lacking. As the Uniform Law Commission and AAN undertake potential revisions to laws and guidelines about determination of brain death,^128–131 clarification of the optimal role of teleneurology services to supplement local teams’ often limited capacities in this domain is needed. Parallel opportunities exist for hospitals and professional societies to update brain death determination protocols to identify optimal approaches to teleneurology-assisted determination of brain death. Given the ethical, social and legal intricacies of this area, it is advisable that teleneurology practice leaders work closely with experts in neuroethics and health law to clarify responsible practice development in this ethically complex domain.

Data Security and Privacy

Considerations surrounding privacy, confidentiality and security of patient information figure prominently in the ethical conduct of teleneurology.¹³² Breaches in patient privacy due to cybersecurity threats carry significant ethical and legal consequences, intersecting again with the principal of non-maleficence. Programs must therefore work to develop robust data-security infrastructure to protect virtual encounters and digital information against cybersecurity vulnerabilities.¹³³ The uniquely sensitive status of neural data amplifies these exigencies.^{134, 135} A variety of security solutions have been used to safeguard patient data, and are the focus of intense ongoing research and development.¹³⁶ Standardized disclosure processes ought to inform users about security protections in place to safeguard virtual encounters and digitally stored information, in addition to potential limitations.¹¹⁴ It is important for clinicians to conduct teleneurology visits in areas that are private, ensuring that content is not inadvertently shared with others in the vicinity, and patients and surrogates should be made generally aware of how information gleaned from the encounter will be documented, stored, and accessed.¹³⁷

Clinicians should be cognizant of local regulations and evolving laws governing the practice of teleneurology to maintain legal compliance. By taking these steps consistently and rigorously, teleneurology clinicians and program developers can help ensure that patients, families and professionals are optimally informed and safeguarded.

AMA Code of Ethics Guidance

In 2016, the American Medical Association (AMA) Council on Ethics and Judicial Affairs, recognizing the profound impact of telemedicine on the normative contours of doctor-patient interactions, issued new guidance entitled “Ethical Practice in Telemedicine.” This guidance was subsequently codified in the AMA Code of Ethics.¹³⁸ The AMA guidance emphasizes that “[a]lthough physicians’ fundamental ethical responsibilities do not change, the continuum of possible patient-physician interactions in telehealth/telemedicine give rise to differing levels of accountability for physicians.”¹³⁸ This statement of telemedicine’s impact is especially true for the practice of neurology, which has witnessed rapid transformations throughout a wide range of subdisciplines, including the advent of telestroke services, teleneurocritical care for remote monitoring and management of patients with life-threatening neurological disorders,¹³⁹ teleconsciousness services for patients with prolonged disorders of consciousness (DoC),^{63, 124} and other subfields that have historically relied heavily upon in-person clinician-patient interactions.^{109, 140–144}

Clarifying clinicians’ ethical responsibilities in light of these novel paradigms of care, the AMA Code of Medical Ethics (Opinion 1.2.12, Ethical Practice in Telemedicine) has issued guidance to ensure appropriate provision of virtual medical care.¹³⁸ Selected key elements of AMA guidance are summarized in Table 1.

Table 1.

Selected key elements of AMA Code of Medical Ethics (Opinion 1.2.12) pertaining to ethical practices in teleneurology.

Selected AMA Code of Medical Ethics (1.2.12) Guidance	Ethical Principle or Theme
Consistently disclose and manage/eliminate conflicts of interest in telemedicine services	Conflicts of Interest
Ensure information provided virtually is accurate	Informed consent Transparency
Assure sufficient cybersecurity infrastructure in place	Privacy & security
Be aware of and inform users about functions and limits of telemedicine and overcome these limitations when possible	Informed consent Transparency Quality improvement
Provide information about how to arrange follow-up after virtual encounter as needed; encourage patients to inform primary physicians (when established) about encounter	Continuity of Care Patient autonomy
Encourage care continuity by “giving consideration to how information can be preserved and accessible for future episodes of care in keeping with patients’ preferences (or the decisions of their surrogates)”	Continuity of Care Patient autonomy
Maintain same professional standards “as expected in in-person interactions, follow appropriate ethical guidelines of relevant specialty societies and adhere to applicable law”	Professionalism and safety
Maintain proficiency in use of relevant technologies	Professionalism Effective practice
Establish/confirm patient’s identify and confirm the appropriateness of telemedicine in each encounter	Privacy & security Effective practice
Tailor informed consent process to educate patients/surrogates on distinctive features of telehealth, in addition to information about medical issues and treatments	Informed consent Effective practice
Appropriately document the virtual encounter	Professionalism and safety Effective practice
Support continued development and refinement of telemedicine technologies	Quality improvement
Advocating policies to ensure equitable access	Justice
Identify and address possible adverse consequences of telemedicine	Safety Quality improvement
Consistently identify and disseminate information about telemedicine outcomes	Transparency Quality improvement

Toward Ethically-Informed Teleneurology

As we have examined, the manifold benefits of teleneurology are accompanied by a broad range of unique ethical issues. Neuroethical considerations intersect with themes of autonomy, beneficence, non-maleficence, justice, informed consent, data privacy, optimal communication and foundational elements of the doctor-patient relationship in teleneurology-enabled contexts. Guided by the ethical principles and normative imperatives explored here, clinicians and practice leaders involved in designing and implementing teleneurology systems are well positioned to identify opportunities to embed personnel with neuroethics expertise to ensure that neuroethical issues are proactively recognized and rigorously addressed. Development of best-practice standards for ethically responsible teleneurology practice with input from diverse stakeholders is needed. Clinicians, practice leaders, information technology specialists, and other stakeholders involved in the development and deployment of teleneurology systems may further benefit from dedicated neuroethics training and institutional neuroethics capacity building to enrich understandings of the distinctive ethical issues in the rapidly evolving practice of teleneurology in our communities and around the world.