key: cord-0964791-xws162ar
authors: Yeboah, Cassandra B.; Harvey, Nailah; Krishnan, Rohan; Lipoff, Jules B.
title: The Impact of COVID-19 on Teledermatology: A Review
date: 2021-05-28
journal: Dermatol Clin
DOI: 10.1016/j.det.2021.05.007
sha: 011c3f934de39a3a9111b67f762a992972187087
doc_id: 964791
cord_uid: xws162ar

The accelerated implementation and use of teledermatology during COVID-19 has met with successes and challenges. This review explores first, how telemedicine was utilized in dermatology prior to the pandemic, the regulatory adaptions made in response to the pandemic and the effectiveness of the rapid implementation of teledermatology during COVID-19, and finally, how teledermatology has expanded in response to the pandemic. This review examines both lessons learned and how teledermatology’s reliance on digital technologies might paradoxically exacerbate healthcare disparities, and finally, considers the future outlook.

Coronavirus disease 2019 has changed the way that medicine is practiced throughout the world. In March of 2020, the World Health Organization (WHO) declared COVID-19 a pandemic and created guidelines in an effort to mitigate the spread of the virus.

Among these guidelines were recommendations to socially distance, quarantine, and suspend all non-urgent in person medical visits (1) . As the information known about COVID-19 has evolved, so have the safety guidelines. The unprecedented situation has forced health care providers across all fields of practice to critically look at how to maintain continuity of services in the changing landscape, and dermatology is no exception. Certainly, dermatology has always been well suited for telemedicine due to its reliance on visual exams. Changes imposed by these recommendations will remain for the foreseeable future, thus many dermatologists have adopted telemedicine to adhere to social distancing while still remaining engaged with their patient populations. Indeed, telemedicine seems especially well suited for maintaining care during a pandemic.

This accelerated implementation and use of teledermatology during COVID-19 has met with successes and challenges. This review explores first, how telemedicine was utilized in dermatology prior to the pandemic, evaluates both the regulatory adaptions made in response to the pandemic and the effectiveness of the rapid implementation of teledermatology, and finally, considers how teledermatology may have expanded for the long term as a result of COVID-19.

In addition, we examine lessons learned, how teledermatology's reliance on digital technologies might paradoxically exacerbate healthcare disparities, and consider the future outlook.

With approximately 1 in 3 people in the United States suffering from skin diseases (2), new and innovative methods of increasing patient outreach are essential to adequately meet the needs of the patient population. In the decades prior to the COVID-19 pandemic, incorporation of teledermatology into practices' offerings was inconsistent and sparse. Limiting factors to implementation included lack of adequate reimbursement, concerns about liability, and licensing restrictions (3).

In the United States, teledermatology was first described in the literature as an adequate avenue for care in 1994, when it was used to deliver care in rural Oregon (4) . Use of teledermatology increased through the 2010s, but remained limited (3, 5) . A 2018 review article found that only implementation (3) . Still, teledermatology programs have succeeded in diverse practice systems: capitated, charitable, and government (3) . A systematic review published in 2010 identified structural barriers to teledermatology implementation in the Department of Veteran Affairs, notably a lack of understanding of organization revenue models and how they might be affected by adaptive changes in workload and compensation (8) . In order for teledermatology to succeed, the review argued that targeted efforts must address both compensation and workload, with operating budgets possibly reallocated to support changes (8) . However, the predominant feefor-service healthcare model in the US had not adapted the changes necessary for teledermatology to succeed, especially given lack of adequate reimbursement pre-COVID-19 to incentivize use (3).

Before the COVID-19 pandemic, many states had parity laws through Medicare, Medicaid, and private insurance companies that allowed for telemedicine reimbursements, but the level of reimbursement varied by state and payer (9) . In fact, Medicare only paid for telemedicine if the patient lived in a rural area and when they left their home to go to a designated clinic, hospital, or medical center for the telemedicine service (10) . By 2019, the American Telemedicine Association had found that 40 states increased their coverage parameters in order to accommodate the increased use of telemedicine (11) . Sixteen states had limited reimbursement to only synchronous telemedicine (real-time video or telephone visits).

Despite the slow progress over the previous decade, with COVID-19, these telemedicine regulatory and policy restrictions evaporated essentially overnight, with the Center for Medicaid and Medicare Services (CMS) enacting bold changes (10) . In all states, laws were relaxed that J o u r n a l P r e -p r o o f required that telemedicine physicians had preexisting in-person relationships with patients before any prescription could be written for patients following virtual visits (9) . Some states have even relaxed or eliminated interstate licensure limits which barred physicians from providing care to patients who lived outside of their jurisdictions, thus providing patients with increased options for care (12) . For example, New Jersey provided a temporary waiver of telemedicine rules to allow for out of state licensed physicians to continue, and perhaps expand, patient care (13) .

Another pre-pandemic law, the Health Insurance Portability and Accountability Act (HIPAA), requires teledermatology visits to meet certain personal health information confidentiality standards (e.g. encryption), but with COVID-19 policy relaxations, the necessity of HIPAAcompliance was reduced. Specifically, CMS waived enforcement of HIPAA health privacy violations against providers acting in good faith (12, 14, 15) . Many platforms for telemedicine visits had previously opted out of these agreements, which left the liability for security and privacy breaches solely on the physician (14) . CMS's waiver of HIPAA enforcement during the public health emergency thus allowed telemedicine, for the moment at least, to be conducted over non-HIPAA compliant platforms (15) . Other regulatory changes brought on during the COVID-19 pandemic included an increased consideration of 'good faith defenses' in relation to HIPAA violations (12) , meaning that leniency would be applied to telemedicine related HIPAA violations that were made non-maliciously. Collectively, these regulatory changes led to increased adoption of telehealth due to necessity to continue care, expanded financial remuneration and decreased risk of financial loss, allowance for the use of non-encrypted platforms to conduct patient visits, and the ability to reach patients without geographic restrictions. (Table 1) J o u r n a l P r e -p r o o f J o u r n a l P r e -p r o o f

The COVID-19 pandemic has led to innovations in teledermatology that will most certainly set new precedents in how it is practiced for years to come. Not only has teledermatology served as a patch to help patients in a difficult time, but also, these disruptive changes pushed telemedicine into the forefront of conversations for reshaping best practices for dermatology care overall..

As an intended effect of regulatory changes implemented during the pandemic, patients were given increasingly diverse options for telemedicine care. These new telemedicine options have been met with satisfaction by both patients and dermatologists. Pre-pandemic studies had revealed equivocal patient satisfaction ratings with teledermatology relative to traditional inperson evaluations, finding no significant differences in satisfaction between patients using solely teledermatology and patients receiving in-person care (16, 17) . During the pandemic, dermatology patients reported positive satisfaction using teledermatology; for example, an observational study conducted in Italy found that 93% of surveyed patients were satisfied with these virtual visits during the pandemic (18) . An observational study of dermatology patients in Cairo, Egypt found 91% overall satisfaction and likelihood for future teledermatology use, with 94% remarking on its usefulness, 87% describing its allowance for quality interaction, 88% noting its ease of use, and 87% expressing its reliability (19) . For US dermatologists practicing during the pandemic, a study of 184 practices found that 89% used teledermatology, while 71%

intended to use teledermatology in the future (20) . In a survey of members conducted by the 

Teletriage in dermatology practices may also increase practice efficiency by decreasing wait times and allowing for patient inquiries to be stratified according to their acuity (22) . During the pandemic, physicians leveraged remote patient monitoring models to collect patient data and triage visits according to importance and severity (23) . One study evaluating effectiveness of dermatoscopic photos for skin lesion diagnosis found this method increased the urgency score for malignant neoplasms, prioritizing them for in-person visits and thus increasing efficiency for both patients and physicians (24) . Moreover, an analysis of teledermatology triage implementation at Zuckerberg San Francisco General Hospital determined that the remote system saved $140 per newly referred patient compared to conventional care systems (25) .

During the pandemic, teledermatology has proven capable of successfully managing diagnosis, triage, and subsequent check-ups for many visits, with in-person appointments still being offered to patients with more pressing concerns or visits unable to be conducted remotely (namely, skin checks and procedures) (26) . Skin conditions proving especially well-suited to telemedicine have included chronic inflammatory conditions such as acne and psoriasis (27 The SAF method has the largest body of evidence for both triaging and maintaining established care with a patient (38, 39) . With COVID-19, SAF proved especially helpful with patients with stable chronic diseases and/or longer-term medications (e.g. patients doing well and simply needing refills) (35) . SAF was also useful in recognizing certain common diagnoses: acne, dermatitis, psoriasis, rashes, and rosacea. On the other hand, as a limitation, pigmented lesions could be triaged but often not definitively diagnosed requiring in person visits (37, 40) .

Similarly, the vast majority of American Academy of Dermatology members surveyed felt that toal body skin examination required in person visits; and in contrast, conditions such as acne did not required in person evaluation (21) . Indeed, total body skin examinations were a major limitation of teledermatology visits of all kinds, requiring in person evaluation. The need to triage skin checks may have led the specialty to reconsider the appropriateness, for individuals and all patients, default recommendations for yearly skin checks and other regular appointments.

The pandemic and its subsequent guidelines caused academic dermatology programs to reevaluate resident involvement and education (41) . Any significant changes to resident education which lasted more than 4 weeks had to be reported to the Executive Director of the Accreditation Council for Graduate Medical Education (ACGME) as it would affect boardcertification eligibility. Thus, a focus on adjusting resident education through teledermatology allowed for residents and fellows to maintain the quality of their education (41) . Not unlike the standard of studying unknown photographs and kodachromes, practicing teledermatology with J o u r n a l P r e -p r o o f both the asynchronous and synchronous methods allowed residents to triage diagnosis, conduct exams, discuss assessments and plans, and present information to patients (41, 42) . Programs also instituted virtual grand rounds featuring teledermatology to aid in resident education (41, 42) , thus expanding telemedicine's reach in new ways.

The impact of COVID-19 was not limited to current dermatology residents. Major adjustments to the residency application process were suggested in a dermatology program director consensus statement which was released ahead of the application cycle. These changes included limiting the number and availability of away rotations, encouraging virtual rotations where applicable and planning for remote interviews (43) .

Early in the COVID-19 pandemic, some felt that dermatology practices could serve as vectors for COVID-19 transmission and recommended that all non-essential visits be cancelled for the safety of patients and staff (33). Many dermatology practices heeded this warning by converting to telemedicine for patient care. This pivot to teledermatology directly helped mitigate the spread of COVID-19 by decreasing the risk of exposure of patients and staff (18) . Evidence shows that within the inpatient setting, use of teledermatology, when compared to in-person dermatology visits, saved PPE and decreased unnecessary exposure to patients and health care professionals (35) . One study also found that newly implemented COVID-19 teledermatology algorithms allowed for most effective triaging and preparation for in the event that it may necessitate an inperson visit, increasing efficiency of practice (22, 37) .

Teledermatology's efficacy may vary in different populations. The elderly, for instance, may require assistance using digital devices (44) . Lack of education into proper use of technology can J o u r n a l P r e -p r o o f limit the efficacy of teledermatology. We must also consider the emerging American population whose first language is not English. Even without the constraints of a pandemic, language barriers can be a social determinant of health impeding delivery of optimal care. Thus, we must anticipate and proactively address how lack of English fluency may affect proficiency and ability to partake in teledermatology (45) .

Despite these challenges, these new approaches during the pandemic to teledermatology implementation serve as proof of concept with the intention to revise and adapt. For instance, additional services could provide caregivers for the elderly and translators for non-English speakers to improve adaptation.

When CMS relaxed HIPAA regulations for telemedicine, the intention was to expand access to care (15) . Still, we must remain vigilant about quality standards to prevent security breaches.

Many platforms being used for telemedicine appointments were developed primarily for insecure chats and are non-encrypted or have security standards inadequate to protect patient information.

These include FaceTime, Facebook Messenger, Google Hangouts, Zoom, and Skype (46) . The major benefits of these platforms include their low barrier for entry and ease of use for most patients and providers. Encryption standards vary; guidance must be provided in order to avoid compromise of patient information. An uptick in cyber attacks on healthcare networks during COVID-19 certainly warrants additional scrutiny. Many hospitals have been targeted in ransomware attacks, in which patient data has been captured and withheld in exchange for money (47) .

Telemedicine may overcome barriers of distance and time, but it may also paradoxically worsen access for some people in unanticipated ways. Essentially, the most well-resourced patients may be overrepresented among telemedicine visits given their access and literacy, whereas other populations (resource limited), may have even more difficulty adapting to a new system (45) .

Barriers to health equity exist across many sectors including education, planning, housing, labor, and health. Unfortunately, this well-described digital divide may be an important contributing factor in disparities. Access to a reliable, high quality internet connection and a smart device correlates with income. In fact, in 2019, 26% of Americans in households earning less than 30,000 were solely reliant on smartphones for their internet access (48) . That same year, it was also reported that 37% of adults in rural areas in the United States lacked broadband internet and 31% lacked access to a computer. In addition, 25% of adults in urban areas lacked access to broadband internet and 27% lacked access to a computer (48) .

Though both rural and urban populations may have limited internet access, many specific populations may be especially at risk when care is dependent upon this access, namely Medicare patients, minorities, and patients whose first language is not English. Measures taken by agencies such as CMS had their intended impact by allowing physicians to expand telemedicine access, for instance Medicare patients are able to complete visits from the comfort and safety of their homes. However, it is important to note that 26% of Medicare patients lack home digital access (50) . Additionally, Medicare patients older than 85, those with a high school education or less, patients experiencing homelessness, Black and Hispanic patients, and patients with disabilities all have decreased digital access (51) . During COVID-19, the number of Spanish speaking patients seeking teledermatology services was reduced compared to 2019 (52) . In 2019, one study found that 9% of Spanish speaking patients scheduled teledermatology appointments J o u r n a l P r e -p r o o f through an outpatient academic clinic compared to 2020 where only 5% scheduled appointments (52) . Dependence on digital frameworks may disproportionately affect these populations already experiencing health disparities; in one specific example, many of these patients do not have reliable email addresses, making it harder to create teledermatology portals for communication (52) .

Certainly it remains important to consider how different telemedicine models could mitigate any possible exacerbation in disparities. A study from Sao Paulo, Brazil, focused on the use of teledermatology consultation by PCPs in individuals older than 60 years old and they found that 67% of patients were treated via teledermatology without in-person visits and subsequently sent back to PCPs for continued care (53, 54) . Another retrospective study, assessing PCP usage of the American Academy of Dermatology's free AccessDerm program looked at the initiation of SAF teledermatology consults in a clinic serving uninsured patients (55) . In this study, 65% of patients did not need in-person evaluation (55) . Additionally, they found an 82% discordance between PCP and teledermatologist pre-consult management plans (55) . The utilization of teledermatology reduced the cost and wait-time associated with in-person visits and inappropriate care (55) . These provider-to-provider teledermatology models can circumvent any limited patient access to broadband internet. Even as demand may push the market toward more direct-to-consumer or direct-to-patient models, direct partnerships between PCPs and dermatologists may prove valuable in many ways: as a learning outlet for PCPs who frequently participate in referrals (54) , with one study demonstrating how PCPs learned to manage dermatologic concerns from repeated use of such a system (56) .

Moving forward, many other barriers can be anticipated and addressed to ensure care continues with telemedicine. For example, financial barriers that limit access can be reduced by offering waivers that cover devices and internet access in underserved populations (57) . In addition to funding, training programs can promote technologic and health literacy for both patients and providers, done through the mail, or in person with a technology support team (57) . For patient populations with especially difficult circumstances (e.g. those experiencing homelessness), telemedicine programs may need to work directly with other established centers such as housing shelters to ensure successful connections (58) .

Lastly, we must be especially mindful of cultural and language barriers in telemedicine implementation. Platforms should operate in multiple languages so that patients can easily navigate systems. To better direct focus towards local needs, governments and programs should work directly with local public health organizations that know and understand the people they wish to serve. These organizations' pre-existing relationships may not only facilitate culturally competency and community buy-in, but may also help with implementation directly.

In sum, addressing the digital divide to ensure telemedicine does not worsen disparities will require a concerted effort from physicians, regulatory bodies, and public health services to ensure access is not limited, and that internet access does not become a new social determinant of health (53) . (Table 2 ) 

Community-based teledermatolgy programs can serve as an adjunct to assist with ease of use

Prior to COVID-19, teledermatology was an already expanding field, albeit used sparingly compared to in-person visits. The option to use teledermatology had been stymied by limited insurance reimbursement for telemedicine visits (6), concern about medico-legal liabilities (8) and medical licensing restrictions (3) . Thus, without adequate support prior to COVID-19, most physicians opted out of using teledermatology (14) .

The COVID-19 pandemic prompted disruptive changes in the regulatory and policy landscape, opening a new age of telemedicine growth and innovation. Dermatology practices and health systems created and adapted new protocols of care for both inpatient and outpatient settings (26, 37) . Practices were able to save PPE and decrease unnecessary exposure of staff and patients to the coronavirus (37, 51). Residency programs were also able to institute teledermatology into resident education (37) , which further ameliorated the concern of exposure. Additionally, the implementation of teledermatology resulted in improved efficiency (37) ; practices and health systems found that they were able to better prepare in advance for procedures and triage patients, thus saving both time and money while continuing follow-ups with established patients (35) . The increased use of teledermatology may open up spots to patients who require in-person visits and increase the efficiency of daily practice. Evidence also showed that teledermatology was an excellent option for common skin diagnoses and follow-up treatments; these common skin disorders include acne, rosacea, psoriasis, eczema, and other common rashes (37, 40, 41) .

Continuity of care has proven a primary concern during the pandemic, and teledermatology allows physicians to continue patient follow-up, especially for patients with chronic diseases and for patients on medium to long-term treatment regimens (35, 51) . Many of these patients are on immunomodulatory drugs, so teledermatology also conveys increased protection against COVID-19 for these patients. Moreover, teledermatology at its core allows physicians to care for patients at a distance, in situations where they may live far from a dermatologist or if they are quarantining (51) .

Teledermatology has been well-suited to the constraints of the COVID-19 pandemic, but limitations must be addressed. In addition to the medico-legal concerns, one rate limiting step to teledermatology is access. Patient access to both secure internet and the necessary technology for teledermatology visits limits many patients who lack digital access in their home or who lack the technological insight to participate in teledermatology (50, 51) . Additionally, the expansion of telemedicine reimbursements frequently favored synchronous video visits and not SAF.

Furthermore, evidence has shown that SAF is much more efficient in terms of response time for consultations, where a SAF dermatology consultation integration improved dermatology consultation time from 84 days to about 5 hours (17) . Reimbursement expansion was an important outcome to boost teledermatology, but the prioritization of synchronous visits over J o u r n a l P r e -p r o o f SAF could lead to possible overutilization of synchronous visits in situations where SAF would be more appropriate for day-to-day efficiency.

Telemedicine policy changes will continue for at least the duration of the public health emergency. This uncertainty poses a potential threat to teledermatology advancement. However, there is a growing need for dermatology services and during this pandemic, teledermatology has proven to be efficient and effective. Therefore, as in-person care returns closer to pre-pandemic levels, we anticipate that teledermatology's use will remain significantly higher than prepandemic and that it will continue to grow, especially for follow-up care and triaging visits. In the long-term, the success of teledermatology will be dependent on federal and state policies and laws, as well as payers. Future policy must consider telemedicine expansion beyond geographic restrictions and further reimbursement increases and utilization of SAF. For sustained growth, government policy makers, physicians, insurance companies, and patient advocacy organizations must partner to create a system to fortify telemedicine with the many challenges of reimbursement, HIPAA compliance, and disparities in patient access to telemedicine.

WHO Declares COVID-19 a Pandemic

It's Telemedicine or No Medicine, Whether Doctors Like It or Not

Ushers in Age of Telemedicine

Teledermatology: one application of telemedicine

Teledermatology in the United States: An Update in a Dynamic Era

Global teledermatology

Overview of international teledermatology

Teledermatology for diagnosis and management of skin conditions: a systematic review

The Legal Landscape of Teledermatology

Medicare Telemedicine Healthcare Provider Fact Sheet: Medicare coverage and payment of virtual services

Update of State-by-State Telehealth Report Cards

The policy dimensions, regulatory landscape, and market characteristics of teledermatology in the United States

COVID-19 Waivers of Licensing Rules

Time to revisit the Health Insurance Portability and Accountability Act (HIPAA)? Accelerated telehealth adoption during the COVID-19 pandemic

Why Loosening HIPAA Requirements in Response to the Coronavirus Was Urgent and Necessary

A systematic review of satisfaction with teledermatology

Prospective Implementation of a Consultative Store-and-Forward Teledermatology Model at a Single Urban Academic Health System with Real Cost Data Subanalysis

Teledermatology for acne during COVID-19: high patients' satisfaction in spite of the emergency

Dermatological consultations in the COVID-19 era: is teledermatology the key to social distancing? An Egyptian experience

Will teledermatology be the silver lining during and after COVID-19?

Dermatologist perceptions of teledermatology implementation and future use after COVID-19: demographics, barriers, and insights

Implementation of a dermatology teletriage system to improve access in an underserved clinic: A retrospective study

Virtual Dermatology: A COVID-19 Update

Would dermoscopic photographs help triage teledermatology consults in the COVID-19 era? Clin Cancer Res

Cost Minimization Analysis of a Teledermatology Triage System in a Managed Care Setting

Teledermatology in the wake of COVID-19: Advantages and challenges to continued care in a time of disarray

Teledermatology in the era of COVID-19: Experience of an academic department of dermatology

Patient Perceptions and Satisfaction With Teledermatology During the COVID-19 Pandemic: A Survey-Based Study

Teledermatology in the times of COVID-19 -a systematic review

Expansion of asynchronous teledermatology during the COVID-19 pandemic

Teledermatology application use in the COVID-19 era

Virtual Visits for Acute, Nonurgent Care: A Claims Analysis of Episode-Level Utilization

Impact of covid-19 pandemic on dermatology practice: results of a web-based, global survey

Dermatology practices as vectors for COVID-19 transmission: A call for immediate cessation of nonemergent dermatology visits

Trends in teledermatology use during clinic reopening after COVID-19 closures

Inpatient teledermatology during the COVID-19 pandemic

Cost Minimization Analysis of a Teledermatology Triage System in a Managed Care Setting

A cost savings analysis of asynchronous teledermatology compared to face-to-face dermatology in Catalonia

Outpatient Teledermatology Implementation During the COVID-19 Pandemic: Challenges and Lessons Learned

Modifications to dermatology residency education during the COVID-19 pandemic

Optimizing teledermatology visits for dermatology resident education during the COVID-19 pandemic

Approaching the dermatology residency application process during a pandemic

Effectively engaging geriatric patients via teledermatology

The digital divide: How COVID-19's telemedicine expansion could exacerbate disparities

Teledermatology: from historical perspective to emerging techniques of the modern era: part I: History, rationale, and current practice

Digital gap between rural and nonrural America persists

Telemedicine, privacy, and information security in the age of COVID-19

Digital divide persists even as lower-income Americans make gains in tech adoption

Assessment of Disparities in Digital Access Among Medicare Beneficiaries and Implications for Telemedicine

Disparities in telemedicine access for Spanish-speaking patients during the COVID-19 crisis

Benefits of Teledermatology for Geriatric Patients: Population-Based Cross-Sectional Study

Teledermatology Addressing Disparities in Health Care Access: a Review. Curr Dermatol Rep

Teledermatology Consultation Can Optimize Treatment of Cutaneous Disease by Nondermatologists in Under-Resourced Clinics

Teledermatology operational considerations, challenges, and benefits: the referring providers' perspective

A Call for Addressing Barriers to Telemedicine: Health Disparities during the COVID-19 Pandemic

Tackling the Digital Divide by Improving Internet and Telehealth Access for Low-Income Populations. California Initiative for Health Equity & Action