Introduction

Affecting almost 10% of the US population, diabetes mellitus is a growing pandemic, with a third having diabetic retinopathy, the leading cause of blindness in the working age population [1]. Annual dilated eye exams are the standard of care to detect advancing, vision threatening, but often asymptomatic retinopathy, in a timely fashion [2], allowing for treatments that preserve and improve vision [3, 4]. Unfortunately, at best, only 60–70% of those with diabetes have an annual dilated eye exam. This percentage averages between 25–35% for low income populations in under resourced settings [5, 6].

Teleophthalmology is the innovative utilization of nonmydriatic fundus camera-based retinopathy examination in non-eye care settings, including primary care offices, using eye doctors to remotely grade images and recommend appropriate follow-up eye care. Although such programs have tremendously improved annual examination rates for retinopathy in low income and under resourced settings [7–9], widespread adoption of such examination technology and processes have yet to occur. Research on patients’ attitudes about teleophthalmology is limited. Understanding how patients perceive the value of using teleophthalmology programs to screen for retinopathy and assess vision in non-eye care settings is important for developing successful programs and increasing its adoption [10, 11]. Qualitative assessment of patient experiences with teleophthalmology through focus groups and interviews allows for improved design and implementation of such programs by understanding local consumer needs [12–14].

Conducting focus groups and qualitative analysis to elicit patient experiences and obtain candid perspectives of their health and health care yield richer insights into local community beliefs that influence adoption of health practices than quantitative questionnaires or surveys alone [12–20]. Cost and access have been identified as the two main barriers of obtaining dilated eye exams from focus groups assessing the knowledge, attitudes, and beliefs of patients with diabetes in urban and rural settings in the US [16, 19, 20]. None of these studies addressed the use of teleophthalmology to examine eyes for diabetic retinopathy.

The majority of work evaluating patient experiences with teleophthalmology has focused on international populations using quantitative surveys [21–27]. One qualitative study from the UK found that participants value teleophthalmology if they understand why it is being recommended and if it is convenient and accessible by safe transportation [28]. One of the few studies to assess teleophthalmology users in the US noted that patients may not understand the reason for these examinations [29, 30]. A survey of US Veterans with diabetes also found that convenience was a key factor in favoring teleophthalmology. However, this cohort had not actually experienced teleophthalmology [31]. A recently published study identified barriers and facilitators of teleophthalmology among rural, white Caucasian patients in Wisconsin who had experienced this type of examination found that the convenience of teleophthalmology was a key facilitator, whereas not knowing enough about teleophthalmology was a key barrier for having such an exam [30]. Our study investigates how patients value having a teleophthalmology examination offered in urban US primary care provider (PCP) practices serving low income, minority patients. We include the perspective of those who have and who have not undergone such a teleophthalmology exam using qualitative analysis.

Methods

This study was approved by University of Rochester’s Research Subjects Review Board as an exempt study (RSRB00065090). The ethics committee approved the verbal consent procedure and did not require written consent due to the nature and the activities of the study. All participants provided informed verbal consent for their participation and for the audio-recordings during initial phone contact to schedule an interview or a focus group. Participants received $25 cash for their participation in the focus group or interview as well as bus tokens as needed for transportation.

Results

Participant characteristics

Participant characteristics are shown in Table 1. The 23 participants all had physician diagnosed type 2 diabetes. Seven had undergone teleophthalmology to assess for diabetic retinopathy in their primary care provider’s office (teleophthalmology group). The dilated exam only group consisted of 16 participants who only had a dilated eye exam with an eye doctor to check for diabetic retinopathy. The teleophthalmology group was slightly younger (p < .01), more likely to be employed (p < .05), and less likely to have an eye doctor (p<0.02). Half of both groups reported some difficulty with distance vision, even with glasses. The majority in both groups also reported trouble with reading while wearing reading glasses.

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Table 1. Participant characteristics (N = 23).

https://doi.org/10.1371/journal.pone.0225300.t001

Main results

Tables 2 and 3 compare the results of open-ended written responses and the subsequent discussion including barriers to obtaining a dilated eye exam, the benefits of teleophthalmology, potential barriers to receiving teleophthalmology, and each participant’s WTP for the teleophthalmology service. The reported results are aggregated as responses were similar between the two groups.

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Table 2. Perceived barriers to receiving dilated eye exam and perceptions of teleophthalmology.

https://doi.org/10.1371/journal.pone.0225300.t002

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Table 3. Willingness to pay for teleophthalmology exam during a primary care provider office visit.

https://doi.org/10.1371/journal.pone.0225300.t003

Barriers to obtaining dilated eye exams.

Using surveys followed by facilitated discussion allowed for richer and more varied responses. During the discussion, almost all participants strongly voiced the lack of insurance coverage for medical care, being on a fixed income, and having a limited budget as barriers to obtaining a dilated eye exam. Cost of care and the cost to access care were main themes in all interviews and focus groups. The discussion also highlighted two additional barriers: transportation challenges and being asymptomatic. Participants commented on the difficulty of convenient parking and safety driving post dilation. Many also spoke about ‘forgetting to make an appointment’ or ‘putting off making an appointment’ especially if they did not have visual or eye symptoms.

Value of a teleophthalmology exam.

Participants listed convenience (48%) and the ability to detect disease early to give oneself ‘peace of mind’ by knowing and being educated on the status of one’s eye health (35%) as reasons to have a teleophthalmology exam at their primary care visit. The value of teleophthalmology included its quickness and convenience, a ‘one stop shop.’ In addition, participants acknowledged value in not only giving reassurance that there was no vision threatening retinopathy but also in allowing for early detection of disease so that ‘something could be done about it’ to allow for potential treatment to prevent vision loss. Personalized education from having the provider review the findings in the retinal photos to understand the disease better was also of value.

Most respondents reported their WTP as the amount of their usual visit copay for the teleophthalmology exam, but actual costs for the exam were not discussed. More than half indicated that they would be WTP $30 or $40 for the teleophthalmology service on their survey. In this small sample, there was no significant relationship between WTP and type of health care insurance, eye care coverage, or employment status. (Table 3)

While missing primary care appointments or ‘not showing up’ and potential ‘poor customer service’ were noted as potential barriers by a few participants, everyone focused on cost of care as the primary barrier during the discussion. Many emphasized that they would ‘want to know the cost’ of the teleophthalmology examination before deciding to have it done. Participants would be more likely to participate if they knew that their insurance would pay for the service as they were ‘tight on budget’ and living ‘dollar to dollar.’ Despite noting limitations in what they could actually afford, participants expressed value for having eye exams to ensure good vision with a few stating they would ‘pay $100 to $200’ for an exam ‘if [they] could afford it.’

The overall experience of participants who had a teleophthalmology exam was positive. They expressed confidence in primary care staff skills for conducting the examination and labeled it as a ‘helpful service.’ Teleophthalmology fit well in their primary care visit and many stated it was an ‘excellent experience.’ They would recommend teleophthalmology to a friend and would be willing to have such an exam again. In addition, everyone in the dilated exam only group, noted that they would be ‘comfortable’ with having a teleophthalmology based examination at their PCP office.

Although three (13%) said they would prefer an in person dilated eye exam with an eye doctor over a teleophthalmology exam, 20 participants (87%) expressed interest in having a teleophthalmology exam at their PCP office if it was recommended by their PCP.

Discussion

Using a qualitative approach, we found that a low income, urban, largely African American sample of patients with type 2 diabetes greatly valued having PCP based teleophthalmology, would recommend such a service, and were willing to pay at least the amount of their usual copay. Cost was an important influencer of value. We are the first to report on WTP as an indicator of the perceived value of teleophthalmology to patients. Our study also highlights the importance of having a facilitated discussion to qualitatively assess knowledge, beliefs, and attitudes among US low-income predominantly African American patients with diabetes as such discussion allowed for richer and more varied responses than surveys requiring participants to answer questions on their own.

We not only identified many of the same barriers to obtaining a dilated eye exam as other US based studies [18–20, 31, 32, 34, 35], but also demonstrated the value of a teleophthalmology service using nonmydriatic retinal cameras in PCP practices in overcoming such barriers. The most common stated value was convenience and the ability to overcome transportation and time management issue, as noted in other international and US studies, including a recent study of a white Caucasian rural population in Wisconsin [21, 23, 27, 30, 31, 34, 35]. Other value included ease of use, ability to detect disease before visual symptoms, and the knowledge provided by the photos and technicians about retinopathy and eye disease, which have been only reported thus far in international studies [21–27]. In addition, the use of nonmydriatic cameras without dilating the eye and avoiding temporary vision impairment was seen as a major advantage of teleophthalmology as noted in the recent Wisconsin study [30]. PCP recommendation and stronger PCP-patient relationships were important patient motivators for using teleophthalmology, similar to other studies from Norway [21] and Wisconsin, USA [20, 30].

The cost of care was the major barrier to obtaining dilated eye exams, as seen in other US based studies [16, 18–20, 31, 34–37]. Cost was universally cited as a potential barrier to obtaining a teleophthalmology based nonmydriatic camera exam even if conveniently offered in the primary care office. Educating patients on the potential costs and value of having a teleophthalmology based examination versus going to see an eye doctor for a dilated comprehensive eye exam may be helpful to encourage informed discussions on eye care especially in low income, underserved populations. Combining patient preferences and WTP can provide a more holistic picture of value for a health service such as teleophthalmology by incorporating economic evaluations, such as cost-utility analysis [38]. A recent systematic review of economic studies demonstrated increased cost savings for using teleophthalmology for retinal screening in patients with diabetes versus traditional exams with an eye doctor especially in populations with a higher prevalence of diabetic retinopathy, including minority, low income groups included in our study [39].

While teleophthalmology was well received, there were some who expressed a strong preference to see their eye doctor. These individuals were among the older ones in the group. They expressed valuing their relationship with their eye care provider and questioned the level of expertise and thoroughness of exam afforded by the primary care based teleophthalmology, a finding similar to a recent study of US Veterans [31]. Thus, ensuring that patients, especially older adults, are comfortable with the quality and reliability of teleophthalmology is important. A recent study among American Indians demonstrated that although the digital divide may be greater among low income minority groups, younger American Indian adults were more familiar with digital communication and technology and may be more apt to adopt such methods for accessing health care [40]. The participants in our study who had experienced teleophthalmology were also younger than those who just has a dilated eye exam, which may also have influenced its overwhelming acceptance in our study.

Strengths of our study include having feedback from those who have used teleophthalmology to evaluate their eyes for diabetic retinopathy. It is also the first known to ask a potential customer’s willingness to pay (WTP) for the teleophthalmology service. Consumer WTP has been studied for other telemedicine services, especially teledermatology, whose store and forward model is similar to the present one used for teleophthalmology [41]. Quicker and more convenient access to the expertise of a dermatologist with increased chance of receiving an accurate diagnosis in a timely fashion were related to higher WTP [41, 42]. Furthermore, the use of a pre-discussion questionnaire followed by facilitated dialogue in our study allowed for richer and more varied responses than either option alone. While many studies have looked at attitudes, beliefs and knowledge around eye care and having a dilated eye exam, especially for underserved US populations, our study is among the few to provide insight on the value and perceptions of teleophthalmology in US low income, minority populations.

Limitations of this study include factors pertaining to the composition of our focus groups and interviews and the use of convenience sampling. We also restricted our population to English speakers who were not legally blind. The small number in the teleophthalmology group limited statistical comparisons. Interpreting our participants’ WTP should be done while considering that all participants expressed the importance of an eye exam and had sought eye care within the last two years. We also chose to ask if participants were WTP discrete values from $0 to $40 in our pre-discussion survey, which may have limited our ability to elicit a full range of WTP values. However, encouraging dialogue around their WTP during the discussion found participants’ WTP ranging from $0 to $100–200. Moreover, WTP and what one actually pays may not be the same [43].

Although teleophthalmology was universally seen as valuable by our participants, cost remains a formidable barrier to obtaining such care and to widespread implementation as recently reviewed by Liu at al. [44]. The issue of cost as a barrier to using teleophthalmology for patients and clinics appear to be unique to the US due to its diverse fee for service insurance system, with the exception of the Veterans Affairs Health System. A review of European studies using teleophthalmology to screen for a variety of eye conditions demonstrated substantial cost savings to their national health systems [45]. However, a review of the current state of teleophthalmology in the US by Rathi et al. noted significant gaps in insurance coverage for teleophthalmology among private and government insurers [46]. Further research to test the relation between a population’s price sensitivity and their value for convenience and other benefits provided by teleophthalmology to remotely diagnose eye disease is needed. In addition, the impact of various billing models, including value based and fee for service payments, on the adoption and sustainability of teleophthalmology should be explored. Such research will better elucidate the value of teleophthalmology and help support its use in non-eye care settings for various subsets of potential users.

Supporting information

Acknowledgments

The authors thank the staff and patients of the primary care clinics who participated in this study.