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Review Article

Smartphone-Based Fundus Imaging–Where Are We Now?

Wintergerst, Maximilian W.M. MD; Jansen, Linus G.; Holz, Frank G. MD; Finger, Robert P. PhD

Author Information
Asia-Pacific Journal of Ophthalmology: July-August 2020 - Volume 9 - Issue 4 - p 308-314
doi: 10.1097/APO.0000000000000303
  • Open

Abstract

With the ubiquity of smartphones in daily life, it is not surprising that their presence is increasing also in the health space. Ten years ago, Lord et al1 estimated that “1 out of every 2 physicians uses a personal digital assistant or smartphone.” This number has increased considerably since then. Smartphones offer a wide variety of applications: they allow for mobile access to patient relevant information and medical databases, can be used for the education of both patients and health care professionals, and of course offer smartphone-based diagnostics.2 Although there are a number of basic ways to use smartphones in medical diagnostics, smartphone-based fundus imaging (SBFI) is one of the more advanced applications requiring additional smartphone modifications.1 When first tried and documented, the smartphone was used with a handheld lens for indirect ophthalmoscopy and as both needed to be as perfectly aligned as possible to achieve sufficient image quality, the examination was quite challenging.1,3,4 Using video mode and extracting still frames and applications to manually adjust the image settings improved the quality of image acquisition.5 During its onset, SBFI already showed potential as an easy to learn option for inexpensive image acquisition with a built-in option for use in telemedical applications. These might be particularly attractive for low- and middle-income settings. Although authors did raise safety concerns regarding utilized light sources (compliance with international standards on ophthalmic instruments, eg, ISO 10940 and ISO 15004) and possible reduced hygiene as the smartphone cannot be disinfected like other medical devices, many classified SBFI as a remarkable innovation in fundus imaging.2,3,5 Today, with the swift advancements in smartphone technology (including continuously improving smartphone camera quality) and a variety of devices available, SBFI is as promising as ever to make eye care more accessible and affordable.

ADVANTAGES OF SBFI OVER CONVENTIONAL DIGITAL FUNDUS IMAGING

There are several advantages of SBFI over conventional digital fundus imaging, which might render it preferable in low- and middle-resources settings. SBFI can make eye care more accessible due to it being more affordable, portable, coming with built-in connectivity and ease of use.5–13 Its mobility also allows for examination of immobilized patients (Fig. 1) and its connectivity offers the potential to be used in telemedical settings. The computing abilities of smartphones in addition enable post-processing and further editing such as image stitching.3,14,15 Using smartphone cameras enables capturing both videos and single images.16,17 Image acquisition can be accomplished by nonexpert examiners creating comparable results to the reference standard.5,15,18–21 Even though image quality is—dependent on the comparator—in general inferior to conventional digital fundus photography, SBFI can be used to sufficiently document various fundus pathologies.16,21–24

FIGURE 1
FIGURE 1:
Smartphone-based fundus imaging of an immobilized patient (iC2, HEINE Optotechnik GmbH).

OVERVIEW ON DIFFERENT APPROACHES FOR SBFI

As mentioned above, SBFI originates from do-it-yourself solutions starting with approaches based on indirect ophthalmoscopy using handheld funduscopy lenses and external light sources until newer smartphones came with a built-in flash, and solutions for direct funduscopy adding a light source closely to the smartphone camera.1–3,5,25 Although some authors reported sufficient image quality and improved handling, others concluded that so far SBFI was an alternative that could not keep up with reference standards regarding image quality and sensitivity in detecting certain diseases.4,25 Aside from those minimalist approaches, different adapters connecting smartphones and lenses have been introduced recently.2,4,6,7,10,14,15,26–44

Most of the available SBFI devices require pupil dilation to achieve acceptable image quality, yet there are devices that are built for image acquisition with an undilated pupil.10,28,29 Although in undilated pupils devices achieve an approximate 20-degree field of view, image acquisition in mydriasis can capture up to 56 degrees (Fig. 2) or even more depending on the indirect ophthalmoscopy lens used.10,27–29 Most devices are designed to image the macula and the optic disc; however, there are some that also capture more peripheral images in satisfying quality.15,30

FIGURE 2
FIGURE 2:
Smartphone-based fundus imaging with an approximately 56 degree field-of-view (Paxos Scope, Verana Health, Inc., equipped with a Pan Retinal 2.2, Volk Optical Inc.).

Apart from that there are significant discrepancies in applicability for disease screening. For example, in diabetic retinopathy, sensitivity of detecting disease ranges from 50% to >90%.4,7,10,14,15,42 Hence, there is a strong need for a comparison of different SBFI approaches and the diseases they are supposed to screen for.43 Furthermore, image quality for SBFI varies substantially and a reference standard for grading of SBFI image quality is warranted.

The possibility of delegating examinations to nonexpert operators, for example, in a telemedical setting, are of particular interest. There have been attempts for training medical students or health care workers in performing SBFI. Most of them conclude that it is easy and fast to learn while still achieving acceptable outcomes.2,6 Depending less on ophthalmologists, who are a scarce resource in low- and middle-income settings, SBFI would make fundus examinations for patients in these settings more accessible.

Accessibility also depends on which smartphones can be used for which devices. A number of SBFI adapters is limited to only 1 or 2 smartphone models.27,36 This restricts their accessibility and it is also problematic in a time where a large number of smartphones with improved features is released every year and older models are outdated quickly. Other SBFI devices either offer casings for a larger number of models and different operating systems or are built in a modular way so that almost any smartphone is compatible with these devices.10,28,29,31

SBFI could potentially improve cost-effectiveness of screening-programs that involve fundus imaging. Obviously, the cost-effectiveness of different devices needs to be evaluated. With do-it-yourself solutions causing no additional cost but for the smartphone and ophthalmoscopy lens, which every ophthalmologist carries, the costs for dedicated SBFI adapters cover a wide range from less than one hundred to several thousand US dollars.10,25,26,32–35,37–41,44,45 Against this background there is a variety of different applications of SBFI from disease screening to use as a digital surrogate for direct ophthalmoscopy in clinical practice (Fig. 3).

FIGURE 3
FIGURE 3:
Overview on the current applications for smartphone-based fundus imaging.

DIABETIC RETINOPATHY

Diabetic retinopathy is the leading cause of visual impairment among working-aged adults worldwide and its prevalence is increasing particularly rapidly in middle-income countries.46–50 Nearly 80% of all persons with diabetes and associated retinopathy live in low- and middle-income countries48,51,52; however, in most of these countries no established screening programs exist.49,51,53–58

There is a significant number of publications on the feasibility of SBFI for the screening of diabetic retinopathy. However, results are conflicting with one study stating that SBFI has “no role in screening for diabetic retinopathy at this time” and others doubting that SBFI can replace mainstream imaging devices like the conventional fundus camera.4,25 There are also reports of inappropriate sensitivity and poor image quality.14 Yet more recent studies present more promising results regarding the use of SBFI for detection of diabetic retinopathy. In those, SBFI presented satisfactory sensitivity and specificity when compared with conventional digital fundus photography or clinical examination.7,10,24,59

GLAUCOMA

Glaucoma is a leading global cause of irreversible visual loss and blindness and a delayed diagnosis is one of the main obstacles to visual outcomes in low- and middle-income countries. SBFI can be utilized in the acquisition of fundus images to evaluate the optic nerve head, for example, to screen for patients at risk of having glaucoma. Images from SBFI can for example be evaluated for optic disc pallor and cup-to-disc ratio.8 Similar to the screening for diabetic retinopathy affordability, connectivity and portability make this an attractive approach, especially when the access to preventive health care is limited.8,9,18,29 No substantial differences were found comparing SBFI with clinical examinations via ophthalmoscopy and a digital retinal camera in previous studies.18,29 However, one study compared undilated and dilated SBFI and found that cup-to-disc evaluation on SBFI after dilation achieved a higher accordance with the reference standard and complete visualization of the optic disc was more often achieved with dilation.8 Yet, overall image quality was still superior with conventional digital fundus imaging.8 Bastawrous et al18 found no difference in image quality when comparing images acquired by experienced ophthalmological photographers to unexperienced personnel.

SBFI shows promise in glaucoma screening and monitoring; however, further development of devices, a better contextualization and inclusion of additional tests are still needed.8,9

RETINOPATHY OF PREMATURITY

Retinopathy of prematurity (ROP) is an important cause of childhood visual impairment. This is particularly the case in middle-income countries, with a high overall premature birth rate and sparse and still-developing neonatal care.60–64 No retinopathy of prematurity screening programs are available in most middle- and low-income countries.64

Many advantages of SBFI also apply to ROP imaging/screening; however, some specific requirements need to be considered. The light sources provided by the smartphones used in the reviewed studies are considered safe for the human eye and when compared with conventional retinal imaging devices used in ROP imaging, SBFI does not require contact with the cornea, which makes it less invasive and potentially also less stressful for the patients (Fig. 4).12,16,21–23 The time needed for the examination and image acquisition by experienced ophthalmologists differs from 1 minute, which is just slightly longer than with a conventional retinal imaging device, to 5 minutes.21–23 SBFI offers promising results when compared with the clinical reference standard, yet there are some conflicting results regarding image quality. Although Goyal et al state that the image quality is not equivalent to conventional digital retinal imaging, another study found that the images taken with SBFI had a higher level of detail and better resolution.21,23 However, SBFI has a smaller field of view with a range of 45 to 90 degree compared with, for example, 130 degree of conventional digital retinal cameras.22,23 It should be mentioned that a larger field of view in SBFI requires a higher power in the lens used, which can compromise feasibility and image quality.21 To achieve larger field of views the computing abilities of the smartphone can be utilized to stitch several images achieving, for example, 90° degree images via post-processing.12 As stated before SBFI can be superior in taking peripheral images.16,22

FIGURE 4
FIGURE 4:
Smartphone-based fundus imaging for retinopathy of prematurity screening and documentation (Paxos Scope, Verana Health, Inc., equipped with a Pan Retinal 2.2, Volk Optical Inc.; left image copyright Boris Airo).

Despite substantial differences in image acquisition and post-processing, image quality obtained was sufficient and SBFI based ROP staging has been reported to reach substantial agreement with the used reference standards and its sensitivity was comparable with indirect ophthalmoscopy.11,16,21–23,65,12,17

EMERGENCY MEDICINE

Day et al66 acquired images with undilated pupils in an emergency room setting. The device utilized seemed more suitable for imaging of the disc than the macula.66 For medical students SBFI appeared to be superior to indirect ophthalmoscopy when detecting an abnormal fundus and it took a shorter time to examine patients with SBFI. In this setting it should be noted once more that the examination can be performed by a nonophthalmologist and still deliver sufficient results.67 The examined patients mostly presented with papilledema, with SBFI having a tendency to overestimate the severity of the swelling.67 Even though this is only a first pilot study and more evidence needs to be created, it shows that SBFI could make fundus examinations accessible in settings in which they are needed, but are currently unavailable due to a lack of resources.

PEDIATRICS

SBFI may facilitate easier ocular imaging and examination in infants and children (Fig. 5). The casings of the devices can be made more children-friendly and attention-grabbing, in particular those which are 3D-printed could be easily altered.68 Changing the color of the light-source to red can reduce photophobia in infants and the examination can be carried out without the use of eye speculums making the examination less stressful for patients.68 Using SBFI in a pediatric setting is, similar to the use in an emergency setting, still in an early stage. The overall features of SBFI do make it a potentially promising approach, but more studies need to be conducted in this field.

FIGURE 5
FIGURE 5:
Smartphone-based fundus imaging in a 4-year-old child (D-EYE, D-EYE S.r.l.).

SBFI FOR TEACHING

Aside from being useful in a clinical setting, SBFI might also be utilized in teaching. Medical students need to be taught ophthalmological diagnostics during their clinical courses. Direct ophthalmoscopy can be difficult to learn and to teach because the instructor does not share the view with the students, whereas in SBFI both share the same view.69,70

Students examined volunteers, mannequins, or fellow students both with and without pupil dilation and SBFI was shown to have a steeper learning curve, provided better results and students felt more comfortable and confident when using it.20,69,70 The participants felt that SBFI also slightly improved their abilities in direct ophthalmoscopy afterwards.70 Mamtora et al20 propose that eventually SBFI could even replace the direct ophthalmoscope in clinical medicine. Using SBFI for teaching is still in its beginnings, although it appears that teaching funduscopy can be made easier and more understandable through SBFI.

WIDE-FIELD IMAGING APPROACHES FOR SBFI

Conventional retinal cameras can acquire images of eg, 130 degree and thus outperform SBFI. However, there are approaches aiming at generating SBFI wide-field images based on post-processing. A montage of 5 single SBFI images can create a high-quality 100-degree image.15 The examination itself takes only 1 minute; however, the automated image stitching is more time-consuming and may take up to 5 minutes.15 A different approach is presented by Toslak et al71: instead of transpupillary illumination, they use a warm white LED with 1.5 Lumen for transpalpebral illumination. Using this approach they were able to create a 152-degree image of the retina in 1 single shot without pupil dilation.71

SBFI AND TELEMEDICINE

Telemedicine is the missing link to provide accessible and affordable screenings, where an expert's opinion is needed for the diagnosis but not for the examination itself.4,11,72 Hence, in a world which is becoming more and more connected and where a majority of people are familiar with the use of smartphones, the combination of SBFI and telemedicine presents a promising approach to involve nonexpert examiners in providing quality health care on a larger scale.4,16 However, there is a need for further evidence, notably when it comes to the use of telemedicine and the acquisition of images through nonexpert operators.4,11,21

COMBINATION OF SBFI AND MACHINE LEARNING

The use of machine learning for analysis of SBFI could make screenings even more accessible. Its application for detection of retinopathy of prematurity and diabetic retinopathy achieved first encouraging results.73–77 Online- and offline-based machine learning algorithms are conceivable, the offline version being more suitable for rural areas in which no stable internet connection might be available.75–77 Machine learning brought together with SBFI may be one way to further reduce the burden of providing affordable and accessible screenings. So far, the presented data are limited to retinopathy of prematurity and diabetic retinopathy with the software typically only being available in combination with specific devices, but with software engineering and smartphone technology advancing rapidly, the prospects are auspicious.

CONCLUSIONS AND OUTLOOK

In summary, there are a large number of different SBFI adapters available to date. All of the presented SBFI approaches are relatively low-cost compared with conventional retinal imaging devices. Furthermore, SBFI is delegable to paramedical staff/technicians and can be implemented in telemedical health service provision. Against this background and because of promising results reviewed herein, it is likely for the smartphone to play an essential role in screening for diabetic retinopathy, glaucoma, and retinopathy of prematurity in low- and middle-income settings.33 In addition, combination with machine learning algorithms might further facilitate applicability in these settings.

However, with significant discrepancies in diagnostic accuracy for intended disease screening and substantially varying SBFI image quality, more studies on the comparison of SBFI devices and a reference standard for grading of SBFI image quality are warranted.

Smartphones have become an integral part of our daily life. It is highly likely that they will continue to do so and emerge even more for purposes beyond including medicine. Technology is progressing at a high pace and with that pace increasing, opportunities and also challenges arise. SBFI is a very promising approach making health care more accessible worldwide at lower costs and hence can be considered a great opportunity. In the coming years it should be made sure that upcoming technology in hardware and software is modular, easily accessible, and thoroughly reviewed to maximize the benefits that can be generated out of these advancements globally.

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Keywords:

smartphone funduscope; smartphone funduscopy; smartphone ophthalmoscope; smartphone ophthalmoscopy; smartphone-based fundus imaging

Copyright © 2020 Asia-Pacific Academy of Ophthalmology. Published by Wolters Kluwer Health, Inc. on behalf of the Asia-Pacific Academy of Ophthalmology.