Feasibility of telemedicine program using a hand-held nonmydriatic retinal camera in Panama

INTRODUCTION

Visual impairment causes a significant global economic burden, resulting in an estimated 30.2% relative reduction in employment and 0.3% GDP loss

. Of the 300 million visually impaired individuals worldwide, 90% live in developing countries

. Furthermore, up to 75% of blindness is considered to be avoidable

. While the majority of the global burden of ocular disease is a result of untreated cataracts, other major contributors include posterior segment conditions such as glaucoma, age-related macular degeneration (AMD), and diabetic retinopathy (DR)

. Retinal pathology may represent an underappreciated contributor to the global burden of eye disease. For instance, the global prevalence of DR is estimated at 35.4%, and as the global incidence of diabetes rises, the burden of visual disease from DR is expected to increase

.In addition, AMD is the leading cause of blindness in people older than 65y worldwide

. Retinal pathology is becoming a larger issue as the global population ages and the prevalence of diabetes increases each year

. Further complicating the picture, screening for retinal pathology is considerably more difficult than anterior ocular conditions; multiple studies have demonstrated that the accuracy of DR screening by nonophthalmic health care providers is lower than rates achieved by ophthalmologists and retinal specialists

.

The burden of ocular disease in Panama is significant, with up to 3.0% of the population blind, and 16.1% with moderate visual impairment

. Although unoperated cataracts are the leading cause of blindness in Panama (66.4%), glaucoma(10.2%), AMD (5.1%), pterygium (2.2%), and DR (1.5%)contribute significantly to the burden of eye disease

.Medical students obtaining retinal images using the Pictor Plus in the remote setting of Bocas del Toro, Panama were able to obtain reasonably high-quality images of the retina, optic nerve, optic vessels and vitreous humor. Image quality by the non-ophthalmologists using a tabletop non-mydriatic fundus camera were grades 4 or 5 in 37%-44% of all images obtained in the FOTO-ED study

. These are comparable to the results presented herein, where 49.61% of images were grade 4 or 5. Another more recent study using a hand-held camerademonstrated 63% excellent quality images (on a four-tiered scale that included grades inadequate, fair, good, and excellent)but these were obtained by ophthalmologic providers in a darkened room, increasing mydriasis and likely improving imaging reliability

. Despite our study demonstrating image quality consistent with the FOTO-ED study, the more recent study implies that more reliable quality may be achieved.Furthermore, we found there were fewer patients with high quality images taken of both eyes (17.1%). Often, confounding factors in older patients (difficulty keeping one eye open,unilateral cataract), may have impaired our ability to capture high quality images in both eyes.

One possible solution to this care gap may come in the form of telemedicine. Telemedicine screening programs using digital fundus photography have shown promising results in the remote diagnosis of DR

. Both hand-held and tabletop retinal cameras have been used to acquire clinically useful images of the retina

. Furthermore, compared to direct ophthalmoscopy, hand-held retinal cameras provide a wider field of view, and have demonstrated improved diagnostic accuracy of DR and optic disc edema by non-ophthalmologic providers to levels comparable with ophthalmologists

.Although non-ophthalmic health care providers typically report lower levels of confidence with direct fundoscopy and demonstrate lower DR screening accuracy compared to trained ophthalmologists

, the wider field of view may help alleviate this concern

. Telemedicine screening for DR is the most well-validated of the ocular telemedicine programs

,but there is evidence to support telemedicine screening and handheld portable fundus camera use for AMD, suspicious optic nerve, retinopathy of prematurity, and papilledema, as well

.

As medical students frequently volunteer to provide medical care abroad

, there may be utility in utilizing medical students in ophthalmologic telemedicine screening programs. If medical students can quickly obtain high quality images of the retina with minimal interruption to clinic workflow, patients with retinal disease might be triaged efficiently when these communities do receive ophthalmologic care. Such a program might also improve monitoring of chronic retinal pathology, such as DR, and improve long-term patient outcomes.

Ethical Approval This study received Institutional Review Board (IRB) approval from the University of California, Irvine(IRB #2019-5579), and was conducted in accordance with the Declaration of Helsinki. Formal informed consent was waived by the IRB given the retrospective nature of the study(expedited, category 5).

SUBJECTS AND METHODS

The Pictor Plus (Volk Optical, Mentor OH) is a relatively inexpensive, hand-held fundus camera with a 45° field of view(nine times that of a standard direct ophthalmoscope)

. The aim of this study is to retrospectively review an ophthalmologic telemedicine program between University of California, Irvine and the Floating Doctors to determine if minimally trained medical students can improve ophthalmic care in Bocas del Toro by obtaining retinal images of sufficient quality to remotely diagnose retinal pathology using a hand-held, nonmydriatic fundus camera.

In June 2018, a group of three medical students volunteered at clinics operated by the Floating Doctors in the province of Bocas del Toro, Panama. Non-mydriatic images of the retina were obtained using the Pictor Plus in adult (18+ years of age)patients at the request of a Floating Doctors provider once it was determined such photos may have diagnostic value. After discussion with Floating Doctors providers, it was agreed that obtaining retinal images would be diagnostically useful in all patients presenting with an ocular complaint, or with a history of diabetes previously diagnosed by the Floating Doctors. The medical students trained with the Pictor Plus for approximately 20h prior to their first day at the Floating Doctors clinic.

All images were sent to two board-certified ophthalmologists at the University of California, Irvine for remote diagnosis.The photos were randomized so that the left and right eye of the same patient would not appear in sequence. Images were analyzed using a modified version of the FOTO-ED scale developed by Bruce

(Figure 1). This is a validated scale used to grade images based on diagnostic utility and ability to visualize individual components of the retina, optic nerve,vessels, and periphery. The reviewers were able to enlarge images and adjust brightness.

Further improvements are necessary to acquire higher quality images more reliably. This may include further training and experience or mydriasis.

RESULTS

Average image quality was fairly consistent between graders, although grader 2 graded more photos as “ideal quality” compared to grader 1. The inter-rater reliability(0.61, or moderate) was lower than reported in the FOTOED study (0.84-0.87, or strong)

. There are several possible explanations for that. Dark rooms were rarely available at Floating Doctors clinics, and, although specific data were not collected on pupil size, the authors observed that many patients had miotic pupils that were difficult to image; the FOTOED study reported small pupils as a predictor of poor image quality

. Age greater than 40 years was also associated with poor image quality in this study

, and our study population was almost entirely composed of older individuals, although again demographic data was not collected. Furthermore,approximately 25% of patients had suspected cataracts, and the image quality was an average of 1.02 points worse in these patients than in those without. Indeed, a study on DR screening by Murgatroyd

found that posterior subcapsular cataract(

=0.004) and reduced near-vision (

=0.006) predicted ungradable status of nonmydriatic photographs. Notably, the prevalence of cataracts may be higher in our sample as we primarily imaged individuals with ocular complaints.

Image quality stratified by the individual component of the posterior segment is shown in Table 2. The vitreous was most reliably imaged (91.76% images able to grade), followed by the optic nerve rim (91.05% images able to grade). High quality images of the fovea were obtained least reliably(69.00% images able to grade). The most common retinal findings included tortuous vessels (20 patients), cotton wool spots (8 patients), drusen (6 patients), optic nerve pallor(7 patients), enlarged cup-to-disc ratio (22 patients), and peripapillary atrophy (22 patients). Image quality in patients with suspected cataracts is shown in Table 3. Image quality was 1.02 points lower in patients with suspected cataracts than those without.

本文以袁家村鐵礦的露天礦山為例，對(duì)其邊坡的穩(wěn)定性進(jìn)行了分析，并研究了該礦區(qū)的邊坡安全穩(wěn)定模擬情況，從而為該礦安全穩(wěn)定生產(chǎn)奠定基礎(chǔ)。

DISCUSSION

Rural populations with limited access to medical care are frequently targets of medical aid organizations

. In particular,Bocas del Toro is a remote archipelago in western Panama where inhabitants lack access to reliable health care

. The primary healthcare provider for the greater than 25 isolated island communities in this region is a non-profit organization stationed in Bocas del Toro (entitled “The Floating Doctors”). This organization is primarily run by volunteer family medicine,emergency medicine, or internal medicine physicians from the United States and Europe, as well as those from Central and South America. However, only very rarely do they have an onsite ophthalmologist, which creates a gap in access to care in the realm of retinal disease.

“玉風(fēng)窯”也是無(wú)形的，但它可以在邱含、陳敏、何炳欽、曾瑾、彭松等一眾成名的藝術(shù)家，也在屈曉鳴、周志斌、邢當(dāng)當(dāng)、李可榮、孫建文、郭越等一幫第三代藝術(shù)家的瓷畫(huà)藝術(shù)里抒發(fā)對(duì)自然世界的迷戀，在青花與釉里紅的美感里展現(xiàn)人類的精神姿態(tài)。本文以“回顧”為主題，穿越將近三十多年的時(shí)間跨度，通過(guò)過(guò)去與現(xiàn)在的人、作品與藝術(shù)價(jià)值的相互對(duì)比，再現(xiàn)當(dāng)年?duì)t火旺盛火紅的“玉風(fēng)窯”盛景。

Seventy patients provided a total of 127 images. Image qualitygraded by two ophthalmologists using the modified FOTOED scale is displayed in Table 1. Average image quality was consistent across graders at 3.30±0.99 [all data are presented as mean±standard deviation (SD), unless otherwise specified] for grader 1 and 3.31±1.22 in grader 2. Modal image quality was 4/5 on the FOTO-ED scale (37.40% of images). Of the 127 images, 62 and 64 images were rated at 4 or higher by grader 1 and grader 2, respectively (48.82% and 50.39%). Thirty patients had at least one eye image with ideal quality (42.86%),while only one patient had no adequate photos taken (1.43%).High quality images (grades 4 or 5) were obtained in both eyes in 12 patients (17.14%). The inter-rater reliability between the two ophthalmologists was 0.614.

One possible solution to improving image quality obtained in rural Panama is to dilate the pupils. Although non-mydriatic fundus photography has been established as effective in screening for diabetic retinopathy (sensitivity 64%-97.9%,specificity 65.6%-98%)

, and previous work has shown that image quality is higher in dilated eyes compared to nondilated eyes

, dilating the eye would almost certainly improve image quality at the expense of causing patient discomfort and disruption to clinic flow. The imaging protocol in this study required no more than five minutes, inflicted minimal discomfort to the patient, and can occur during the natural waiting period between initial intake (where ocular complaint or history of uncontrolled diabetes was ascertained)and the visit with the provider. This seamless incorporation into clinic flow maximized value to the Floating Doctors while minimizing distraction. Dilating the eye complicates screening and may limit widespread implementation of an ophthalmologic telemedicine program in a busy clinic.Although the Pictor Plus has an eye cup that blocks light into the eye that is being imaged, an eye patch may be placed over the contralateral eye to limit the consensual pupillary reflex and improve nonmydriatic imaging in bright lighting conditions.A non-mydriatic camera with a wider view angle may also improve image utility by virtue of imaging a larger retinal area to reveal pathology beyond the 45-degree field

.

The most common retinal findings included torturous vessels,cotton wool spots, drusen, optic nerve pallor, enlarged cup-todisc ratio and peripapillary atrophy. Neovascularization and hemorrhage were not seen, but there were several patients with chorioretinal scars. While there is no gold standard to compare these results with, this suggests that retinal imaging to screen for disease may improve adverse visual outcomes in Bocas del Toro (Panama), and a hand-held nonmydriatic fundus camera in the hands of minimally trained medical students may successfully achieve this goal.

In conclusion, addressing the significant global burden of eye disease is especially challenging in remote areas without routine access to eye care. Retinal pathology such as DR and macular degeneration are two diseases increasing in prevalence as the global population ages and the prevalence of diabetes increases. This study described the quality of images obtained through a telemedicine screening program for retinal disease among rural island communities comprising an archipelago in Bocas del Toro, Panama. We obtained retinal images using a hand-held nonmydriatic digital camera and reported high image quality in both eyes of only 17% of patients, possibly due to small pupillary diameters. Further improvements are necessary to acquire higher quality images more reliably.

Himstead AS: Experimental design,data collection, data analysis, manuscript authorship; Prasad J Experimental design, data collection, manuscript authorship;Melucci S: Experimental design, data collection, manuscript authorship; Gustafson KM: Blinded image review, manuscript review; Israelsen PE: Blinded image review, manuscript review; Browne A: Idea conception, experimental design,manuscript review.

這話讓秀容川很意外，秀容兵是秀容月明統(tǒng)領(lǐng)的一支部隊(duì)，軍紀(jì)嚴(yán)明，驍勇善戰(zhàn)，后來(lái)，秀容月明怨恨朝廷不給他升官，降了胡人。消息傳出，舉國(guó)震驚，十萬(wàn)秀容兵更是放聲大哭。這蔣春豬若真是秀容兵，當(dāng)大罵秀容月明才對(duì)，怎會(huì)稱他為英雄？

None;

None;

None;

None;

None;

None.

1 Marques AP, Ramke J, Cairns J, Butt T, Zhang JH, Muirhead D, Jones I, Tong B, Swenor BK, Faal H, Bourne RRA, Frick KD, Burton MJ.Global economic productivity losses from vision impairment and blindness.

2021;35:100852.

2 Muecke J, Sia DIT, Newland H, Casson RJ, Selva D. Perspective on ophthalmic support in countries of the developing world.

2013;41(3):263-271.

3 Flaxman SR, Bourne RRA, Resnikoff S, Ackland P, Braithwaite T,Cicinelli MV, Das A, Jonas JB, Keeffe J, Kempen JH, Leasher J,Limburg H, Naidoo K, Pesudovs K, Silvester A, Stevens GA, Tahhan N, Wong TY, Taylor HR, Vision Loss Expert Group of the Global Burden of Disease Study. Global causes of blindness and distance vision impairment 1990-2020: a systematic review and Meta-analysis.

2017;5(12):e1221-e1234.

4 DeBuc DC. The role of retinal imaging and portable screening devices in tele-ophthalmology applications for diabetic retinopathy management.

2016;16(12):132.

5 Jin K, Lu HT, Su ZA, Cheng CM, Ye J, Qian DH. Telemedicine screening of retinal diseases with a handheld portable non-mydriatic fundus camera.

2017;17(1):89.

6 Dunn HP, Browning SD, Thomson D, Yates WB, McCluskey P, Keay L, White AJ, Fraser CL. Impact on patient management of nonmydriatic fundus photography compared to direct ophthalmoscopy in a regional Australian emergency department.

2022;34(2):186-193.

7 Crispín Milart PH, Prieto-Egido I, Díaz Molina CA, Martínez-Fernández A. Detection of high-risk pregnancies in low-resource settings: a case study in Guatemala.

2019;16(1):80.

8 Jezek T, Bamodu OA. A cross-country comparison of malaria policy as a premise for contextualized appropriation of foreign aid in global health.

2021;19:93.

9 Bhatter P, Cao L, Crochetiere A, Raefsky SM, Cuevas LR, Enendu K,Frisch EH, Shumway C, Gore C, Browne AW. Using a macro lens for anterior segment imaging in rural Panama.

2020;26(11):1414-1418.

10 Maa AY, Patel S, Chasan JE, Delaune W, Lynch MG. Retrospective evaluation of a teleretinal screening program in detecting multiple nondiabetic eye diseases.

2017;23(1):41-48.

11 Biswas P, Batra S, Majji AB, Natarajan S, Sachdev M, Verma L,Sharma N, Honavar SG, Sinha S, Porwal AC, Prasad RK, Bawankule P, Saxena R, Narayanan R, Raman R, Nag S, Ghosh P. The All India Ophthalmological Society - Academic and Research Committee pan-India diabetic retinopathy project “Fixing the missing link”: prevalence data from West Bengal.

2021;69(11):3103-3109.

12 Korn Malerbi F, Lelis dal Fabbro A, Botelho Vieira Filho JP, Franco LJ. The feasibility of smartphone based retinal photography for diabetic retinopathy screening among Brazilian Xavante Indians.

2020;168:108380.

13 Malerbi FK, Andrade RE, Morales PH, Stuchi JA, Lencione D, de Paulo JV, Carvalho MP, Nunes FS, Rocha RM, Ferraz DA, Belfort R, Jr. Diabetic retinopathy screening using artificial intelligence and handheld smartphone-based retinal camera.

2021;2021:1932296820985567.

14 Queiroz MS, Carvalho JXD, Bortoto SF, Matos MRD, Malerbi FK.Diabetic retinopathy screening in urban primary care setting with a handheld smartphone-based retinal camera. 2020.

15 Bedard C, Liu SS, Patterson C, Gerstein H, Griffith L. Systematic review: can non-mydriatic cameras accurately detect diabetic retinopathy?

2017;129:154-159.

16 Hong KR, Collon S, Chang D, Thakalli S, Welling J, Oliva M, Peralta E, Gurung R, Ruit S, Tabin G, Myung D, Thapa S. Teleophthalmology through handheld mobile devices: a pilot study in rural Nepal.

2019;8(1):10.7309/jmtm.8.1.1.

17 Bursztyn L, Woodward MA, Cornblath WT, Grabe HM, Trobe JD, Niziol L, de Lott LB. Accuracy and reliability of a handheld,nonmydriatic fundus camera for the remote detection of optic disc edema.

2018;24(5):344-350.

18 Yao XC, Son T, Ma JC. Developing portable widefield fundus camera for teleophthalmology: technical challenges and potential solutions.

(

) 2022;247(4):289-299.

19 Palermo BJ, D'Amico SL, Kim BY, Brady CJ. Sensitivity and specificity of handheld fundus cameras for eye disease: a systematic review and pooled analysis.

2021:S0039-S6257(21)00210-1.

20 Rajalakshmi R, Prathiba V, Arulmalar S, Usha M. Review of retinal cameras for global coverage of diabetic retinopathy screening.

(

) 2021;35(1):162-172.

21 Alm M, Hautala N, Bloigu R, Huhtakangas J. Comparison of optic disc evaluation methods in neurology emergency patients.

2019;140(6):449-451.

22 Goyal A, Gopalakrishnan M, Anantharaman G, Chandrashekharan DP, Thachil T, Sharma A. Smartphone guided wide-field imaging for retinopathy of prematurity in neonatal intensive care unit - a Smart ROP (SROP) initiative.

2019;67(6):840-845.

23 Prakalapakorn SG, Freedman SF, Hutchinson AK, Wallace DK,Stinnett SS, Riggins JW, Gallaher KJ. Evaluating a portable,noncontact fundus camera for retinopathy of prematurity screening by nonophthalmologist health care workers.

2018;2(8):864-871.

24 Rassiwala J, Vaduganathan M, Kupershtok M, Castillo FM, Evert J.Global health educational engagement - a tale of two models.

2013;88(11):1651-1657.

25 Bruce BB, Lamirel C, Biousse V, Ward A, Heilpern KL, Newman NJ,Wright DW. Feasibility of nonmydriatic ocular fundus photography in the emergency department: phase I of the FOTO-ED study.

2011;18(9):928-933.

26 L?pez M, Brea I, Yee RT, Yi R, Carles V, Broce A, Limburg H, Silva JC. Survey on avoidable blindness and visual impairment in Panama.

2014;36(6):355-360.

27 Lamirel C, Bruce BB, Wright DW, Delaney KP, Newman NJ, Biousse V. Quality of nonmydriatic digital fundus photography obtained by nurse practitioners in the emergency department: the FOTO-ED study.

2012;119(3):617-624.

28 Murgatroyd H, Cox A, Ellingford A, Ellis JD, MacEwen CJ, Leese GP.Can we predict which patients are at risk of having an ungradeable digital image for screening for diabetic retinopathy?

(

)2008;22(3):344-348.

29 Deb-Joardar N, Germain N, Thuret G, Manoli P, Garcin AF, Millot L, Gavet Y, Estour B, Gain P. Screening for diabetic retinopathy by ophthalmologists and endocrinologists with pupillary dilation and a nonmydriatic digital camera.

2005;140(5):814-821.e2.

30 Wang BQ, Toslak D, Alam MN, Chan RVP, Yao XC. Contact-free trans-pars-planar illumination enables snapshot fundus camera for nonmydriatic wide field photography.

2018;8(1):8768.