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Keywords:
Retinopathy of prematurity
Rural
Outreach
Screening
Laser
Telemedicine
India
Middle-income countries such as India are suffering from the third epidemic of retinopathy of prematurity (ROP). Improved survival and lower infant mortality rates have resulted in an increased number of
preterm survivors in rural areas that unfortunately lack ROP specialists. We report our experience of a
publiceprivate partnership in rural India of an ongoing telemedicine program Karnataka Internet
Assisted Diagnosis of Retinopathy of Prematurity program KIDROP that provides ROP screening by nonphysicians. The analysis of 20,214 imaging sessions of 7106 from 36 rural centers in 77 months of activity
are presented. The overall incidence of any stage and treatment requiring ROP was 22.39% and 3.57%
respectively. We found a higher incidence of severe ROP in private (7.1%) vs government centers (1.7%).
Fifty of the 254 babies (19.69%) who underwent treatment were outside the American screening
guidelines cut-off. The report compares other real-world tele-ROP programs, summarizes the impact,
and provides future strategies for outreach ROP screening in middle-income countries.
2015 Elsevier Ltd. All rights reserved.
1. Introduction
Retinopathy of prematurity (ROP) is one of the leading causes of
preventable infant blindness worldwide [1,2]. Since the 1990s the
focus of ROP as a public health problem has shifted from the
industrialized world to middle-income nations [1,2]. Countries
with improving economies and standard of living have also shown
rapid improvement in the survival of their infants. Infant mortality
rates in India have fallen in the past two decades resulting in
increased numbers of survivors, even in the rural areas. With
decreasing mortality, emphasis on intact survival is now the new
benchmark of neonatal quality of life in government-based child
health programs [3,4]. Despite this, factors such as a high birth rate,
declining infant mortality, improved survival of low-birth-weight
babies, and lack of uniform neonatal care increase the
http://dx.doi.org/10.1016/j.siny.2015.05.002
1744-165X/ 2015 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Vinekar A, et al., Role of tele-medicine in retinopathy of prematurity screening in rural outreach centers in
India e A report of 20,214 imaging sessions in the KIDROP program, Seminars in Fetal & Neonatal Medicine (2015), http://dx.doi.org/10.1016/
j.siny.2015.05.002
A. Vinekar et al. / Seminars in Fetal & Neonatal Medicine xxx (2015) 1e11
Fig. 1. A level III technician performs Retcam imaging on an infant in a rural neonatal intensive care unit. In the foreground, the project manager uploads images to the server for
remote viewing and reporting by the retinopathy of prematurity expert.
Please cite this article in press as: Vinekar A, et al., Role of tele-medicine in retinopathy of prematurity screening in rural outreach centers in
India e A report of 20,214 imaging sessions in the KIDROP program, Seminars in Fetal & Neonatal Medicine (2015), http://dx.doi.org/10.1016/
j.siny.2015.05.002
A. Vinekar et al. / Seminars in Fetal & Neonatal Medicine xxx (2015) 1e11
Fig. 2. Map of India and Karnataka state with the two study zones, namely North Zone (red outline) and Central Zone (blue outline).
2.3. Imaging
2.4. Reporting and data management
At each session, technicians perform a modied PHOTO-ROP
group imaging sequence called the KIDROP sequence to include
seven (minimum) images per eye [5]. These included a dilated
anterior segment image taken without any lens on the camera, and
the other posterior segment images obtained with the 130 (ROP
lens). These included the disc and macula center and the four
extreme peripheries e temporal, inferior, nasal and superior e with
the attempt to image the ora serrata in all cases. Additional images
of any pathology were obtained at the discretion of the technician.
All images were captured in video mode and the relevant stills were
saved in the database. All sessions were performed under topical
anesthesia (proparacain 0.5%) either in the NICU, the step-down
room or the outpatient department in the pediatric unit of the
respective hospital. All infants born with birth weight of 2000 g or
34 weeks of gestational age were included for ROP screening.
Standard ROP screening guidelines were followed [21,22]. Treatment in the program was done by laser photoablation using the
ETROP guidelines with the 532 nm green laser. As far as possible the
treatment was performed at the rural center by the ROP specialist
traveling from Bangalore, thereby obviating the need for the infant
to travel to the city. In cases where this was not possible due to
Once the images had been obtained and saved on the Retcam
Shuttle software, the technician reported these images using the
decision-aiding algorithm (Fig. 3) based on the redeorangeegreen
triage described previously [5]. The level III technicians decide on
the follow-up based on the images they have captured, by comparison with previous visits for progression or regression, assessment of contributing systemic factors, postnatal age and social
factors including timing of discharge and venue of follow-up.
Images were also uploaded via a USB data card onto a secure,
indigenous platform, which uses the TeleCare Software (i2i Telesolutions and Telemedicine Pvt. Ltd, Bangalore). The data were
hosted on a secure server that was managed by the private company with the agreement that the data would be transferred to the
Center for Development of Advanced Computing (CDAC, Bangalore)
server when required. The reporting template used by the remote
expert on his/her smartphone or laptop uses the International
Classication of Retinopathy of Prematurity (ICROP) classication
and Early Treatment for Retinopathy of Prematurity (ETROP)
grading for treatment in a drop-down menu for rapid click. The
ROP specialist to read and generate the report uses a validated
Please cite this article in press as: Vinekar A, et al., Role of tele-medicine in retinopathy of prematurity screening in rural outreach centers in
India e A report of 20,214 imaging sessions in the KIDROP program, Seminars in Fetal & Neonatal Medicine (2015), http://dx.doi.org/10.1016/
j.siny.2015.05.002
A. Vinekar et al. / Seminars in Fetal & Neonatal Medicine xxx (2015) 1e11
Fig. 3. Three-way, decision-aiding algorithm of the Karnataka Internet Assisted Diagnosis of Retinopathy of Prematurity program (KIDROP) that technicians use to grade images that
they capture in the absence of retinopathy of prematurity specialists. (Reproduced with permission from Table 2, p. 44 in Vinekar A, Gilbert C, Dogra M, et al. The KIDROP model of
combining strategies for providing retinopathy of prematurity screening in underserved areas in India using wide-eld imaging, tele-medicine, non-physician graders and smart
phone reporting. Indian J Ophthalmol 2014;62:41e9.)
and October 1st, 2012 to February 28th, 2015 for CK zone. This is
~77.5 cumulative months of program activity. During this period,
2345 visits to 36 rural NICUs in 13 district headquarters were
completed. In all, 20,214 infant imaging sessions were completed
and analyzed. The zonal demographic details are summarized in
Table 1.
During this period, 7106 premature infants weighing either
2000 g or 34 weeks of gestational age were screened for ROP. Of
these, 3728 (52.5%) were male and the remaining 3378 (47.5%) were
female; 306 (4.3%) were born <1000 g birth weight, 3986 (56.1%)
were >1500 g, of whom 660 (9.3%) were >2000 g birth weight and
included due to the gestational age cut-off on the pediatrician's
suggestion. Of the 7016 infants, 2059 were born <30 (28.9%) weeks
of gestational age and the remainder at <30 weeks. On the pediatricians suggestion or based on the birth weight cut-off, 1381 babies
(19.4%) at >34 weeks screening cut-off were included. The birth
weight and gestational age distribution of the study cohort is
summarized in Table 2.
Of the 7106 babies, 1591 (22.39%) had any stage of ROP, of whom
254 (15.96%) or 3.57% of all those screened required treatment. Of
these 254 babies who underwent laser, 50 babies (19.69%) were
>1500 g at birth and >30 weeks of gestational age. These babies
would have been missed if the American screening guidelines had
been used [23]. No infant in the study region developed unscreened
stage 4 or 5 ROP. The ROP stage distribution of the study cohort is
summarized in Table 3. During the study period 508 eyes (254
Table 1
Demographic and enrollment details of infants screened in the rural program in the two zones of intervention.
Parameter
Total
No. of districts
Active period (months)
Distance travelled (km)
No. of NICUs
Government NICUs
Private NICUs
NICU visits
New babies enrolled
Imaging sessions
Images
6
48.5
203,003
17 (4008 babies)
6 (2072 babies)
11 (1936 babies)
1269
4008
11,063
154,906
6
29
140,105
19 (3098 babies)
8 (2574 babies)
11 (524 babies)
1076
3098
9151
128,256
13
77.7
343,108
36 (7106 babies)
14 (4646 babies)
22 (2460 babies)
2345
7106
20,214
283,162
Please cite this article in press as: Vinekar A, et al., Role of tele-medicine in retinopathy of prematurity screening in rural outreach centers in
India e A report of 20,214 imaging sessions in the KIDROP program, Seminars in Fetal & Neonatal Medicine (2015), http://dx.doi.org/10.1016/
j.siny.2015.05.002
A. Vinekar et al. / Seminars in Fetal & Neonatal Medicine xxx (2015) 1e11
Table 2
Birth weight and gestational age distribution of the study cohort (n 7106 infants).
Parameter
North Zone
No. of babies
4008
Sex (M:F)
2177:1831
Birth weight (% of all babies, n 7106)
1000 g
168
1001e1500 g
1619
1501e1750 g
969
1751e2000 g
832
2001 g
420
Gestational age (% of all babies, n 7106)
30 weeks
1134
31e32 weeks
941
33e34 week
1002
35 weeks
931
Central Zone
Total
3098
1551:1547
7106
P < 0.001
138
1195
787
738
240
306 (4.3%)
2814 (39.6%)
1756 (24.71%)
1570 (22.09%)
660 (9.3%)
925
844
879
450
2059
1785
1881
1381
(28.98%)
(25.12%)
(26.47%)
(19.43%)
Table 3
Retinopathy of prematurity (ROP) stage distribution of the study cohort (n 7106
infants).
Parameter
North Zone
(n 4008)
No ROP
3026 (75.5%)
Any stage ROP
982 (24.5%)
Treated ROP
181 (4.52%)
ROP stage distribution (% of all ROP)
Stage 1
378
Stage 2
493
Stage 2 with plus
10
Stage 3
65
Stage 4
0
Stage 5
0
APROP
32
Central Zone
(n 3098)
Total
(n 7106)
2489 (80.34%)
609 (19.66%)
73 (2.36%)
5515 (77.61%)
1591 (22.39%)
254 (3.57%)
127
463
0
17
0
0
6
505 (31.74%)
956 (60.1%)
10 (0.63%)
82 (5.13%)
0
0
38 (2.4%)
Table 4
Government vs private center comparison of study cohort.
Parameter
Government centers
Private centers
Total
P-value
Centers
Visits
Sessions
New babies
Male:female
Birth weight (g)
<1000
1001e1500
1501e1750
1751e2000
2001
Gestational age (weeks)
<30
31e32
33e34
35
ROP stages
All stages
Any stage ROP
Treatment requiring ROP (%)
Proportion of treatment requiring ROP to all ROP
14
1328
12,175
4646
2329:2317
22
1017
8038
2460
1399:1061
36
2345
20,214
7106
<0.001
<0.001
206
1804
1153
1114
369
100
1010
603
456
291
306
2814
1756
1570
660
<0.001
1309
1112
1279
946
750
673
602
435
2059
1785
1881
1381
<0.001
770
770/4646 (16.57%)
79/4646 (1.7%)
79/770 (10.23%)
821
821/2460 (33.38%)
175/2460 (7.11%)
175/821 (21.32%)
1591
1591/7106 (22.4%)
254/7106 (3.57%)
254/1591 (15.96%)
<0.001
0.0024
<0.001
<0.001
<0.001
Please cite this article in press as: Vinekar A, et al., Role of tele-medicine in retinopathy of prematurity screening in rural outreach centers in
India e A report of 20,214 imaging sessions in the KIDROP program, Seminars in Fetal & Neonatal Medicine (2015), http://dx.doi.org/10.1016/
j.siny.2015.05.002
Program
Time period
reported
Region
Device
No. of
infants
Imaging personnel
Grading/reporting
Outcome measures
Results
Lorenz et al.
[32]
2001e2007
East Bavaria,
Germany
1222
Ells et al.
[30]
2000e2001
Alberta, Canada
Referral-warranted (RW)ROP
Weaver and
Murdock
[33]
2007e2011
Montana, USA
One Retcam II in a
single NICU
137
Pediatric ophthalmologists
(retrospective analysis)
RW-ROP
Fijalkowski
et al [34]
SUNDROP
2005 to 2010
Three NICUs
511
NICU nurse
ROP specialist.
Every infant received indirect
ophthalmoscopy examinations
until termination criteria were
achieved or until treatment.
(1) Treatment-warranted
(TW)-ROP
(2) ETROP type 1
(3) Adverse anatomical
events
Urban, semi-urban
and rural,
multicenter, India
Six districts,
35 NICUs
(300 km radius) from
the cohort of 81 NICUs
1601
64
25 certied non-physicians:
NICU nurses (44%), neonatal
nurse practitioners (24%),
ophthalmic photographers
(8%), ocular coherence
tomography technician (4%),
an ophthalmic medical
technologist (4%), and
individuals with non-clinical
backgrounds (16%)
RW-ROP
44
Shah et al.
[35]
Quinn et al.
[36]
E-ROP
2011 to 2013
A. Vinekar et al. / Seminars in Fetal & Neonatal Medicine xxx (2015) 1e11
Please cite this article in press as: Vinekar A, et al., Role of tele-medicine in retinopathy of prematurity screening in rural outreach centers in
India e A report of 20,214 imaging sessions in the KIDROP program, Seminars in Fetal & Neonatal Medicine (2015), http://dx.doi.org/10.1016/
j.siny.2015.05.002
Table 5
Comparison of real world tele-ROP programs worldwide.
Current
report
2011 to date
Rural, multicenter,
India
7106
A. Vinekar et al. / Seminars in Fetal & Neonatal Medicine xxx (2015) 1e11
examining surgeon, which is unfortunately difcult to assess. Besides, IO has several problems even among the ROP experts. In the
landmark CRYO ROP study, the initial diagnosis of threshold disease
in 12% of eyes was overruled on subsequent examination within
three days by another examiner [24]. Inter-observer variation could
be minimized if experts opined on an image rather than on a live
patient [25]. Furthermore, with ROP training not being mandatory
in medical college curricula in India and only few postgraduate
courses in ophthalmology imparting indirect ophthalmoscopy
training to residents and fellows, the so-called gold standard for
ROP screening appears to be an inadequate tool in tackling the
current burden, even as its relevance is being questioned the world
over [26].
Alternate methods of screening in outreach centers therefore
needed exploration. Retinal imaging and telemedicine models offer
viable options. Wide-eld digital imaging (WFDI) for ROP screening
was rst suggested in 1999 [27] and a proof of concept demonstrated in 2000 [28]. Images were read remotely by readers. There
was difculty in commenting on zone 3 disease, perhaps due to the
limitations of the older devices [29]. However, WFDI fared better
than conventional examinations with indirect ophthalmoscopy (IO)
in giving a more accurate longitudinal follow-up [30]. In the USA,
WFDI as the primary means of screening was demonstrated in the
Stanford University Network for Diagnosis of Retinopathy of Prematurity (SUNDROP) program. The program used indirect
ophthalmoscopy only if the Retcam image was diagnosed to have a
referral-warranted ROP or the baby was discharged from the NICU
[31]. The program since then has demonstrated the utility of the
store-and-forward, hub-and-spoke method in which the remote
expert opined on the images captured by trained nurses [32].
The KIDROP tele-ROP program in India was initiated in 2008. It
trained and employed accredited cadres of Retcam trained technicians who used an indigenously created triage algorithm to
determine on site whether the baby needed follow-up, needed
treatment, or could be discharged. A summary of real-world teleROP programs is detailed in Table 5. This is the rst program from a
middle-income country to implement tele-ROP in a rural area. In
the study region, there was no ROP screening prior to the intervention, making the KIDROP program the only means of providing
ROP screening to these infants. The program is undergoing
expansion to other Indian states through the national task on ROP,
supported by the Government of India.
There were three unique aspects of the program: (1) nonphysicians (level IeIII technicians) were allowed to report and
analyze the images as the rst point of contact, thereby providing
the diagnosis and decision to the rural mother before she left the
center; (2) there were no mandated indirect ophthalmoscopy examinations at any point either to continue follow-up or to terminate screening. This strategy has allowed the onus of screening care
to be shifted to the rural center, thereby obviating the dependence
on the limited few experts from the cities; (3) the program aims at
detecting any stage, not just treatment requiring disease. This differs from other programs that used referral-warranted criteria as
their end-point [33e37]. This multicenter report summarizes data
from the initial 77.5 months of program activity exclusively from
rural centers. In all the centers under study, there was no ROP
program prior to KIDROP's intervention and none of their babies
underwent any ROP screening.
Our experience provides new insights into ROP screening in
rural villages as well as the feasibility and sustenance of a telemedicine program for outreach centers. There are six major ndings on ROP demographics of our study. (1) Rural ROP incidence in
this rural multicenter study was 22.39% and treatment-requiring
ROP was 3.57%. This is lower than that for a single rural district
hospital that we reported earlier [14] (41.5% and 10.2%
Please cite this article in press as: Vinekar A, et al., Role of tele-medicine in retinopathy of prematurity screening in rural outreach centers in
India e A report of 20,214 imaging sessions in the KIDROP program, Seminars in Fetal & Neonatal Medicine (2015), http://dx.doi.org/10.1016/
j.siny.2015.05.002
A. Vinekar et al. / Seminars in Fetal & Neonatal Medicine xxx (2015) 1e11
Fig. 4. A frequent scenario in rural, public neonatal intensive care units, which lack infrastructure and are overburdened with large number of admissions.
respectively), but is comparable to some urban centers [9], suggesting that ROP is a signicant rural problem. Urban centers may
be reporting higher ROP either because of the sicker infants they
manage or because they may be using a higher concentration of
oxygen. This needs further research and will need the analysis of
oxygen and other neonatal care practices in rural vs urban centers.
(2) The data suggest that 4% of all admissions are <1000 g and that
up to 29% of babies enrolled are born <30 weeks of gestational age,
indicating the improved survival of these at-risk infants in rural
centers. (3) There appear to be regional differences in the severity
and type of ROP documented. North Karnataka centers have more
aggressive posterior ROP (84% of all cases of APROP) compared to
the central zone. Since the former is more backward with respect to
human developmental indices, further investigation on correlating
-vis the more
the level of neonatal care in these centers vis-a
developed central zone is needed. (4) Private hospitals appear to be
dealing with a greater incidence of any stage ROP (33% vs 16%) and
severe disease (7.1% vs 1.7%) needing treatment compared to government centers. This is not because lighter and younger babies
are being managed in the former (Table 4) but could be due to
higher systemic comorbidities in these babies or because of more
aggressive preterm management in the private hospitals. These
associations need further investigation. (5) The data suggest that
Fig. 5. Continuum of care of a preterm baby to prevent or reduce the occurrence and severity of retinopathy of prematurity. NICU, neonatal intensive care unit.
Please cite this article in press as: Vinekar A, et al., Role of tele-medicine in retinopathy of prematurity screening in rural outreach centers in
India e A report of 20,214 imaging sessions in the KIDROP program, Seminars in Fetal & Neonatal Medicine (2015), http://dx.doi.org/10.1016/
j.siny.2015.05.002
A. Vinekar et al. / Seminars in Fetal & Neonatal Medicine xxx (2015) 1e11
Fig. 6. Mothers wait with their infants being dilated for retinopathy of prematurity (ROP) screening on the Retcam in a rural center. This opportunity is used to promote awareness
about ROP as well as immunization, breastfeeding, and well-baby practices.
Please cite this article in press as: Vinekar A, et al., Role of tele-medicine in retinopathy of prematurity screening in rural outreach centers in
India e A report of 20,214 imaging sessions in the KIDROP program, Seminars in Fetal & Neonatal Medicine (2015), http://dx.doi.org/10.1016/
j.siny.2015.05.002
10
A. Vinekar et al. / Seminars in Fetal & Neonatal Medicine xxx (2015) 1e11
Practice points
This is the first multicenter rural retinopathy of prematurity (ROP) study and covers a population of >23 million.
Non-physician technicians can use wide-field digital imaging to screen for ROP as the primary method of
screening.
Technicians can be trained to capture images as well as
grade and report the disease, obviating the need for the
scarce ROP specialist in the outreach.
There is a large proportion of premature infants born <30
weeks of gestational age and <1000 g at birth who are
surviving in rural centers.
There is considerable regional variation in the severity of
ROP within the same state and this could be related to
neonatal care and overall developmental indices.
Private NICUs appear to have a higher incidence of any
stage of ROP as well as severe disease compared to their
government counterparts.
A larger proportion of males are cared for in private
hospitals compared to females, suggesting a gender bias.
This is not evidenced in the public hospitals.
Nearly 20% of babies undergoing treatment were outside
the American screening guidelines and would have been
missed.
There was no case of unscreened stage 5 ROP in any
center during the study period.
Research directions
The cost/benefit utility analysis of this telemedicine program for ROP screening in rural outreach centers needs to
be assessed.
Innovations in low-cost infant retinal cameras that can be
situated in each center and connected to a central cloudbased server managed by ROP specialists or trained
technicians or image readers would increase the
coverage and accessibility of the program.
The impact of this program in training of health care
personnel, including obstetricians, pediatricians, nursing
and paramedical staff in the NICUs and special newborn
care units in the judicious use of oxygen and monitoring
of ROP needs to be studied.
Please cite this article in press as: Vinekar A, et al., Role of tele-medicine in retinopathy of prematurity screening in rural outreach centers in
India e A report of 20,214 imaging sessions in the KIDROP program, Seminars in Fetal & Neonatal Medicine (2015), http://dx.doi.org/10.1016/
j.siny.2015.05.002
A. Vinekar et al. / Seminars in Fetal & Neonatal Medicine xxx (2015) 1e11
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Please cite this article in press as: Vinekar A, et al., Role of tele-medicine in retinopathy of prematurity screening in rural outreach centers in
India e A report of 20,214 imaging sessions in the KIDROP program, Seminars in Fetal & Neonatal Medicine (2015), http://dx.doi.org/10.1016/
j.siny.2015.05.002