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Seminars in Fetal & Neonatal Medicine xxx (2015) 1e11

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Seminars in Fetal & Neonatal Medicine


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Review

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
Anand Vinekar a, *, Chaitra Jayadev a, Shwetha Mangalesh a, b, Bhujang Shetty a,
Dharmapuri Vidyasagar c, d
a

Narayana Nethralaya Postgraduate Institute of Ophthalmology, Bangalore, India


Duke University, Durham, NC, USA
University of Illinois, Chicago, IL, USA
d
M.S. Ramaiah Medical College, Bangalore, India
b
c

s u m m a r y
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

* Corresponding author. Address: Narayana Nethralaya Postgraduate Institute of


Ophthalmology, Bangalore, India. Fax: 91 80 23377329.
E-mail address: anandvinekar@yahoo.com (A. Vinekar).

vulnerability of these babies to unscreened ROP blindness in rural


areas [5,6]. If detected on time, ROP blindness is largely preventable
and has thus gained public importance in countries such as India,
which have mandated ROP and universal screening [3]. Yet, the
operational guidelines and road map remain incomplete and the
infrastructure to execute these services remains grossly inadequate.
Countries such as India and China together account for more
than half of the total number of premature infants born, with India
alone accounting for 3.5 million preterm infants annually [4].
Whereas the incidence of ROP in India varies from 38% to 52% of
at-risk babies in urban areas [7e13], rural ROP has recently been
reported to be comparable [14e16]. The incidence of treatable ROP
is ~5e10% and this accounts for >60,000 infants annually who may
progress to treatment requiring disease in India alone [17]. With
<100 ROP specialists, most of whom practice in the cities, the vast
majority of rural preterm infants remain unscreened, or are
screened too late when they present with stage 5 disease to tertiary
care centers in larger cities [18].
The Karnataka Internet Assisted Diagnosis of Retinopathy of
Prematurity program (KIDROP) is a telemedicine project initiated in

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

Bangalore, in the south Indian state of Karnataka, in 2008. It was the


rst endeavor to address the lack of rural ROP specialists by
employing trained and accredited technicians who use portable,
wide-eld, digital, ocular, imaging cameras, namely the Retcam
Shuttle (Clarity MSI, Pleasanton, CA, USA) to capture, analyze and
report images of at-risk infants in rural outreach centers on a
weekly rotation within designated rural zones [5,19]. Remote city
ROP specialists provide diagnostic and treatment services to these
demarcated zones. The ongoing program has undergone considerable expansion in the past six years through the support of the state
and federal government, to include more centers throughout the
state and train other states also (unpublished data). To the best of
our knowledge, this is the rst multicenter, rural outreach ROP
incidence report collated through a telemedicine approach. All
centers in this study received ROP screening exclusively through
teams of non-physicians using tele-ROP exclusively managed
through a publiceprivate partnership (PPP) (Fig. 1).
We hope that our experience of 20,214 infant retinal imaging
sessions from 36 rural neonatal intensive care units (NICUs) would
help in further expansion of ROP services using tele-ROP in India
and other middle-income countries with similar demographics. We
also discuss the merits and demerits of a publicly supported private
ROP screening program in India.
2. Methods
2.1. KIDROP outreach team
The KIDROP method of screening has been described before
[5,19,20]. Briey, after initiation in 200 as a stand-alone program by
Narayana Nethralaya Postgraduate Institute of Ophthalmology
(NNPIO), Bangalore, the program was expanded a publiceprivate
partnership under the aegis of the National Rural Health Mission
(NRHM), Ministry of Health and Family Welfare, Government of
Karnataka in 2009. The data in this manuscript are derived exclusively from these PPP centers. The Institution Review Board, the
Research Committee and the Ethics Committee of NNPIO have
approved this program. The data haves been audited and veried
by the Ministry of Health & Family Welfare periodically during the
program.

The regional zones under study for this manuscript comprise


two geographically adjacent but distinct entities, namely the North
Karnataka (NK) and the Central Karnataka (CK) zones (Fig. 2).
Together, they cover a population of ~23 million and an area of
89,000 km2. Training and accreditation was initiated in 2009 in NK
with the eldwork starting in 2011 and 2012 in NK and CK,
respectively. Briey, ophthalmic technicians, optometrists or
ophthalmic assistants are trained in a stepwise manner on a
mannequin, then on babies with support and independently and
adjudged on 20 criteria. The candidates must obtain high scores
(>85%) in their qualifying examinations before they are certied.
The program manager, who has a degree in business administration, health care, public health or program development is trained
in the technique, program implementation, nancial and data
management and counseling skills [5]. Each zone has a complete
team comprising a project manager, a single level III technician
and a driver. An indigenously developed 20-point score (STAT
score) graded the ability of technicians (levels IeIII) to image and
decide follow-up based on a three-way algorithm. Whereas a level
III technician's decisions agreed with 94.3% of those of an ROP
specialist (ophthalmologist), only 0.4% of infants needing treatment
were missed. The grading of technicians and roles of each member
has been described elsewhere [5]. The equipment entrusted to each
team consists of a mini-van (Tempo Traveller, India), a Retcam
Shuttle (Clarity MSI), a portable laser (532 nm green, Nidek in NK
and Iridex in CK) with laser indirect ophthalmoscopy (LIO) delivery,
a laptop with data connectivity, Tele-Care software (i2i Telesolutions, Bangalore, India) and consumables.
2.2. Enrollment
Each team travelled on a xed schedule and covered up to ve
NICUs (maximum) on a single day by visiting one district headquarter daily by weekly rotation. Besides these scheduled centers,
other NICUs were visited on call or babies were brought into one
of the visited centers using the REDROP method [20]. All government district hospitals in each zone were covered. In addition,
private NICUs that agreed to participate and refer babies for ROP
screening without charging the family were offered the service at
no cost. The recurrent costs incurred included travel and

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).

accommodation of the zonal teams and their salaries and were


funded by the NRHM, through NNPIO.

logistic reasons, the infant was transferred to the closest district


hospital where the baby could be lasered or to NNPIO, and the
parents were compensated for the travel expenses.

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.)

indigenously created ROP iPhone app [5]. The submitted report


bears the digital signature of the ROP expert and reaches the
project manager. The turnaround-time cycle has been described
before and is within a few minutes of upload [19]. In all cases the
diagnosis and decision (follow-up/discharge/treat) is communicated to the parent at the end of each session. No parent leaves the
rural center without counseling by the project manager and a
written documentation of the communication on the ROP card.
Registers in the NICU and softcopies of the data are constantly
updated. As far as possible, mothers are shown the retinal images of
their infants during the counseling, thereby promoting their
involvement and better compliance to follow-up. The mobile
numbers of parents are obtained and entered into the software
system for subsequent alerts and reminders. By the end of the
session, the information is shared with the treating neonatal doctors and staff.
All statistical analysis was done using IBM SPSS version 20 and
jmp pro 11 (SAS, Cary, NC, USA). The chi-square test was applied to
analyze the data in the two zones and proportion statistics was
applied to determine the difference between the government and
the private sectors.
3. Results
The period of data analysis of this ongoing program covers the
period of February 14th, 2011 to February 28th, 2015 for NK zone

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

North Zone (initiated Feb 14th, 2011)

Central Zone (initiated Oct 1st, 2012)

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

NICU, neonatal intensive care units.

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%)

APROP, aggressive posterior retinopathy of prematurity.

babies) underwent primary laser. Of these, three babies (six eyes)


were lost to follow-up before complete regression could be documented, one baby progressed to stage 5 ROP in one eye following
treatment, and two babies had unfavorable outcome in both eyes
following laser treatment. Thus, 11 eyes had unfavorable outcomes
and the remaining 497 eyes had favorable structural outcomes
accounting for 97.83%.

3.1. Comparison of experience in government vs private centers


We performed a sub-analysis to compare the distribution and
outcome between the government and private centers. Of the 36
NICUs, 14 (38.9%) were government and the remaining 22 (61.1%)
were private hospitals. There were more visits to the government
centers than the private hospitals (1328 vs 1017). The government
centers always had patients for screening or review and hence were
visited more frequently, which was not the case in private hospitals,
which scheduled appointments for both screenings and reviews.
This also translated to higher new enrollments from the government compared to private centers (4646 vs 2460 respectively,
P < 0.001). A greater proportion of males were screened in private
hospitals compared to the government centers (private, male:female 1.32 vs government, male:female 1.00; P < 0.001). The
smallest birth weights (<1000 g) and the lowest gestational age
(<30 weeks) were screened in the government centers (67.3% and
63.6% respectively, P < 0.001). The incidence of ROP (all stages) was
16.57% (770/4646) in the government compared to 33.38% in the
private centers (P < 0.001). The incidence of treatment requiring
disease of all those screened was also more in the private centers
compared to the government centers (7.11% vs 1.7% respectively,
P < 0.001) and more infants with the disease progressed to treatment requiring ROP in private compared to the government babies
(21.32% vs 10.23% respectively, P < 0.001). The details of this subanalysis are represented in Table 4.
4. Discussion
The World Health Organization's Born too soon report has
shifted the focus of care of premature infants from industrialized
countries to middle-income nations such as India, which currently
leads the order of countries with the highest burden of prematurity
[4]. Unfortunately, ROP screening programs have not been able to
keep up with improving neonatal care practices and remained
grossly inadequate. In India today, there are very few ROP specialists and they only cater to a handful of NICUs in the main cities,
exposing the vast majority of unscreened rural Indian premature
infants to a risk of ROP-related blindness.
Thus far, indirect ophthalmoscopy (IO) has been considered the
gold standard in ROP screening. It assumes competency of the

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

ROP, retinopathy of prematurity.

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

Five Retcam 120 units


installed in ve NICUs

1222

Same day or next day by remote


pediatric ophthalmologist.
Report sent via email

(1) Clinically relevant ROP


(2) Suspected treatmentrequiring (ST)-ROP
(3) Treatment-requiring
(TR)-ROP

Sensitivity for ST-ROP was


100%
Positive predictive value for
TR-ROP was 82.4%

Ells et al.
[30]

2000e2001

Alberta, Canada

One Retcam 120

Senior resident, general


ophthalmologist or pediatric
ophthalmologist.
Ophthalmologists continued
to perform indirect
ophthalmoscopy on site
ROP specialist

ROP specialist who imaged.


Indirect ophthalmoscopy and
Retcam imaging was done on
each baby each time

Referral-warranted (RW)ROP

Weaver and
Murdock
[33]

2007e2011

Montana, USA

One Retcam II in a
single NICU

137

Registered nurse and a


neonatal nurse practitioner

Pediatric ophthalmologists
(retrospective analysis)

RW-ROP

Fijalkowski
et al [34]
SUNDROP

2005 to 2010

Stanford, CA, USA

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

Level III accredited ROP


imaging technicians
travelling between centers

Read remotely on smart phone


by ROP specialist.
During validation indirect
ophthalmoscopy comparison

(1) Any stage ROP


(2) Redeorangeegreen
decision-aiding KIDROP
algorithm

64

Specialist ROP nurse

Nurse imaged, graded and


proposed follow-up which was
compared with an ROP expert

(1) Any stage ROP


(2) RW-ROP

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%)

Two remote, non-physician


readers, who were study
certied.
Every baby had Retcam imaging
along with clinical examination
by study ROP specialist

RW-ROP

Sensitivity 100%, specicity


96%.
Positive predictive value 92%,
negative predictive value
100%
Sensitivity of 100% and a
specicity of 96.3% for
detecting type 1 ROP. The
positive predictive value of
detecting type 1 ROP was
61.5%. The negative
predictive value was 100%
No TW-ROP was missed and
no adverse outcome noted.
TW-ROP had 100% sensitivity,
99.8% specicity, 93.8%
positive predictive value,
100% negative predictive
(1) 94.3% of decisions agree
with ROP expert
(2) Level III technician missed
0.4% of treatment requiring
ROP
(3) The sensitivity, specicity,
positive predictive value and
negative predictive value for
treatment grade disease were
95.7, 93.2, 81.5 and 98.6,
respectively
Agreement of plan in 84.8% of
cases.
Sensitivity, specicity,
positive predictive value, and
negative predictive value of
ROP grading were 91.7%,
80.6%, 45.8% and 98.2%
respectively
Remote grading of images of
an eye at a single session had
sensitivity of 81.9% and
specicity of 90.1%.
When both eyes were
considered for RW-ROP, the
sensitivity was 90.0%,
specicity of 87.0%, negative
predictive value of 97.3%, and
positive predictive value of
62.5%

Vinekar et al. 2008 to date


[5]
KIDROP

44

Shah et al.
[35]

13-month period: ? New Zealand


2012e2013 (dates
not provided)

Two level II NICUs


using a Retcam shuttle
that travelled between
these centers (20 km)

Quinn et al.
[36]
E-ROP

2011 to 2013

Study centers had their 1257


own Retcam and ROP
specialist

12 USA and one


Canada

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.

ROP, retinopathy of prematurity; NICU, neonatal intensive care unit.

Current
report

2011 to date

Rural, multicenter,
India

36 rural NICUs, 600


e800 km radius, two
zones of six districts
each

7106

Two teams with level III


technician and project
manager each travelling
within respective zones

The respective imaging


technicians onsite.
Images viewed and validated
remotely by ROP expert

(1) Any stage ROP


(2) Treatment grade ROP
(3) Decision to discharge
from ROP screening

Technicians validated as per


KIDROP algorithm.
Government vs private
hospital, regional variations
discussed

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

there is a bias towards the male child. Whereas the government


centres show a more even gender ratio distribution, private hospitals show a higher proportion of males enrolled (Table 4,
P < 0001). We have reported this unfortunate trend from a citybased public hospital, and it is likely that parents would preferentially use nancial resources for the treatment of a male child in a
private hospital or because practitioners could be more aggressively managing male infants [20]. (6) Our data show that 20% of
babies who required treatment would have been missed for
screening if the American screening guidelines (1500 g and 30
weeks) [23] had been used. This suggests that middle-income
countries such as India need to develop their own screening
guidelines based on their regional variability and data [10,21].
The program has also provided insights into the feasibility of a
telemedicine program for unscreened rural outreach centers. First,
the mechanism of implementation through a publiceprivate
partnership appears to be a good approach. The advantages are
that a large part of the capital expenditure and running costs are
borne by the government. There is also a better buy-in of the
government health care system into childhood blindness, the
large deserving government hospitals which struggle with inadequate infrastructure and a heavy case load (Fig. 4). The PPP
support could also translate into its integration with the

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.

government insurance schemes making ROP screening more


universally acceptable and accessible. The PPP also provides
increased program visibility and advocacy. The disadvantages of
the PPP in our experience lie in the fact that there are frequent
changes and transfers of the bureaucracy, leading to delays in
program implementation. There is also need to protect intellectual
property especially where there are innovations in program strategies, technology used and ideologies implemented. Several
KIDROP centers that were being offered free ROP screening were
auctioned to third parties as part of the tendering process of the
government. Whereas integration into the government system is
inevitable, the mechanism of such technology and skill transfer
must be documented and executed to safeguard the interests of
the program handlers. Further, delays in implementation and
reimbursement of salaries and running costs place a considerable
nancial burden on the private organization that supports or
manages the program. Further, the program needs increased
participation from ophthalmologists in the government sector. A
special cadre of Team B ophthalmologists was trained at the
initiation of the program, but the involvement has been suboptimal. Finally, the maternal and child health department rather than
the department of ophthalmology should head an ROP program as
it provides wider coverage, better integration into the child health
clinics and better utilization of the resources.
With the Government of India expanding neonatal care through
the backbone of public-hospital-based special newborn care
units (SNCUs), the role of the pediatrician and neonatologist in
ROP screening has become paramount. Strategies must be
enhanced to sensitize and train SNCU nurses on good oxygen
supplementation practices, setting the right alarm, need for pulse
oximetry, judicious use of oxygen during admission and transfer to
another SNCU and strict adherence to the written protocol for inclusion into ROP screening. The involvement of the obstetrician in
ROP management must also be strengthened through awareness
and training including avoiding multifecundity, use of antenatal
steroids, impressing the parents about the dangers of prematurity
including ROP and communicating the same with the treating
neonatologist (Fig. 5) Through the KIDROP program we have
attempted nurse sensitization in all centers where screening is
performed and have attempted collaboration with the treating

obstetric units and public health departments where available, to


promote healthy newborn care practices including immunization,
kangaroo mother care, and breastfeeding. This is performed while
the mothers are waiting with their infants during dilatation, as
they are more receptive to such advice from the health care
practitioners (Fig. 6).
The limitations of the study lie in the fact that the denominator
of the total number of at-risk babies from each hospital are not
ascertained. This is largely due to the fact that registers are not
maintained in most hospitals in these outreach zones. Our teams
have attempted to collect data from the labor ward/birth register to
determine the total number of at-risk babies at each visit. Second,
neonatal and maternal risk factors are not reliably documented in
the inpatient or discharge summary, making it difcult to determine the risk factor analysis in the study cohort.
In conclusion, ROP screening in the rural outreach is possible
with a telemedicine program that is managed by non-physicians
provided they are accredited, monitored and accountable at all
levels of care. The debate about utilizing trained non-physicians or
technicians in this important task and their ability to diagnose ROP
correctly is relevant, but must be viewed in light of the fact that
these rural infants have no screening mechanism in the absence of
the current strategy. In the USA, 86e100% [38,39] of malpractice
claims in ROP were due to screening failure and follow-up at the
center and in the community [40]. More recently, the E-ROP study
in North America supported the validity of remote evaluation by
non-physicians to read referral-warranted ROP, but the delay in the
reports which they found would make it difcult in a program
which KIDROP which relies solely on this strategy [36].
The ideal strategy for middle-income nations would be the use
of low-cost wide-eld infant retinal cameras which can be used
onsite by the resident nursing or medical staff, a cloud-based image
reservoir which can be accessed and reported by ROP experts, and a
prompt referral system to treat those infants whose disease progresses. Only a paradigm shift in the way we currently manage ROP
can prevent blindness in the millions of premature infants born
worldwide. Strategies to integrate ROP into universal screening are
already being piloted in India [41]. A greater awareness and training
among pediatricians, obstetricians, ophthalmologists, nurses and
parents is required to tackle this burden of ROP blindness.

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.

Conict of interest statement


None declared.
Funding sources
The rural outreach component of KIDROP is supported through a
public-private partnership between the The National Rural Health
Mission, Government of India and Government of Karnataka with
Narayana Nethralaya Postgraduate Institute of Ophthalmology,
Bangalore, India.
Acknowledgements
We acknowledge the following for their support in this program: North Karnataka team: Dr Siddesh Kumar, Mr Muralidhar

Gayakwad, Mr Ravishankar Kandagal, Mr Sudendra Babu; Central


Zone team: Dr Prakash Suranagi, Mr Madhava Prasad Padaki, Mr
Someshwara Matad, Mr Manjunatha Kalleshappa; KIDROP's headquarter team: Mr Praveen Sharma, Mr Sivakumar Munusamy, Mr
Krishnan Narasimha, Mr Srinivas Gowda.
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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

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