Acta Ophthalmologica 2010
Stanford University Network for Diagnosis of Retinopathy of Prematurity (SUNDROP): 24-month experience with telemedicine screening Yohko Murakami, Ruwan A. Silva, Atul Jain, Eleonora M. Lad, Jarel Gandhi and Darius M. Moshfeghi Department of Ophthalmology, Stanford University, California, USA
ABSTRACT. Purpose: To report the 24-month experience of the Stanford University Network for Diagnosis of Retinopathy of Prematurity (SUNDROP) telemedicine initiative. Methods: Retrospective analysis of the SUNDROP archival data gathered between 1 December 2005 and 30 November 2007 to evaluate this diagnostic technology for ROP screening. One hundred and sixty consecutively enrolled infants meeting ROP examination criteria were screened with the RetCam II and evaluated by the SUNDROP reading centre at Stanford University. Nurses obtained five or six images in each eye. All patients also received a dilated examination within 1 week of discharge. Outcomes included treatmentwarranted retinopathy of prematurity (TW-ROP) and anatomical outcomes. Results: In the initial 24-month period, the SUNDROP telemedicine initiative has not missed any TW-ROP. A total of 160 infants (320 eyes) were imaged, resulting in 669 exams and 7556 images. Seven infants were identified with TW-ROP; six underwent laser photocoagulation and one regressed spontaneously. The sensitivity was 100%, with specificity of 99.4%. No patient progressed to retinal detachment or other adverse outcomes. Conclusion: The SUNDROP telemedicine screening initiative for ROP has been proven to have a high degree of sensitivity and specificity for the identification of treatment-warranted disease. All cases of treatment-warranted disease were captured. There were no adverse outcomes. Key words: retinopathy of prematurity – retrospective study – ROP – telemedicine
Acta Ophthalmol. 2010: 88: 317–322 ª 2009 The Authors Journal compilation ª 2009 Acta Ophthalmol
doi: 10.1111/j.1755-3768.2009.01715.x
Introduction Retinopathy of prematurity (ROP) is a leading cause of childhood blindness in the USA and is characterized by
abnormal vasoproliferation in the premature infant retina (Committee for the Classification of Retinopathy of Prematurity 1984). Early detection through regular screening exams and
prompt treatment when indicated are critical in decreasing severe vision loss, retinal detachment and other adverse outcomes (Early Treatment for Retinopathy of Prematurity Cooperative Group 2003). The traditional standard for the diagnosis of ROP is binocular indirect ophthalmoscopy (BIO) with scleral depression by an experienced ophthalmologist (Committee for the Classification of Retinopathy of Prematurity 1984; American Academy of Pediatrics 1997, 2001, 2006). Recent revisions to the screening guidelines for ROP issued by a joint statement between the American Academy of Ophthalmology, the American Association for Pediatric Ophthalmology and Strabismus and the American Academy of Pediatrics effectively increased the number of infants to be screened by 33% by broadening the patient population for which screening is indicated (American Academy of Pediatrics 1997, 2001, 2006). This coincides with both an increasing incidence of premature births (Martin et al. 2006) and a projected decline in the number of paediatric ophthalmologists (Good 2007), which would exacerbate the already large mismatch in supply and demand for ROP screening. The time-consuming, poorly compensated ROP screening exams coupled with the high rates of medico-legal suits relating to ROP cases represent further obstacles in
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increasing the number of qualified specialists who willingly screen for ROP (American Academy of Ophthalmology 2006). Telemedicine has been cited as a potential solution to this dilemma (Grigsby & Sanders 1998; Bashshur et al. 2000; Good & Gendron 2007); it utilizes remote clinicians more efficiently in screening for ROP through the use of wide-angle fundus photographs. Previous studies have demonstrated the effectiveness and accuracy of wide-angle photography in diagnosing various stages of ROP compared with the gold-standard dilated BIO exam (Schwartz et al. 2000; Yen et al. 2002; Ells et al. 2003; Chiang et al. 2005, 2006a, 2006b, 2007a, 2007b; Balasubramanian et al. 2006; Wallace et al. 2007a, 2008; Ells et al. 2008; Lajoie et al. 2008). In the last decade, the specificity and sensitivity of telemedicine in diagnosing ROP has increased steadily because of advances in imaging technology, the increasing expertise of the nurses trained to take the photographs and better performance of remote interpreters (Schwartz et al. 2000; Yen et al. 2002; Ells et al. 2003, 2008; Chiang et al. 2005, 2006a, 2006b, 2007a, 2007b; Balasubramanian et al. 2006; Wallace et al. 2007a; Lajoie et al. 2008). In order to truly assess the value of telemedicine as an ROP screening regimen, an evaluation of its effectiveness without the use of a simultaneous bedside examination is warranted. While one study examined the accuracy of telemedicine in evaluating plus disease without a clinical assessment (Wallace et al. 2007a, 2007b, 2007c), no study to date has examined the ability of telemedicine to diagnose various clinical stages of ROP without a simultaneous bedside exam – as is the final intent of the technology. The Stanford University Network for Diagnosis of Retinopathy of Prematurity (SUNDROP) was created with the goal of providing quaternary ROP screening services to the larger San Francisco Bay Area community. All infants in this network were evaluated remotely via digital images collected by the RetCam II (Clarity Medical Systems, Pleasanton, California, USA) without a simultaneous indirect ophthalmological examina-
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tion unless this was eventually indicated by photographic findings. The purpose of this study is to report and evaluate the first 24 months of data from the SUNDROP telemedicine initiative.
Materials and Methods This retrospective analysis was approved by the Institutional Review Board of the Stanford University School of Medicine. All infants at four different Neonatal Intensive Care Units (NICUs) who met published ROP screening criteria (American Academy of Pediatrics 2006) were screened using the SUNDROP protocol between 1 December 2005 and 30 November 2007. NICU nurse training
All wide-angle images were obtained by a trained team of NICU nurses using the RetCam II (Clarity Medical Systems, Pleasanton, CA, USA). The team consisted of two or three nurses, one in charge of obtaining the digital imaging per protocol while the remainder positioned the infant and monitored vital signs throughout the exam. Clarity Medical Systems provided initial training in the use of the RetCam II with a certified ophthalmic photographer, using both mannequins and live infants. The nurses were observed and critiqued on technique. Following a single training session, the nurses obtained photographs on their own, under orders from the supervising physician (D.M.M.). No nurse had received previous training in any area of ophthalmic photography. Subsequent training was provided as needed by both the certified ophthalmic photographer and the physician (D.M.M.). Photography protocol
Patients were dilated with 2.5% phenylephrine and 1% tropicamide 30–60 min prior to examination. Feedings were discontinued 2 hr preand post-examination, in accordance with aspiration precaution guidelines. Cardiac rate and oxygen saturation were monitored closely to prevent bradycardia and apnea throughout the exam. If signs of either condition were present, the examination was
halted until the infant was deemed stable to continue. A topical anaesthetic (0.5% proparacaine) was administered in each eye before examination. A sterile lid speculum was used to open the eye and provide adequate exposure for photography. 2.5% hydroxypropyl methylcellulose was used to couple the digital camera lens to the infant’s cornea. Digital images were taken by a trained NICU nurse and stored on the RetCam II hard drive. The goal was to obtain five clearly focused fundus images in each eye using the 130 C lens: (i) optic nerve centred; (ii) optic nerve superior; (iii) optic nerve inferior; (iv) optic nerve nasal; and (v) optic nerve temporal. Images were captured as necessary until they were deemed to be of adequate quality for examination. An iris shot in each eye was added later during the first year, in accordance with new screening recommendations published that year (to assess pupillary dilatation and iris vascular engorgement as signs of plus disease) (Committee for the Classification of Retinopathy of Prematurity 2005). In cases of inadequate exposure, artifact, poor visualization of the periphery or lack of a complete standardized image set, a repeat telemedicine evaluation was performed within 48 hr. The frequency of imaging sessions was as per the joint-statement recommendations for ROP screening (American Academy of Pediatrics 2006) with imaging substituted for bedside indirect ophthalmoscopy (i.e. zone II, stage 2 ROP without plus disease would receive a weekly imaging session) (American Academy of Pediatrics 2006). An exception to this occurred when telemedicine identified treatmentwarranted ROP (TW-ROP); in this case, the infant was followed (as per the joint statement’s recommended schedule) with BIO instead of fundus imaging. Image transfer
The images were transmitted to the remote expert reader (by D.M.M.) in one of two ways: via secure email after the images were uploaded to a flash drive and transferred to a computer; or via courier on a DVD. Demographic data were sent via fax to the reader and subsequently archived.
Acta Ophthalmologica 2010
Outcomes
Outcomes included TW-ROP and anatomical outcomes such as vision loss and retinal detachment. TW-ROP criteria were based on the Early Treatment Retinopathy of Prematurity (ETROP) study recommendations for peripheral retinal ablation for any eye with type 2 disease or greater, threshold disease, any plus disease and any stage 4 or higher disease (Committee for the Classification of Retinopathy of Prematurity 1984; Flynn 1985; Early Treatment for Retinopathy of Prematurity Cooperative Group 2003). A diagnosis of TW-ROP by SUNDROP initiated a subsequent mandatory bedside examination by the physician (D.M.M.). All treatment decisions were based on the indirect ophthalmoscopic exam findings. TWROP represents only those cases that required treatment after both a SUNDROP TW-ROP diagnosis and a bedside exam by the physician. Patients whose disease regressed spontaneously were not classified as TW-ROP. All patients received a mandatory bedside exam within 1 week of discharge from the NICU by one paediatric retina specialist (D.M.M.). Patients were no longer screened by the SUNDROP protocol if they received laser, incisional surgery or were discharged. Statistical analysis
All data were analysed using statistical software (microsoft excel; Microsoft, Seattle, Washington, USA). Sensitivity, specificity, positive predictive values (PPVs) and negative predictive values (NPVs) were calculated and used to assess the usefulness of the RetCam II photographic readings.
Results In its initial 24-month period, SUNDROP has not missed any cases of TW-ROP. Enrolment began on 1
December 2005 and was completed on 30 November 2007. A total of 160 infants (320 eyes) were imaged, resulting in 669 exams and 7556 unique images. The average number of images per patient imaging session was 11.6, and the median number of images per patient imaging session was 12 (range 2–32 images). The mean birth weight of the infants examined was 1225.6 g and the mean gestational age at birth was 28.9 weeks. Refer to Table 1 for baseline characteristics. Seven infants were diagnosed with TW-ROP by telemedical evaluation. Each of these infants was then examined at the bedside using BIO with scleral depression to confirm the disease state. Of these infants, six were identified with TW-ROP that prompted laser photocoagulation, after which every infant exhibited complete disease regression. Of these six TW-ROP cases, four had pathology in zone I (one with stage 3 ⁄ pre-plus disease, three with stage 2 disease). The remaining two TW-ROP cases had zone II, stage 2 ROP with pre-plus disease. The final infant thought to have TW-ROP by telemedical evaluation was not deemed to have TW-ROP by BIO and regressed spontaneously. At no point in the study did any patient experience severe vision loss or progress to retinal detachment, retrolental mass, macular fold or other adverse anatomical outcomes. Repeat RetCam II evaluations were performed within 48 hr in instances of inadequate exposure, artifact, poor visualization of the periphery or lack of a complete standardized image set. All disease requiring treatment was successfully identified with the SUNDROP protocol, with confirmatory BIO within 1 week of discharge corroborating this in all cases. As per the joint-statement protocols, infants not identified as having TW-ROP were maintained in SUNDROP with scheduled fundus evaluation until they
Table 1. Demographic data. Characteristics
Total
Average per patient (range)
Number of patients (eyes) Number of exams Number of images Birth weight Estimated gestational age
160 (320) 669 7556
N⁄A 4.2 11.6 1225.6 28.9
(1–22) (2–32) g (523–2941 g) weeks (20–37 weeks)
Table 2. RetCam II and clinical examination findings. Clinical findings
examination
RetCam II findings Positive Negative Total Positive 6 Negative 0 Total examinations 6
1 153 154
7 153 160
reached a postmenstrual age (PMA) of 45 weeks, maintaining a stable clinical course, and until complete regression of any degree of actualized ROP as determined by binocular indirect ophthalmoscopy. Digital photography using the RetCam II system, assessed remotely by an experienced retina specialist, was successful in identifying all cases of TW-ROP. Compared to BIO, SUNDROP has a sensitivity of 100% and a specificity of 99.4% in detecting TW-ROP. The PPV of SUNDROP was 85.7% and the NPV was 100%. Refer to Table 2 for clinical RetCam II findings.
Discussion The 24-month evaluation of the SUNDROP telemedicine initiative shows excellent sensitivity (100%) and specificity (99.4%). These results are superior to our previously reported results at 12 and 18 months (Murakami et al. 2008; Silva et al. 2009). Sensitivity has remained high at 100% and specificity has continued to increase, from 95% at 12 months to 98.9% at 18 months and 99.4% at the 24-month evaluation. Most importantly, the NPV of SUNDROP telemedicine screening has remained at 100% across the three evaluation time-points, while the PPV has increased from 50% at 12 months to 85.7% at 18 months and has since remained stable. The rise in PPV appears to be a result of the near quadrupling of enrolment into SUNDROP between the first and second year of analysis with a consequent increase in the absolute number of actual TW-ROP cases within the study. Thus, the initially low PPV at 12 months probably reflects a statistical artifact from low enrolment in year one of SUNDROP. The current study’s design is something of a departure from prior studies (Schwartz et al. 2000; Yen et al.
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2000, 2002; Roth et al. 2001; Ells et al. 2003; Sommer et al. 2003; Chiang et al. 2006a, 2006b, 2007a, 2007b; Shah et al. 2006; Wu et al. 2006), which have evaluated telemedicine through comparison of fundus photographs obtained at the time of a corresponding BIO. Our intended omission of parallel BIOs for every imaging session in SUNDROP was specifically designed to better approximate telemedicine’s projected future use. In this sense the SUNDROP initiative’s design was primarily to identify all infants requiring treatment, which is distinct from evaluating telemedicine’s ability to identify any stage of ROP. The former definition adheres more strictly to the essence of a screening test, namely its rudimentary purpose of identifying disease that lies above a critical ‘action’ threshold necessitating treatment (Frankenburg 1974). According to this definition, the SUNDROP screening network continues to demonstrate excellent efficacy as an ROP screening tool at its 24-month evaluation. Of particular importance is the high sensitivity and NPV observed at 2 years, as verified by BIO exams given to all non-treated ROP infants at the time of discharge. In this way false negatives, in terms of ROP requiring intervention, would have been identified by what is now considered the gold standard for ROP screening. To date, no cases of ROP (at any stage) appear to have been missed by telemedicine in the SUNDROP initiative although, again, we cannot exclude the possibility that some forms of ROP have regressed spontaneously in the absence of treatment before the infant’s discharge exam. However, in this hypothetical instance such disease, by definition, did not require treatment. Our results demonstrate continued progress in ROP screening using telemedicine when placed in the context of the numerous prior studies. Early reports by Yen et al. (2000, 2002) reported ‘insufficient’ sensitivity (46– 76%) but good specificity (95–100%) in the images’ ability to capture disease. Improved image quality with regard to addressing inadequate exposure, artifact and poor peripheral fundus visualization improved sensitivity to 82.4%, with specificity observed to be 93.8% by Roth et al. (2001); mean-
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while, Ells et al. (2003) reported 100% sensitivity and 96% specificity of telemedicine for detecting referral-warranted ROP (RW-ROP). Studies by Wu et al. (2006) and Sommer et al. (2003) note an NPV of 100%, which demonstrates that every infant with disease was successfully identified by the digital images. Related studies by Chiang et al. (2006a, 2006b) demonstrated similarly high accuracy of remote diagnosis by expert screeners, with an inter-rater reliability (j) of 0.743 between screeners when stratifying for the type of ROP. The Photographic Screening for Retinopathy of Prematurity (PHOTO-ROP) Study is the first prospective, multicentre evaluation of telemedicine screening comparing it with the reference standard of onsite indirect ophthlamoscopic diagnosis to date; it reports an ‘excellent’ diagnostic sensitivity for referralwarranted disease, as defined by ETROP guidelines (Balasubramanian et al. 2006; Ells et al. 2008). Most recently, a German multicentre clinical study, again comparing fundus image interpretation with BIO, reported the image interpretation to be 100% sensitive in detecting ROP requiring treatment with a PPV of 88.2% (Lorenz et al. 2009). The study screened 1222 premature infants in five east Bavarian NICUs and identified 28 cases requiring treatment. Although encouraging, several caveats confound interpretation of the results such as the study’s external validity (babies were screened using arguably less stringent German screening guidelines such as gestational age < 32 weeks), its use of ophthalmologists to perform the imaging and using the same unblinded ophthalmologist to perform image interpretation after screening using BIO in a large percentage of infants. Commentary is also warranted regarding a recent review that concluded that there is ‘insufficient data to recommend that retinal imaging be adopted by NICUs’ (Kemper et al. 2008), based largely on claims that ‘retinal imaging would almost surely miss some cases of sight-threatening ROP’ (Kemper et al. 2008). This conclusion apparently stems from the authors’ review of selected ROP literature, with the low sensitivities noted by Yen et al. (2000, 2002), Roth et al. (2001), Chiang et al. (2005, 2006a,
2006b) and the PHOTO-ROP trial being perhaps the most influential (Fauchere et al. 2008). However, the authors failed to account for several relevant caveats of these studies when arriving at their conclusion. Firstly, although the review authors maintained that only original articles evaluating sensitivity for detecting RW-ROP were included in the review, they included reports by Yen et al. (2000, 2002) and Roth et al. (2001) that specifically cited sensitivities for detecting any stage of ROP. This is significant primarily because in both of these studies, every case where ROP was not identified by telemedicine evaluation had disease present only in peripheral zone 2 or zone 3 (either stage 1 or stage 2 disease) and the pathology regressed spontaneously in all cases. Regarding their analysis of data reported by Chiang et al. (2005, 2006a, 2006b), the review authors failed to note that the low sensitivities observed in these studies (relative to comparative studies) may have arisen from the stated inexperience of the telemedicine evaluators in terms of both reviewing RetCam images and ROP in general. This may explain the much-improved screening sensitivity of telemedicine Chiang et al. (2007a, 2007b) noted in a follow-up study that they performed. In this study, the sensitivity of telemedicine screening by three retinal specialists with extensive RetCam experience for the detection of mild or worse ROP, prethreshold or worse ROP and TW-ROP (at 36 ± 1 weeks PMA) was 92.9%, 100% and 100% (Chiang et al. 2007a, 2007b) – a remarkably high rate by any screening standard. Although the review authors also comment on the PHOTO-ROP trial’s sensitivity of 92%, no analysis from this study is yet available regarding the stage or location of ROP missed or whether these cases regressed spontaneously (Fauchere et al. 2008). The two other studies reviewed both report a sensitivity of 100% for detecting RW-ROP (Ells et al. 2003; Wu et al. 2006). The sum total of these salient details adds considerable weight against the review article’s assertion that telemedicine would prove unreliable in identifying sight-threatening ROP. In the present study, a sensitivity of 100% and a specificity of 99.4% designate the SUNDROP telemedicine
Acta Ophthalmologica 2010
network a near perfect screening method by screening standards not limited to ophthalmology (Akobeng 2007a, 2007b, 2007c). These predictive values exceed those reported for widely accepted screening methods in other fields, such as mammography for breast cancer and remote stethoscopy in the detection of paediatric heart disease (Belmont et al. 1995; Sable 2002; Finley et al. 2006; Taplin et al. 2008). For example, meta-analysis of mammography screening shows a sensitivity of 79.6% and mean specificity of 90.2% in detecting breast cancer (Taplin et al. 2008). In paediatric cardiology, a sensitivity of 87–94% and an NPV of 75% are deemed acceptable for the use of remote stethoscopy (Belmont et al. 1995; Sable 2002; Finley et al. 2006). Despite these lower predictive values, both mammograms and remote stethoscopy are accepted as standards of care within their fields (Belmont et al. 1995; Sable 2002; Finley et al. 2006; Armstrong et al. 2007; Qaseem et al. 2007). Another notable discussion regards the accuracy of ROP screening’s reference standard. Several studies have reported that remote interpretation of digital images diagnoses stages of ROP earlier than physicians at the bedside (Ells et al. 2003, 2008; Balasubramanian et al. 2006). While all telemedicine studies to date have been designed to compare their results against this reference standard (Schwartz et al. 2000; Yen et al. 2000, 2002; Roth et al. 2001; Ells et al. 2003; Sommer et al. 2003; Chiang et al. 2007b; Shah et al. 2006; Wu et al. 2006), digital image-based examinations may not be inherently less accurate than ophthalmoscopy (Lajoie et al. 2008; Scott et al. 2008). Additionally, inter-rater reliability between ophthalmoscopic and telemedicine-based evaluations show that the latter may be more accurate in some cases (Scott et al. 2008). Although a comparison of these modalities is useful, it is important to note that SUNDROP was designed to employ telemedicine not as a replacement for bedside examinations, but rather as their supplement. In this way the process of ROP screening can be streamlined so that the more time-intensive and financially burdensome BIO exam can be reserved for higher-risk infants.
Previous findings that digital imagebased readings provided treatment recommendations up to 2 weeks earlier than BIO exams have been attributed to a lack of time strain experienced by physicians using telemedicine to screen for ROP (Good 2007; Wallace et al. 2007a). In other words, traditional paediatric ROP screening involves physicians aiming to minimize stress for the infants and often results in brief, rushed BIO exams (Javitt et al. 1993). Telemedicine circumvents this dilemma by providing flexibility to NICU personnel in imaging the fundus of these sometimes unstable patients when it is least physiologically risky for them. Furthermore, because traditional exam results are recorded with a manual sketch of the infant’s fundus, objectivity in reviewing prior exam results to trace disease progression is likely to be compromised. In this regard, the digital images procured for telemedicine offer a distinct advantage over indirect ophthalmoscopic exams given the permanent, objective record of the eye that they provide. Although not a primary motivation for telemedicine’s implementation, the benefit of procuring such data with regard to medicolegal disputes is considerable (Good 2007). The implementation of telemedicine as a primary screening tool for ROP carries several other benefits. Most pressing is its aforementioned ability to address the widening margin between the population eligible for ROP screening and the number of willing screeners (Martin et al. 2006; American Academy of Ophthalmology 2006). A corollary to this is that community hospital NICU patients, many of whom would not otherwise have access to regular ophthalmological screening, could effectively have access to quaternary care. This, in effect, would preclude the need for unnecessary and sometimes risky patient transport with an attendant improvement in cost-effectiveness for all involved parties (Jackson et al. 2008). Furthermore, studies have shown RetCam imaging to provide modest health benefits for infants over traditional BIO, because the imaging sessions involve less physiological stress for them than the typical fundoscopic exam (Laws et al. 1996; Wright et al. 1998). From a broader perspective,
obtaining photodocumentation of ROP retinas has already proven useful in documenting previously unknown responses to therapy (Vinekar et al. 2008) as well as providing insight into examiner variability in disease staging (Chiang et al. 2006a, 2006b, 2007a, 2007b). This 24-month interval evaluation of the SUNDROP telemedicine network demonstrates the continued feasibility and efficacy of using telemedicine in ROP screening without employing a simultaneous bedside exam. The results show excellent sensitivity in detecting TW- ROP using wide-angle digital photography obtained by a trained nurse, with remote interpretation by an experienced specialist. The lack of an accompanying indirect ophthalmoscopic exam (except at discharge) in this report allows a closer simulation of future telemedicine use in the field as a sole screening tool, while simultaneously enhancing sensitivity – a remote screener was perhaps more likely to refer a case knowing that there would be no accompanying bedside BIO exam. The results of this article are intended to help evaluate and integrate telemedicine as a regular screening methodology for premature infants at risk of developing ROP, and to improve the quality, accessibility, delivery and cost of ROP care.
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Received on February 23rd, 2009. Accepted on July 14th, 2009. Correspondence: Darius M. Moshfeghi Stanford University 1225 Crane Street Suite 202 Menlo Park California 94025 USA Tel: + 1 650 323 0231 Fax: + 1 650 323 0237 Email:
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