Graefes Arch Clin Exp Ophthalmol (2008) 246:135–141 DOI 10.1007/s00417-007-0608-3
PEDIATRICS
The Brückner test: extended distance improves sensitivity for ametropia Michael Gräf & Annette Jung
Received: 19 March 2007 / Revised: 8 May 2007 / Accepted: 8 May 2007 / Published online: 30 June 2007 # Springer-Verlag 2007
Abstract Background The Brückner test is usually performed at a distance of 1 m. Due to optical reasons, the test should detect ametropia more sensitively at an extended distance. We compared the sensitivity of the test to detect unilateral ametropia at a distance of 4 m versus the traditional distance of 1 m. Patients and methods In this study, five blinded experienced observers (experts) performed the Brückner transillumination test on five emmetropic subjects (age 22.3 +/− 2.3 years) at a distance of 1 m which was then extended up to 4 m. Unilateral ametropia was simulated by both spherical and cylindrical lenses of −1, −2, −3, −4, and +1, +2, +3, +4 diopters in front of one eye and a plano lens in front of the other eye in a randomised order. Controls with plano lenses in front of both eyes were interspersed. The test was considered positive in case of any difference between the red reflexes of both eyes. For spherical ametropia, the procedure was repeated with 25 medical students who examined one subject each. Results At a distance of 1 m, unilateral myopia/hypermetropia of more than 1 diopter was detected in 78.7%/71.3% by experts and in 34.7%/53.3% by students. At 4 m, detection rates increased to 99.3%/96.0% and 98.7%/100% respectively. Rates of false positive findings for experts vs students were 3.1% vs 1.5% at 1 m and 4.0% vs 3.0% at M. Gräf (*) Department of Ophthalmology, University of Giessen, Friedrichstr. 18, 35385 Giessen, Germany e-mail:
[email protected] A. Jung Department of Ophthalmology, University of Giessen, Friedrichstr. 18, 35392 Giessen, Germany
4 m. For unilateral astigmatism, experts’ detection rates were similar at 1 m (64.7%/70.0%) and lower at 4 m (91.7%/90.3%), depending on the astigmatism axis. Conclusions The sensitivity of the Brückner reflex for anisometropia improves by extension of the examination distance, especially in the hands of less experienced observers. To detect ametropia more sensitively, a test distance of 4 m is recommended. Keywords Amblyopia . Anisometropia . Brückner test . Vision screening
Introduction Amblyopia is estimated to affect approximately 2–5% of the population in western countries, and is a significant preventable cause of vision loss in children and adults [1–4]. Amblyogenic risk factors include ptosis, media opacity, strabismus, and refractive error. When these risk factors are detected at an early age, amblyopia can be prevented or minimized more effectively [4–6]. One significant limiting factor of most amblyopia screening programs is the reliance on the subjective responses of the child being tested [7]. Early detection of amblyopia and amblyogenic risk factors requires objective methods which are independent of any verbal response of the child. The Brückner reflex is a readily available screening tool that can be used with newborns, infants and preverbal children by non-ophthalmologists [8, 9]. The test allows sensitive detection of media opacity [8–10]. Strabismus and refractive error can be detected by an abnormal red reflex, although with a much lower sensitivity [8, 9, 11]. The test is performed with a direct ophthalmoscope. Looking through the ophthalmoscope, the examiner can see the
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patient’s pupil shining red, caused by the light reflected by the fundus of the eye. Provided there is central fixation, the red reflex represents the patient’s foveola, whereas in children 8 months of age and older usually a characteristic dimming of the fundus reflex occurs compared to parafoveolar regions [8, 9]. Traditionally, the Brückner reflex is described to be performed at a distance of 1 m or less by simultaneously illuminating both eyes of a patient, and comparing the colour and brightness of the pupillary red reflexes for symmetry [4, 8–14]. Red reflexes have to be symmetric in both eyes. Any asymmetry in the brightness and colour of the red reflexes is strongly predictive of amblyogenic risk factors including ametropia, strabismus, media opacity, or chorioretinal disease [8–11]. Considering optical basics, the examination distance must be an essential factor influencing the Brückner reflex in case of refractive error. Weakness of the red reflex caused by myopia or hypermetropia which is not compensated by accommodation should become more striking at a greater test distance from the eye or from the far point of the eye respectively, because of the divergent optical path of the reflected light, and in particular the perceived reflex disparity between eyes that are anisometropic should increase with increasing test distance (Fig. 1). In this study, the sensitivity of the Brückner reflex to detect unilateral spherical and astigmatic refractive error was examined with regard to the test distance. Given that the Brückner reflex is primarily used by non-ophthalmologists as a tool to detect ametropia, the test results of experienced observers and medical students were compared.
Fig. 1 Simplified optical path of the Brückner reflex. An emmetropic eye focuses the reflected light to a parallel bundle. In hypermetropia (accommodation relaxed) and myopia, the reflected light is not parallel. Extending the distance, the part of light reaching the examiner’s pupil becomes progressively smaller and the red reflex is reduced
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Methods In a single blinded study, we tested the ability of five experienced observers out of the ophthalmologic personnel of our department (experts) to find red reflex asymmetry in five test subjects with spherical ametropia at a distance of 1 m, which was then extended to 4 m. Informed consent was obtained for all participants of the study which adhered to the tenets of the Declaration of Helsinki. The subjects were 22.3 +/− 2.3 years old and emmetropic (spherical equivalent 0.37 D +/− 0.37 D). Exclusion criteria were hypermetropia >1.0 diopter, astigmatism or anisometropia >0.5 diopter, myopia, strabismus, and any organic eye disease. Unilateral spherical hypermetropia was simulated by a lens of − 1, −2, −3, and −4 diopters in front of the subject’s one eye and a plano lens in front of the other eye. To create an arbitrary order of test conditions, the protocol writer mixed the lenses on a table beside the subject and then placed one lens after the other, each together with the plano lens, in front of the right and the left eye of the subject. Within this pseudorandomised sequence of test conditions, each condition (e.g., anisometropia of 2 diopters) was at any time repeated with the opposite position of the lenses, and the sequence of the in-total eight anisometropic and additional four interspersed control conditions with a plano lens in front of both eyes was unpredictable for the observers. The same procedure was repeated using lenses of +1, +2, +3, and +4 diopters to simulate unilateral myopia. In a second setting, unilateral astigmatism was induced. Hypermetropic astigmatism with the rule was simulated by cylindrical lenses of −1, −2, −3, −4 diopters (axis 90°). Four control conditions with plano lenses in front of both eyes were interspersed. Hypermetropic astigmatism against the rule was simulated by cylindrical lenses of −1, −2, −3, −4 diopters (axis 0°). Myopic astigmatism both with and against the rule was simulated using cylindrical lenses of +1, +2, +3 und +4 diopters (axis 0° and 90° resp.). The lenses were slightly tilted, if necessary, to avoid a disturbing reflex from the surface of the lens. The test was performed at a low room illumination (100-150 Lx) with a direct ophthalmoscope (Beta 200, Heine Optotechnik, 82211 Herrsching, Germany) held vertically. The subjects were instructed to fixate the light of the ophthalmoscope. The observers had to decide whether (test positive) or not (test negative) an inter-ocular difference of the Brückner reflex was visible through the ophthalmoscope at a distance of 1 m and/or at a distance of 4 m. For comparison with non-experienced observers, 25 medical students were trained in a single session how to perform the test. After the training phase, they had to examine one emmetropic subject each, in whom unilateral myopia was simulated with a plano lens in front of one eye and a spherical lens of +1, +2, +3, +4 diopters in front of the
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other eye, in an unpredictable order of the lens power and the side of the emmetropic eye. Four control conditions with plano lenses in front of both eyes were interspersed. The same procedure was repeated with induced unilateral hypermetropia using spherical lenses of −1, −2, −3, and −4 diopters. In a pilot study, the test was applied to 55 consecutive orthotropic outpatients, irrespective of age, because the aim of this study was just to compare test sensitivities at two distances. In this comparison, both red reflex asymmetry and also symmetric weakness of the red reflex were considered pathologic. Test results were compared with the refraction in cycloplegia. Statistics For each simulated anisometropia situation, test sensitivity was calculated as the ratio of correct positive findings and the total number of tests (experts, n=50; students, n=25) for ametropia, separately for 1 m and 4 m test distance. Test specificity was calculated separately for 1 m and 4 m distance as the ratio of correct negative findings and the total number of control conditions (experts, n = 200; students, n=200, at each distance). Confidence intervals of sensitivity and specificity for each ametropia situation were calculated by the formula of Hald [15]. Results The decision of the observers usually did not take longer than 3 seconds for one distance. Figure 2 shows an example of findings with simulated anisometropia of different degrees at a distance of 4 m. Unilateral spherical ametropia Experts detected unilateral myopia of 1, 2, 3, and 4 diopters in 60%, 80%, 74% and 82% of 50 tests at 1 m, and in 100%, 100%, 98%, and 100% of 50 tests at 4 m. Percentages and confidence intervals are given in Table 1. Of the cases detected, the myopic eye yielded the weaker red reflex in 117 of 148 tests (79.1%) at 1 m, and in 195 of 199 tests (98.0%) at 4 m. This means that at the greater distance the myopic eye could be detected more reliably by the weaker red reflex. Unilateral hypermetropia of 1, 2, 3, and 4 diopters was detected in 34%, 58%, 76%, and 80% of 50 tests at 1 m and in 52%, 94%, 96%, and 98% of 50 tests at 4 m. The weaker red reflex corresponded to the hypermetropic eye in 76.6% at 1 m and in 90.0% at 4 m. This means that also in unilateral hypermetropia and in anisohypermetropia the more ametropic eye can be more reliably identified at the extended distance. Out of 225 controls, 3.1% were false positive at 1 m and 4.0% at 4 m distance. Students detected unilateral myopia of 1, 2, 3, and 4 diopters in 32%, 28%, 40% and 36% of 25 tests at 1 m, and
Fig. 2 Emmetropia of both eyes (a) and simulated hypermetropia of the left eye (anisometropia) of 1 diopter (b), 2 diopters (c), 3 diopters (d), and 4 diopters (e) at 4 m distance. For comparison, simulated myopia of the left eye of 1 diopter (f)
in 68%, 100%, 100%, and 100% of 25 tests at 4 m. While they detected unilateral hypermetropia of 1, 2, 3, and 4 diopters in not more than 8%, 40%, 56%, and 64% at 1 m, they recognized it in 60%, 100%, 100%, and 100% at 4 m (Table 1). False positive findings occurred in 1.5% and 3% of 200 controls at 1 m and 4 m respectively. Unilateral astigmatism At a distance of 1 m, the experts detected hypermetropic astigmatism with (in parenthesis, against) the rule of 1, 2, 3 and 4 diopters 44% (44%), 58% (60%), 76% (66%), and 88% (72%) of 50 tests. Myopic astigmatism with (against) the rule was detected in 50% (22%), 60% (48%), 60% (70%), and 70% (80%) of 50 tests. At a distance of 4 m, hypermetropic astigmatism was detected in 62% (46%), 88% (72%), 100% (82%), and 100% (100%) of 50 tests and myopic astigmatism in 44% (74%), 74% (98%), 86% (100%), and 92% (100%) of 50 tests (Table 2). Of 400 emmetropic controls at each distance, 5.5% and 5.25% were false positive at 1 m and 4 m, respectively.
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Table 1 Sensitivity and specificity (in %; 95% confidence intervals in brackets) of the Brückner reflex to detect unilateral spherical ametropia with contralateral emmetropia Simulated unilateral ametropia
Experts 1 m (C.I.)
Experts 4 m (C.I.)
Students 1 m (C.I.)
Students 4 m (C.I.)
Hypermetropia 1 D Hypermetropia 2 D Hypermetropia 3 D Hypermetropia 4 D Myopia 1 D Myopia 2 D Myopia 3 D Myopia 4 D False positive tests
34 (22–49) 58 (43–71) 76 (62–87) 80 (66–90) 60 (45–73) 80 (66–90) 74 (59–85) 82 (68–91) 96.9 (93.4–98.6)
52 (38–66) 94 (83–98) 96 (85–99) 98 (89–100) 100 (91–100) 100 (91–100) 98 (89–100) 100 (91–100) 96.0 (92.3–98.0)
8 (1–28) 40 (22–61) 56 (35–75) 64 (43–81) 32 (16–54) 28 (13–50) 40 (22–61) 36 (19–57) 98.5 (95.3–99.6)
60 (45–73) 100 (91–100) 100 (91–100) 100 (91–100) 68 (46–84) 100 (91–100) 100 (91–100) 100 (91–100) 97.0 (93.3–98.8)
Clinical application Fifty-five patients were tested by an experienced observer (either ophthalomologist or orthoptist). When anisometropia (spherical equivalent) of 1 diopter, astigmatism of 2 diopters, and hypermetropia or myopia (spherical equivalent) of 3 diopters or more were considered significant, 40 patients had significant refractive errors. Of these 40 patients, 13 (32.5%) were detected at 1 m and 31 (77.5%) at 4 m distance. A false positive test occurred at 1 m distance in one and at 4 m distance in three of the residual 15 patients with a lower ametropia.
Discussion Ametropia cannot reliably be detected by the Brückner reflex. This well-known fact is illustrated by Table 3 which shows that in real test situations even experienced observers may overlook severe hypermetropia. Nevertheless a significant proportion of ametropia cases (77.5%) were recognized at the extended distance, while at the traditional distance, not more than 32.5% became obvious. Simulated anisometropia was also detected more reliably at a test distance of 4 m. Our experienced observers found
85% of unilateral hypermetropia of 1 diopter or more, and even 96% of unilateral hypermetropia of 2 diopters or more, vs only 62% and 71% respectively at the traditional distance of 1 m. Detection of unilateral myopia of 1 diopter or more increased from 74% at 1 m to 99.5% at a distance of 4 m. The correct localization rate due to the weakening of the red reflex in the myopic eye improved from 79.2% at 1 m to 98.5% at 4 m distance. This weakening—occurring with the extension of the distance—also allows for recognition of isomyopia. Isometropic hypermetropia in contrast will only be visible by an intermittent or permanent dim out of the red reflex when accommodation relaxes during the examination. Detection rates for simulated unilateral astigmatism were somewhat lower than those for unilateral spherical ametropia. They also improved at the extended distance. Therefore, examination at a longer distance, which requires only a few seconds, can be recommended. If the consulting room is very small, the test will be possible through the open door before the child enters the room. Since many newborns still have significant ametropia which disappears due to physiologic emmetropization, it is sufficient to start testing at the long distance at an age of about 4 months, albeit this is also possible in younger children. During the first months of life, the Brückner reflex
Table 2 Sensitivity and specificity (in %; 95% confidence intervals in brackets) of the Brückner reflex (performed by experts) to detect unilateral astigmatism with contralateral emmetropia Simulated astigmatism
With the rule 1 m (C.I.)
Against the rule 1 m (C.I.)
With the rule 4 m (C.I.)
Hypermetropic Hypermetropic Hypermetropic Hypermetropic Myopic 1 D Myopic 2 D Myopic 3 D Myopic 4 D Specificity
44 58 76 88 50 60 60 70
44 60 66 72 22 48 70 80
62 (47–75) 46 (32–61) 88 (75–95) 72 (57–83) 100 (91–100) 82 (68–91) 100 (91–100) 100 (91–100) 44 (30–59) 74 (59–85) 74 (59–85) 98 (89–100) 86 (43–94) 100 (91–100) 92 (80–97) 100 (91–100) 94.75 (92.0–96.6)
1 2 3 4
D D D D
(30–59) (43–72) (62–86) (75–95) (36–64) (45–73) (45–73) (55–82) 94.5 (91.7–96.4)
(30–59) (45–73) (51–78) (57–83) (12–36) (34–62) (55–82) (66–90)
Against the rule 4 m (C.I.)
Age
29 y 5y 20 y 23 y 21 y 9y 2y 3y 2y 6y 1y 4y
27 y 6m 47 y 5y 13 y 5y 1y 5y 1y 6m 6y 2y 3y 9y 15 y 13 y 5y 7y 49 y 18 y 23 y 5y 6y 2y 6y 4y 5y 1y
Pat.
RV ZT HS GV SB WT BN GG BP HM MF KE
GO ST JM SJ DR LP KG SL GC LM SB FL LN ZT PJ PM SA BT KM KD FK GM AA GL LH FJ KN NK
Correct negative −0.25 sph +0.25 sph 0 0 +0.25 sph comb −0.5 cyl×90° +0.5 sph +1.25 sph comb −0.50 cyl×101° +0.5 sph comb −0.25 cyl×21° +2.0 sph +1.5 sph +0.75 sph comb −0.75 cyl×15° +1.75 sph Correct positive −4.0 sph +7.0 sph comb −1.0 cyl X0° −0.75 cyl×52° +0.5 sph +1.75 sph comb −0.25 cyl×167° +8.5 sph comb −2.25 cyl×6° +2.75 sph comb −2.0 cyl×33° +7.75 sph comb −0.25 cyl×23° +6.25 sph comb −1.5 cyl×144° +6.0 sph comb −2.0 cyl×0° +6.5 sph comb −1.5 cyl×21° +5.0 sph comb −0.75 cyl×82° +3.0 sph comb −0.75 cyl×177° +3.75 sph comb −1.5 cyl×171° +7.0 sph comb −1.0 cyl×90° +5.25 sph comb −3.5 cyl×163° +1.75 sph comb −0,25 cyl×135° +2.5 sph comb −0.5 cyl×125° +3.0 sph +0.25 sph comb −0.75 cyl×140° +1.5 sph comb −0.25 cyl×8° +6.5 sph comb −3.0 cyl×6° +6.25 sph comb −2.0 cyl×164° +5.25 sph comb −0,25 cyl×2° +3.5 sph comb −1.5 cyl×95° +4.0 sph comb −1.25 cyl×10° +2.5 sph comb −3.0 cyl×6° +6.0 sph comb −1.5 cyl×23°
Refraction OD
0 +9.0 sph comb −1.5 cyl×0° +3.75 sph comb −1.5 cyl×16° +1.5 sph +4.25 sph comb −0.5 cyl×165° +7.75 sph comb −2.75 cyl×178° +3.0 sph comb −1.50 cyl×170° +8.25 sph comb −2.75 cyl×7° +7.75 sph comb −2.5 cyl×13° +6.0 sph comb −2.5 cyl×0° +4.5 sph comb −0.75 cyl×176° +6.25 sph comb −0.25 cyl×91° +7.75 sph comb −1.5 cyl×179° +2.25 sph comb −0.25 cyl×176° +7.0 sph comb −1.5 cyl×5° +5.5 sph comb −2.75 cyl×176° +3.0 sph comb −2.0 cyl×170° +0.5 sph comb −4.0 cyl×1° +2.0 sph +1.75 sph +4.25 sph comb −0.75 cyl×41° +7.25 sph comb −3.0 cyl×170° +7.5 sph comb −3.25 cyl×4° +7,0 sph +2.5 sph comb −1.0 cyl×72° +4.5 sph comb −1.75 cyl×164° +3.0 sph comb −1.0 cyl×8° +6.25 sph comb −1.75 cyl×155°
0 +0.5 sph +0.25 sph −0.5 sph 0 +0.25 sph +1.0 sph comb −0.5 cyl×117° +0.75 sph comb −0.5 cyl×134° +1.75 sph +1.75 sph comb −0.25 cyl×7° +1.25 sph comb −0.5 cyl×179° +2.0 sph
Refraction OS
OD>OS OD>OS OD>OS OD>OS OD>OS OD=OS OD
OS OD>OS normal normal normal normal normal normal normal normal normal normal normal normal normal normal normal
normal normal normal normal normal normal normal normal normal normal normal normal
1m
ODOS OD>OS OD>OS OD=OS ODOS OD>OS ODOS OD>OS ODOS OD=OS OD=OS OD>OS OD=OS OD>OS OD
normal normal normal normal normal normal normal normal normal normal normal normal
4m
Table 3 Results of the Brückner reflex performed by experts in orthotropic patients with their pupils undilated and comparison with cycloplegic refraction (OD>OS, red reflex brighter in OD, OD
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normal normal OD>OS +2.5 sph comb −0.5 cyl×2° +1.5 sph +2.0 sph comb −1.25 cyl×171°
OD>OS ODOS
normal normal normal normal normal normal normal normal normal −0.25 sph comb −2.25 cyl×88° −3.0 sph comb −0.75 cyl×177° +1.0 sph comb −3.5cyl×0° +0.12 sph comb −0.25 cyl×90° +4.0 sph comb −1.0 cyl×0° +8.5 sph comb −1.0 cyl×1° +7.25 sph comb −0.75 cyl×149° +2.25 sph comb −0.75 cyl×15° +6.0 sph comb −1.25 cyl×8°
normal normal normal normal normal normal normal normal normal
normal normal normal +6.0 sph comb −1.25 cyl×166° −0.5 sph comb −3.0 cyl×63° +4.0 sph comb −2.5 cyl×0°
+5.25 sph comb −0.75 cyl×177° +0.75 sph comb −0.75 cyl×88° +4.0 sph comb −2.5 cyl×0° False negative −0.25 sph comb −2.75 cyl×88° +0.5 sph comb −0.75 cyl×19° +1.0 sph comb −3.5 cyl×0° +1.75 sph comb −0.75 cyl×121° +4.0 sph comb −1.00 cyl×0° +7.5 sph comb −1.25 cyl×4° +8.0 sph comb −1.25 cyl×44° +2.5 sph comb −1.25 cyl×177° +5.25 sph comb −1.0 cyl×147° False positive +1.75 sph comb −0.25 cyl×174° +1.5 sph +1.5 sph comb −0.5 cyl×2° 5y 9y 5m
22 y 2y 1y 48 y 1m 4y 7y 4y 1y
6y 1y 6y
DP MV AM
MJ KJ CA SH HF HT SS SJ FK
AI BJ KA
1m Refraction OS Refraction OD Age Pat.
Table 3 (continued)
OD=OS OD>OS OD=OS
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is primarily important to detect cataract and other organic disorders, which is more easily achieved at short distances of 0.5 m and less. If the child sleeps, reflectory lid opening can easily be elicited by holding the child upright between the hands, stabilizing the head, and moving the child up and down with an oscillating frequency of 1/s to 2/s. The comparison of experts and students clearly shows that asymmetry of the red reflex had to be more pronounced to be recognized by students. At the traditional distance, students detected a significantly lower rate of anisometropia, but they also had a lower rate of false positive findings. It was surprising that at a distance of 4 m, results of students and experts were equal. This can be explained by the greater red reflex asymmetries at that distance. On the basis of this result and the results in the patients group, it is recommended that the test should be performed at a distance of 4 m to detect refractive error, while for detection of strabismus, small cataract, and organic eye disorders a short distance is advantageous. Nevertheless, test sensitivity is not sufficient to detect amblyogenic refractive error, because of: (1) possible accommodative compensation of severe ametropia, (2) lacking red reflex asymmetry in the case of hypermetropia of one and myopia of the other eye, and (3) limited observer sensitivity. Paysse et al. compared the ability of pediatric residents to differentiate an asymmetric from a symmetric red reflex in ten patients and six control subjects. Four patients were anisometropic (by 2.25 to 5.5 diopters) without strabismus [4]. In the entire group, the pediatric residents achieved a sensitivity of 61% and a specificity of 71% for the Brückner reflex [4]. The mean correct score was 65% using the Brückner reflex at the traditional distance, versus 82% using a photorefractor [4]. Gole and Douglas reported a sensitivity of 86% and a specificity of not more than 65% for the Brückner reflex when performed by a medical student [16]. In both studies mentioned, the test distance was 1 m. In our patients group, a sensitivity of only 32.5% was achieved at that distance, and a specificity of 93.3%, which is not very reliable due to the small number of emmetropic patients in our group. At the 4 m distance, sensitivity was 77.5% and specificity was 80%. Of course, sensitivity and specificity rates in such studies depend on patient selection and observers’ experience. These rates are not representative for a real screening in early infancy, e.g. performed by a pediatrist. The essential result of this study is that the Brückner test, albeit that it does not sufficiently detect refractive error, is an excellent complement and a possibility for pediatrists, ophthalmologists, and orthoptists to recognize severe eye disorder very early. The sensitivity of the test to detect refractive error improves at a greater distance. Therefore, the test should not only be performed at near, but also at a distance of 4 m.
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