Retinal hemorrhages: what are we talking about? Alex V. Levin, MD, MHSc, FRCSC
W
e should be very proud. Since the initial recognition by Guthkelch in 19711 that retinal hemorrhages are a manifestation of repeated acceleration-deceleration abusive injury with or without impact of the head (shaken baby syndrome), a unique form of abusive head trauma, an enormous volume of research has been conducted to help us better understand the pathophysiology, differential diagnosis, and diagnostic implications of retinal hemorrhages in a child’s eyes. Multiple lines of research, including clinical studies, post mortem studies, studies of perpetrator confessions, studies of children who have conditions other than shaken baby syndrome that might manifest with some similar findings, finite element analysis, animal studies, and studies with dummy models have all pointed us to understand the important role of the unique forces that result in this condition and the high diagnostic specificity of severe multilayered retinal hemorrhages extending throughout the retina to the ora serrata, particularly in the presence of retinoschisis and paramacular folds.2 Yet, despite the informal and individual attempts of many authors to categorize retinal hemorrhages by various novel systems and the more formal attempts of other authors to test descriptive and grading systems, we still lack a common language. Terms like mild, moderate, and severe fail us. We need something better. A system that allows us to describe retinal hemorrhages must be practical. Virtually every study to date has used retinal photographs as the template from which the descriptive data was collected. Not all centers have retinal photography, and its high costs may remain prohibitive for many years in many places. Retinal photography also is subject to problems of full image collection to the ora serrata, contrast issues (which may make retinal hemorrhages harder to discern), artifact, blur, pixilation, and the difficulty in obtaining images particularly in children, who are either poorly dilated or unable to render their eyes still enough for imaging. Many of us will remember the days of intricate retinal drawings, which were very helpful for a number of conditions but perhaps somewhat impractical in today’s age of electronic medical records.
See accompanying articles on pages 523 and 529. Author affiliations: Pediatric Ophthalmology and Ocular Genetics, Wills Eye Hospital, Thomas Jefferson University, Philadelphia, Pennsylvania Funded in part by The Foerderer Fund and The Robison Harley Endowed Chair in Pediatric Ophthalmology and Ocular Genetics. Correspondence: Alex V. Levin, MD, MHSc, FRCSC, Wills Eye Hospital, 840 Walnut Street, Philadelphia, PA 19107 (email: [email protected]). J AAPOS 2014;18:521-522. Copyright Ó 2014 by the American Association for Pediatric Ophthalmology and Strabismus. 1091-8531/$36.00 http://dx.doi.org/10.1016/j.jaapos.2014.11.002
Journal of AAPOS
Sometimes the sheer number of retinal hemorrhages would make such a drawing difficult. We need a system that ensures that key salient features of the hemorrhagic retinopathy are captured in a bedside tool that is easy to use. Perhaps, a good detailed prose description of what the ophthalmologist sees is irreplaceable. Even so, we do need some better objective description modality for the purposes of research and communication between providers, and perhaps even in the court room, in this highly medicolegally sensitive area. A descriptive tool must respect the biology of the disease. The grading system used for retinopathy of prematurity is a good example. The zones that were developed clearly reflect the biology of the developing retina with, for example, the temporal periphery being the last to vascularize. In shaken baby syndrome, multiple lines of research have clearly indicated to us the importance of vitreoretinal traction in the development of the retinal findings. With the vitreous being most attached at the retinal periphery and the posterior pole in children, hemorrhages tend to be most concentrated in these areas. Several studies have shown the significance of peripheral hemorrhages in making a diagnosis of abuse.3,4 Likewise, vitreoretinal traction leads to the critical macular finding of retinoschisis. As many of these abused children have increased intracranial pressure, one must be able to describe the typical peripapillary hemorrhages seen in this scenario to differentiate them from more widespread hemorrhages that would not usually be due to the intracranial pressure.5 Likewise, a description system must also be able to capture features which have diagnostic significance such as the perivascular hemorrhages and sheathing in vasculitis and the infiltrates of leukemia. A description system must allow us to categorize the type of hemorrhage, number of hemorrhages and the layer at which they lie, since these are also factors that have been shown to be associated with a higher risk of shaken baby syndrome.6,7 Eventually, we will move beyond the idea of a description tool, to a tool which is capable of grading for severity and diagnostic significance. Just as many papers3,6,7 have reviewed the literature and told us the increasing specificity that a hemorrhagic retinopathy has for shaken baby syndrome in the presence of an increasing number, variety, and distribution of retinal hemorrhages, an ideal description system can also serve for grading severity and diagnostic significance. This requires a test that goes beyond inter- and intraobserver reliability. Rather, one needs to conduct prospective clinical studies using the system to test its ability to discriminate situations where a clinical diagnosis of child abuse, or other disorders, has already been made by appropriate multidisciplinary teams. Just as our scoring system for retinopathy of prematurity
521
522
Levin
allows us to assess the severity of that disease, so must we have a tool for hemorrhagic retinopathy which does the same. In this issue of the Journal of AAPOS we are presented with two papers that attempt to give us a description and grading tool for retinal hemorrhages. Bhardwaj and colleauges8 perhaps misleadingly use the phrase “grading system for retinal hemorrhages” in their title: the ability to grade severity is not tested. Although certainly a very valid attempt, and well studied, it suffers from the typical challenges that virtually every similar study has faced. The designation of “mild” hemorrhages (in this case fewer than 10) is arbitrary. Its severity arm is so complicated that it may be difficult to use. The investigators choose the fovea as the center of their zones without biologic justification. Using only two zones betrays the details necessary for full description of a hemorrhagic retinopathy, although it artificially increases the chance of obtaining inter- and intraobserver reliability. By using only two observers, the power of the statistical significance remains in question. And, once again it relies on photographs without bedside testing. In the paper by Longmuir and colleagues,9 we again find ourselves relying on photographs, but now with a graphics tool that traces retinal hemorrhages to measure total surface area. This system is tested in a clinical study for its utility in identifying child abuse. It does show some correlation between the surface area covered by hemorrhage and abuse. Yet the tool does not consider the diagnostic implications of such findings as retinoschisis, actual location (as opposed to amount) and type of retinal hemorrhages, or the patterns of retinal hemorrhage. So we are left with two interesting papers with valid attempts to help improve our ability to describe retinal hemorrhages, for which the authors should be congratulated, yet we fall short once again of our need for a robust internationally agreed upon description, classification, and grading tool. Other groups have tried valiantly to come up with description and grading tools but met similar challenges.10-14 Every system differs in terms of methods and zones. We combined the works of several groups to suggest a description system which might be “better” but still suffers from complexity and the lack of testing at the bedside.12 And, the question of grading for clinical significance remains. So where do we go from here? Clearly, consensus is needed. But just as clearly, we have many different viewpoints and approaches to reconcile. Using the experience of investigators from many fields of medicine where
Volume 18 Number 6 / December 2014 description and scoring tools were developed, we need to have a process for dialogue to develop an internationally recognized description tool that can then be tested for its grading power. A group interested in advancing this agenda is having its first meeting at AAPOS in New Orleans in 2015. It will be an informal gathering, but the first step in getting this process along the road. With the collaboration of leaders in the field such as Drs. Gil Binenbaum, Brian Forbes, and Patrick Watts, we will try to get this started. Interested? Send me an email at alevin@ willseye.org. Ultimately, a robust description and grading tool will improve our research, education, clinical care, and forensic analysis of these difficult cases. References 1. Guthkelch A. Infantile subdural haematoma and its relationship to whiplash injuries. Br Med J 1971;2:430-31. 2. Levin AV. Retinal hemorrhage in abusive head trauma. Pediatrics 2010;126:961-70. 3. Togioka BM, Arnold MA, Bathurst MA, et al. Retinal hemorrhages and shaken baby syndrome: an evidence-based review. J Emerg Med 2009;37:98-106. 4. Bechtel K, Stoessel K, Leventhal JM, et al. Characteristics that distinguish accidental from abusive injury in hospitalized young children with head trauma. Pediatrics 2004;114:165-8. 5. Shiau T, Levin A. Retinal hemorrhages in children: the role of intracranial pressure. Arch Pediatr Adolesc Med 2012. 6. Binenbaum G, Mirza-George N, Christian CW, Forbes BJ. Odds of abuse associated with retinal hemorrhages in children suspected of child abuse. J AAPOS 2009;13:268-72. 7. Maguire SA, Kemp AM, Lumb RC, Farewell DM. Estimating the probability of abusive head trauma: a pooled analysis. Pediatrics 2011;128:e550-64. 8. Bhardwaj G, Jacobs MB, Martin FJ, et al. Grading system for retinal hemorrhages in abusive head trauma: clinical description and reliability study. J AAPOS 2014;18:523-8. 9. Longmuir SQ, Oral R, Walz AE, et al. Quantitative measurement of retinal hemorrhages in suspected victims of child abuse. J AAPOS 2014;18:529-33. 10. Fleck BW, Tandon A, Jones PA, Mulvihill AO, Minns RA. An interrater reliability study of a new ’zonal’ classification for reporting the location of retinal haemorrhages in childhood for clinical, legal and research purposes. Br J Ophthalmol 2010;94:886-90. 11. Chhabra MS, Bonsall DJ, Cassedy AE, Wallace GH, Schoenberger SD, West CE. Reliability of grading retinal hemorrhages in abusive head trauma. J AAPOS 2013;17:343-6. 12. Levin A, Cordovez J, Leiby B, Pequignot E, Tandon A. Retinal hemorrhages in abusive head trauma: finding a common language. Trans Am Ophthalmol Soc 2014. 13. Mulvihill AO, Jones P, Tandon A, Fleck BW, Minns RA. An interobserver and intra-observer study of a classification of RetCam images of retinal haemorrhages in children. Br J Ophthalmol 2011;95:99-104. 14. Tandon A, McIntyre S, Yu A, et al. Retinal haemorrhage description tool. Br J Ophthalmol 2011;95:1719-22.
Journal of AAPOS
W
e should be very proud. Since the initial recognition by Guthkelch in 19711 that retinal hemorrhages are a manifestation of repeated acceleration-deceleration abusive injury with or without impact of the head (shaken baby syndrome), a unique form of abusive head trauma, an enormous volume of research has been conducted to help us better understand the pathophysiology, differential diagnosis, and diagnostic implications of retinal hemorrhages in a child’s eyes. Multiple lines of research, including clinical studies, post mortem studies, studies of perpetrator confessions, studies of children who have conditions other than shaken baby syndrome that might manifest with some similar findings, finite element analysis, animal studies, and studies with dummy models have all pointed us to understand the important role of the unique forces that result in this condition and the high diagnostic specificity of severe multilayered retinal hemorrhages extending throughout the retina to the ora serrata, particularly in the presence of retinoschisis and paramacular folds.2 Yet, despite the informal and individual attempts of many authors to categorize retinal hemorrhages by various novel systems and the more formal attempts of other authors to test descriptive and grading systems, we still lack a common language. Terms like mild, moderate, and severe fail us. We need something better. A system that allows us to describe retinal hemorrhages must be practical. Virtually every study to date has used retinal photographs as the template from which the descriptive data was collected. Not all centers have retinal photography, and its high costs may remain prohibitive for many years in many places. Retinal photography also is subject to problems of full image collection to the ora serrata, contrast issues (which may make retinal hemorrhages harder to discern), artifact, blur, pixilation, and the difficulty in obtaining images particularly in children, who are either poorly dilated or unable to render their eyes still enough for imaging. Many of us will remember the days of intricate retinal drawings, which were very helpful for a number of conditions but perhaps somewhat impractical in today’s age of electronic medical records.
See accompanying articles on pages 523 and 529. Author affiliations: Pediatric Ophthalmology and Ocular Genetics, Wills Eye Hospital, Thomas Jefferson University, Philadelphia, Pennsylvania Funded in part by The Foerderer Fund and The Robison Harley Endowed Chair in Pediatric Ophthalmology and Ocular Genetics. Correspondence: Alex V. Levin, MD, MHSc, FRCSC, Wills Eye Hospital, 840 Walnut Street, Philadelphia, PA 19107 (email: [email protected]). J AAPOS 2014;18:521-522. Copyright Ó 2014 by the American Association for Pediatric Ophthalmology and Strabismus. 1091-8531/$36.00 http://dx.doi.org/10.1016/j.jaapos.2014.11.002
Journal of AAPOS
Sometimes the sheer number of retinal hemorrhages would make such a drawing difficult. We need a system that ensures that key salient features of the hemorrhagic retinopathy are captured in a bedside tool that is easy to use. Perhaps, a good detailed prose description of what the ophthalmologist sees is irreplaceable. Even so, we do need some better objective description modality for the purposes of research and communication between providers, and perhaps even in the court room, in this highly medicolegally sensitive area. A descriptive tool must respect the biology of the disease. The grading system used for retinopathy of prematurity is a good example. The zones that were developed clearly reflect the biology of the developing retina with, for example, the temporal periphery being the last to vascularize. In shaken baby syndrome, multiple lines of research have clearly indicated to us the importance of vitreoretinal traction in the development of the retinal findings. With the vitreous being most attached at the retinal periphery and the posterior pole in children, hemorrhages tend to be most concentrated in these areas. Several studies have shown the significance of peripheral hemorrhages in making a diagnosis of abuse.3,4 Likewise, vitreoretinal traction leads to the critical macular finding of retinoschisis. As many of these abused children have increased intracranial pressure, one must be able to describe the typical peripapillary hemorrhages seen in this scenario to differentiate them from more widespread hemorrhages that would not usually be due to the intracranial pressure.5 Likewise, a description system must also be able to capture features which have diagnostic significance such as the perivascular hemorrhages and sheathing in vasculitis and the infiltrates of leukemia. A description system must allow us to categorize the type of hemorrhage, number of hemorrhages and the layer at which they lie, since these are also factors that have been shown to be associated with a higher risk of shaken baby syndrome.6,7 Eventually, we will move beyond the idea of a description tool, to a tool which is capable of grading for severity and diagnostic significance. Just as many papers3,6,7 have reviewed the literature and told us the increasing specificity that a hemorrhagic retinopathy has for shaken baby syndrome in the presence of an increasing number, variety, and distribution of retinal hemorrhages, an ideal description system can also serve for grading severity and diagnostic significance. This requires a test that goes beyond inter- and intraobserver reliability. Rather, one needs to conduct prospective clinical studies using the system to test its ability to discriminate situations where a clinical diagnosis of child abuse, or other disorders, has already been made by appropriate multidisciplinary teams. Just as our scoring system for retinopathy of prematurity
521
522
Levin
allows us to assess the severity of that disease, so must we have a tool for hemorrhagic retinopathy which does the same. In this issue of the Journal of AAPOS we are presented with two papers that attempt to give us a description and grading tool for retinal hemorrhages. Bhardwaj and colleauges8 perhaps misleadingly use the phrase “grading system for retinal hemorrhages” in their title: the ability to grade severity is not tested. Although certainly a very valid attempt, and well studied, it suffers from the typical challenges that virtually every similar study has faced. The designation of “mild” hemorrhages (in this case fewer than 10) is arbitrary. Its severity arm is so complicated that it may be difficult to use. The investigators choose the fovea as the center of their zones without biologic justification. Using only two zones betrays the details necessary for full description of a hemorrhagic retinopathy, although it artificially increases the chance of obtaining inter- and intraobserver reliability. By using only two observers, the power of the statistical significance remains in question. And, once again it relies on photographs without bedside testing. In the paper by Longmuir and colleagues,9 we again find ourselves relying on photographs, but now with a graphics tool that traces retinal hemorrhages to measure total surface area. This system is tested in a clinical study for its utility in identifying child abuse. It does show some correlation between the surface area covered by hemorrhage and abuse. Yet the tool does not consider the diagnostic implications of such findings as retinoschisis, actual location (as opposed to amount) and type of retinal hemorrhages, or the patterns of retinal hemorrhage. So we are left with two interesting papers with valid attempts to help improve our ability to describe retinal hemorrhages, for which the authors should be congratulated, yet we fall short once again of our need for a robust internationally agreed upon description, classification, and grading tool. Other groups have tried valiantly to come up with description and grading tools but met similar challenges.10-14 Every system differs in terms of methods and zones. We combined the works of several groups to suggest a description system which might be “better” but still suffers from complexity and the lack of testing at the bedside.12 And, the question of grading for clinical significance remains. So where do we go from here? Clearly, consensus is needed. But just as clearly, we have many different viewpoints and approaches to reconcile. Using the experience of investigators from many fields of medicine where
Volume 18 Number 6 / December 2014 description and scoring tools were developed, we need to have a process for dialogue to develop an internationally recognized description tool that can then be tested for its grading power. A group interested in advancing this agenda is having its first meeting at AAPOS in New Orleans in 2015. It will be an informal gathering, but the first step in getting this process along the road. With the collaboration of leaders in the field such as Drs. Gil Binenbaum, Brian Forbes, and Patrick Watts, we will try to get this started. Interested? Send me an email at alevin@ willseye.org. Ultimately, a robust description and grading tool will improve our research, education, clinical care, and forensic analysis of these difficult cases. References 1. Guthkelch A. Infantile subdural haematoma and its relationship to whiplash injuries. Br Med J 1971;2:430-31. 2. Levin AV. Retinal hemorrhage in abusive head trauma. Pediatrics 2010;126:961-70. 3. Togioka BM, Arnold MA, Bathurst MA, et al. Retinal hemorrhages and shaken baby syndrome: an evidence-based review. J Emerg Med 2009;37:98-106. 4. Bechtel K, Stoessel K, Leventhal JM, et al. Characteristics that distinguish accidental from abusive injury in hospitalized young children with head trauma. Pediatrics 2004;114:165-8. 5. Shiau T, Levin A. Retinal hemorrhages in children: the role of intracranial pressure. Arch Pediatr Adolesc Med 2012. 6. Binenbaum G, Mirza-George N, Christian CW, Forbes BJ. Odds of abuse associated with retinal hemorrhages in children suspected of child abuse. J AAPOS 2009;13:268-72. 7. Maguire SA, Kemp AM, Lumb RC, Farewell DM. Estimating the probability of abusive head trauma: a pooled analysis. Pediatrics 2011;128:e550-64. 8. Bhardwaj G, Jacobs MB, Martin FJ, et al. Grading system for retinal hemorrhages in abusive head trauma: clinical description and reliability study. J AAPOS 2014;18:523-8. 9. Longmuir SQ, Oral R, Walz AE, et al. Quantitative measurement of retinal hemorrhages in suspected victims of child abuse. J AAPOS 2014;18:529-33. 10. Fleck BW, Tandon A, Jones PA, Mulvihill AO, Minns RA. An interrater reliability study of a new ’zonal’ classification for reporting the location of retinal haemorrhages in childhood for clinical, legal and research purposes. Br J Ophthalmol 2010;94:886-90. 11. Chhabra MS, Bonsall DJ, Cassedy AE, Wallace GH, Schoenberger SD, West CE. Reliability of grading retinal hemorrhages in abusive head trauma. J AAPOS 2013;17:343-6. 12. Levin A, Cordovez J, Leiby B, Pequignot E, Tandon A. Retinal hemorrhages in abusive head trauma: finding a common language. Trans Am Ophthalmol Soc 2014. 13. Mulvihill AO, Jones P, Tandon A, Fleck BW, Minns RA. An interobserver and intra-observer study of a classification of RetCam images of retinal haemorrhages in children. Br J Ophthalmol 2011;95:99-104. 14. Tandon A, McIntyre S, Yu A, et al. Retinal haemorrhage description tool. Br J Ophthalmol 2011;95:1719-22.
Journal of AAPOS
![[Between anxiolytics and sedation: what are we talking about?].](/assets/img/hold.png)
