- Email: [email protected]
The optic nerve sheath hemorrhage is a non-specific finding in cases of suspected child abuse
Journal of Forensic and Legal Medicine 36 (2015) 43e48
Contents lists available at ScienceDirect
Journal of Forensic and Legal Medicine j o u r n a l h o m e p a g e : w w w . e l s e v i e r . c o m / l o c a t e / j fl m
Clinical practice
The optic nerve sheath hemorrhage is a non-specific finding in cases of suspected child abuse Marc De Leeuw a, b, c, Emile Beuls a, * , Philippe G. Jorens d, Paul Parizel e, Werner Jacobs a a
Department of Forensic Medicine and Pathology, Antwerp University Hospital, University of Antwerp, Wilrijkstraat 10, B-2650 Edegem, Belgium Community Hospital Aalst, Merestraat 80, B-9300 Aalst, Belgium c Decanaat University of Gent, De pintelaan, 185, 9000 Gent, Belgium d Department of Intensive Care Medicine, Antwerp University Hospital, University of Antwerp Wilrijkstraat 10, B-2650 Edegem, Belgium e Department of Radiology, Antwerp University Hospital, University of Antwerp, Wilrijkstraat 10, B-2650 Edegem, Belgium b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 7 October 2014 Received in revised form 12 May 2015 Accepted 24 August 2015 Available online 1 September 2015
In young infants, the triad consisting of acute encephalopathy, retinal hemorrhages, and a subdural hematoma is a nonspecific finding. It has traumatic and non-traumatic etiologies. The triad may be found among a vast spectrum of natural diseases. Optic nerve sheath hemorrhage in infants is typically detected at autopsy. It is a nonspecific finding that can be found in traumatic and non-traumatic etiologies. Neither the triad nor the ONSH are pathognomonic for an abusive head injury. Opposite to the triad, the spectrum of non-traumatic etiologies of ONSH is limited. In infants ONSH rarely occurs in spontaneous subarachnoidal hemorrhage or in infectious conditions. Our results show that the clinical significance of the optic nerve sheath hemorrhage in the forensic work-up of fatal cases of alleged abusive head injury is its limited differential diagnosis. Only after careful differential diagnosis ONSH may contribute to the diagnosis of AHT. However, the main limitation of our study is the sampling bias, as the eyes are usually removed when abusive head trauma is suspected. © 2015 Elsevier Ltd and Faculty of Forensic and Legal Medicine. All rights reserved.
Keywords: Abusive head trauma Optic nerve sheath hemorrhage Retinal hemorrhage Postmortem examination Retinal hemorrhage
1. Introduction For decades the classic triad or the combination of subdural hematoma (SDH), acute brain damage, and retinal hemorrhages (RH), formed the basis of the shaken baby syndrome (SBS). However, attributing these brain and ocular injuries to shaking was questioned1 following experiments concluding that manual shaking could not cause the triad injuries. Without at least head impact.2e6 The issue remains a hotly debated area in forensic medicine5,7e18. Recent experiments on lambs proved that shaking alone can result in fatal brain damage.19 However, none of the shaken lambs show any evidence of bleeding in the retina, the optic nerve or the uvea (iris, ciliary body and choroid). The less mechanistic term abusive head trauma (AHT) preferably is used.20 The triad of injuries has traumatic and non-traumatic etiologies. The spectrum of non-traumatic etiologies is vast for each of the three components and can be found in infectious, metabolic, and genetic diseases, as well as in coagulation disorders. Optic nerve sheath hemorrhage (ONSH) is detected only during postmortem examination. An ONSH has been visualized on a CT * Corresponding author. E-mail address: [email protected] (E. Beuls).
scan performed on a 53-year-old male with Terson Syndrome (TS), a severe spontaneous subarachnoidal hemorrhage (SAH) associated with a vitreous bleeding and an ONSH.21 ONSH is a non-specific finding that can be caused by traumatic and non-traumatic etiologies. It may occur after fatal head injuries, in crashes such as motor vehicle accidents (MVA), and in unusual scenarios, such as when a television set topples over, and in one case of a stairway fall.22e28 It is extremely rare to find ONSH and RH accompanying TS in infants,29e34, The occurrence of ONSH in an infant with TS has been described in only three infant cases.35e37 RH may accompany infectious diseases 38, but little is known about the incidence of ONSH in conjunction with infectious conditions. Only one case of meningitis with sepsis (Group A Streptococcus), RH, and ONSH, with the infectious process extending into the optic nerve sheaths, has been reported.39 In this case, the retina was not involved in the infectious process. ONSH has been linked to an abrupt rise in intracranial pressure (ICP)40 only in adults e not in infants or in pathologies other than SAH.32 Papilledema is a hallmark of increased ICP, and small nervefiber layer hemorrhages commonly occur with dilation of the optic nerve sheath.34 No other support could be found in the literature.
http://dx.doi.org/10.1016/j.jflm.2015.08.009 1752-928X/© 2015 Elsevier Ltd and Faculty of Forensic and Legal Medicine. All rights reserved.
44
M.D. Leeuw et al. / Journal of Forensic and Legal Medicine 36 (2015) 43e48
This paper aims to report the detailed analysis of five judicial files, in order to assess the clinical significance of ONSH in the presence of the triad, in the work up of cases of alleged abusive head trauma. 2. Forensic material and methods The five cases of ONSH originated from 48 judicial cases under criminal investigation by various courts in the jurisdiction of the Courts of Appeals of Antwerp and Ghent. Approval to study these judicial cases, whether ongoing or after judicial ruling, was given by the Attorney General of Antwerp and Ghent. Because the Attorney General approved the disclosure of cases for scientific research that were from time to time still under “secrecy of the judicial investigation,” approval of an ethical committee was not sought. To safeguard the “secrecy of the judicial investigation,” the authors presented the cases anonymously to the best possible extent. The authors had access to details from the criminal files, including police interrogations of suspects, and to the medico-legal reports (forensic autopsy, forensic investigation, forensic medical examination, and seized medical files). In the analysis, 145 parameters were searched for, divided into 16 groups. ONSH was included in a second analysis for the purpose of this study. 38 of the 48 files were deemed appropriate to undertake the analysis. The files were provided as they were collected in the archives of the courts under the heading of child maltreatment without further specifications. The stories or confession of the caregivers had to admit as described in the files and has to be seen as quotes not as facts and without the possibilities to change or verify them. From the 38 complete files 21 were files of death infants. Autopsies were performed in 17 out of these 21 death cases. RH was found in nine cases and both RH and ONSH were found in five cases. In one of these five cases (Case 1) only the right optic nerve (ON) was examined and an ONSH was found. In another case, the ON also was examined in only one eye but no ONSH was found. The autopsy reports in 11 cases did not note an (ON) examination. Images were not available in the court archives so that illustrations cannot be added to the text. 3. Results 3.1. Description of five forensic cases 3.1.1. Case 1 A 25-month-old infant was hospitalized after convulsions evolving quickly into a deep comatose condition. He then was sedated and intubated, and quickly transferred to the University hospital. There were with ecchymoses all over the body and face at the right side, a torn frenulum of the upper lip, and scleral bleeding in the left eye. A CT scan showed a bilateral temporal subgaleal hematoma (SGH), no visible skull fracture, and a right frontal SDH with mass effect. Diffuse cerebral edema with a white cerebellar signs. Subarachnoidal blood was found over the tentorium. A funduscopy showed several superficial intraretinal hemorrhages, 5 right, 1 left side, a normal posterior pole and retinal periphery. Two and a half hours after the CT scan, the neurosurgeon urgently evacuated the massive acute SDH. The infant died 6 days later. The parents’ initial stories were inconsistent. Later they confessed to have brutally maltreated the infant nearly continuing, but they denied ever to have shaken the infant. The autopsy also showed residual subdural bleeding and a swollen brain with tonsillar and uncal herniation and contusional hemorrhages. Only the right eye with optic nerve was removed and examined. Resorbing retinal bleedings and perineural hemorrhages
around the optic nerve were found. Reconstruction of the time sequences indicated that a lucid interval (LI) of 8 h occurred from the occurrence of the ultimate violent act at noon until 8 p.m., before the convulsions started and the infant collapsed. The father was sentenced to prison because of cruel treatment, and not for shaken-impact AHT. 3.1.2. Case 2 Emergency personnel were called when a nine-week-old male infant with no previous health problems suddenly collapsed. Upon arrival, they found an unresponsive infant who was cyanotic, had no spontaneous respiration (apnea) and had maximally dilated pupils. Despite resuscitation and intensive care treatment, the infant died two days later. CT and MR showed a thin-film type of SDH over both parietal areas, with an interhemispheric extension and brain edema. The radiologists interpreted the different blood components in the collections as indicating different dates of trauma or re-bleeds. A bilateral intraretinal RH was found with retinal detachment and vitreous extension. Laboratory tests showed low initial hemoglobin of 4.9, low hematocrit of 16.4, a low red blood cell count of 1.75, and a platelet count of 423,000. No clot formation was observed. Seven hours after administration of blood and fresh frozen plasma, the laboratory values and the coagulation tests normalized, with an INR (International Normalized Ratio) of 1.58. The infant died 30 h after admission. The postmortem examination showed a small focal impact point with an underlying galea bleeding of 2 1 cm and a smaller one at the left frontal and temporal side. There were some small scalp bleedings at the left parietal side and, but there was no skull fracture. Deep intramuscular bleeding was found over the right scapula. Two recent small ecchymoses were found centrally located at the back of the infant, along with two small abrasions at the neck and additional reanimation injuries at the ventral and dorsal thorax. A perineurial ONSH was shown macroscopically and microscopically. Deposits of iron, together with fresh red blood cells, were seen as an indication of recent and less recent bleedings at the leptomeninges. Postmortem re-examination of the blood samples taken during life showed prolonged prothrombin time (PT) and activated partial thromboplastin time (aPTT). Because of inadequate preservation of the blood samples, postmortem coagulation tests were considered inconclusive. The infant had not experienced any previous health problems. More particularly there were no signs of easy bleeding, and no hereditary health problems were reported. The parents, who were with the infant prior to the collapse, had no explanation for what had happened. The infant had not experienced any previous health problems, particularly signs of easy bleeding, and no hereditary health problems were reported. Social workers’ and judicial investigations revealed no reason to suspect the parents. An accidental head trauma was considered more probable than an AHT. No prosecution was pursued. 3.1.3. Case 3 The biological father of a 28-week-old female infant brought the child to a nanny at 5 a.m. in good health and with no previous problems. Three and a half hours later, the infant woke up, cried, and drank half a bottle of milk. She then collapsed suddenly, became limp, and fell into a deep coma. The nanny and then the general practitioner attempted resuscitation. The infant was brought to the emergency department and died two days after admission. Imaging showed a parieto-occipital right SDH with interhemispheric and tentorial extension, with an overlying skull fracture extending over the lambdoid suture and subgaleal hematoma over the area of the skull fracture. Bleeding points were seen in the left parietal area. The postmortem examination also showed
M.D. Leeuw et al. / Journal of Forensic and Legal Medicine 36 (2015) 43e48
an edematous brain with tentorial and tonsillar herniations and blood around the brain stem. Epidural and subdural bleeding occurred at the cervical cord and bilateral extensive RHs and ONSH. The forensic pathologist described anoxemic encephalopathy. The parents said that the infant had fallen from the changing table six weeks earlier, and then offered another story about a wooden box falling on or near the infant's head two days before the collapse. Neither event seemed to have caused any injury. No in-depth investigations were conducted of the nanny or of the circumstances at the time that the infant collapsed, and no confessions or prosecutions occurred. No remote skeletal injuries were found. 3.1.4. Case 4 A 33-week-old female infant, who was with the mother and her friend for two months, collapsed early in the morning after experiencing severe continuous bowel problems during the night. Upon arrival of emergency personnel, the infant was already dead. Postmortem examination showed ecchymoses all over the head and the face and on the front and back of the trunk. The latter were not fresh. An abdominal investigation revealed purulent peritonitis caused by a rectal tear as a result of forced anal and rectal penetration. Contusional lesions were found intraorally, most likely from sexual penetration. Lacerations of the small intestine and suprarenal hemorrhages were detected and were believed to be caused by blunt abdominal trauma. A SDH a few millimeters thin was found extending over the convexity of the right hemisphere and along the falx. RHs and ONSHs were observed without further specification. Hemorrhagic contusional areas were observed in the brain and brain edema, as well as long-bone fractures, one femur fracture, and one double-fracture of the tibia. The friend, who denied any wrongdoing, was brought before a grand jury and charged principally with sexual abuse with lethal complications. The suspicion of an assumed shaking-type AHT was not given relevance in the prosecution and in the verdict. 3.1.5. Case 5 A four-month-old male infant was pronounced dead on arrival at the hospital after an apparent sudden collapse. Reanimation attempts were unsuccessful. Emergency doctors were unsuccessful in reviving him. No traumatic skull lesions were found at postmortem examination. There were bruises on the left buttock. The postmortem examination showed a large SDH over both hemispheres of the brain, at the base of the brain, and in the posterior fossa. Large clots of blood were found at the interhemispheric fissure. Some subarachnoidal blood was found at the skull base and in the foramen magnum. Neomembranes at the cerebral side of the SDH were beginning to form. Both eyes showed massive hemorrhage in the nerve sheath of the ON, with local expansion in the peri-ocular tissue. There was extensive bleeding in the different layers of the retina, with a smaller, local, retinal detachment. There was brain edema. There were small contusion areas in the frontal left and parietal right regions. Healed fractures of the fourth rib at both sides symmetrically at the ventral axial line were observed, as well as a healed fracture of the right tibia and a fracture of the distal metaphyse of the left femur at the knee. At approximately midnight the night before, a friend of the mother had hit the infant on the face with his flat hand and in the stomach with his fist. He had then shaken the infant very hard, holding the baby's thorax with his hands, which he later demonstrated. He also held the baby upside down. He said this was the first time he had shaken the infant, although he admitted to other previous maltreatments, such as pulling the infant's legs. The infant was put in bed after being shaken, but the adults worried because the infant had lost consciousness and was nonresponsive. The mother confessed that the infant had difficult eating habits and that
45
both she and her friend had often shaken him when he refused to eat. The friend's mother was sentenced to psychiatric confinement. 4. Discussion Fatal head injuries are rare in children younger than two years of age.41 The frequency of ONSH in purely accidental head trauma deaths is unknown. The triad in the presence of an ONSH may be of clinical significance. The number of natural diseases known to cause an ONSH is limited. In the work up of an alleged AHT ONSH would narrow the spectrum of etiologies of natural causes of infant death. A thorough differential diagnosis however remains mandatory. 4.1. ONSH and abuse In 1986, Lambert42 offered the first description of an ONSH in association with shaken baby syndrome (SBS). Since then, early 43 and more recent studies have shown that ONSH is common in AHT and must be sought in every postmortem examination of an infant 23,44e47 Some studies43,48,49 have accepted that ONSH is a nonspecific finding that is common among victims of AHT. Furthermore, the overwhelming presence of ONSH in AHT cases in other studies23,24,29,47,50e53 is often the result of patient selection bias, resulting in circular reasoning about the significance of ONSH in an infant death. The diagnosis of AHT is mostly based on the longstanding consideration of certain events e including the triad; the assumption of acceleration/deceleration (A/D) forces based on caregivers’ accounts; the absence of external signs of head impact; remote fractures; discrepancies in the history told by caregivers; and confessions e as hallmarks of SBS. It is also obvious that more autopsies including removal of the orbital content are performed in cases of suspected abuse than in cases of fatal infectious or genetic diseases, or in cases of infant deaths following accidental head trauma without any sign of abuse. 4.2. A second look at the examination of selected patients The number of postmortem examinations of the optic nerve in our study was low. The reason for this could not be traced. Removal of the eye and the optic nerve, however, has not always been current practice, not even in major forensic departments.52,54 A second look at the five cases shows that all cases involved brain damage, RH and SDH, and an ONSH, as well as obvious signs of external impact all over the body and head. Surprisingly, in none of the five cases has the role of ONSH been a point of interest in the discussion concerning decision making about the cause of the fatal event. The diagnosis of AHT has to be made first.55 The diagnosis could be based on confession as in the cases 1 and 5. Relying on review studies and meta-analyses,56e59 probability studies60 and or prediction analyses61 yields more. Determining the underlying mechanism is a more difficult task. Confession cannot imply a physical mechanism. In case 1 only small dots of RH are found while the SDH was a frontal space-occupying mass in the frontal subdural compartment. Together with the external head lesions and bruises all over the body, in the face and in the sclera these findings are rather characteristic for an severe accidental non-inflicted head trauma23,57,60,62,63 although the presence of few RHs cannot exclude the diagnosis of AHT.64 The confessions of brutal treatment here confirms the inflicted character of this “blunt impact type” AHT. The presence of an ONSH in such a severe impact head trauma is not surprising.
46
M.D. Leeuw et al. / Journal of Forensic and Legal Medicine 36 (2015) 43e48
In the cases 2,3, and 4 an extensive RH, a characteristic film and midline SDH, an apnea ad admission and external visible lesions on the head and the trunk provide a high index of suspicion for an AHT.62 Nevertheless a careful differential diagnosis still needs to be done. An ONSH only but reduces the spectrum of aetiologies to be considered. In case 2 an AHT was diagnosed despite the absence of confessions but a coagulation disorder which could not be investigated further at postmortem was the reason of doubt and withdrawal of the diagnosis of AHT. A similar problem was found in literature in a case where a triad and an ONSH were found after a rather low height fall of a stairway (1.42 m). A mild form of von Willebrand disease Type I was uncovered.65 The allegation of AHT was therefore rejected. However the list of coagulation disorders is extensive and when no previous signs of minor bleedings are reported in an infant or in the family, even in suspicion of AHT, it is a major task which is rarely worthwhile to consider.66 In our case the probability of the presence of an underlying condition predisposing to bleeding was extremely low. Unlike SDH or RH, an ONSH caused by an underlying coagulation disorder has never been mentioned. The authors did not considered an haematological disorder while laboratory investigations during life as well the postmortem histological examinations of all organs did not suggest haematological abnormalities. Furthermore, there was doubt about the dating of the traumatic event due to the different densities in the SDH on the CT scan. The CT scan was not the instrument that contributed to the dating of the initial injury. The combination of fresh, high-density components with older, low-density components may occur very soon after a trauma.67 The reasons not to prosecute the caregivers in this case of a highly suspected AHT were incorrect. ONSH may be caused by the severe traumatic head impact but also shaking is not excluded. The cervical epidural and subdural hemorrhages in case 3 would probably signify forceful movement of the head out of the normal range of motion of the cervical spine. It means that the infant was shaken. Cervical spine injuries are rather rarely reported in AHT suspected cases.68 Given the signs of severe impact on the head with also a skull fracture, most likely both the shaking and the head impact are responsible for the brain and ocular injuries. The diagnostic accuracy for AHT improves when multiple pathologies including RH, ONSH, skull fracture and intracranial hemorrhage are present, and lesions on the cervical spine and its contents may be added to this list.6,53 The complete lack of prosecution in this obvious shaken and impact AHT case 3 is difficult to accept. ONSH may be caused whether by shaking or by impact. In case 4 the occurrence of RH and ONSH, in association with peritonitis with sepsis, might casts some doubt on the diagnosis of a fatal accidental or non-accidental head trauma. In this case, sepsis is the more probable primary cause of death. The correlation between an infectious condition with sepsis and ONSH cannot be considered nonexistent although anecdotal in only one case report. In this case report, already mentioned in the Introduction 39 an incidental congenital disorder of glycosylation was found through a histology of the brain and there were no signs of vasculitis. The case was described as a mimic of a non-accidental injury (NAI). It is understandable that a meningeal infection can continue into the subarachnoidal space around the optic nerve which terminates in the optic nerve head at the lamina cribrosa. Due to this anatomical barrier the retina itself was not involved in the infectious process. Hypothetically, the hemorrhages in the optic nerve sheath accompanied by inflammation of the optic nerve sheath could be compared with the RH that has been correlated with coagulation disorders in the critically ill infant,38 as can occur in sepsis or in a combination of meningitis and sepsis. One could hypothesize that a similar process occurred in the development of ONSH in sepsis.
Therefore, infectious diseases, whether or not they are secondarily involved in a coagulation disorder, must be included in the differential diagnosis on the occurrence of ONSH. Nevertheless the external lesions of head and trunk61 as well as the previous remote fractures in mind, an AHT factor was correctly taken into consideration, with the contribution of ONSH and RH in retrospect being somewhat doubtful. In case 5 the head trauma may be suspected for an AHT since it has been confessed that the head trauma was intentional. Nevertheless the characteristic complex of an extensive, multilayered RH, a film of SDH with extension from the midline, brain damage, apnea57,60,61 are found, as well as remnants of long bone fractures, but in the absence of external impact lesions point to a pure shaking AHT. However also slapping the infant's face with a flat hand before shaking the infant was confessed. Impact to the head with or against an object with a smooth padded surface such as a slap in the face not necessarily cause visible lesions.3,48 It seems however doubtful that a slap in the face should cause an ONSH which more likely has to be expected after severe head impact. In this case, in the absence of natural diseases and signs of impact shaking as cause of the findings as well as of ONSH seemed acceptable. In our limited series of postmortem examinations of AHT cases ONSH occurs in shaking and shaking-impact as well as in pure blunt impact AHT. Its presence does not contribute to the determination of the underlying mechanism of an AHT. Many unanswered questions remain regarding the presence of ONSH in other natural conditions, such as a concurrent infectious disease with sepsis, as well as a secondary coagulation disorder. Moreover, the relationship of the occurrence of ONSH in the presence of a primary coagulation disorder is a totally unknown and remains a less probable natural etiology of ONSH. The limited knowledge on the natural causes of ONSH is due to the factthat the optic nerve cannot be examined in living patients. While RH can be easily detected by fundoscopy, ONSH can only be examined during the postmortem examination. The limited number of ONSH may stem from the completely different anatomical and vascular architecture of the optic nerve, which consists of a heavily myelinated white matter bundle, surrounded by an extension of the intracranial leptomeninges, including the subarachnoidal space. Furthermore, the pathophysiologic mechanisms causing ONSH remain speculative.1,23,48,49 Like for other eye findings such as RH, retinal folds, and retinoschisis caution is urged in interpreting ONSH outside the context until good evidence is available.28,69 5. Conclusion ONSH is a non-specific finding and occurs as a result of both traumatic and non-traumatic etiologies. The clinical significance of ONSH might be that it narrows considerably the differential diagnosis in the work-up of a suspected AHT, given that natural etiologies of RH, SDH and brain damage, substantially exceed those known of ONSH. However the major limitation in this study is the small number of cases in which eyes are removed while the figures also show that the number of cases in which eyes are removed in forensic practice is small and biased towards suspicious head trauma cases, bringing a limitation to the current knowledge of the differential diagnosis list in ONSH. Conflict of interest There is no conflict of interest. Funding None declared.
M.D. Leeuw et al. / Journal of Forensic and Legal Medicine 36 (2015) 43e48
Ethical approval None.
References 1. Squier W. The “shaken baby” syndrome: pathology and mechanisms. Acta Neuropathol 2011;122:519e42. 2. Duhaime A, Gennerelli T, Thibault L, Bruce DA, Margulies SS, Wiser R. The shaken baby syndrome. A clinical, pathological, and biomechanical study. J Neurosurg 1987;66:409e15. 3. Duhaime AC, Christian CW, Rorke LB, Zimmerman RA. Nonaccidental head injury in infantsethe “shaken-baby syndrome”. N Engl J Med 1998;338:1822e9. 4. Lloyd J, Willey EN, Galaznik JG, Lee III WE, Luttner SE. Biomechanical evaluation of head kinematics during infant shaking versus pediatric activities of daily living. J Forensic Biomechanics 2011;2:1e9. 5. Scheimberg I, Mack J. “Shaken baby syndrome” and forensic pathology. Forensic Sci Med Pathol 2014 Jun;10(2):242e3. 6. Squier W. The triad of retinal haemorrhage, subdural haemorrhage and encephalopathy in an infant unassociated with evidence of physical injury is not the result of shaking, but is most likely to have been caused by a natural disease: Yes. J Prim Health Care 2011;3:159e61. 7. Rorke-Adams LB. The triad of retinal haemorrhage, subdural haemorrhage and encephalopathy in an infant unassociated with evidence of physical injury is not the result of shaking, but is most likely to have been caused by a natural disease: No. J Prim Health Care 2011;3:161e3. 8. Godfrey ME. Response to the back to back debate about the effects of shaking a baby, in the absence of any impact trauma. J Prim Health Care 2011;3:253e4. 9. Galaznik JG. Response to the back to back debate about the effects of shaking a baby, in the absence of any impact trauma. J Prim Health Care 2011;3:252e3. 10. Wojcik D. Response to the back to back debate about the effects of shaking a baby, in the absence of any impact trauma. J Prim Health Care 2011;3:253. 11. Goodyear-Smith F. The challenging and complex nature of primary health care. J Prim Health Care 2011;3:178e9. 12. Byard RW. “Shaken baby syndrome” and forensic pathology: an uneasy interface. Forensic Sci Med Pathol 2014;10:239e41. 13. Greeley CS. “Shaken baby syndrome” and forensic pathology. Forensic Sci Med Pathol 2014;10:253e5. 14. Smith C. “Shaken baby syndrome” and forensic pathology. Forensic Sci Med Pathol 2014;10:256e8. 15. Cohen MC, Ramsay DA. “Shaken baby syndrome” and forensic pathology. Forensic Sci Med Pathol 2014;10:244e5. 16. Squier W. “Shaken baby syndrome” and forensic pathology. Forensic Sci Med Pathol 2014;10:248e50. 17. Case M. Shaken baby syndrome” and forensic pathology. Forensic Sci Med Pathol 2014;10:246e7. 18. Sperhake JP, Matschke J. “Shaken baby syndrome” and forensic pathology. Forensic Sci Med Pathol 2014;10:251e2. 19. Finnie JW, Blumbergs PC, Manavis J, Turner RJ, Helps S, Vink R, et al. Neuropathological changes in a lamb model of non-accidental head injury (the shaken baby syndrome). J Clin Neurosci 2012;19:1159e64. 20. Christian CW, Block R. Committee on child abuse and neglect; american academy of pediatrics. Abusive head trauma in infants and children. Pediatrics 2009;123:1409e11. 21. Gauntt CD, Sherry RG, Kannan C. Terson syndrome with bilateral optic nerve sheath hemorrhage. J Neuro Ophthalmol 2007;27:193e4. 22. Kivlin JD, Currie ML, Greenbaum VJ, Simons KB, Jentzen J. Retinal hemorrhages in children following fatal motor vehicle crashes: a case series. Arch Ophthalmol 2008;126:800e4. 23. Wygnanski-Jaffe T, Levin AV, Shafiq A, Smith C, Enzenauer RW, Elder JE, et al. Postmortem orbital findings in shaken baby syndrome. Am J Ophthalmol 2006;142:233e40. 24. Gilliland MGF, Luckenbach MW, Chenier TC. Systemic and ocular findings in 169 prospectively studied child deaths: retinal hemorrhages usually mean child abuse. Forensic Sci Int 1994;68:117e32. 25. Gnanaraj L, Gilliland MG, Yahya RR, Rutka JT, Drake J, et al. Ocular manifestations of crush head injury in children. Eye 2007;21:5e10. 26. Deisch J, Quinton R, Gruszecki AC. Craniocerebral trauma inflicted by television falls. J Forensic Sci 2011;56:1049e53. 27. Platt MS, Stanley C. TV tip-over morbidity and mortality in children. J Forensic Sci 2011;56:1364e7. 28. Lantz PE, Sinal SH, Stanton CA, Weaver Jr RG. Perimacular retinal folds from childhood head trauma. Br Med J 2004;328:754e6. 29. Forbes BJ, Rubin SE, Margolin E, Levin AV. Evaluation and management of retinal hemorrhages in infants with and without abusive head trauma. J AAPOS 2010;14:267e73. 30. Vincent ALV, Kelly P. Retinal haemorrhages in inflicted traumatic brain injury: the ophthalmologist in court. Clin Exp Ophthalmol 2010;38:521e32. 31. Ko F, Knox DL. The ocular pathology of terson's syndrome. Ophthalmology 2010; Jul;(117). 1423e9.e2. 32. Medele RJ, Stummer W, Mueller AJ, Steiger HJ, Reulen HJ. Terson's syndrome in subarachnoid hemorrhage and severe brain injury accompanied by acutely raised intracranial pressure. J Neurosurg 1998;88:851e4.
47
33. Schloff S, Mullaney PB, Armstrong DC, Simantirakis E, Humphreys RP, Myseros JS, et al. Retinal findings in children with intracranial hemorrhage. Ophthalmology 2002;109:1472e6. 34. Levin AV. Retinal hemorrhage in abusive head trauma. Pediatrics 2010;126: 961e70. 35. Mena OJ, Paul I, Reichard RR. Ocular findings in raised intracranial pressure: a case of terson syndrome in a seven-month-old infant. Am J Forensic Med Pathol 2011;32:55e7. 36. Weissgold DJ, Budenz DL, Hood I, Rorke LB. Ruptured vascular malformation masquerading as battered/shaken baby syndrome: a nearly tragic mistake. Surv Ophthalmol 1995;39:509e12. 37. Bhardwaj G, Jacobs MB, Moran KT, Tan K. Terson syndrome with ipsilateral severe hemorrhagic retinopathy in a 7-month-old child. J AAPOS 2010;14: 441e3. 38. Agrawal S, Peters MJ, Adams GG, Pierce CM. Prevalence of retinal hemorrhages in critically ill children. Pediatrics 2012;129:1388e96. 39. Ong BB, Gole GA, Robertson T, McGill J, de Lore D, Crawford M. Retinal hemorrhages associated with meningitis in a child with a congenital disorder of glycosylation. Forensic Sci Med Pathol 2009;5:307e12. 40. Müller PJ, Deck JH. Intraocular and optic nerve sheath hemorrhage in cases of sudden intracranial hypertension. J Neurosurg 1974;41:160e6. 41. Gill JR, Goldfeder LB, Armbrustmacher V, Coleman A, Mena H, Hirsch CS. Fatal head injury in children younger than 2 years in New York city and an overview of the shaken baby syndrome. Arch Pathol Lab Med 2009;133:619e27. 42. Lambert SR, Johnson TE, Hoyt CS. Optic nerve sheath and retinal hemorrhages associated with the shaken baby syndrome. Arch Ophthalmol 1986;104: 1509e12. 43. Budenz D, Farber M, Mirchandani H, Park H, Rorke L. Ocular and optic nerve hemorrhages in abused infants with intracranial injuries. Ophthalmology 1994;101:559e65. 44. Mungan NK. Update on shaken baby syndrome: ophthalmology. Curr Opin Ophthalmol 2007; Sep;18:392e7. 45. Chiesa A, Duhaime AC. Abusive head trauma. Pediatr Clin N. Am 2009;56: 317e31. 46. Coats B, Binenbaum G, Peiffer RL, Forbes BJ, Margulies SS. Ocular hemorrhages in neonatal porcine eyes from single, rapid rotational events. Invest Ophthalmol Vis Sci 2010;51:4792e7. 47. Emerson MV, Jakobs E, Green WR. Ocular autopsy and histopathologic features of child abuse. Ophthalmology 2007;114:1384e94. 48. Case ME. Inflicted traumatic brain injury in infants and young children. Brain Pathol 2008;18:571e82. 49. Wygnanski-Jaffe T, Morad Y, Levin AV. Pathology of retinal hemorrhage in abusive head trauma. Forensic Sci Med Pathol 2009;5:291e7. 50. Gilles EE, McGregor ML, Levy-Clarke G. Retinal hemorrhage asymmetry in inflicted head injury: a clue to pathogenesis? J Pediatr 2003;143:494e9. 51. Kivlin JD, Simons KB, Lazoritz S, Ruttum MS. Shaken baby syndrome. Ophthalmology 2000;107:1246e54. 52. Matschke J, Püschel K, Glatzel M. Ocular pathology in shaken baby syndrome and other forms of infantile non-accidental head injury. Int J Leg Med 2009;123: 189e97. 53. Bhardwaj G, Chowdhury V, Jacobs MB, Moran KT, Martin FJ, Coroneo MT, et al. A systematic review of the diagnostic accuracy of ocular signs in pediatric abusive head trauma. Ophthalmology 2010;117. 983e92.e17. 54. John SM, Jones P, Kelly P, Vincent A. Fatal pediatric head injuries: a 20-year review of cases through the Auckland Coroner's office. Am J Forensic Med Pathol 2013;34:277e82. 55. Narang S, Clarke J. Abusive head trauma: past, present, and future. J Child Neurol 2014;29:1747e56. 56. Piteau SJ, Ward MG, Barrowman NJ, Plint AC. Clinical and radiographic characteristics associated with abusive and nonabusive head trauma: a systematic review. Pediatrics 2012;130:315e23. 57. Maguire SA, Watts PO, Shaw AD, Holden S, Taylor RH, Watkins WJ, et al. Retinal haemorrhages and related findings in abusive and non-abusive head trauma:a systematic review. Eye 2013;27:28e36. 58. Maguire S, Pickerd N, Farewell D, Mann M, Tempest V, Kemp AM. Which clinical features distinguish inflicted from non-inflicted brain injury? A systematic review. Arch Dis Child 2009;94:860e7. 59. Kemp AM, Jaspan T, Griffiths J, Stoodley N, Mann MK, Tempest V, et al. Neuroimaging: what neuroradiological features distinguish abusive from non-abusive head trauma? A systematic review. Arch Dis Child 2011;96: 1103e12. 60. Maguire SA, Kemp AM, Lumb RC, Farewell DM. Estimating the probability of abusive head trauma: a pooled analysis. Pediatrics 2011;128. e550e64. 61. Hymel KP, Armijo-Garcia V, Foster R, Frazier TN, Stoiko M, Christie LM, et al. Pediatric brain injury research network (PediBIRN) investigators. Validation of a clinical prediction rule for pediatric abusive head trauma. Pediatrics 2014;134. e1537e44. 62. Vinchon M, Defoort-Dhellemmes S, Desurmont M, Dhellemmes P. Accidental and nonaccidental head injuries in infants: a prospective study. J Neurosurg 2005;102:380e4. 63. Vinchon M, de Foort-Dhellemmes S, Desurmont M, Delestret I. Confessed abuse versus witnessed accidents in infants: comparison of clinical, radiological, and ophthalmological data in corroborated cases. Child Nerv Syst 2010;26:637e45.
48
M.D. Leeuw et al. / Journal of Forensic and Legal Medicine 36 (2015) 43e48
64. Margolin EA, Dev LS, Trobe JD. Prevalence of retinal hemorrhages in perpetrator-confessed cases of abusive head trauma. Arch Ophthalmol 2010;128:795. 65. Lantz PE, Couture DE. Fatal acute intracranial injury, subdural hematoma, and retinal hemorrhages caused by stairway fall. J Forensic Sci 2011;56:1648e53. 66. Carpenter SL, Abshire TC, Anderst JD. Section on hematology/oncology and committee on child abuse and neglect of the American Academy of Pediatrics. Evaluating for suspected child abuse: conditions that predispose to bleeding. Pediatrics 2013;131. e1357e73.
67. Adamsbaum C, Grabar S, Mejean N, Rey-Salmon C. Abusive head trauma: judicial admissions highlight violent and repetitive shaking. Pediatrics 2010;126:546e55. 68. Bandak FA. Shaken baby syndrome: a biomechanics analysis of injury mechanisms. Forensic Sci Int 2005;151:71e9. 69. Oshima T, Yoshikawa H, Ohtani M, Mimasaka S. Examination of postmortem retinal folds: a non-invasive study. J Forensic Leg Med 2015;30:16e20.
Contents lists available at ScienceDirect
Journal of Forensic and Legal Medicine j o u r n a l h o m e p a g e : w w w . e l s e v i e r . c o m / l o c a t e / j fl m
Clinical practice
The optic nerve sheath hemorrhage is a non-specific finding in cases of suspected child abuse Marc De Leeuw a, b, c, Emile Beuls a, * , Philippe G. Jorens d, Paul Parizel e, Werner Jacobs a a
Department of Forensic Medicine and Pathology, Antwerp University Hospital, University of Antwerp, Wilrijkstraat 10, B-2650 Edegem, Belgium Community Hospital Aalst, Merestraat 80, B-9300 Aalst, Belgium c Decanaat University of Gent, De pintelaan, 185, 9000 Gent, Belgium d Department of Intensive Care Medicine, Antwerp University Hospital, University of Antwerp Wilrijkstraat 10, B-2650 Edegem, Belgium e Department of Radiology, Antwerp University Hospital, University of Antwerp, Wilrijkstraat 10, B-2650 Edegem, Belgium b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 7 October 2014 Received in revised form 12 May 2015 Accepted 24 August 2015 Available online 1 September 2015
In young infants, the triad consisting of acute encephalopathy, retinal hemorrhages, and a subdural hematoma is a nonspecific finding. It has traumatic and non-traumatic etiologies. The triad may be found among a vast spectrum of natural diseases. Optic nerve sheath hemorrhage in infants is typically detected at autopsy. It is a nonspecific finding that can be found in traumatic and non-traumatic etiologies. Neither the triad nor the ONSH are pathognomonic for an abusive head injury. Opposite to the triad, the spectrum of non-traumatic etiologies of ONSH is limited. In infants ONSH rarely occurs in spontaneous subarachnoidal hemorrhage or in infectious conditions. Our results show that the clinical significance of the optic nerve sheath hemorrhage in the forensic work-up of fatal cases of alleged abusive head injury is its limited differential diagnosis. Only after careful differential diagnosis ONSH may contribute to the diagnosis of AHT. However, the main limitation of our study is the sampling bias, as the eyes are usually removed when abusive head trauma is suspected. © 2015 Elsevier Ltd and Faculty of Forensic and Legal Medicine. All rights reserved.
Keywords: Abusive head trauma Optic nerve sheath hemorrhage Retinal hemorrhage Postmortem examination Retinal hemorrhage
1. Introduction For decades the classic triad or the combination of subdural hematoma (SDH), acute brain damage, and retinal hemorrhages (RH), formed the basis of the shaken baby syndrome (SBS). However, attributing these brain and ocular injuries to shaking was questioned1 following experiments concluding that manual shaking could not cause the triad injuries. Without at least head impact.2e6 The issue remains a hotly debated area in forensic medicine5,7e18. Recent experiments on lambs proved that shaking alone can result in fatal brain damage.19 However, none of the shaken lambs show any evidence of bleeding in the retina, the optic nerve or the uvea (iris, ciliary body and choroid). The less mechanistic term abusive head trauma (AHT) preferably is used.20 The triad of injuries has traumatic and non-traumatic etiologies. The spectrum of non-traumatic etiologies is vast for each of the three components and can be found in infectious, metabolic, and genetic diseases, as well as in coagulation disorders. Optic nerve sheath hemorrhage (ONSH) is detected only during postmortem examination. An ONSH has been visualized on a CT * Corresponding author. E-mail address: [email protected] (E. Beuls).
scan performed on a 53-year-old male with Terson Syndrome (TS), a severe spontaneous subarachnoidal hemorrhage (SAH) associated with a vitreous bleeding and an ONSH.21 ONSH is a non-specific finding that can be caused by traumatic and non-traumatic etiologies. It may occur after fatal head injuries, in crashes such as motor vehicle accidents (MVA), and in unusual scenarios, such as when a television set topples over, and in one case of a stairway fall.22e28 It is extremely rare to find ONSH and RH accompanying TS in infants,29e34, The occurrence of ONSH in an infant with TS has been described in only three infant cases.35e37 RH may accompany infectious diseases 38, but little is known about the incidence of ONSH in conjunction with infectious conditions. Only one case of meningitis with sepsis (Group A Streptococcus), RH, and ONSH, with the infectious process extending into the optic nerve sheaths, has been reported.39 In this case, the retina was not involved in the infectious process. ONSH has been linked to an abrupt rise in intracranial pressure (ICP)40 only in adults e not in infants or in pathologies other than SAH.32 Papilledema is a hallmark of increased ICP, and small nervefiber layer hemorrhages commonly occur with dilation of the optic nerve sheath.34 No other support could be found in the literature.
http://dx.doi.org/10.1016/j.jflm.2015.08.009 1752-928X/© 2015 Elsevier Ltd and Faculty of Forensic and Legal Medicine. All rights reserved.
44
M.D. Leeuw et al. / Journal of Forensic and Legal Medicine 36 (2015) 43e48
This paper aims to report the detailed analysis of five judicial files, in order to assess the clinical significance of ONSH in the presence of the triad, in the work up of cases of alleged abusive head trauma. 2. Forensic material and methods The five cases of ONSH originated from 48 judicial cases under criminal investigation by various courts in the jurisdiction of the Courts of Appeals of Antwerp and Ghent. Approval to study these judicial cases, whether ongoing or after judicial ruling, was given by the Attorney General of Antwerp and Ghent. Because the Attorney General approved the disclosure of cases for scientific research that were from time to time still under “secrecy of the judicial investigation,” approval of an ethical committee was not sought. To safeguard the “secrecy of the judicial investigation,” the authors presented the cases anonymously to the best possible extent. The authors had access to details from the criminal files, including police interrogations of suspects, and to the medico-legal reports (forensic autopsy, forensic investigation, forensic medical examination, and seized medical files). In the analysis, 145 parameters were searched for, divided into 16 groups. ONSH was included in a second analysis for the purpose of this study. 38 of the 48 files were deemed appropriate to undertake the analysis. The files were provided as they were collected in the archives of the courts under the heading of child maltreatment without further specifications. The stories or confession of the caregivers had to admit as described in the files and has to be seen as quotes not as facts and without the possibilities to change or verify them. From the 38 complete files 21 were files of death infants. Autopsies were performed in 17 out of these 21 death cases. RH was found in nine cases and both RH and ONSH were found in five cases. In one of these five cases (Case 1) only the right optic nerve (ON) was examined and an ONSH was found. In another case, the ON also was examined in only one eye but no ONSH was found. The autopsy reports in 11 cases did not note an (ON) examination. Images were not available in the court archives so that illustrations cannot be added to the text. 3. Results 3.1. Description of five forensic cases 3.1.1. Case 1 A 25-month-old infant was hospitalized after convulsions evolving quickly into a deep comatose condition. He then was sedated and intubated, and quickly transferred to the University hospital. There were with ecchymoses all over the body and face at the right side, a torn frenulum of the upper lip, and scleral bleeding in the left eye. A CT scan showed a bilateral temporal subgaleal hematoma (SGH), no visible skull fracture, and a right frontal SDH with mass effect. Diffuse cerebral edema with a white cerebellar signs. Subarachnoidal blood was found over the tentorium. A funduscopy showed several superficial intraretinal hemorrhages, 5 right, 1 left side, a normal posterior pole and retinal periphery. Two and a half hours after the CT scan, the neurosurgeon urgently evacuated the massive acute SDH. The infant died 6 days later. The parents’ initial stories were inconsistent. Later they confessed to have brutally maltreated the infant nearly continuing, but they denied ever to have shaken the infant. The autopsy also showed residual subdural bleeding and a swollen brain with tonsillar and uncal herniation and contusional hemorrhages. Only the right eye with optic nerve was removed and examined. Resorbing retinal bleedings and perineural hemorrhages
around the optic nerve were found. Reconstruction of the time sequences indicated that a lucid interval (LI) of 8 h occurred from the occurrence of the ultimate violent act at noon until 8 p.m., before the convulsions started and the infant collapsed. The father was sentenced to prison because of cruel treatment, and not for shaken-impact AHT. 3.1.2. Case 2 Emergency personnel were called when a nine-week-old male infant with no previous health problems suddenly collapsed. Upon arrival, they found an unresponsive infant who was cyanotic, had no spontaneous respiration (apnea) and had maximally dilated pupils. Despite resuscitation and intensive care treatment, the infant died two days later. CT and MR showed a thin-film type of SDH over both parietal areas, with an interhemispheric extension and brain edema. The radiologists interpreted the different blood components in the collections as indicating different dates of trauma or re-bleeds. A bilateral intraretinal RH was found with retinal detachment and vitreous extension. Laboratory tests showed low initial hemoglobin of 4.9, low hematocrit of 16.4, a low red blood cell count of 1.75, and a platelet count of 423,000. No clot formation was observed. Seven hours after administration of blood and fresh frozen plasma, the laboratory values and the coagulation tests normalized, with an INR (International Normalized Ratio) of 1.58. The infant died 30 h after admission. The postmortem examination showed a small focal impact point with an underlying galea bleeding of 2 1 cm and a smaller one at the left frontal and temporal side. There were some small scalp bleedings at the left parietal side and, but there was no skull fracture. Deep intramuscular bleeding was found over the right scapula. Two recent small ecchymoses were found centrally located at the back of the infant, along with two small abrasions at the neck and additional reanimation injuries at the ventral and dorsal thorax. A perineurial ONSH was shown macroscopically and microscopically. Deposits of iron, together with fresh red blood cells, were seen as an indication of recent and less recent bleedings at the leptomeninges. Postmortem re-examination of the blood samples taken during life showed prolonged prothrombin time (PT) and activated partial thromboplastin time (aPTT). Because of inadequate preservation of the blood samples, postmortem coagulation tests were considered inconclusive. The infant had not experienced any previous health problems. More particularly there were no signs of easy bleeding, and no hereditary health problems were reported. The parents, who were with the infant prior to the collapse, had no explanation for what had happened. The infant had not experienced any previous health problems, particularly signs of easy bleeding, and no hereditary health problems were reported. Social workers’ and judicial investigations revealed no reason to suspect the parents. An accidental head trauma was considered more probable than an AHT. No prosecution was pursued. 3.1.3. Case 3 The biological father of a 28-week-old female infant brought the child to a nanny at 5 a.m. in good health and with no previous problems. Three and a half hours later, the infant woke up, cried, and drank half a bottle of milk. She then collapsed suddenly, became limp, and fell into a deep coma. The nanny and then the general practitioner attempted resuscitation. The infant was brought to the emergency department and died two days after admission. Imaging showed a parieto-occipital right SDH with interhemispheric and tentorial extension, with an overlying skull fracture extending over the lambdoid suture and subgaleal hematoma over the area of the skull fracture. Bleeding points were seen in the left parietal area. The postmortem examination also showed
M.D. Leeuw et al. / Journal of Forensic and Legal Medicine 36 (2015) 43e48
an edematous brain with tentorial and tonsillar herniations and blood around the brain stem. Epidural and subdural bleeding occurred at the cervical cord and bilateral extensive RHs and ONSH. The forensic pathologist described anoxemic encephalopathy. The parents said that the infant had fallen from the changing table six weeks earlier, and then offered another story about a wooden box falling on or near the infant's head two days before the collapse. Neither event seemed to have caused any injury. No in-depth investigations were conducted of the nanny or of the circumstances at the time that the infant collapsed, and no confessions or prosecutions occurred. No remote skeletal injuries were found. 3.1.4. Case 4 A 33-week-old female infant, who was with the mother and her friend for two months, collapsed early in the morning after experiencing severe continuous bowel problems during the night. Upon arrival of emergency personnel, the infant was already dead. Postmortem examination showed ecchymoses all over the head and the face and on the front and back of the trunk. The latter were not fresh. An abdominal investigation revealed purulent peritonitis caused by a rectal tear as a result of forced anal and rectal penetration. Contusional lesions were found intraorally, most likely from sexual penetration. Lacerations of the small intestine and suprarenal hemorrhages were detected and were believed to be caused by blunt abdominal trauma. A SDH a few millimeters thin was found extending over the convexity of the right hemisphere and along the falx. RHs and ONSHs were observed without further specification. Hemorrhagic contusional areas were observed in the brain and brain edema, as well as long-bone fractures, one femur fracture, and one double-fracture of the tibia. The friend, who denied any wrongdoing, was brought before a grand jury and charged principally with sexual abuse with lethal complications. The suspicion of an assumed shaking-type AHT was not given relevance in the prosecution and in the verdict. 3.1.5. Case 5 A four-month-old male infant was pronounced dead on arrival at the hospital after an apparent sudden collapse. Reanimation attempts were unsuccessful. Emergency doctors were unsuccessful in reviving him. No traumatic skull lesions were found at postmortem examination. There were bruises on the left buttock. The postmortem examination showed a large SDH over both hemispheres of the brain, at the base of the brain, and in the posterior fossa. Large clots of blood were found at the interhemispheric fissure. Some subarachnoidal blood was found at the skull base and in the foramen magnum. Neomembranes at the cerebral side of the SDH were beginning to form. Both eyes showed massive hemorrhage in the nerve sheath of the ON, with local expansion in the peri-ocular tissue. There was extensive bleeding in the different layers of the retina, with a smaller, local, retinal detachment. There was brain edema. There were small contusion areas in the frontal left and parietal right regions. Healed fractures of the fourth rib at both sides symmetrically at the ventral axial line were observed, as well as a healed fracture of the right tibia and a fracture of the distal metaphyse of the left femur at the knee. At approximately midnight the night before, a friend of the mother had hit the infant on the face with his flat hand and in the stomach with his fist. He had then shaken the infant very hard, holding the baby's thorax with his hands, which he later demonstrated. He also held the baby upside down. He said this was the first time he had shaken the infant, although he admitted to other previous maltreatments, such as pulling the infant's legs. The infant was put in bed after being shaken, but the adults worried because the infant had lost consciousness and was nonresponsive. The mother confessed that the infant had difficult eating habits and that
45
both she and her friend had often shaken him when he refused to eat. The friend's mother was sentenced to psychiatric confinement. 4. Discussion Fatal head injuries are rare in children younger than two years of age.41 The frequency of ONSH in purely accidental head trauma deaths is unknown. The triad in the presence of an ONSH may be of clinical significance. The number of natural diseases known to cause an ONSH is limited. In the work up of an alleged AHT ONSH would narrow the spectrum of etiologies of natural causes of infant death. A thorough differential diagnosis however remains mandatory. 4.1. ONSH and abuse In 1986, Lambert42 offered the first description of an ONSH in association with shaken baby syndrome (SBS). Since then, early 43 and more recent studies have shown that ONSH is common in AHT and must be sought in every postmortem examination of an infant 23,44e47 Some studies43,48,49 have accepted that ONSH is a nonspecific finding that is common among victims of AHT. Furthermore, the overwhelming presence of ONSH in AHT cases in other studies23,24,29,47,50e53 is often the result of patient selection bias, resulting in circular reasoning about the significance of ONSH in an infant death. The diagnosis of AHT is mostly based on the longstanding consideration of certain events e including the triad; the assumption of acceleration/deceleration (A/D) forces based on caregivers’ accounts; the absence of external signs of head impact; remote fractures; discrepancies in the history told by caregivers; and confessions e as hallmarks of SBS. It is also obvious that more autopsies including removal of the orbital content are performed in cases of suspected abuse than in cases of fatal infectious or genetic diseases, or in cases of infant deaths following accidental head trauma without any sign of abuse. 4.2. A second look at the examination of selected patients The number of postmortem examinations of the optic nerve in our study was low. The reason for this could not be traced. Removal of the eye and the optic nerve, however, has not always been current practice, not even in major forensic departments.52,54 A second look at the five cases shows that all cases involved brain damage, RH and SDH, and an ONSH, as well as obvious signs of external impact all over the body and head. Surprisingly, in none of the five cases has the role of ONSH been a point of interest in the discussion concerning decision making about the cause of the fatal event. The diagnosis of AHT has to be made first.55 The diagnosis could be based on confession as in the cases 1 and 5. Relying on review studies and meta-analyses,56e59 probability studies60 and or prediction analyses61 yields more. Determining the underlying mechanism is a more difficult task. Confession cannot imply a physical mechanism. In case 1 only small dots of RH are found while the SDH was a frontal space-occupying mass in the frontal subdural compartment. Together with the external head lesions and bruises all over the body, in the face and in the sclera these findings are rather characteristic for an severe accidental non-inflicted head trauma23,57,60,62,63 although the presence of few RHs cannot exclude the diagnosis of AHT.64 The confessions of brutal treatment here confirms the inflicted character of this “blunt impact type” AHT. The presence of an ONSH in such a severe impact head trauma is not surprising.
46
M.D. Leeuw et al. / Journal of Forensic and Legal Medicine 36 (2015) 43e48
In the cases 2,3, and 4 an extensive RH, a characteristic film and midline SDH, an apnea ad admission and external visible lesions on the head and the trunk provide a high index of suspicion for an AHT.62 Nevertheless a careful differential diagnosis still needs to be done. An ONSH only but reduces the spectrum of aetiologies to be considered. In case 2 an AHT was diagnosed despite the absence of confessions but a coagulation disorder which could not be investigated further at postmortem was the reason of doubt and withdrawal of the diagnosis of AHT. A similar problem was found in literature in a case where a triad and an ONSH were found after a rather low height fall of a stairway (1.42 m). A mild form of von Willebrand disease Type I was uncovered.65 The allegation of AHT was therefore rejected. However the list of coagulation disorders is extensive and when no previous signs of minor bleedings are reported in an infant or in the family, even in suspicion of AHT, it is a major task which is rarely worthwhile to consider.66 In our case the probability of the presence of an underlying condition predisposing to bleeding was extremely low. Unlike SDH or RH, an ONSH caused by an underlying coagulation disorder has never been mentioned. The authors did not considered an haematological disorder while laboratory investigations during life as well the postmortem histological examinations of all organs did not suggest haematological abnormalities. Furthermore, there was doubt about the dating of the traumatic event due to the different densities in the SDH on the CT scan. The CT scan was not the instrument that contributed to the dating of the initial injury. The combination of fresh, high-density components with older, low-density components may occur very soon after a trauma.67 The reasons not to prosecute the caregivers in this case of a highly suspected AHT were incorrect. ONSH may be caused by the severe traumatic head impact but also shaking is not excluded. The cervical epidural and subdural hemorrhages in case 3 would probably signify forceful movement of the head out of the normal range of motion of the cervical spine. It means that the infant was shaken. Cervical spine injuries are rather rarely reported in AHT suspected cases.68 Given the signs of severe impact on the head with also a skull fracture, most likely both the shaking and the head impact are responsible for the brain and ocular injuries. The diagnostic accuracy for AHT improves when multiple pathologies including RH, ONSH, skull fracture and intracranial hemorrhage are present, and lesions on the cervical spine and its contents may be added to this list.6,53 The complete lack of prosecution in this obvious shaken and impact AHT case 3 is difficult to accept. ONSH may be caused whether by shaking or by impact. In case 4 the occurrence of RH and ONSH, in association with peritonitis with sepsis, might casts some doubt on the diagnosis of a fatal accidental or non-accidental head trauma. In this case, sepsis is the more probable primary cause of death. The correlation between an infectious condition with sepsis and ONSH cannot be considered nonexistent although anecdotal in only one case report. In this case report, already mentioned in the Introduction 39 an incidental congenital disorder of glycosylation was found through a histology of the brain and there were no signs of vasculitis. The case was described as a mimic of a non-accidental injury (NAI). It is understandable that a meningeal infection can continue into the subarachnoidal space around the optic nerve which terminates in the optic nerve head at the lamina cribrosa. Due to this anatomical barrier the retina itself was not involved in the infectious process. Hypothetically, the hemorrhages in the optic nerve sheath accompanied by inflammation of the optic nerve sheath could be compared with the RH that has been correlated with coagulation disorders in the critically ill infant,38 as can occur in sepsis or in a combination of meningitis and sepsis. One could hypothesize that a similar process occurred in the development of ONSH in sepsis.
Therefore, infectious diseases, whether or not they are secondarily involved in a coagulation disorder, must be included in the differential diagnosis on the occurrence of ONSH. Nevertheless the external lesions of head and trunk61 as well as the previous remote fractures in mind, an AHT factor was correctly taken into consideration, with the contribution of ONSH and RH in retrospect being somewhat doubtful. In case 5 the head trauma may be suspected for an AHT since it has been confessed that the head trauma was intentional. Nevertheless the characteristic complex of an extensive, multilayered RH, a film of SDH with extension from the midline, brain damage, apnea57,60,61 are found, as well as remnants of long bone fractures, but in the absence of external impact lesions point to a pure shaking AHT. However also slapping the infant's face with a flat hand before shaking the infant was confessed. Impact to the head with or against an object with a smooth padded surface such as a slap in the face not necessarily cause visible lesions.3,48 It seems however doubtful that a slap in the face should cause an ONSH which more likely has to be expected after severe head impact. In this case, in the absence of natural diseases and signs of impact shaking as cause of the findings as well as of ONSH seemed acceptable. In our limited series of postmortem examinations of AHT cases ONSH occurs in shaking and shaking-impact as well as in pure blunt impact AHT. Its presence does not contribute to the determination of the underlying mechanism of an AHT. Many unanswered questions remain regarding the presence of ONSH in other natural conditions, such as a concurrent infectious disease with sepsis, as well as a secondary coagulation disorder. Moreover, the relationship of the occurrence of ONSH in the presence of a primary coagulation disorder is a totally unknown and remains a less probable natural etiology of ONSH. The limited knowledge on the natural causes of ONSH is due to the factthat the optic nerve cannot be examined in living patients. While RH can be easily detected by fundoscopy, ONSH can only be examined during the postmortem examination. The limited number of ONSH may stem from the completely different anatomical and vascular architecture of the optic nerve, which consists of a heavily myelinated white matter bundle, surrounded by an extension of the intracranial leptomeninges, including the subarachnoidal space. Furthermore, the pathophysiologic mechanisms causing ONSH remain speculative.1,23,48,49 Like for other eye findings such as RH, retinal folds, and retinoschisis caution is urged in interpreting ONSH outside the context until good evidence is available.28,69 5. Conclusion ONSH is a non-specific finding and occurs as a result of both traumatic and non-traumatic etiologies. The clinical significance of ONSH might be that it narrows considerably the differential diagnosis in the work-up of a suspected AHT, given that natural etiologies of RH, SDH and brain damage, substantially exceed those known of ONSH. However the major limitation in this study is the small number of cases in which eyes are removed while the figures also show that the number of cases in which eyes are removed in forensic practice is small and biased towards suspicious head trauma cases, bringing a limitation to the current knowledge of the differential diagnosis list in ONSH. Conflict of interest There is no conflict of interest. Funding None declared.
M.D. Leeuw et al. / Journal of Forensic and Legal Medicine 36 (2015) 43e48
Ethical approval None.
References 1. Squier W. The “shaken baby” syndrome: pathology and mechanisms. Acta Neuropathol 2011;122:519e42. 2. Duhaime A, Gennerelli T, Thibault L, Bruce DA, Margulies SS, Wiser R. The shaken baby syndrome. A clinical, pathological, and biomechanical study. J Neurosurg 1987;66:409e15. 3. Duhaime AC, Christian CW, Rorke LB, Zimmerman RA. Nonaccidental head injury in infantsethe “shaken-baby syndrome”. N Engl J Med 1998;338:1822e9. 4. Lloyd J, Willey EN, Galaznik JG, Lee III WE, Luttner SE. Biomechanical evaluation of head kinematics during infant shaking versus pediatric activities of daily living. J Forensic Biomechanics 2011;2:1e9. 5. Scheimberg I, Mack J. “Shaken baby syndrome” and forensic pathology. Forensic Sci Med Pathol 2014 Jun;10(2):242e3. 6. Squier W. The triad of retinal haemorrhage, subdural haemorrhage and encephalopathy in an infant unassociated with evidence of physical injury is not the result of shaking, but is most likely to have been caused by a natural disease: Yes. J Prim Health Care 2011;3:159e61. 7. Rorke-Adams LB. The triad of retinal haemorrhage, subdural haemorrhage and encephalopathy in an infant unassociated with evidence of physical injury is not the result of shaking, but is most likely to have been caused by a natural disease: No. J Prim Health Care 2011;3:161e3. 8. Godfrey ME. Response to the back to back debate about the effects of shaking a baby, in the absence of any impact trauma. J Prim Health Care 2011;3:253e4. 9. Galaznik JG. Response to the back to back debate about the effects of shaking a baby, in the absence of any impact trauma. J Prim Health Care 2011;3:252e3. 10. Wojcik D. Response to the back to back debate about the effects of shaking a baby, in the absence of any impact trauma. J Prim Health Care 2011;3:253. 11. Goodyear-Smith F. The challenging and complex nature of primary health care. J Prim Health Care 2011;3:178e9. 12. Byard RW. “Shaken baby syndrome” and forensic pathology: an uneasy interface. Forensic Sci Med Pathol 2014;10:239e41. 13. Greeley CS. “Shaken baby syndrome” and forensic pathology. Forensic Sci Med Pathol 2014;10:253e5. 14. Smith C. “Shaken baby syndrome” and forensic pathology. Forensic Sci Med Pathol 2014;10:256e8. 15. Cohen MC, Ramsay DA. “Shaken baby syndrome” and forensic pathology. Forensic Sci Med Pathol 2014;10:244e5. 16. Squier W. “Shaken baby syndrome” and forensic pathology. Forensic Sci Med Pathol 2014;10:248e50. 17. Case M. Shaken baby syndrome” and forensic pathology. Forensic Sci Med Pathol 2014;10:246e7. 18. Sperhake JP, Matschke J. “Shaken baby syndrome” and forensic pathology. Forensic Sci Med Pathol 2014;10:251e2. 19. Finnie JW, Blumbergs PC, Manavis J, Turner RJ, Helps S, Vink R, et al. Neuropathological changes in a lamb model of non-accidental head injury (the shaken baby syndrome). J Clin Neurosci 2012;19:1159e64. 20. Christian CW, Block R. Committee on child abuse and neglect; american academy of pediatrics. Abusive head trauma in infants and children. Pediatrics 2009;123:1409e11. 21. Gauntt CD, Sherry RG, Kannan C. Terson syndrome with bilateral optic nerve sheath hemorrhage. J Neuro Ophthalmol 2007;27:193e4. 22. Kivlin JD, Currie ML, Greenbaum VJ, Simons KB, Jentzen J. Retinal hemorrhages in children following fatal motor vehicle crashes: a case series. Arch Ophthalmol 2008;126:800e4. 23. Wygnanski-Jaffe T, Levin AV, Shafiq A, Smith C, Enzenauer RW, Elder JE, et al. Postmortem orbital findings in shaken baby syndrome. Am J Ophthalmol 2006;142:233e40. 24. Gilliland MGF, Luckenbach MW, Chenier TC. Systemic and ocular findings in 169 prospectively studied child deaths: retinal hemorrhages usually mean child abuse. Forensic Sci Int 1994;68:117e32. 25. Gnanaraj L, Gilliland MG, Yahya RR, Rutka JT, Drake J, et al. Ocular manifestations of crush head injury in children. Eye 2007;21:5e10. 26. Deisch J, Quinton R, Gruszecki AC. Craniocerebral trauma inflicted by television falls. J Forensic Sci 2011;56:1049e53. 27. Platt MS, Stanley C. TV tip-over morbidity and mortality in children. J Forensic Sci 2011;56:1364e7. 28. Lantz PE, Sinal SH, Stanton CA, Weaver Jr RG. Perimacular retinal folds from childhood head trauma. Br Med J 2004;328:754e6. 29. Forbes BJ, Rubin SE, Margolin E, Levin AV. Evaluation and management of retinal hemorrhages in infants with and without abusive head trauma. J AAPOS 2010;14:267e73. 30. Vincent ALV, Kelly P. Retinal haemorrhages in inflicted traumatic brain injury: the ophthalmologist in court. Clin Exp Ophthalmol 2010;38:521e32. 31. Ko F, Knox DL. The ocular pathology of terson's syndrome. Ophthalmology 2010; Jul;(117). 1423e9.e2. 32. Medele RJ, Stummer W, Mueller AJ, Steiger HJ, Reulen HJ. Terson's syndrome in subarachnoid hemorrhage and severe brain injury accompanied by acutely raised intracranial pressure. J Neurosurg 1998;88:851e4.
47
33. Schloff S, Mullaney PB, Armstrong DC, Simantirakis E, Humphreys RP, Myseros JS, et al. Retinal findings in children with intracranial hemorrhage. Ophthalmology 2002;109:1472e6. 34. Levin AV. Retinal hemorrhage in abusive head trauma. Pediatrics 2010;126: 961e70. 35. Mena OJ, Paul I, Reichard RR. Ocular findings in raised intracranial pressure: a case of terson syndrome in a seven-month-old infant. Am J Forensic Med Pathol 2011;32:55e7. 36. Weissgold DJ, Budenz DL, Hood I, Rorke LB. Ruptured vascular malformation masquerading as battered/shaken baby syndrome: a nearly tragic mistake. Surv Ophthalmol 1995;39:509e12. 37. Bhardwaj G, Jacobs MB, Moran KT, Tan K. Terson syndrome with ipsilateral severe hemorrhagic retinopathy in a 7-month-old child. J AAPOS 2010;14: 441e3. 38. Agrawal S, Peters MJ, Adams GG, Pierce CM. Prevalence of retinal hemorrhages in critically ill children. Pediatrics 2012;129:1388e96. 39. Ong BB, Gole GA, Robertson T, McGill J, de Lore D, Crawford M. Retinal hemorrhages associated with meningitis in a child with a congenital disorder of glycosylation. Forensic Sci Med Pathol 2009;5:307e12. 40. Müller PJ, Deck JH. Intraocular and optic nerve sheath hemorrhage in cases of sudden intracranial hypertension. J Neurosurg 1974;41:160e6. 41. Gill JR, Goldfeder LB, Armbrustmacher V, Coleman A, Mena H, Hirsch CS. Fatal head injury in children younger than 2 years in New York city and an overview of the shaken baby syndrome. Arch Pathol Lab Med 2009;133:619e27. 42. Lambert SR, Johnson TE, Hoyt CS. Optic nerve sheath and retinal hemorrhages associated with the shaken baby syndrome. Arch Ophthalmol 1986;104: 1509e12. 43. Budenz D, Farber M, Mirchandani H, Park H, Rorke L. Ocular and optic nerve hemorrhages in abused infants with intracranial injuries. Ophthalmology 1994;101:559e65. 44. Mungan NK. Update on shaken baby syndrome: ophthalmology. Curr Opin Ophthalmol 2007; Sep;18:392e7. 45. Chiesa A, Duhaime AC. Abusive head trauma. Pediatr Clin N. Am 2009;56: 317e31. 46. Coats B, Binenbaum G, Peiffer RL, Forbes BJ, Margulies SS. Ocular hemorrhages in neonatal porcine eyes from single, rapid rotational events. Invest Ophthalmol Vis Sci 2010;51:4792e7. 47. Emerson MV, Jakobs E, Green WR. Ocular autopsy and histopathologic features of child abuse. Ophthalmology 2007;114:1384e94. 48. Case ME. Inflicted traumatic brain injury in infants and young children. Brain Pathol 2008;18:571e82. 49. Wygnanski-Jaffe T, Morad Y, Levin AV. Pathology of retinal hemorrhage in abusive head trauma. Forensic Sci Med Pathol 2009;5:291e7. 50. Gilles EE, McGregor ML, Levy-Clarke G. Retinal hemorrhage asymmetry in inflicted head injury: a clue to pathogenesis? J Pediatr 2003;143:494e9. 51. Kivlin JD, Simons KB, Lazoritz S, Ruttum MS. Shaken baby syndrome. Ophthalmology 2000;107:1246e54. 52. Matschke J, Püschel K, Glatzel M. Ocular pathology in shaken baby syndrome and other forms of infantile non-accidental head injury. Int J Leg Med 2009;123: 189e97. 53. Bhardwaj G, Chowdhury V, Jacobs MB, Moran KT, Martin FJ, Coroneo MT, et al. A systematic review of the diagnostic accuracy of ocular signs in pediatric abusive head trauma. Ophthalmology 2010;117. 983e92.e17. 54. John SM, Jones P, Kelly P, Vincent A. Fatal pediatric head injuries: a 20-year review of cases through the Auckland Coroner's office. Am J Forensic Med Pathol 2013;34:277e82. 55. Narang S, Clarke J. Abusive head trauma: past, present, and future. J Child Neurol 2014;29:1747e56. 56. Piteau SJ, Ward MG, Barrowman NJ, Plint AC. Clinical and radiographic characteristics associated with abusive and nonabusive head trauma: a systematic review. Pediatrics 2012;130:315e23. 57. Maguire SA, Watts PO, Shaw AD, Holden S, Taylor RH, Watkins WJ, et al. Retinal haemorrhages and related findings in abusive and non-abusive head trauma:a systematic review. Eye 2013;27:28e36. 58. Maguire S, Pickerd N, Farewell D, Mann M, Tempest V, Kemp AM. Which clinical features distinguish inflicted from non-inflicted brain injury? A systematic review. Arch Dis Child 2009;94:860e7. 59. Kemp AM, Jaspan T, Griffiths J, Stoodley N, Mann MK, Tempest V, et al. Neuroimaging: what neuroradiological features distinguish abusive from non-abusive head trauma? A systematic review. Arch Dis Child 2011;96: 1103e12. 60. Maguire SA, Kemp AM, Lumb RC, Farewell DM. Estimating the probability of abusive head trauma: a pooled analysis. Pediatrics 2011;128. e550e64. 61. Hymel KP, Armijo-Garcia V, Foster R, Frazier TN, Stoiko M, Christie LM, et al. Pediatric brain injury research network (PediBIRN) investigators. Validation of a clinical prediction rule for pediatric abusive head trauma. Pediatrics 2014;134. e1537e44. 62. Vinchon M, Defoort-Dhellemmes S, Desurmont M, Dhellemmes P. Accidental and nonaccidental head injuries in infants: a prospective study. J Neurosurg 2005;102:380e4. 63. Vinchon M, de Foort-Dhellemmes S, Desurmont M, Delestret I. Confessed abuse versus witnessed accidents in infants: comparison of clinical, radiological, and ophthalmological data in corroborated cases. Child Nerv Syst 2010;26:637e45.
48
M.D. Leeuw et al. / Journal of Forensic and Legal Medicine 36 (2015) 43e48
64. Margolin EA, Dev LS, Trobe JD. Prevalence of retinal hemorrhages in perpetrator-confessed cases of abusive head trauma. Arch Ophthalmol 2010;128:795. 65. Lantz PE, Couture DE. Fatal acute intracranial injury, subdural hematoma, and retinal hemorrhages caused by stairway fall. J Forensic Sci 2011;56:1648e53. 66. Carpenter SL, Abshire TC, Anderst JD. Section on hematology/oncology and committee on child abuse and neglect of the American Academy of Pediatrics. Evaluating for suspected child abuse: conditions that predispose to bleeding. Pediatrics 2013;131. e1357e73.
67. Adamsbaum C, Grabar S, Mejean N, Rey-Salmon C. Abusive head trauma: judicial admissions highlight violent and repetitive shaking. Pediatrics 2010;126:546e55. 68. Bandak FA. Shaken baby syndrome: a biomechanics analysis of injury mechanisms. Forensic Sci Int 2005;151:71e9. 69. Oshima T, Yoshikawa H, Ohtani M, Mimasaka S. Examination of postmortem retinal folds: a non-invasive study. J Forensic Leg Med 2015;30:16e20.