Acta Neuropathologica

, 122:519 | Cite as

The “Shaken Baby” syndrome: pathology and mechanisms

  • Waney Squier


The “Shaken Baby” syndrome (SBS) is the subject of intense controversy; the diagnosis has in the past depended on the triad of subdural haemorrhage (SDH), retinal haemorrhage and encephalopathy. While there is no doubt that infants do suffer abusive injury at the hands of their carers and that impact can cause catastrophic intracranial damage, research has repeatedly undermined the hypothesis that shaking per se can cause this triad. The term non-accidental head injury has therefore been widely adopted. This review will focus on the pathology and mechanisms of the three physiologically associated findings which constitute the “triad” and are seen in infants suffering from a wide range of non-traumatic as well as traumatic conditions. “Sub” dural bleeding in fact originates within the deep layers of the dura. The potential sources of SDH include: the bridging veins, small vessels within the dura itself, a granulating haemorrhagic membrane and ruptured intracranial aneurysm. Most neuropathologists do not routinely examine eyes, but the significance of this second arm of the triad in the diagnosis of Shaken Baby syndrome is such that it merits consideration in the context of this review. While retinal haemorrhage can be seen clinically, dural and subarachnoid optic nerve sheath haemorrhage is usually seen exclusively by the pathologist and only rarely described by the neuroradiologist. The term encephalopathy is used loosely in the context of SBS. It may encompass anything from vomiting, irritability, feeding difficulties or floppiness to seizures, apnoea and fulminant brain swelling. The spectrum of brain pathology associated with retinal and subdural bleeding from a variety of causes is described. The most important cerebral pathology is swelling and hypoxic–ischaemic injury. Mechanical shearing injury is rare and contusions, the hallmark of adult traumatic brain damage, are vanishingly rare in infants under 1 year of age. Clefts and haemorrhages in the immediate subcortical white matter have been assumed to be due to trauma but factors specific to this age group offer other explanations. Finally, examples of the most common causes of the triad encountered in clinical diagnostic and forensic practice are briefly annotated.


Shaken baby syndrome Subdural haemorrhage Retinal haemorrhage Infant encephalopathy Axonal injury Subcortical haemorrhage Cerebral venous sinus thrombosis Subpial haemorrhage 



I am deeply indebted to Horace Gardner for assisting me with the section on retinal haemorrhages, to Julie Mack for providing images of brain scans and for helpful criticism and advice. Drs. Dirk Van Varenbergh, Alex Michotte and Michel Piette kindly sent me the case illustrated in Fig. 15 and Pat Lantz sent image 4b and helpful comments. John Plunkett and Jan Leestma made helpful comments on the manuscript. Above all I am grateful to the parents who have allowed me to study their babies’ brains and have contributed so much to our learning.


  1. 1.
    Adams JH, Graham DI, Murray LS, Scott G (1982) Diffuse axonal injury due to nonmissile head injury in humans: an analysis of 45 cases. Ann Neurol 12:557–563PubMedCrossRefGoogle Scholar
  2. 2.
    Adamsbaum C, Grabar S, Mejean N, Rey-Salmon C (2010) Abusive head trauma: judicial admissions highlight violent and repetitive shaking. Pediatrics 126:546–555PubMedCrossRefGoogle Scholar
  3. 3.
    Aoki N, Masuzawa H (1984) Infantile acute subdural hematoma. Clinical analysis of 26 cases. J Neurosurg 61:273–280PubMedCrossRefGoogle Scholar
  4. 4.
    Aoki N (1990) Chronic subdural hematoma in infancy. Clinical analysis of 30 cases in the CT era. J Neurosurg 73:201–205PubMedCrossRefGoogle Scholar
  5. 5.
    Arbogast KB, Margulies SS, Christian CW (2005) Initial neurologic presentation in young children sustaining inflicted and unintentional fatal head injuries. Pediatrics 116:180–184PubMedCrossRefGoogle Scholar
  6. 6.
    Au-Yong IT, Wardle SP, McConachie NS, Jaspan T (2009) Isolated cerebral cortical tears in children: aetiology, characterisation and differentiation from non-accidental head injury. Br J Radiol 82:735–741PubMedCrossRefGoogle Scholar
  7. 7.
    Auer LM, Ishiyama N, Hodde KC, Kleinert R, Pucher R (1987) Effect of intracranial pressure on bridging veins in rats. J Neurosurg 67:263–268PubMedCrossRefGoogle Scholar
  8. 8.
    Barnes PD (2011) Imaging of nonaccidental injury and the mimics: issues and controversies in the era of evidence-based medicine. Radiol Clin North Am 49:205–229PubMedCrossRefGoogle Scholar
  9. 9.
    Bell JE (2005) The Neuropathology of non-accidental head injury. In: Minns R (ed) Shaking and other non-accidental head injuries in children. Mac Keith, LondonGoogle Scholar
  10. 10.
    Berfelo FJ, Kersbergen KJ, van Ommen CH, Govaert P, van Straaten HL, Poll-The BT, van Wezel-Meijler G, Vermeulen RJ, Groenendaal F, de Vries LS, de Haan TR (2010) Neonatal cerebral sinovenous thrombosis from symptom to outcome. Stroke 41:1382–1388PubMedCrossRefGoogle Scholar
  11. 11.
    Bhardwaj G, Chowdhury V, Jacobs MB, Moran KT, Martin FJ, Coroneo MT (2010) A systematic review of the diagnostic accuracy of ocular signs in pediatric abusive head trauma. Ophthalmology 117:983–992, e917Google Scholar
  12. 12.
    Boyle JD, Boyle EM (2011) Born just a few weeks early: does it matter? Arch Dis Child Fetal Neonatal EdGoogle Scholar
  13. 13.
    Brennan LK, Rubin D, Christian CW, Duhaime AC, Mirchandani HG, Rorke-Adams LB (2009) Neck injuries in young pediatric homicide victims. J Neurosurg Pediatr 3:232–239PubMedCrossRefGoogle Scholar
  14. 14.
    Browder J, Kaplan HA, Krieger AJ (1975) Venous lakes in the suboccipital dura mater and falx cerebelli of infants: surgical significance. Surg Neurol 4:53–55PubMedGoogle Scholar
  15. 15.
    Buis DR, van Ouwerkerk WJ, Takahata H, Vandertop WP (2006) Intracranial aneurysms in children under 1 year of age: a systematic review of the literature. Childs Nerv Syst 22:1395–1409PubMedCrossRefGoogle Scholar
  16. 16.
    Byard RW, Blumbergs P, Rutty G, Sperhake J, Banner J, Krous HF (2007) Lack of evidence for a causal relationship between hypoxic–ischemic encephalopathy and subdural hemorrhage in fetal life, infancy, and early childhood. Pediatr Dev Pathol 10:348–350PubMedCrossRefGoogle Scholar
  17. 17.
    Caffey J (1972) On the theory and practice of shaking infants. Its potential residual effects of permanent brain damage and mental retardation. Am J Dis Child 124:161–169PubMedGoogle Scholar
  18. 18.
    Caffey J (1974) The whiplash shaken infant syndrome: manual shaking by the extremities with whiplash-induced intracranial and intraocular bleedings, linked with residual permanent brain damage and mental retardation. Pediatrics 54:396–403PubMedGoogle Scholar
  19. 19.
    Caldarelli M, Di RC, Romani R (2002) Surgical treatment of chronic subdural hygromas in infants and children. Acta Neurochir (Wien) 144:581–588CrossRefGoogle Scholar
  20. 20.
    Calder IM, Hill I, Scholtz CL (1984) Primary brain trauma in non-accidental injury. J ClinPathol 37:1095–1100CrossRefGoogle Scholar
  21. 21.
    Cantu RC, Gean AD (2010) Second-impact syndrome and a small subdural hematoma: an uncommon catastrophic result of repetitive head injury with a characteristic imaging appearance. J Neurotrauma 27:1557–1564PubMedCrossRefGoogle Scholar
  22. 22.
    Case ME, Graham MA, Handy TC, Jentzen JM, Monteleone JA (2001) Position paper on fatal abusive head injuries in infants and young children. Am J Forensic Med Pathol 22:112–122PubMedCrossRefGoogle Scholar
  23. 23.
    Case ME (2007) Abusive head injuries in infants and young children. Leg Med (Tokyo) 9:83–87CrossRefGoogle Scholar
  24. 24.
    Chamnanvanakij S, Rollins N, Perlman JM (2002) Subdural hematoma in term infants. Pediatr Neurol 26:301–304PubMedCrossRefGoogle Scholar
  25. 25.
    Chen XH, Johnson VE, Uryu K, Trojanowski JQ, Smith DH (2009) A lack of amyloid beta plaques despite persistent accumulation of amyloid beta in axons of long-term survivors of traumatic brain injury. Brain Pathol 19:214–223PubMedCrossRefGoogle Scholar
  26. 26.
    Christian CW, Taylor AA, Hertle RW, Duhaime AC (1999) Retinal hemorrhages caused by accidental household trauma. J Pediatr 135:125–127PubMedCrossRefGoogle Scholar
  27. 27.
    Christian CW, Block R (2009) Abusive head trauma in infants and children. Pediatrics 123:1409–1411PubMedCrossRefGoogle Scholar
  28. 28.
    Cohen MC, Scheimberg I (2008) Evidence of occurrence of intradural and subdural hemorrhage in the perinatal and neonatal period in the context of hypoxic ischemic encephalopathy. An observational study from two referral institutions in the United Kingdom. Pediatr Dev Pathol 1Google Scholar
  29. 29.
    Cohen MC, Sprigg A, Whitby EH (2010) Subdural hemorrhage, intradural hemorrhage and hypoxia in the pediatric and perinatal post mortem: are they related? An observational study combining the use of post mortem pathology and magnetic resonance imaging. Forensic SciInt 200:100–107CrossRefGoogle Scholar
  30. 30.
    Colbert CA, Holshouser BA, Aaen GS, Sheridan C, Oyoyo U, Kido D, Ashwal S (2010) Value of cerebral microhemorrhages detected with susceptibility-weighted MR Imaging for prediction of long-term outcome in children with nonaccidental trauma. Radiology 256:898–905PubMedCrossRefGoogle Scholar
  31. 31.
    Cory CZ, Jones BM (2003) Can shaking alone cause fatal brain injury? A biomechanical assessment of the Duhaime shaken baby syndrome model. Med Sci Law 43:317–333PubMedCrossRefGoogle Scholar
  32. 32.
    Crown Prosecution S (2011) Non-accidental head injury (nahi, formerly referred to as shaken baby syndrome [SBS])—prosecution approach.
  33. 33.
    Cushing H, In Goodrich JT (2000) Reprint of “concerning surgical intervention for the intracranial hemorrhages of the new-born” by Harvey Cushing, M.D. 1905. Childs Nerv Syst 16:484–492PubMedCrossRefGoogle Scholar
  34. 34.
    Dandy W (1929) Where is cerebrospinal fluid absorbed? J Am Med AssocGoogle Scholar
  35. 35.
    Dias MS (2010) The case for shaking. In: Jenny C (ed) Child abuse and neglect. Elsevier SaundersGoogle Scholar
  36. 36.
    Dolinak D, Smith C, Graham DI (2000) Hypoglycaemia is a cause of axonal injury. Neuropathol Appl Neurobiol 26:448–453PubMedCrossRefGoogle Scholar
  37. 37.
    Duhaime AC, Gennarelli TA, Thibault LE, Bruce DA, Margulies SS, Wiser R (1987) The shaken baby syndrome. A clinical, pathological, and biomechanical study. J Neurosurg 66:409–415PubMedCrossRefGoogle Scholar
  38. 38.
    Duhaime AC, Gennarelli TA, Sutton LN, Schut L (1988) “Shaken baby syndrome”: A misnomer? J Pediatr Neurosci 4:77–86Google Scholar
  39. 39.
    Duhaime AC, Alario AJ, Lewander WJ, Schut L, Sutton LN, Seidl TS, Nudelman S, Budenz D, Hertle R, Tsiaras W (1992) Head injury in very young children: mechanisms, injury types, and ophthalmologic findings in 100 hospitalized patients younger than 2 years of age. Pediatrics 90:179–185PubMedGoogle Scholar
  40. 40.
    Duhaime AC, Christian CW, Rorke LB, Zimmerman RA (1998) Nonaccidental head injury in infants–the “shaken-baby syndrome”. N Engl J Med 338:1822–1829PubMedCrossRefGoogle Scholar
  41. 41.
    Dupuis O, Silveira R, Dupont C, Mottolese C, Kahn P, Dittmar A, Rudigoz RC (2005) Comparison of “instrument-associated” and “spontaneous” obstetric depressed skull fractures in a cohort of 68 neonates 2. Am J Obstet Gynecol 192:165–170PubMedCrossRefGoogle Scholar
  42. 42.
    Ebbs Justice D (2011) Report to the attorney general: Shaken baby death review. OntarioGoogle Scholar
  43. 43.
    Edlow JA, Caplan LR (2000) Avoiding pitfalls in the diagnosis of subarachnoid hemorrhage. N Engl J Med 342:29–36PubMedCrossRefGoogle Scholar
  44. 44.
    Eichler F, Krishnamoorthy K, Grant PE (2007) Magnetic resonance imaging evaluation of possible neonatal sinovenous thrombosis. Pediatr Neurol 37:317–323PubMedCrossRefGoogle Scholar
  45. 45.
    Eisenbrey AB (1979) Retinal hemorrhage in the battered child. Childs Brain 5:40–44PubMedGoogle Scholar
  46. 46.
    Emerson MV, Jakobs E, Green WR (2007) Ocular autopsy and histopathologic features of child abuse. Ophthalmology 114:1384–1394PubMedCrossRefGoogle Scholar
  47. 47.
    Ewing-Cobbs L, Prasad M, Kramer L, Louis PT, Baumgartner J, Fletcher JM, Alpert B (2000) Acute neuroradiologic findings in young children with inflicted or noninflicted traumatic brain injury. Childs NervSyst 16:25–33CrossRefGoogle Scholar
  48. 48.
    Feng JF, Jiang JY, Bao YH, Liang YM, Pan YH (2008) Traumatic subdural effusion evolves into chronic subdural hematoma: Two stages of the same inflammatory reaction? Med Hypotheses 70:1147–1149PubMedCrossRefGoogle Scholar
  49. 49.
    Fineschi V, Turillazzi E, Neri M, Pomara C, Riezzo I (2009) Histological age determination of venous thrombosis: a neglected forensic task in fatal pulmonary thrombo-embolism. Forensic SciInt 186:22–28CrossRefGoogle Scholar
  50. 50.
    Fox RJ (1996) Anatomic details of intradural channels in the parasagittal dura: a possible pathway for flow of cerebrospinal fluid. Neurosurgery 39:84–91PubMedCrossRefGoogle Scholar
  51. 51.
    Frasier L et al. (2006) In: Frasier L (ed) Abusive head trauma in infants and children, G W MedicalGoogle Scholar
  52. 52.
    Friede RL (1972) Subpial hemorrhage in infants. J Neuropathol Exp Neurol 31:548–556PubMedCrossRefGoogle Scholar
  53. 53.
    Friede RL (1989) Subdural haematomas, hygromas and effusions. In: Friede RL (ed) Developmental neuropathology. Springer, Gottingen, pp 198–208Google Scholar
  54. 54.
    Gage LJ, Harris RV et al (2005) EWCA. Crim 1980Google Scholar
  55. 55.
    Gardner HB (2007) A witnessed short fall mimicking presumed shaken baby syndrome (inflicted childhood neurotrauma). Pediatr Neurosurg 43:433–435PubMedCrossRefGoogle Scholar
  56. 56.
    Geddes JF, Vowles GH, Beer TW, Ellison DW (1997) The diagnosis of diffuse axonal injury: implications for forensic practice. Neuropathol Appl Neurobiol 23:339–347PubMedCrossRefGoogle Scholar
  57. 57.
    Geddes JF, Hackshaw AK, Vowles GH, Nickols CD, Whitwell HL (2001) Neuropathology of inflicted head injury in children. I. Patterns of brain damage. Brain 124:1290–1298PubMedCrossRefGoogle Scholar
  58. 58.
    Geddes JF, Vowles GH, Hackshaw AK, Nickols CD, Scott IS, Whitwell HL (2001) Neuropathology of inflicted head injury in children. II. Microscopic brain injury in infants. Brain 124:1299–1306PubMedCrossRefGoogle Scholar
  59. 59.
    Geddes JF, Tasker RC, Hackshaw AK, Nickols CD, Adams GG, Whitwell HL, Scheimberg I (2003) Dural haemorrhage in non-traumatic infant deaths: does it explain the bleeding in ‘shaken baby syndrome?’. Neuropathol Appl Neurobiol 29:14–22PubMedCrossRefGoogle Scholar
  60. 60.
    Ghosh PS, Ghosh D (2011) Subdural hematoma in infants without accidental or nonaccidental injury: benign external hydrocephalus, a risk factor. Clin PediatrGoogle Scholar
  61. 61.
    Gilles EE, McGregor ML, Levy-Clarke G (2003) Retinal hemorrhage asymmetry in inflicted head injury: a clue to pathogenesis? J Pediatr 143:494–499PubMedCrossRefGoogle Scholar
  62. 62.
    Gorini C, Philbin K, Bateman R, Mendelowitz D (2010) Endogenous inhibition of the trigeminally evoked neurotransmission to cardiac vagal neurons by muscarinic acetylcholine receptors. J Neurophysiol 104:1841–1848PubMedCrossRefGoogle Scholar
  63. 63.
    Guthkelch AN (1971) Infantile subdural haematoma and its relationship to whiplash injuries. Br Med J 2:430–431PubMedCrossRefGoogle Scholar
  64. 64.
    Hadley MN, Sonntag VK, Rekate HL, Murphy A (1989) The infant whiplash-shake injury syndrome: a clinical and pathological study. Neurosurgery 24:536–540PubMedCrossRefGoogle Scholar
  65. 65.
    Haines DE, Harkey HL, al Mefty O (1993) The “subdural” space: a new look at an outdated concept. Neurosurgery 32:111–120PubMedCrossRefGoogle Scholar
  66. 66.
    Hall JR, Reyes HM, Horvat M, Meller JL, Stein R (1989) The mortality of childhood falls. J Trauma 29:1273–1275PubMedCrossRefGoogle Scholar
  67. 67.
    Hershkovitz I, Greenwald C, Rothschild BM, Latimer B, Dutour O, Jellema LM, Wish-Baratz S, Pap I, Leonetti G (1999) The elusive diploic veins: anthropological and anatomical perspective. AmJ Phys Anthropol 108:345–358CrossRefGoogle Scholar
  68. 68.
    Herzberger E, Rotem Y, Braham J (1956) Remarks on thirty-three cases of subdural effusion in infancy. Arch Dis Child 31:44–50PubMedCrossRefGoogle Scholar
  69. 69.
    Hobbs C, Childs AM, Wynne J, Livingston J, Seal A (2005) Subdural haematoma and effusion in infancy: an epidemiological study. Arch Dis Child 90:952–955PubMedCrossRefGoogle Scholar
  70. 70.
    Holbourn A (1943) Mechanics of head injuries. The Lancet:438Google Scholar
  71. 71.
    Hoogstraate SR, Lequin MH, Huysman MA, Ahmed S, Govaert PP (2009) Apnoea in relation to neonatal temporal lobe haemorrhage. Eur J Paediatr Neurol 13:356–361PubMedCrossRefGoogle Scholar
  72. 72.
    Hortobagyi T, Wise S, Hunt N, Cary N, Djurovic V, Fegan-Earl A, Shorrock K, Rouse D, Al Sarraj S (2007) Traumatic axonal damage in the brain can be detected using beta-APP immunohistochemistry within 35 min after head injury to human adults 1. Neuropathol Appl Neurobiol 33:226–237PubMedCrossRefGoogle Scholar
  73. 73.
    Huang AH, Robertson RL (2004) Spontaneous superficial parenchymal and leptomeningeal hemorrhage in term neonates. AJNR Am J Neuroradiol 25:469–475PubMedGoogle Scholar
  74. 74.
    Hurley M, Dineen R, Padfield CJ, Wilson S, Stephenson T, Vyas H, McConachie N, Jaspan T (2010) Is there a causal relationship between the hypoxia-ischaemia associated with cardiorespiratory arrest and subdural haematomas? An observational study. Br J Radiol 83:736–743PubMedCrossRefGoogle Scholar
  75. 75.
    Hwang SK, Kim SL (2000) Infantile head injury, with special reference to the development of chronic subdural hematoma. Childs Nerv Syst 16:590–594PubMedCrossRefGoogle Scholar
  76. 76.
    Hymel KP, Jenny C, Block RW (2002) Intracranial hemorrhage and rebleeding in suspected victims of abusive head trauma: addressing the forensic controversies. Child Maltreat 7:329–348PubMedCrossRefGoogle Scholar
  77. 77.
    Ikeda A, Sato O, Tsugane R, Shibuya N, Yamamoto I, Shimoda M (1987) Infantile acute subdural hematoma. Childs Nerv Syst 3:19–22PubMedCrossRefGoogle Scholar
  78. 78.
    Jaspan T, Narborough G, Punt JA, Lowe J (1992) Cerebral contusional tears as a marker of child abuse—detection by cranial sonography. Pediatr Radiol 22:237–245PubMedCrossRefGoogle Scholar
  79. 79.
    Johnson MW, Stoll L, Rubio A, Troncoso J, Pletnikova O, Fowler DR, Li L (2011) Axonal injury in young pediatric head trauma: a comparison study of beta-amyloid precursor protein (beta-APP) immunohistochemical staining in traumatic and nontraumatic deaths*. J Forensic SciGoogle Scholar
  80. 80.
    Johnston M, Armstrong D, Koh L (2007) Possible role of the cavernous sinus veins in cerebrospinal fluid absorption. Cerebrospinal Fluid Res 4:3PubMedCrossRefGoogle Scholar
  81. 81.
    Keeling J (2009) Paediatric forensic medicine and pathology. Edward ArnoldGoogle Scholar
  82. 82.
    Keeling JW (1993) Fetal and neonatal pathology. Springer, LondonGoogle Scholar
  83. 83.
    Kinney HC, Thach BT (2009) The sudden infant death syndrome. N Engl J Med 361:795–805PubMedCrossRefGoogle Scholar
  84. 84.
    Kinney HC, Broadbelt KG, Haynes RL, Rognum IJ, Paterson DS (2011) The serotonergic anatomy of the developing human medulla oblongata: implications for pediatric disorders of homeostasis. J Chem Neuroanat 41:182–199PubMedCrossRefGoogle Scholar
  85. 85.
    Kors EE, Terwindt GM, Vermeulen FL, Fitzsimons RB, Jardine PE, Heywood P, Love S, van den Maagdenberg AM, Haan J, Frants RR, Ferrari MD (2001) Delayed cerebral edema and fatal coma after minor head trauma: role of the CACNA1A calcium channel subunit gene and relationship with familial hemiplegic migraine. Ann Neurol 49:753–760PubMedCrossRefGoogle Scholar
  86. 86.
    Koumellis P, McConachie NS, Jaspan T (2008) Spinal subdural hematomas in children with non accidental head injury. Arch Dis ChildGoogle Scholar
  87. 87.
    Lantz PE, Stanton CA (2006) Postmortem detection and evaluation of retinal hemorrhages. Am Acad Forensic Sci 271Google Scholar
  88. 88.
    Lapillonne A (2010) Vitamin D deficiency during pregnancy may impair maternal and fetal outcomes. Med Hypotheses 74:71–75PubMedCrossRefGoogle Scholar
  89. 89.
    Larroche J-C (1977) Lesions of haemorrhagic type, mainly venous. Developmental pathology of the neonate. Excerpta Medica, Amsterdam, pp 355–398Google Scholar
  90. 90.
    Leach JL, Fortuna RB, Jones BV, Gaskill-Shipley MF (2006) Imaging of cerebral venous thrombosis: current techniques, spectrum of findings, and diagnostic pitfalls. Radiographics: a review publication of the Radiological Society of North America, Inc 26(Suppl 1):S19–S41; discussion S42–13Google Scholar
  91. 91.
    Leestma JE (2005) Case analysis of brain-injured admittedly shaken infants: 54 cases, 1969–2001. Am J Forensic Med Pathol 26:199–212PubMedCrossRefGoogle Scholar
  92. 92.
    Leestma JE (2009) Forensic neuropathology. CRC Press, Taylor and Francis GroupGoogle Scholar
  93. 93.
    Levin AV, Forbes B, Alexander R, Jenny C (2010) Information statement. Abusive head trauma/shaken baby syndrome. American Academy of Ophthalmology, San FranciscoGoogle Scholar
  94. 94.
    Lindenberg R, Freytag E (1969) Morphology of brain lesions from blunt trauma in early infancy. Arch Pathol 87:298–305PubMedGoogle Scholar
  95. 95.
    Loh JK, Lin CL, Kwan AL, Howng SL (2002) Acute subdural hematoma in infancy. Surg Neurol 58:218–224PubMedCrossRefGoogle Scholar
  96. 96.
    Looney CB, Smith JK, Merck LH, Wolfe HM, Chescheir NC, Hamer RM, Gilmore JH (2007) Intracranial hemorrhage in asymptomatic neonates: prevalence on MR images and relationship to obstetric and neonatal risk factors. Radiology 242:535–541PubMedCrossRefGoogle Scholar
  97. 97.
    Lu H, Zhao J, Li M, Cheng Y, Li Y, You X, Zhao Y (2010) Microvessel changes after post-ischemic benign and malignant hyperaemia: experimental study in rats. BMC Neurol 10:24PubMedCrossRefGoogle Scholar
  98. 98.
    Mack J, Squier W, Eastman JT (2009) Anatomy and development of the meninges: implications for subdural collections and CSF circulation. Pediatr Radiol 39:200–210PubMedCrossRefGoogle Scholar
  99. 99.
    Maguire S, Pickerd N, Farewell D, Mann M, Tempest V, Kemp AM (2009) Which clinical features distinguish inflicted from non-inflicted brain injury? A systematic review. Arch Dis Child 94:860–867PubMedCrossRefGoogle Scholar
  100. 100.
    Manole MD, Kochanek PM, Fink EL, Clark RS (2009) Postcardiac arrest syndrome: focus on the brain. Curr Opin Pediatr 21:745–750PubMedCrossRefGoogle Scholar
  101. 101.
    Marmarou A (2007) A review of progress in understanding the pathophysiology and treatment of brain edema. Neurosurg Focus 22:E1Google Scholar
  102. 102.
    Matshes E (2010) Retinal and optic nerve sheath haemorrhages are not pathognomonic of abusive head injury. Abstract American Association of Forensic Sciences ConferenceGoogle Scholar
  103. 103.
    Matshes E, Rea E (2011) Shaken infants die of neck trauma, not brain trauma. Acad Forensic Pathol 1:b–kGoogle Scholar
  104. 104.
    Maxeiner H (1997) Detection of ruptured cerebral bridging veins at autopsy. Forensic SciInt 89:103–110CrossRefGoogle Scholar
  105. 105.
    Maxeiner H (2001) Demonstration and interpretation of bridging vein ruptures in cases of infantile subdural bleedings. J Forensic Sci 46:85–93PubMedGoogle Scholar
  106. 106.
    McLellan NJ, Prasad R, Punt J (1986) Spontaneous subhyaloid and retinal haemorrhages in an infant. Arch Dis Child 61:1130–1132PubMedCrossRefGoogle Scholar
  107. 107.
    McNeely PD, Atkinson JD, Saigal G, O’Gorman AM, Farmer JP (2006) Subdural hematomas in infants with benign enlargement of the subarachnoid spaces are not pathognomonic for child abuse. AJNR Am J Neuroradiol 27:1725–1728PubMedGoogle Scholar
  108. 108.
    Menkes JH, Sarnat HB, Maria BL (2006) Child neurology, 7th ednGoogle Scholar
  109. 109.
    Moharir MD, Shroff M, Stephens D, Pontigon AM, Chan A, MacGregor D, Mikulis D, Adams M, DeVeber G (2010) Anticoagulants in pediatric cerebral sinovenous thrombosis: a safety and outcome study. Ann Neurol 67:590–599PubMedGoogle Scholar
  110. 110.
    Mokri B, Parisi JE, Scheithauer BW, Piepgras DG, Miller GM (1995) Meningeal biopsy in intracranial hypotension: meningeal enhancement on MRI. Neurology 45:1801–1807PubMedGoogle Scholar
  111. 111.
    Molina DK, Clarkson A, Farley KL, Farley NJ (2011) A review of blunt force injury homicides of children aged 0 to 5 years in Bexar County, Texas, from 1988 to 2009. Am J Forensic Med PatholGoogle Scholar
  112. 112.
    Mori T, Katayama Y, Kawamata T (2006) Acute hemispheric swelling associated with thin subdural hematomas: pathophysiology of repetitive head injury in sports. Acta Neurochir Suppl 96:40–43PubMedCrossRefGoogle Scholar
  113. 113.
    Muller PJ, Deck JH (1974) Intraocular and optic nerve sheath hemorrhage in cases of sudden intracranial hypertension. J Neurosurg 41:160–166PubMedCrossRefGoogle Scholar
  114. 114.
    Munro D, Merrit HH (1936) Surgical pathology of subdural hematoma. Based on a study of one hundred and five cases. Arch Neurol Psychiatry 35:64–78Google Scholar
  115. 115.
    Nosaka M, Ishida Y, Kimura A, Kondo T (2009) Time-dependent appearance of intrathrombus neutrophils and macrophages in a stasis-induced deep vein thrombosis model and its application to thrombus age determination. IntJ Legal Med 123:235–240CrossRefGoogle Scholar
  116. 116.
    Nosaka M, Ishida Y, Kimura A, Kondo T (2010) Time-dependent organic changes of intravenous thrombi in stasis-induced deep vein thrombosis model and its application to thrombus age determination. Forensic SciInt 195:143–147CrossRefGoogle Scholar
  117. 117.
    Oehmichen M, Schleiss D, Pedal I, Saternus KS, Gerling I, Meissner C (2008) Shaken baby syndrome: re-examination of diffuse axonal injury as cause of death. Acta Neuropathol 116:317–329PubMedCrossRefGoogle Scholar
  118. 118.
    Oi S, Di Rocco C (2006) Proposal of “evolution theory in cerebrospinal fluid dynamics” and minor pathway hydrocephalus in developing immature brain. Childs NervSyst 22:662–669CrossRefGoogle Scholar
  119. 119.
    Ommaya AK, Goldsmith W, Thibault L (2002) Biomechanics and neuropathology of adult and paediatric head injury. Br J Neurosurg 16:220–242PubMedCrossRefGoogle Scholar
  120. 120.
    Papaiconomou C, Zakharov A, Azizi N, Djenic J, Johnston M (2004) Reassessment of the pathways responsible for cerebrospinal fluid absorption in the neonate. Childs Nerv Syst 20:29–36PubMedCrossRefGoogle Scholar
  121. 121.
    Papasian NC, Frim DM (2000) A theoretical model of benign external hydrocephalus that predicts a predisposition towards extra-axial hemorrhage after minor head trauma. Pediatr Neurosurg 33:188–193PubMedCrossRefGoogle Scholar
  122. 122.
    Park CK, Choi KH, Kim MC, Kang JK, Choi CR (1994) Spontaneous evolution of posttraumatic subdural hygroma into chronic subdural haematoma. Acta Neurochir (Wien) 127:41–47CrossRefGoogle Scholar
  123. 123.
    Pittman T (2003) Significance of a subdural hematoma in a child with external hydrocephalus. Pediatr Neurosurg 39:57–59PubMedCrossRefGoogle Scholar
  124. 124.
    Plunkett J (1999) Sudden death in an infant caused by rupture of a basilar artery aneurysm. Am J Forensic Med Pathol 20:211–214PubMedCrossRefGoogle Scholar
  125. 125.
    Prange MT, Coats B, Duhaime AC, Margulies SS (2003) Anthropomorphic simulations of falls, shakes, and inflicted impacts in infants. J Neurosurg 99:143–150PubMedCrossRefGoogle Scholar
  126. 126.
    Ramenghi LA, Govaert P, Fumagalli M, Bassi L, Mosca F (2009) Neonatal cerebral sinovenous thrombosis. Semin Fetal Neonatal Med 14:278–283PubMedCrossRefGoogle Scholar
  127. 127.
    Reddie IC, Bhardwaj G, Dauber SL, Jacobs MB, Moran KT (2010) Bilateral retinoschisis in a 2-year-old following a three-storey fall. Eye (Lond) 24:1426–1427CrossRefGoogle Scholar
  128. 128.
    Reichard RR, Smith C, Graham DI (2005) The significance of beta-APP immunoreactivity in forensic practice. Neuropathol Appl Neurobiol 31:304–313PubMedCrossRefGoogle Scholar
  129. 129.
    Richardson JD, Vasko MR (2002) Cellular mechanisms of neurogenic inflammation. J Pharmacol Exp Ther 302:839–845PubMedCrossRefGoogle Scholar
  130. 130.
    Roach ES, Golomb MR, Adams R, Biller J, Daniels S, DeVeber G, Ferriero D, Jones BV, Kirkham FJ, Scott RM, Smith ER (2008) Management of stroke in infants and children: a scientific statement from a Special Writing Group of the American Heart Association Stroke Council and the Council on Cardiovascular Disease in the Young. Stroke 39:2644–2691PubMedCrossRefGoogle Scholar
  131. 131.
    Rogers CB, Itabashi HH, Tomiyasu U, Heuser ET (1998) Subdural neomembranes and sudden infant death syndrome. JForensic Sci 43:375–376Google Scholar
  132. 132.
    Rooks VJ, Eaton JP, Ruess L, Petermann GW, Keck-Wherley J, Pedersen RC (2008) Prevalence and Evolution of Intracranial Hemorrhage in Asymptomatic Term Infants. AJNR Am J NeuroradiolGoogle Scholar
  133. 133.
    Roth S, Raul JS, Ludes B, Willinger R (2007) Finite element analysis of impact and shaking inflicted to a child. Int J Legal Med 121:223–228PubMedCrossRefGoogle Scholar
  134. 134.
    Royal College of P (2009) Report of a meeting on the pathology of traumatic head injury in childrenGoogle Scholar
  135. 135.
    Ruddick C, Ward Platt MP, De San LC (2009) Head trauma outcomes of verifiable falls in newborn babies. Arch Dis ChildGoogle Scholar
  136. 136.
    Rutty GN, Squier WM, Padfield CJ (2005) Epidural haemorrhage of the cervical spinal cord: a post-mortem artefact? Neuropathol Appl Neurobiol 31:247–257PubMedCrossRefGoogle Scholar
  137. 137.
    Safar P, Behringer W, Bottiger BW, Sterz F (2002) Cerebral resuscitation potentials for cardiac arrest. Crit Care Med 30:S140–S144PubMedCrossRefGoogle Scholar
  138. 138.
    Saukko P, Knight B (2004) Knight’s forensic pathology. Arnold LondonGoogle Scholar
  139. 139.
    Sebire G, Tabarki B, Saunders DE, Leroy I, Liesner R, Saint-Martin C, Husson B, Williams AN, Wade A, Kirkham FJ (2005) Cerebral venous sinus thrombosis in children: risk factors, presentation, diagnosis and outcome. Brain 128:477–489PubMedCrossRefGoogle Scholar
  140. 140.
    Shannon P, Smith CR, Deck J, Ang LC, Ho M, Becker L (1998) Axonal injury and the neuropathology of shaken baby syndrome. Acta Neuropathol (Berl) 95:625–631CrossRefGoogle Scholar
  141. 141.
    Si Z, Luan L, Kong D, Zhao G, Wang H, Zhang K, Yu T, Pang Q (2008) MRI-based investigation on outflow segment of cerebral venous system under increased ICP condition. EurJ Med Res 13:121–126Google Scholar
  142. 142.
    Simon B, Letourneau P, Vitorino E, McCall J (2001) Pediatric minor head trauma: indications for computed tomographic scanning revisited. J Trauma 51:231–237PubMedCrossRefGoogle Scholar
  143. 143.
    Slaughter L, Egelhoff J, Balmakund T (2009) Neurologic outcome in neonatal temporal lobe hemorrhagic venous infarcts. J Child Neurol 24:1236–1242PubMedCrossRefGoogle Scholar
  144. 144.
    Smith C, Bell JE, Keeling JW, Risden RA (2003) Dural haemorrhage in nontraumatic infant deaths: does it explain the bleeding in ‘shaken baby syndrome’? Geddes JE et al. A response. Neuropathol Appl Neurobiol 29:411–412PubMedCrossRefGoogle Scholar
  145. 145.
    Smith CS, M (2007) Acquired diseases of the nervous system. In: Keeling JYK, T (ed) Fetal and neonatal pathology. Springer, LondonGoogle Scholar
  146. 146.
    Smith D (1957) Preretinal and optic nerve sheath hemorrhage:pathological and experimental aspects in subarachnoid hemorrhage. Trans Am Acad Ophthalmol Otolaryngol 61:201–211PubMedGoogle Scholar
  147. 147.
    Squier W (2008) Shaken baby syndrome: the quest for evidence. Dev Med Child Neurol 50:10–14PubMedCrossRefGoogle Scholar
  148. 148.
    Squier W, Lindberg E, Mack J, Darby S (2009) Demonstration of fluid channels in human dura and their relationship to age and intradural bleeding. Childs Nerv Syst 25:925–931PubMedCrossRefGoogle Scholar
  149. 149.
    Squier W, Mack J (2009) The neuropathology of infant subdural haemorrhage. Forensic SciInt 187:6–13CrossRefGoogle Scholar
  150. 150.
    Squier W, Austin T, Anslow P, Weller RO (2011) Infant subcortical cystic leucomalacia: a distinct pathological entity resulting from impaired fluid handling. Early Hum DevGoogle Scholar
  151. 151.
    Squier W, Scheimberg I, Smith C (2011) Spinal nerve root beta-APP staining in infants is not a reliable indicator of trauma. Forensic Sci IntGoogle Scholar
  152. 152.
    Stam AH, Luijckx GJ, Poll-The BT, Ginjaar IB, Frants RR, Haan J, Ferrari MD, Terwindt GM, van den Maagdenberg AM (2009) Early seizures and cerebral oedema after trivial head trauma associated with the CACNA1A S218L mutation. J Neurol Neurosurg Psychiatry 80:1125–1129PubMedCrossRefGoogle Scholar
  153. 153.
    Starling SP, Patel S, Burke BL, Sirotnak AP, Stronks S, Rosquist P (2004) Analysis of perpetrator admissions to inflicted traumatic brain injury in children. Arch Pediatr Adolesc Med 158:454–458PubMedCrossRefGoogle Scholar
  154. 154.
    Stein KM, Ruf K, Ganten MK, Mattern R (2006) Representation of cerebral bridging veins in infants by postmortem computed tomography. Forensic SciInt 163:93–101CrossRefGoogle Scholar
  155. 155.
    Stroobandt G, Evrard P, Laterre C (1978) Pathogenesis of persistent subdural effusions in infants (author’s transl). Neuro Chirurgie 24:47–51PubMedGoogle Scholar
  156. 156.
    Su CS, Lan MY, Chang YY, Lin WC, Liu KT (2009) Clinical features, neuroimaging and treatment of spontaneous intracranial hypotension and magnetic resonance imaging evidence of blind epidural blood patch. Eur Neurol 61:301–307PubMedCrossRefGoogle Scholar
  157. 157.
    Takiguchi T, Yamaguchi S, Tezuka M, Furukawa N, Kitajima T (2006) Compression of the subarachnoid space by the engorged epidural venous plexus in pregnant women. Anesthesiology 105:848–851PubMedCrossRefGoogle Scholar
  158. 158.
    Talvik I, Alexander RC, Talvik T (2008) Shaken baby syndrome and a baby’s cry. Acta Paediatr 97:782–785PubMedCrossRefGoogle Scholar
  159. 159.
    Tan M, Deveber G, Shroff M, Moharir M, Pontigon AM, Widjaja E, Kirton A (2011) Sagittal sinus compression is associated with neonatal cerebral sinovenous thrombosis. Pediatrics 128:e429–e435PubMedCrossRefGoogle Scholar
  160. 160.
    Taylor GA (1992) Intracranial venous system in the newborn. Radiology 183Google Scholar
  161. 161.
    Thornton E, Ziebell JM, Leonard AV, Vink R (2010) Kinin receptor antagonists as potential neuroprotective agents in central nervous system injury. Molecules 15:6598–6618PubMedCrossRefGoogle Scholar
  162. 162.
    Tubbs RS, Salter EG, Wellons JC, III, Blount JP, Oakes WJ (2007) The sphenoparietal sinus. Neurosurgery 60:ONS9-12Google Scholar
  163. 163.
    Valdueza JM, von Munster T, Hoffman O, Schreiber S, Einhaupl KM (2000) Postural dependency of the cerebral venous outflow. Lancet 355:200–201PubMedCrossRefGoogle Scholar
  164. 164.
    van der Kuip M, Hoogland PV, Groen RJ (1999) Human radicular veins: regulation of venous reflux in the absence of valves. Anat Rec 254:173–180PubMedCrossRefGoogle Scholar
  165. 165.
    Vieira JP, Luis C, Monteiro JP, Temudo T, Campos MM, Quintas S, Nunes S (2010) Cerebral sinovenous thrombosis in children: clinical presentation and extension, localization and recanalization of thrombosis. Eur J Paediatr Neurol 14:80–85PubMedCrossRefGoogle Scholar
  166. 166.
    Vignes JR, Dagain A, Guerin J, Liguoro D (2007) A hypothesis of cerebral venous system regulation based on a study of the junction between the cortical bridging veins and the superior sagittal sinus. Laboratory investigation. J Neurosurg 107:1205–1210PubMedCrossRefGoogle Scholar
  167. 167.
    Vinchon M, Noizet O, Defoort-Dhellemmes S, Soto-Ares G, Dhellemmes P (2002) Infantile subdural hematomas due to traffic accidents. Pediatr Neurosurg 37:245–253PubMedCrossRefGoogle Scholar
  168. 168.
    Vinchon M, Defoort-Dhellemmes S, Desurmont M, Dhellemmes P (2005) Accidental and nonaccidental head injuries in infants: a prospective study. J Neurosurg 102:380–384PubMedGoogle Scholar
  169. 169.
    Vinchon M, Delestret I, Defoort-Dhellemmes S, Desurmont M, Noule N (2010) Subdural hematoma in infants: can it occur spontaneously? Data from a prospective series and critical review of the literature. Childs Nerv Syst 26:1195–1205PubMedCrossRefGoogle Scholar
  170. 170.
    Vinchon M, Desurmont M, Soto-Ares G, De Foort-Dhellemmes S (2010) Natural history of traumatic meningeal bleeding in infants: semiquantitative analysis of serial CT scans in corroborated cases. Childs Nerv Syst 26:755–762PubMedCrossRefGoogle Scholar
  171. 171.
    Voigt GE, Lowenhielm CG, Ljung CB (1977) Rotational cerebral injuries near the superior margin of the brain. Acta Neuropathol 39:201–209PubMedCrossRefGoogle Scholar
  172. 172.
    Volpe JJ (2009) Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances. Lancet Neurol 8:110–124PubMedCrossRefGoogle Scholar
  173. 173.
    Vowles GH, Scholtz CL, Cameron JM (1987) Diffuse axonal injury in early infancy. J Clin Pathol 40:185–189PubMedCrossRefGoogle Scholar
  174. 174.
    Watts P, Obi E (2008) Retinal folds and retinoschisis in accidental and non-accidental head injury. Eye (Lond) 22:1514–1516CrossRefGoogle Scholar
  175. 175.
    Welch K, Friedman V (1960) The cerebrospinal fluid valves. Brain 83:454–469PubMedCrossRefGoogle Scholar
  176. 176.
    Wells RG, Sty JR (2003) Traumatic low attenuation subdural fluid collections in children younger than 3 years. Arch Pediatr Adolesc Med 157:1005–1010PubMedCrossRefGoogle Scholar
  177. 177.
    Whitby EH, Griffiths PD, Rutter S, Smith MF, Sprigg A, Ohadike P, Davies NP, Rigby AS, Paley MN (2004) Frequency and natural history of subdural haemorrhages in babies and relation to obstetric factors. Lancet 363:846–851PubMedCrossRefGoogle Scholar
  178. 178.
    Wintermark M, Lepori D, Cotting J, Roulet E, van Melle G, Meuli R, Maeder P, Regli L, Verdun FR, Deonna T, Schnyder P, Gudinchet F (2004) Brain perfusion in children: evolution with age assessed by quantitative perfusion computed tomography. Pediatrics 113:1642–1652PubMedCrossRefGoogle Scholar
  179. 179.
    Wolfe SQ, Bhatia S, Green B, Ragheb J (2007) Engorged epidural venous plexus and cervical myelopathy due to cerebrospinal fluid overdrainage: a rare complication of ventricular shunts. Case report. J Neurosurg 106:227–231PubMedGoogle Scholar
  180. 180.
    Wu YW, Miller SP, Chin K, Collins AE, Lomeli SC, Chuang NA, Barkovich AJ, Ferriero DM (2002) Multiple risk factors in neonatal sinovenous thrombosis. Neurology 59:438–440PubMedGoogle Scholar
  181. 181.
    Yamashima T, Friede RL (1984) Why do bridging veins rupture into the virtual subdural space? J Neurol Neurosurg Psychiatry 47:121–127PubMedCrossRefGoogle Scholar
  182. 182.
    Yang JY, Chan AK, Callen DJ, Paes BA (2010) Neonatal cerebral sinovenous thrombosis: sifting the evidence for a diagnostic plan and treatment strategy. Pediatrics 126:e693–e700PubMedCrossRefGoogle Scholar
  183. 183.
    Yu Y, Chen J, Si Z, Zhao G, Xu S, Wang G, Ding F, Luan L, Wu L, Pang Q (2010) The hemodynamic response of the cerebral bridging veins to changes in ICP. Neuro Crit Care 12:117–123Google Scholar
  184. 184.
    Zahl SM, Wester K (2008) Routine measurement of head circumference as a tool for detecting intracranial expansion in infants: what is the gain? A nationwide survey. Pediatrics 121:e416–e420PubMedCrossRefGoogle Scholar
  185. 185.
    Zahl SM, Egge A, Helseth E, Wester K (2011) Benign external hydrocephalus: a review, with emphasis on management. Neurosurg RevGoogle Scholar
  186. 186.
    Zenker W, Bankoul S, Braun JS (1994) Morphological indications for considerable diffuse reabsorption of cerebrospinal fluid in spinal meninges particularly in the areas of meningeal funnels. An electron microscopical study including tracing experiments in rats. Anat Embryol (Berl) 189:243–258Google Scholar
  187. 187.
    Zenker W, Kubik S (1996) Brain cooling in humans—anatomical considerations. Anat Embryol (Berl) 193:1–13CrossRefGoogle Scholar
  188. 188.
    Zhang ET, Inman CB, Weller RO (1990) Interrelationships of the pia mater and the perivascular (Virchow-Robin) spaces in the human cerebrum. J Anat 170:111–123PubMedGoogle Scholar
  189. 189.
    Zimmerman RA, Bilaniuk LT, Bruce D, Schut L, Uzzell B, Goldberg HI (1979) Computed tomography of craniocerebral injury in the abused child. Radiology 130:687–690PubMedGoogle Scholar
  190. 190.
    Zuccaro G, Arganaraz R, Villasante F, Ceciliano A (2010) Neurosurgical vascular malformations in children under 1 year of age. Childs Nerv Syst 26:1381–1394PubMedCrossRefGoogle Scholar

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© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Department of Neuropathology, West WingJohn Radcliffe HospitalOxfordUK

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