Skip to main content

Advertisement

SpringerLink
Log in

The “Shaken Baby” syndrome: pathology and mechanisms

  • Review
  • Published:
Acta Neuropathologica Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14
Fig. 15

Similar content being viewed by others

References

  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 12:557–563

    Article  PubMed  CAS  Google Scholar 

  2. Adamsbaum C, Grabar S, Mejean N, Rey-Salmon C (2010) Abusive head trauma: judicial admissions highlight violent and repetitive shaking. Pediatrics 126:546–555

    Article  PubMed  Google Scholar 

  3. Aoki N, Masuzawa H (1984) Infantile acute subdural hematoma. Clinical analysis of 26 cases. J Neurosurg 61:273–280

    Article  PubMed  CAS  Google Scholar 

  4. Aoki N (1990) Chronic subdural hematoma in infancy. Clinical analysis of 30 cases in the CT era. J Neurosurg 73:201–205

    Article  PubMed  CAS  Google Scholar 

  5. Arbogast KB, Margulies SS, Christian CW (2005) Initial neurologic presentation in young children sustaining inflicted and unintentional fatal head injuries. Pediatrics 116:180–184

    Article  PubMed  Google Scholar 

  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 82:735–741

    Article  PubMed  CAS  Google Scholar 

  7. Auer LM, Ishiyama N, Hodde KC, Kleinert R, Pucher R (1987) Effect of intracranial pressure on bridging veins in rats. J Neurosurg 67:263–268

    Article  PubMed  CAS  Google Scholar 

  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 49:205–229

    Article  PubMed  Google Scholar 

  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, London

    Google Scholar 

  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 41:1382–1388

    Article  PubMed  Google Scholar 

  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, e917

    Google Scholar 

  12. Boyle JD, Boyle EM (2011) Born just a few weeks early: does it matter? Arch Dis Child Fetal Neonatal Ed

  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 3:232–239

    Article  PubMed  Google Scholar 

  14. Browder J, Kaplan HA, Krieger AJ (1975) Venous lakes in the suboccipital dura mater and falx cerebelli of infants: surgical significance. Surg Neurol 4:53–55

    PubMed  CAS  Google Scholar 

  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 22:1395–1409

    Article  PubMed  CAS  Google Scholar 

  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 10:348–350

    Article  PubMed  Google Scholar 

  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 124:161–169

    PubMed  CAS  Google Scholar 

  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 54:396–403

    PubMed  CAS  Google Scholar 

  19. Caldarelli M, Di RC, Romani R (2002) Surgical treatment of chronic subdural hygromas in infants and children. Acta Neurochir (Wien) 144:581–588

    Article  CAS  Google Scholar 

  20. Calder IM, Hill I, Scholtz CL (1984) Primary brain trauma in non-accidental injury. J ClinPathol 37:1095–1100

    Article  CAS  Google Scholar 

  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 27:1557–1564

    Article  PubMed  Google Scholar 

  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 22:112–122

    Article  PubMed  CAS  Google Scholar 

  23. Case ME (2007) Abusive head injuries in infants and young children. Leg Med (Tokyo) 9:83–87

    Article  Google Scholar 

  24. Chamnanvanakij S, Rollins N, Perlman JM (2002) Subdural hematoma in term infants. Pediatr Neurol 26:301–304

    Article  PubMed  Google Scholar 

  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 19:214–223

    Article  PubMed  Google Scholar 

  26. Christian CW, Taylor AA, Hertle RW, Duhaime AC (1999) Retinal hemorrhages caused by accidental household trauma. J Pediatr 135:125–127

    Article  PubMed  CAS  Google Scholar 

  27. Christian CW, Block R (2009) Abusive head trauma in infants and children. Pediatrics 123:1409–1411

    Article  PubMed  Google Scholar 

  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 1

  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 200:100–107

    Article  Google Scholar 

  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 256:898–905

    Article  PubMed  Google Scholar 

  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 43:317–333

    Article  PubMed  CAS  Google Scholar 

  32. Crown Prosecution S (2011) Non-accidental head injury (nahi, formerly referred to as shaken baby syndrome [SBS])—prosecution approach. http://www.cps.gov.uk/legal/l_to_o/non_accidental_head_injury_cases/

  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 16:484–492

    Article  PubMed  CAS  Google Scholar 

  34. Dandy W (1929) Where is cerebrospinal fluid absorbed? J Am Med Assoc

  35. Dias MS (2010) The case for shaking. In: Jenny C (ed) Child abuse and neglect. Elsevier Saunders

  36. Dolinak D, Smith C, Graham DI (2000) Hypoglycaemia is a cause of axonal injury. Neuropathol Appl Neurobiol 26:448–453

    Article  PubMed  CAS  Google Scholar 

  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 66:409–415

    Article  PubMed  CAS  Google Scholar 

  38. Duhaime AC, Gennarelli TA, Sutton LN, Schut L (1988) “Shaken baby syndrome”: A misnomer? J Pediatr Neurosci 4:77–86

    Google Scholar 

  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 90:179–185

    PubMed  CAS  Google Scholar 

  40. Duhaime AC, Christian CW, Rorke LB, Zimmerman RA (1998) Nonaccidental head injury in infants–the “shaken-baby syndrome”. N Engl J Med 338:1822–1829

    Article  PubMed  CAS  Google Scholar 

  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 192:165–170

    Article  PubMed  Google Scholar 

  42. Ebbs Justice D (2011) Report to the attorney general: Shaken baby death review. Ontario

  43. Edlow JA, Caplan LR (2000) Avoiding pitfalls in the diagnosis of subarachnoid hemorrhage. N Engl J Med 342:29–36

    Article  PubMed  CAS  Google Scholar 

  44. Eichler F, Krishnamoorthy K, Grant PE (2007) Magnetic resonance imaging evaluation of possible neonatal sinovenous thrombosis. Pediatr Neurol 37:317–323

    Article  PubMed  Google Scholar 

  45. Eisenbrey AB (1979) Retinal hemorrhage in the battered child. Childs Brain 5:40–44

    PubMed  CAS  Google Scholar 

  46. Emerson MV, Jakobs E, Green WR (2007) Ocular autopsy and histopathologic features of child abuse. Ophthalmology 114:1384–1394

    Article  PubMed  Google Scholar 

  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 16:25–33

    Article  CAS  Google Scholar 

  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 70:1147–1149

    Article  PubMed  Google Scholar 

  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 186:22–28

    Article  Google Scholar 

  50. Fox RJ (1996) Anatomic details of intradural channels in the parasagittal dura: a possible pathway for flow of cerebrospinal fluid. Neurosurgery 39:84–91

    Article  PubMed  CAS  Google Scholar 

  51. Frasier L et al. (2006) In: Frasier L (ed) Abusive head trauma in infants and children, G W Medical

  52. Friede RL (1972) Subpial hemorrhage in infants. J Neuropathol Exp Neurol 31:548–556

    Article  PubMed  CAS  Google Scholar 

  53. Friede RL (1989) Subdural haematomas, hygromas and effusions. In: Friede RL (ed) Developmental neuropathology. Springer, Gottingen, pp 198–208

    Google Scholar 

  54. Gage LJ, Harris RV et al (2005) EWCA. Crim 1980

  55. Gardner HB (2007) A witnessed short fall mimicking presumed shaken baby syndrome (inflicted childhood neurotrauma). Pediatr Neurosurg 43:433–435

    Article  PubMed  Google Scholar 

  56. Geddes JF, Vowles GH, Beer TW, Ellison DW (1997) The diagnosis of diffuse axonal injury: implications for forensic practice. Neuropathol Appl Neurobiol 23:339–347

    Article  PubMed  CAS  Google Scholar 

  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 124:1290–1298

    Article  PubMed  CAS  Google Scholar 

  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 124:1299–1306

    Article  PubMed  CAS  Google Scholar 

  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 29:14–22

    Article  PubMed  CAS  Google Scholar 

  60. Ghosh PS, Ghosh D (2011) Subdural hematoma in infants without accidental or nonaccidental injury: benign external hydrocephalus, a risk factor. Clin Pediatr

  61. Gilles EE, McGregor ML, Levy-Clarke G (2003) Retinal hemorrhage asymmetry in inflicted head injury: a clue to pathogenesis? J Pediatr 143:494–499

    Article  PubMed  Google Scholar 

  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 104:1841–1848

    Article  PubMed  CAS  Google Scholar 

  63. Guthkelch AN (1971) Infantile subdural haematoma and its relationship to whiplash injuries. Br Med J 2:430–431

    Article  PubMed  CAS  Google Scholar 

  64. Hadley MN, Sonntag VK, Rekate HL, Murphy A (1989) The infant whiplash-shake injury syndrome: a clinical and pathological study. Neurosurgery 24:536–540

    Article  PubMed  CAS  Google Scholar 

  65. Haines DE, Harkey HL, al Mefty O (1993) The “subdural” space: a new look at an outdated concept. Neurosurgery 32:111–120

    Article  PubMed  CAS  Google Scholar 

  66. Hall JR, Reyes HM, Horvat M, Meller JL, Stein R (1989) The mortality of childhood falls. J Trauma 29:1273–1275

    Article  PubMed  CAS  Google Scholar 

  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 108:345–358

    Article  CAS  Google Scholar 

  68. Herzberger E, Rotem Y, Braham J (1956) Remarks on thirty-three cases of subdural effusion in infancy. Arch Dis Child 31:44–50

    Article  PubMed  CAS  Google Scholar 

  69. Hobbs C, Childs AM, Wynne J, Livingston J, Seal A (2005) Subdural haematoma and effusion in infancy: an epidemiological study. Arch Dis Child 90:952–955

    Article  PubMed  CAS  Google Scholar 

  70. Holbourn A (1943) Mechanics of head injuries. The Lancet:438

  71. Hoogstraate SR, Lequin MH, Huysman MA, Ahmed S, Govaert PP (2009) Apnoea in relation to neonatal temporal lobe haemorrhage. Eur J Paediatr Neurol 13:356–361

    Article  PubMed  Google Scholar 

  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 33:226–237

    Article  PubMed  CAS  Google Scholar 

  73. Huang AH, Robertson RL (2004) Spontaneous superficial parenchymal and leptomeningeal hemorrhage in term neonates. AJNR Am J Neuroradiol 25:469–475

    PubMed  Google Scholar 

  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 83:736–743

    Article  PubMed  CAS  Google Scholar 

  75. Hwang SK, Kim SL (2000) Infantile head injury, with special reference to the development of chronic subdural hematoma. Childs Nerv Syst 16:590–594

    Article  PubMed  CAS  Google Scholar 

  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 7:329–348

    Article  PubMed  Google Scholar 

  77. Ikeda A, Sato O, Tsugane R, Shibuya N, Yamamoto I, Shimoda M (1987) Infantile acute subdural hematoma. Childs Nerv Syst 3:19–22

    Article  PubMed  CAS  Google Scholar 

  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 22:237–245

    Article  PubMed  CAS  Google Scholar 

  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 Sci

  80. Johnston M, Armstrong D, Koh L (2007) Possible role of the cavernous sinus veins in cerebrospinal fluid absorption. Cerebrospinal Fluid Res 4:3

    Article  PubMed  Google Scholar 

  81. Keeling J (2009) Paediatric forensic medicine and pathology. Edward Arnold

  82. Keeling JW (1993) Fetal and neonatal pathology. Springer, London

    Google Scholar 

  83. Kinney HC, Thach BT (2009) The sudden infant death syndrome. N Engl J Med 361:795–805

    Article  PubMed  CAS  Google Scholar 

  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 41:182–199

    Article  PubMed  Google Scholar 

  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 49:753–760

    Article  PubMed  CAS  Google Scholar 

  86. Koumellis P, McConachie NS, Jaspan T (2008) Spinal subdural hematomas in children with non accidental head injury. Arch Dis Child

  87. Lantz PE, Stanton CA (2006) Postmortem detection and evaluation of retinal hemorrhages. Am Acad Forensic Sci 271

  88. Lapillonne A (2010) Vitamin D deficiency during pregnancy may impair maternal and fetal outcomes. Med Hypotheses 74:71–75

    Article  PubMed  CAS  Google Scholar 

  89. Larroche J-C (1977) Lesions of haemorrhagic type, mainly venous. Developmental pathology of the neonate. Excerpta Medica, Amsterdam, pp 355–398

  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 S42–13

  91. Leestma JE (2005) Case analysis of brain-injured admittedly shaken infants: 54 cases, 1969–2001. Am J Forensic Med Pathol 26:199–212

    Article  PubMed  Google Scholar 

  92. Leestma JE (2009) Forensic neuropathology. CRC Press, Taylor and Francis Group

  93. Levin AV, Forbes B, Alexander R, Jenny C (2010) Information statement. Abusive head trauma/shaken baby syndrome. American Academy of Ophthalmology, San Francisco

  94. Lindenberg R, Freytag E (1969) Morphology of brain lesions from blunt trauma in early infancy. Arch Pathol 87:298–305

    PubMed  CAS  Google Scholar 

  95. Loh JK, Lin CL, Kwan AL, Howng SL (2002) Acute subdural hematoma in infancy. Surg Neurol 58:218–224

    Article  PubMed  Google Scholar 

  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 242:535–541

    Article  PubMed  Google Scholar 

  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 10:24

    Article  PubMed  Google Scholar 

  98. Mack J, Squier W, Eastman JT (2009) Anatomy and development of the meninges: implications for subdural collections and CSF circulation. Pediatr Radiol 39:200–210

    Article  PubMed  Google Scholar 

  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 94:860–867

    Article  PubMed  CAS  Google Scholar 

  100. Manole MD, Kochanek PM, Fink EL, Clark RS (2009) Postcardiac arrest syndrome: focus on the brain. Curr Opin Pediatr 21:745–750

    Article  PubMed  Google Scholar 

  101. Marmarou A (2007) A review of progress in understanding the pathophysiology and treatment of brain edema. Neurosurg Focus 22:E1

    Google Scholar 

  102. Matshes E (2010) Retinal and optic nerve sheath haemorrhages are not pathognomonic of abusive head injury. Abstract American Association of Forensic Sciences Conference

  103. Matshes E, Rea E (2011) Shaken infants die of neck trauma, not brain trauma. Acad Forensic Pathol 1:b–k

    Google Scholar 

  104. Maxeiner H (1997) Detection of ruptured cerebral bridging veins at autopsy. Forensic SciInt 89:103–110

    Article  CAS  Google Scholar 

  105. Maxeiner H (2001) Demonstration and interpretation of bridging vein ruptures in cases of infantile subdural bleedings. J Forensic Sci 46:85–93

    PubMed  CAS  Google Scholar 

  106. McLellan NJ, Prasad R, Punt J (1986) Spontaneous subhyaloid and retinal haemorrhages in an infant. Arch Dis Child 61:1130–1132

    Article  PubMed  CAS  Google Scholar 

  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 27:1725–1728

    PubMed  CAS  Google Scholar 

  108. Menkes JH, Sarnat HB, Maria BL (2006) Child neurology, 7th edn

  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 67:590–599

    PubMed  CAS  Google Scholar 

  110. Mokri B, Parisi JE, Scheithauer BW, Piepgras DG, Miller GM (1995) Meningeal biopsy in intracranial hypotension: meningeal enhancement on MRI. Neurology 45:1801–1807

    PubMed  CAS  Google Scholar 

  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 Pathol

  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 96:40–43

    Article  PubMed  CAS  Google Scholar 

  113. Muller PJ, Deck JH (1974) Intraocular and optic nerve sheath hemorrhage in cases of sudden intracranial hypertension. J Neurosurg 41:160–166

    Article  PubMed  CAS  Google Scholar 

  114. Munro D, Merrit HH (1936) Surgical pathology of subdural hematoma. Based on a study of one hundred and five cases. Arch Neurol Psychiatry 35:64–78

    Google Scholar 

  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 123:235–240

    Article  Google Scholar 

  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 195:143–147

    Article  CAS  Google Scholar 

  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 116:317–329

    Article  PubMed  Google Scholar 

  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 22:662–669

    Article  Google Scholar 

  119. Ommaya AK, Goldsmith W, Thibault L (2002) Biomechanics and neuropathology of adult and paediatric head injury. Br J Neurosurg 16:220–242

    Article  PubMed  CAS  Google Scholar 

  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 20:29–36

    Article  PubMed  CAS  Google Scholar 

  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 33:188–193

    Article  PubMed  CAS  Google Scholar 

  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) 127:41–47

    Article  CAS  Google Scholar 

  123. Pittman T (2003) Significance of a subdural hematoma in a child with external hydrocephalus. Pediatr Neurosurg 39:57–59

    Article  PubMed  Google Scholar 

  124. Plunkett J (1999) Sudden death in an infant caused by rupture of a basilar artery aneurysm. Am J Forensic Med Pathol 20:211–214

    Article  PubMed  CAS  Google Scholar 

  125. Prange MT, Coats B, Duhaime AC, Margulies SS (2003) Anthropomorphic simulations of falls, shakes, and inflicted impacts in infants. J Neurosurg 99:143–150

    Article  PubMed  Google Scholar 

  126. Ramenghi LA, Govaert P, Fumagalli M, Bassi L, Mosca F (2009) Neonatal cerebral sinovenous thrombosis. Semin Fetal Neonatal Med 14:278–283

    Article  PubMed  Google Scholar 

  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) 24:1426–1427

    Article  CAS  Google Scholar 

  128. Reichard RR, Smith C, Graham DI (2005) The significance of beta-APP immunoreactivity in forensic practice. Neuropathol Appl Neurobiol 31:304–313

    Article  PubMed  CAS  Google Scholar 

  129. Richardson JD, Vasko MR (2002) Cellular mechanisms of neurogenic inflammation. J Pharmacol Exp Ther 302:839–845

    Article  PubMed  CAS  Google Scholar 

  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 39:2644–2691

    Article  PubMed  Google Scholar 

  131. Rogers CB, Itabashi HH, Tomiyasu U, Heuser ET (1998) Subdural neomembranes and sudden infant death syndrome. JForensic Sci 43:375–376

    CAS  Google Scholar 

  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 Neuroradiol

  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 121:223–228

    Article  PubMed  Google Scholar 

  134. Royal College of P (2009) Report of a meeting on the pathology of traumatic head injury in children

  135. Ruddick C, Ward Platt MP, De San LC (2009) Head trauma outcomes of verifiable falls in newborn babies. Arch Dis Child

  136. Rutty GN, Squier WM, Padfield CJ (2005) Epidural haemorrhage of the cervical spinal cord: a post-mortem artefact? Neuropathol Appl Neurobiol 31:247–257

    Article  PubMed  CAS  Google Scholar 

  137. Safar P, Behringer W, Bottiger BW, Sterz F (2002) Cerebral resuscitation potentials for cardiac arrest. Crit Care Med 30:S140–S144

    Article  PubMed  Google Scholar 

  138. Saukko P, Knight B (2004) Knight’s forensic pathology. Arnold London

  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 128:477–489

    Article  PubMed  CAS  Google Scholar 

  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) 95:625–631

    Article  CAS  Google Scholar 

  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 13:121–126

    CAS  Google Scholar 

  142. Simon B, Letourneau P, Vitorino E, McCall J (2001) Pediatric minor head trauma: indications for computed tomographic scanning revisited. J Trauma 51:231–237

    Article  PubMed  CAS  Google Scholar 

  143. Slaughter L, Egelhoff J, Balmakund T (2009) Neurologic outcome in neonatal temporal lobe hemorrhagic venous infarcts. J Child Neurol 24:1236–1242

    Article  PubMed  Google Scholar 

  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 29:411–412

    Article  PubMed  CAS  Google Scholar 

  145. Smith CS, M (2007) Acquired diseases of the nervous system. In: Keeling JYK, T (ed) Fetal and neonatal pathology. Springer, London

  146. Smith D (1957) Preretinal and optic nerve sheath hemorrhage:pathological and experimental aspects in subarachnoid hemorrhage. Trans Am Acad Ophthalmol Otolaryngol 61:201–211

    PubMed  CAS  Google Scholar 

  147. Squier W (2008) Shaken baby syndrome: the quest for evidence. Dev Med Child Neurol 50:10–14

    Article  PubMed  Google Scholar 

  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 25:925–931

    Article  PubMed  CAS  Google Scholar 

  149. Squier W, Mack J (2009) The neuropathology of infant subdural haemorrhage. Forensic SciInt 187:6–13

    Article  Google Scholar 

  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 Dev

  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 Int

  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 80:1125–1129

    Article  PubMed  CAS  Google Scholar 

  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 158:454–458

    Article  PubMed  Google Scholar 

  154. Stein KM, Ruf K, Ganten MK, Mattern R (2006) Representation of cerebral bridging veins in infants by postmortem computed tomography. Forensic SciInt 163:93–101

    Article  Google Scholar 

  155. Stroobandt G, Evrard P, Laterre C (1978) Pathogenesis of persistent subdural effusions in infants (author’s transl). Neuro Chirurgie 24:47–51

    PubMed  CAS  Google Scholar 

  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 61:301–307

    Article  PubMed  Google Scholar 

  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 105:848–851

    Article  PubMed  Google Scholar 

  158. Talvik I, Alexander RC, Talvik T (2008) Shaken baby syndrome and a baby’s cry. Acta Paediatr 97:782–785

    Article  PubMed  Google Scholar 

  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–e435

    Article  PubMed  Google Scholar 

  160. Taylor GA (1992) Intracranial venous system in the newborn. Radiology 183

  161. Thornton E, Ziebell JM, Leonard AV, Vink R (2010) Kinin receptor antagonists as potential neuroprotective agents in central nervous system injury. Molecules 15:6598–6618

    Article  PubMed  CAS  Google Scholar 

  162. Tubbs RS, Salter EG, Wellons JC, III, Blount JP, Oakes WJ (2007) The sphenoparietal sinus. Neurosurgery 60:ONS9-12

  163. Valdueza JM, von Munster T, Hoffman O, Schreiber S, Einhaupl KM (2000) Postural dependency of the cerebral venous outflow. Lancet 355:200–201

    Article  PubMed  CAS  Google Scholar 

  164. van der Kuip M, Hoogland PV, Groen RJ (1999) Human radicular veins: regulation of venous reflux in the absence of valves. Anat Rec 254:173–180

    Article  PubMed  Google Scholar 

  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 14:80–85

    Article  PubMed  CAS  Google Scholar 

  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 107:1205–1210

    Article  PubMed  Google Scholar 

  167. Vinchon M, Noizet O, Defoort-Dhellemmes S, Soto-Ares G, Dhellemmes P (2002) Infantile subdural hematomas due to traffic accidents. Pediatr Neurosurg 37:245–253

    Article  PubMed  Google Scholar 

  168. Vinchon M, Defoort-Dhellemmes S, Desurmont M, Dhellemmes P (2005) Accidental and nonaccidental head injuries in infants: a prospective study. J Neurosurg 102:380–384

    PubMed  Google Scholar 

  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 26:1195–1205

    Article  PubMed  Google Scholar 

  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 26:755–762

    Article  PubMed  Google Scholar 

  171. Voigt GE, Lowenhielm CG, Ljung CB (1977) Rotational cerebral injuries near the superior margin of the brain. Acta Neuropathol 39:201–209

    Article  PubMed  CAS  Google Scholar 

  172. Volpe JJ (2009) Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances. Lancet Neurol 8:110–124

    Article  PubMed  Google Scholar 

  173. Vowles GH, Scholtz CL, Cameron JM (1987) Diffuse axonal injury in early infancy. J Clin Pathol 40:185–189

    Article  PubMed  CAS  Google Scholar 

  174. Watts P, Obi E (2008) Retinal folds and retinoschisis in accidental and non-accidental head injury. Eye (Lond) 22:1514–1516

    Article  CAS  Google Scholar 

  175. Welch K, Friedman V (1960) The cerebrospinal fluid valves. Brain 83:454–469

    Article  PubMed  CAS  Google Scholar 

  176. Wells RG, Sty JR (2003) Traumatic low attenuation subdural fluid collections in children younger than 3 years. Arch Pediatr Adolesc Med 157:1005–1010

    Article  PubMed  Google Scholar 

  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 363:846–851

    Article  PubMed  CAS  Google Scholar 

  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 113:1642–1652

    Article  PubMed  Google Scholar 

  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 106:227–231

    PubMed  Google Scholar 

  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 59:438–440

    PubMed  Google Scholar 

  181. Yamashima T, Friede RL (1984) Why do bridging veins rupture into the virtual subdural space? J Neurol Neurosurg Psychiatry 47:121–127

    Article  PubMed  CAS  Google Scholar 

  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–e700

    Article  PubMed  Google Scholar 

  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 12:117–123

    Google Scholar 

  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–e420

    Article  PubMed  Google Scholar 

  185. Zahl SM, Egge A, Helseth E, Wester K (2011) Benign external hydrocephalus: a review, with emphasis on management. Neurosurg Rev

  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) 189:243–258

    CAS  Google Scholar 

  187. Zenker W, Kubik S (1996) Brain cooling in humans—anatomical considerations. Anat Embryol (Berl) 193:1–13

    Article  CAS  Google Scholar 

  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 170:111–123

    PubMed  CAS  Google Scholar 

  189. Zimmerman RA, Bilaniuk LT, Bruce D, Schut L, Uzzell B, Goldberg HI (1979) Computed tomography of craniocerebral injury in the abused child. Radiology 130:687–690

    PubMed  CAS  Google Scholar 

  190. Zuccaro G, Arganaraz R, Villasante F, Ceciliano A (2010) Neurosurgical vascular malformations in children under 1 year of age. Childs Nerv Syst 26:1381–1394

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

  1. Department of Neuropathology, West Wing, John Radcliffe Hospital, Oxford, OX3 9DU, UK

    Waney Squier

Authors
  1. Waney Squier
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Waney Squier.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Squier, W. The “Shaken Baby” syndrome: pathology and mechanisms. Acta Neuropathol 122, 519–542 (2011). https://doi.org/10.1007/s00401-011-0875-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00401-011-0875-2

Keywords

Search

Navigation