|Year : 2018 | Volume
| Issue : 3 | Page : 174-178
Spontaneous subdural hemorrhage due to ruptured arteriovenous malformation in a child
Nor Fadhilah Madon1, Ahmad Hafizam Hasmi1, Khairul Anuar Zainun2, Hapizah Mohd Nawawi3
1 Department of Forensic Medicine, National Institute of Forensic Medicine, Hospital Kuala Lumpur, Ministry of Health Malaysia, Kuala Lumpur, Malaysia
2 Department of Forensic Medicine, Hospital Sungai Buloh, Jalan Hospital, Selangor, Malaysia
3 Institute of Pathology, Laboratory and Forensic Medicine, Universiti Teknologi MARA, Sungai Buloh Campus, Jalan Hospital, Selangor, Malaysia
|Date of Web Publication||28-Sep-2018|
Dr. Hapizah Mohd Nawawi
Faculty of Medicine, Institute of Pathology, Laboratory and Forensic Medicine, Universiti Teknologi MARA, Sungai Buloh Campus, Jalan Hospital, 47000 Sungai Buloh, Selangor
Source of Support: None, Conflict of Interest: None
Spontaneous subdural hemorrhage (SDH) is an uncommon nontraumatic bleed of the brain, involving the dura and arachnoid mater. SDH commonly occurs due to tearing of bridging veins; however, SDH from the rupture of arteriovenous malformation (AVM) is an uncommon phenomenon, particularly in children. We report a case of atypical SDH in a 1-year-old child with AVM and a history of alleged abuse. Autopsy revealed SDH in the right parietal and middle cranial fossa without any external or internal injuries to the head, brain, or other parts of the body. Histopathological examination and immunohistochemical staining of the brain tissue revealed an abnormal distribution of arteries and veins of various sizes and architecture. From a detailed histopathological examination of the brain and meticulous investigation of vascular abnormalities, we conclude the cause of acute SDH to be due to a ruptured AVM.
Keywords: Arteriovenous malformations, child abuse, spontaneous subdural hemorrhage
|How to cite this article:|
Madon NF, Hasmi AH, Zainun KA, Nawawi HM. Spontaneous subdural hemorrhage due to ruptured arteriovenous malformation in a child. J Forensic Sci Med 2018;4:174-8
|How to cite this URL:|
Madon NF, Hasmi AH, Zainun KA, Nawawi HM. Spontaneous subdural hemorrhage due to ruptured arteriovenous malformation in a child. J Forensic Sci Med [serial online] 2018 [cited 2019 Feb 17];4:174-8. Available from: http://www.jfsmonline.com/text.asp?2018/4/3/174/242516
| Introduction|| |
Spontaneous subdural hemorrhage (SDH) is an uncommon phenomenon, and it often results from tearing of bridging veins in the subdural space.,, The causes of SDH without traumatic brain injury include rupture of cortical artery or pial arteriovenous (AV) fistulae, AV malformation (AVM), or an intracranial aneurysm.,,, AVMs of the brain are congenital vascular lesions that can occur at any age. Although AVMs are rare in the pediatric age group, it is estimated to represent 3% of all AVM cases,,, and they have the tendency to rupture more frequently than in adults.,,,,,, This is because most pediatric AVMs are only detected after rupture. AVMs are defects in the vascular system, consisting of tangles of abnormal blood vessels (nidus) in which the feeding arteries are directly connected to a venous drainage network without interposition of a capillary bed. The direct AV shunting due to lack of capillaries between the feeding arterial and draining venous components of AVMs eventually results in hypertrophy of the arterial and venous components of the AVMs. However, the exact mechanism of such malformations is still unknown. In this article, we report a case of spontaneous SDH in a child due to ruptured AVM who had been allegedly abused by his babysitter.
| Case Report|| |
A 1-year-old boy with the underlying glucose-6-phosphate dehydrogenase (G6PD) deficiency suddenly developed seizures which resolved spontaneously at his babysitter's house. The child, however, did not regain consciousness following that episode and was brought by his father to a nearby clinic before being subsequently referred to the Kuala Lumpur General Hospital. All postmortem is done as per police order. Hence, no consent is required prior to postmortem. Furthermore, this case report has been approved by the Ministry of Health Malaysia to be published in the journal (KKM.NIHSEC.800-4/4/1 Jld 56(23) on 5th April 2018. Further history check from the parents revealed that the child was otherwise well with no history of head trauma or any past medical illness. There were no complications of G6PD deficiency in the past, such as a history of prolonged jaundice, exchange blood transfusion or hemolytic crisis, and no previous history of hospitalization. The growth and development of the child was appropriate to his age. He came from a nonconsanguinous marriage with no family history of coagulative disorder such as hemophilia or seizures. His elder sibling was healthy. Clinical neurological examination showed that the child was drowsy with a Glasgow Coma Scale of 6/15, sluggish light reflex of both pupils, and hypertonia of all the four limbs. Computed tomography (CT) brain showed SDH over the right fronto-temporo-parietal region with cerebral edema [Figure 1]a. There was no evidence of extended injury to the head or any other parts of the body. Subsequently, the child was intubated for cerebral protection. Serial CT scans showed worsening of SDH and cerebral edema. Skeletal survey demonstrated that there were no fractures in any other part of the body. Examination by the ophthalmologist revealed extensive bilateral retinal and preretinal hemorrhages.
|Figure 1: (a) Plain computed tomography brain of the child which showed subdural bleed over the right fronto-temporo-parietal region with generalized cerebral oedema. (b and c) A photomicrograph of the right and left retina showed extensive retinal hemorrhages involving multiple layers of the retina (H and E, ×100)|
Click here to view
No surgical intervention was done for the SDH as his prognosis was poor. Eventually, the child succumbed to death 2 days later. During autopsy, external examination of the head revealed no significant injuries and fractures of skull vault or base of the skull. Internal examination of the head showed SDH with 5 g of blood clots seen at the right parietal and the middle cranial fossa. A detailed examination revealed SDH consisting of blood clot mixed with fresh blood but without any brown and/or gelatinous collections [Figure 2]. There was no evidence of head trauma, such as subgaleal hemorrhage of the scalp. The brain was edematous, weighing 1020 g with flattened gyri and obliteration of the sulci. Retinal hemorrhages were seen bilaterally, both grossly and on histological examination [Figure 1]b and [Figure 1]c. Serial tissue sections were taken from the brain and histological examinations of these cut sections revealed numerous vessels, both arteries and veins of various calibers traversing through the brain parenchyma, with abnormally thickened wall separated by gliotic tissue without evidence of prior hemorrhage [Figure 3]. Most of the vessels were veins, even though they appeared to be arterial, due to higher-than-normal pressure in these veins, leading to “arterialization” of the veins. In addition, they become thickened by deposition of collagen in their walls, as highlighted by Masson Trichrome stain [Figure 4]. Several thromboses were also found in the lesions, which are characteristic findings of AVM. In addition, the site of AV anastomosis also could not be identified in any of the tissue sections. Features of diffuse axonal injury of the brain suggestive of direct head trauma were absent under microscopic examination. All these findings were consistent with the diagnosis of AVM.
|Figure 2: Subdural hemorrhage with blood clots seen at the right parietal and the right middle cranial fossa. Typical morphology of arteriovenous malformation described as a tangled network of worm-like vascular channels was not obviously seen in the present case|
Click here to view
|Figure 3: Histological findings of arteriovenous malformation in the cut sections of the brain. (a) A microphotograph shows abnormal vessels with variable calibers and forms (arrow head) traversing through the brain parenchyma (arrow) (H and E, ×40). (b) A microphotograph shows neural tissue in between the abnormally dilated vessels, with gliotic changes (H and E, ×40). (c) The site of arteriovenous anastomosis (arrow head) traversing through the brain parenchyma (arrow) which could not be identified in the tissue section (H and E, ×40). (d) A microphotograph depicts the ruptured arteriovenous malformation with surrounding hemorrhage and thrombosis (arrow head) (H and E, ×40)|
Click here to view
|Figure 4: (a) Photomicrograph shows the presence of arteries (Elastica van Gieson, ×40). (b) The abnormal thickened vessel walls due to deposition of collagen fibers (Masson Trichrome, ×40). (c) The endothelial cells in the abnormal vessels were stained by immunohistochemistry CD31 (×40). (d) Positive immunostaining with SMA, a marker for smooth muscle cells (×40). Positive SMA and CD31 are indications that the vessels are in fact veins and arteries. (e) Negative immunostaining with D2-40, a marker for lymphatic endothelium (×40), further proves that the lesions are vascular in origin|
Click here to view
| Discussion|| |
AVMs are defects in the vascular system, consisting of tangles of abnormal blood vessels (nidus) in which the feeding arteries are directly connected to a venous drainage networkwithout any interpositioning of a capillary bed. Direct AV shunting due to lack of capillaries between the arterial and venous components of AVMs causes hypertrophy of the arterial and venous components of AVMs. Hypothetically, based on the embryological basis of AVMs, they are either due to the persistence of a primitive AV connection or a new connection which develops between the arterial and venous components following a normal closure process. Although the exact mechanisms of how these malformations occur are still unknown, it is postulated that most malformations occur during the 3rd week of embryogenesis. Blamek et al. proposed that AVMs are formed by a mutation early in embryogenesis, during which the absorption of multiple pial-dural subarachnoid veins happens with subsequent dynamic events that lead to growth.
From autopsy findings, the prevalence of AVMs is estimated to be between 0.06% and 0.11%. Although AVMs are less common in pediatric age group, they are still the most frequent abnormality of intracranial circulation in childhood, resulting in spontaneous intraparenchymal hemorrhage in children. Affected children may present with a history of recurrent seizures or headaches,,, hydrocephalus, raised intracranial pressure, papilledema, ataxia, motor weakness, and impaired level of consciousness., AVMs are most commonly located in the supratentorial region, but can also be found in cerebellar hemispheres and vermis. Most cases of cranial AVMs present with hemorrhage, in which, intraparenchymal hemorrhage is the most common feature, followed by intraventricular hemorrhage (IVH) and subarachnoid hemorrhage (SAH). Rarely do they present with SDH. To date, only one case of acute posterior fossa SDH was reported as a result of ruptured cerebellar AVM. These patients displayed signs and symptoms of intraparenchymal hemorrhage, IVH, and SAH because most AVMs are located in the subcortical region and triangular in shape, with the base pointing toward the cerebral cortex and the apex toward the ventricular system. With regard to the retinal hemorrhages, it is undeniable that repeated acceleration-deceleration injury with or without blunt head impact in cases of abusive head trauma may also lead to retinal hemorrhages, subdural hematoma, brain swelling, or encephalopathy and/or occult fractures. In this case, the extensive retinal hemorrhage is most likely due to extensive brain edema and is not associated with any injury or abusive head trauma. The preponderance of evidence points toward vitreoretinal traction as the causative mechanism for the retinal hemorrhage. Repetitive abusive acceleration-deceleration forces may induce direct damage to vessels, perhaps with a secondary disruption of auto-regulation. However, there is little evidence to suggest that increased intracranial or intrathoracic pressure plays a significant role in retinal hemorrhage formation in abusive head trauma. They may have influence in conjunction with other factors such as an imbalance of sodium chemistry, hypoxia, anemia and brain injury-induced coagulopathy, and potential factors currently under study, such as Vitamin C levels and thrombophilia in modulating the appearance of hemorrhages. This is due to the fact that no correlation was found between raised intracranial pressure levels, raised intrathoracic pressure levels, or side of the brain involved with the presence or severity of the retinal hemorrhages. Nonetheless, in this case, we found that the subdural bleeding came from a ruptured AVM involving multiple sites and the subsequent hypoxia led to the development of retinal hemorrhages. Since the pathogenesis of SDH was not known initially, other possible causes of spontaneous SDH were ruled out, such as the underlying coagulopathy disorder, anticoagulant medications, or any intracranial tumors. The child also did not undergo any interventional procedures such as CSF shunting, craniotomy, and lumbar puncture, all of which may lead to spontaneous SDH. Hence, detailed examination of the brain was conducted, which subsequently led to the detection of a cerebral AVM, which in the end disproved the allegation of nonaccidental head injury. This is a rare and unique case with an important learning point where an alleged child abuse death due to head injury was revealed to be actually due to a ruptured AVM. The family alleged that the child was abused by his babysitter. Following hospitalization, a CT scan was performed which showed the presence of SDH. At this point, the actual cause of SDH could not be confirmed; hence, a postmortem was performed which unraveled that SDH in this case was due to natural cause and AVM, instead of child abuse-related trauma.
| Conclusion|| |
This case illustrates the importance of a comprehensive autopsy along with histopathological examination in allegedly nonaccidental head injury cases. This is crucial as the outcome of the autopsy will have legal implications to the alleged perpetrator.
The authors wish to thank the Director-General of Health, Malaysia, for his permission to publish this article. We also like to express our sincere gratitude toward the fellow colleagues, especially Dr. Chng Kay Ly and Dr. Ahmad Zulkefly, for their contributions in this article. Last but not the least, we appreciate the guidance and supervision of the Director of National Institute of Forensic Medicine, Malaysia.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Drake CG. Subdural haematoma from arterial rupture. J Neurosurg 1961;18:597-601.
Kondziolka D, Bernstein M, ter Brugge K, Schutz H. Acute subdural hematoma from ruptured posterior communicating artery aneurysm. Neurosurgery 1988;22:151-4.
McDermott M, Fleming JF, Vanderlinden RG, Tucker WS. Spontaneous arterial subdural hematoma. Neurosurgery 1984;14:13-8.
Byun HS, Patel PP. Spontaneous subdural hematoma of arterial origin: Report of two cases. Neurosurgery 1979;5:611-3.
Datta NN, Chan KY, Kwok JC, Poon CY. Posterior fossa subdural hematoma due to ruptured arteriovenous malformation: Case report. Neurosurgical Focus 2000;8: 2-3.
Di Rocco C, Tamburrini G, Rollo M. Cerebral arteriovenous malformations in children. Acta Neurochir (Wien) 2000;142:145-56.
Humphreys RP, Hoffman HJ, Drake JM, Rutka JT. Choices in the 1990s for the management of pediatric cerebral arteriovenous malformations. Pediatr Neurosurg 1996;25:277-85.
Millar C, Bissonnette B, Humphreys RP. Cerebral arteriovenous malformations in children. Can J Anaesth 1994;41:321-31.
Kiriş T, Sencer A, Sahinbaş M, Sencer S, Imer M, Izgi N, et al.
Surgical results in pediatric Spetzler-Martin Grades I-III intracranial arteriovenous malformations. Childs Nerv Syst 2005;21:69-74.
Hoh BL, Ogilvy CS, Butler WE, Loeffler JS, Putman CM, Chapman PH. Multimodality treatment of nongalenic arteriovenous malformations in pediatric patients. Neurosurgery 2000;47:346-358.
Kondziolka D, Humphreys RP, Hoffman HJ, Hendrick EB, Drake JM. Arteriovenous malformations of the brain in children: A forty year experience. Can J Neurol Sci 1992;19:40-5.
Wilkins RH. Natural history of intracranial vascular malformations: A review. Neurosurgery 1985;16:421-30.
Jankowitz BT, Vora N, Jovin T, Horowitz M. Treatment of pediatric intracranial vascular malformations using onyx-18. J Neurosurg Pediatr 2008;2:171-6.
Choi HJ, Lee JI, Nam KH, Ko JK. Acute spontaneous subdural hematoma due to rupture of a tiny cortical arteriovenous malformation. J Korean Neurosurg Soc 2015;58:547-9.
Gaballah M, Storm PB, Rabinowitz D, Ichord RN, Hurst RW, Krishnamurthy G, et al.
Intraoperative cerebral angiography in arteriovenous malformation resection in children: A single institutional experience. J Neurosurg Pediatr 2014;13:222-8.
Blamek S, Larysz D, Miszczyk L. Stereotactic linac radiosurgery and hypofractionated stereotactic radiotherapy for pediatric arteriovenous malformations of the brain: Experiences of a single institution. Childs Nerv Syst 2013;29:651-6.
Matson DD, Ingraham FD. Neurosurgery of Infancy and Childhood. United Kingdom: Thomas; 1969.
Zheng T, Wang QJ, Liu YQ, Cui XB, Gao YY, Lai LF, et al.
Clinical features and endovascular treatment of intracranial arteriovenous malformations in pediatric patients. Childs Nerv Syst 2014;30:647-53.
Nair AP, Kumar R, Mehrotra A, Srivastava AK, Sahu RN, Nair P, et al.
Clinical, radiological profile and outcome in pediatric Spetzler-Martin Grades I-III arteriovenous malformations. Childs Nerv Syst 2012;28:593-8.
Matsumura H, Makita Y, Someda K, Kondo A. Arteriovenous malformations in the posterior fossa. J Neurosurg 1977;47:50-6.
Sturm V, Knecht PB, Landau K, Menke MN. Rare retinal haemorrhages in translational accidental head trauma in children. Eye (Lond) 2009;23:1535-41.
Schloff S, Mullaney PB, Armstrong DC, Simantirakis E, Humphreys RP, Myseros JS,et al
. Retinal findings in children with intracranial hemorrhage. Ophthalmology 2002;109:1472-6.
Marshall DH, Brownstein S, Dorey MW, Addison DJ, Carpenter B. The spectrum of postmortem ocular findings in victims of shaken baby syndrome. Can J Ophthalmol 2001;36:377-83.
[Figure 1], [Figure 2], [Figure 3], [Figure 4]