Pcdiatr Ncurosurg 1991-92:17:163-168
©1991-92 S. Karger AG. Basel 10 16-2291/9I -92/0173-0163 S 2.75/0
Complications of Hemorrhagic Stroke in Children Robin P. Humphreys Department of Surgery and Anatomy, University of Toronto, and Division of Neurosurgery. The Hospital for Sick Children. Toronto. Canada
Key Words. Stroke Pediatric • Complications • Arteriovenous malformations • Intracranial aneurysm • Coagulation disorders Abstract. The complications of hemorrhagic stroke in children begin first with one's failure to establish the correct diagnosis or from the lack of knowledge of attendant phenomena and second, from those events which occur before, during or because of the treatment provided for specific lesions. The fundamental principles of history gathering, clin ical evaluation and appropriate neuroimaging will direct safe, uncomplicated patient care. This paper will examine those complications which may arise during the treatment of pediatric aneurysm, arteriovenous malformation and venous angiomas, newborn intraventricular hemorrhage, and cerebral hemorrhage associated with either a preexistent coagulopathy or neoplasm.
The problem of stroke in children was put into perspec tive by the 1973 Report of the Joint Committee for Stroke Facilities [ 1]. Children can suffer either ischemic or he morrhagic cerebrovascular events but from causes which differ from such occurrences in adults. Hence several ce rebrovascular hemorrhagic events may happen in the pe diatric age group (table 1). The complications which may result from these conditions begin first with the failure to establish the correct diagnosis or from the lack of appreci ation of the attendant phenomena and second, from those which occur before, during or because of the treatment provided for specific lesions. This paper will examine the complications which may arise from some of the lesions capable of producing hem orrhage within the child’s nervous system.
Table 1. Causes of hemorrhagic stroke in childhood Structural abnormalities of the intracranial vasculature Arterial aneurysms Vascular malformations Venous and sinus occlusive disease Intraventricular/parenchymal hemorrhage in the newborn Germinal matrix/choroid plexus/AVM Hematological disorders Leukemia Thrombocytopenia Hemophilia Sickle cell disease Neoplasia Hemorrhage into preexistent neoplasm Substance abuse Amphetamines
While there are certain recognizable settings for the ap pearance of cerebrovascular disease in the adult, the warn ings of stroke in children are notable by their absence. With the exception of the vein of Galen malformation in the infant which presents with unexplained congestive heart failure, or the presence of another major system dis-
order capable of causing brain hemorrhage, most chil dren's strokes occur as a totally unexpected neurologic ictus. Furthermore, because of the relative rarity of pedi atric stroke, the clinician may be mislead into believing that the current neurologic event is due to a more common childhood malady.
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The Clinical Evaluation Most often the child with a cerebral hemorrhage is quite ill. The neurosurgeon is advised to seek expert pedi atric medical advice when the possibility of an associated major system abnormality exists. If an infant is also in heart failure from a high-flow intracranial arterial-venous fistula or the older child has a coincident coagulation dis turbance then such consultations can only provide infor mation which will assist in the best treatment path for the child |2|. Moreover, the neurosurgeon may have to stand aside while the cardiologist or hematologist initiates their treatment in order to make the rest of the operative care safe for the surgeon and child. For the neurosurgeon to begin treatment without full appreciation of the causes of the stroke may lead to troubling consequences. The Nature and Timing o f Neuroimaging The first computed tomographic (CT) scan will in most circumstances show blood in brain parenchyma, ventricu lar cavity and /or subarachnoid spaces. It must now be de cided whether additional neuroimaging is required and if so of what kind. For example, computed tomography is all that is required for the child who suffers an intracranial bleed in association with leukemia or another coagulopa thy. But if it cannot be determined whether the hemor rhage arose because of a structural abnormality of blood vessels or a preexistent tumor, then additional imaging is necessary. While magnetic resonance imaging (MRI) might provide new information, the safety and time taken to obtain such in a very ill child who requires respiratory support could preclude the study. If the CT scan suggests that an intracranial aneurysm or arteriovenous malfor mation (AVM) is responsible for the child's hemorrhage, then ‘aggressive and intensive angiographic study’ is necessary to understand ‘their morphology and charac
teristics’ [3J. The decision to proceed with urgent arte riography must be based on the acuteness of the child’s condition, and the timing and intentions of operative inter vention.
Complications Relating to Lesions The various lesions of particular interest to the surgeon which are capable of producing cerebral hemorrhage will be examined with regard to the complications which may result from their preoperative and surgical treatment. At tention will also be paid to complication avoidance. Intracranial Aneurysms The symptomatic intracranial aneurysm is so uncom mon in children that a discussion of the complications re lating to its care could not be as exhaustive as those for treatment of the adult problem. For the adult, the mortal ity and morbidity relating to the aneurysm depend on the condition of the patient at the time of surgery, the time span since the last subarachnoid hemorrhage (SAH). the nature of the procedure performed, and the experience and judgement of the surgeon [4]. The specific features which relate to the aneurysm which occurs in the child, and which in turn may influence the care given are [5] as fol lows. (A) The incidental, unruptured aneurysm is so ex traordinarily rare in children [3] that every effort should be taken to prove that such a suspected lesions is indeed an aneurysm. If so proven, then the aneurysm’s obliteration is recommended given the child's anticipated life span. (B) The congenital saccular aneurysm may not necessari ly be found nestled in the crotch of two vessels nor have a definable neck. The surgeon should expect unusual vascu lar anatomy with regard to the location of the aneurysm. (C) An unusual number are giant aneurysms, a fact which may not be appreciated from preoperative arteriography because of partial thrombosis within the sac. (D) At least 20% of children's intracranial aneurysms will have a my cotic or traumatic origin, and these possibilities must be kept in mind during treatment. For example, the mycotic aneurysm on occasion will spontaneously thrombose. (E) Most children declare their intracranial aneurysm with SAH. Unfortunately, as few as 15% will present in a good SAH grade. (F) The operative treatment of a child’s aneu rysm will on occasion require certain unorthodox or inno vative techniques for its obliteration. With these idiosyncrasies of the child's aneurysm in mind, the treating surgeon will have a little more advan tage with regard to the prevention of complications.
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The History Is Critical For the most part, the child’s past medical history is un varnished and can be quickly gathered. It is critical that the physician match the child’s present neurologic condi tion with the alleged events leading up to it as well as any other relevant past medical data. Accurate historical infor mation is necessary to guide the surgeon through the correct diagnostic and treatment paths. What is the rele vance of any of the omnipresent head injury mentioned in almost every child’s past history? A child found uncon scious on the floor is usually thought to have suffered an injury instead of a spontaneous intracranial hemorrhage. That attitude may prompt incorrect investigation and treatment.
Arteriovenous Malformations The special features of AVM management with regard to complication avoidance are the following. Angiographically Occult Lesions. Some vascular mal formations are angiographically ‘cryptic' and might there fore seem innocent [6|. These lesions usually lie within the middle cerebral artery territory but are not demonstrat ed on arteriography. They represent potential complica tions for two reasons: (a) an apparently simple operation for a clot or seizure focus may become a little more trying if a small tangle of vessels is encountered, and (b) even when an AVM is suspected and a hematoma removed, the location of the AVM vessels may be quite uncertain and their residual may trigger a subsequent delayed hemor rhage. Postoperative arteriography is mandatory in this circumstance. Whether to Operate? This question is not often faced by the surgeon who treats the child with a cerebral AVM as in the majority of children the lesion has bled and an op eration must proceed to evacuate hematoma and remove the malformation [7], But there will be a few cases where the malformation is deep, small and buried in critical tis sue (e.g. hypothalamus, or brain stem) and where it may be possible to remove clot, but not the nidus. For these children as well as the few who have had a single convul sion from a large rolandic region lesion, the decision to operate will be difficult indeed. Alternative therapies must be considered. The complications - hemorrhage and seizures - of the untreated arteriovenous malformation have been studied in some detail over the last several years. Recent reports for adults indicate that the rate of major rebleeding is 4% per year and the mortality 1% per year |8]. The combined rate of major morbidity and mortality is 2.7% per year. Naturally, figures are not available for children. But given that a greater number of children (79%) present with hem orrhage than do adults (62%), and that the mortality from the child’s AVM which bleeds is 25%. we have concluded on the basis of our studies that for a 10-year-old child with an AVM which has bled once, the chance of dying from SAH over the next 70 years is 20%. This compares with a risk of 29% mortality in adults over a 20-year period [91. Wherever possible, we recommend excision of the lesion to protect the child against future bleeding episodes. The Timing o f Surgery. AVM surgery is usually diffi cult, and should ideally be carried out under optimum con ditions. Complications arise when the case extends over many hours, and the operating team becomes fatigued. Troublesome bleeding within the malformation can be ex asperating, and the surgeon who is fatigued and impatient
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will run the risk of accelerating an annoying situation to one which borders on the dangerous. It is our advice that unless a life-threatening clot requires urgent evacuation, the definitive operation should wait for an arbitrary period of 2-7 days and then be carried out as a well-planned de liberate effort. The entire team can prepare their strategies, the artériographie studies be fully examined and most of all the surgeon be thoroughly rested. Locations o f AVM. The child's AVM is often small and awkwardly situated. Some thought to lie on the cerebral surface are instead buried just below it and have as their only sign an unusually straightened artery which takes an unexpected turn and disappears into a sulcus. If the sur geon is not aware of this possibility, then harm may come if random dissection proceeds. Complications may also arise if the surgeon does not properly plan the approach for the lesions which lie along the midline structures and are similarly hidden just below the cortex. In effect, the surgeon will be working around at least one right angle to circumscribe a lesion which for example is located in the medial right occipi tal lobe. Deep Choroidal Supply. The commonest complication arising during the management of the child’s AVM is one’s failure to recognize the choroidal contribution to the malformation. The posterior choroidal system in particu lar supplies many of these lesion and it can be responsible for deep bleeding in the AVM bed at a time when it was thought that the malformation otherwise had been ex cised. The residual nidus of the malformation is that part glued onto the choroid plexus. One’s discipline in this matter is not to consider the lesion totally removed until the ventricular cavity. CSF and choroid plexus have been visualized. The Single Draining Vein. All neurosurgeons are aware of the hazards which arise if the venous drainage to an AVM is sacrified before all of the arterial input has been obliterated. A conscious effort is thus made to protect at least one vein during the dissection about the malforma tion. This rule is paramount in the child as very frequent ly there is only one major draining vein from the entire le sion. Although there are frequently minor exit routes through the choroidal venous system, the surgeon should not rely upon those and instead protect the major superfi cial draining vein until the end of the case. The surgeon should not be disheartened if that vein remains ‘red’ until the very end even when all other deep connections have been severed. Characteristically there is a small artery which runs beneath the dilated vein and both structures are thus clipped and divided simultaneously.
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Complications of Hemorrhagic Stroke in Children
Residual Malformation/Recurrent Bleeding. The ex perienced surgeon usually knows whether total removal of a cerebral AVM has been achieved by the conclusion of the case. On the one hand a deliberate decision may have been made to stage the procedure, with a second attempt planned after an interval. There will be other times when the postoperative arteriogram (mandatory) shows resi dual malformation and a reoperation becomes necessary to excise the residual lesion. Such is also responsible for con tinued bleeding in the bed of the malformation, which tends to arise from tiny ‘coils’ of vessels lying within the adjacent brain white matter. These must be circumscribed and excised. Normal Perfusion Pressure Breakthrough. The phe nomenon of 'breakthrough' as originally described has not been encountered in our children [10]. That may repre sent the combination of the small size of many pediatric AVMs and the protection which children have with regard to their cerebral circulation. Ischemic symptoms alone with evidence of poor filling of the normal hemispheral branches because of the sump effect of the AVM are not characteristic features seen in children’s arteriograms. Neurologic Deficit. Children show a remarkable degree of recovery after treatment of their AVM and associated cerebral hemorrhage. What begins as a substantial neuro logic deficit improves dramatically after the malformation entangled in gliotic brain tissue is excised. With the intent of total removal of the lesion, we found that 27% of chil dren had a fixed neurologic deficit postoperatively |7|. This usually relates to the extent of the cerebral hemato ma. which is present preoperatively. Postoperative Seizures. A postoperative seizure disor der is not a common occurrence after removal of a child's AVM. Indeed, 70-73% of patients with a chronic seizure disturbance relating to cerebral AVM will be complete ly free of such events after surgical excision of the lesion 17, 11, 12]. There is however an 11% risk of postopera tive convulsions developing in children who did not have seizures preoperatively [71. The child with a large ce rebral hematoma is particularly liable to this complication. Complications o f Interventional Intravascular Proce dures. Complications from interventional procedures arise from emboli passing into normal arteries, or when bal loons or glue do not remain at the target [13], An addition al hazard from the latter technique occurs when the glue bonds the introductory catheter in situ. Venous Angiomas With more neuroimaging being performed for a varie ty of neurologic complaints, the venous angioma is more
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common than previously known. Recent studies have in dicated that many of these lesions have no associated symptoms [14|. However, in some instances, the lesion may be complicated by hemorrhage (distinctly uncom mon), seizures or transient focal deficits. The risk of these complications is low, and likely far less than the risks to be encountered if the lesion is excised [14]. These lesions run a benign course and the angioma represents physiological ly essential venous drainage from the brain. There have been experiences with the attempted resection of a venous angioma and associated hematoma, which have had disasterous outcomes. Intraventricular Hemorrhage in the Newborn The complication of note is the failure to recognize the cause of a spontaneous intraventricular hemorrhage which occurs in a full-term neonate. Such may be dismissed as a variant of a germinal plate hemorrhage, when instead in a few instances a structural vascular lesion is responsible [15]. A certain skepticism on the part of the clinician is re quired when assessing these babies and the case must be studied thoroughly with MRI and arteriography. If de fined, the lesion must be removed. Cerebral Hemorrhage Associated with Coagulopathy The cerebral hemorrhage which occurs in association with a coagulopathy may occur at the time of first diagno sis, or as a terminal event in a child whose blood dyscrasia has been under treatment for some time. To avoid the complications of recurrent or continued bleeding in the child with an otherwise benign coagulopathy the surgeon must seek expert hematological assistance so that the medical and surgical programs can be coordinated [2. 16|. For example, the child who has suffered an intracranial hemorrhage in association with idiopathic thrombocyto penic purpura must first have the diagnosis confirmed by bone marrow aspiration. Emergency splenectomy is next required in patients with subarachnoid or parenchymal hemorrhage who also show evidence of bleeding at other sites at the time of diagnosis of the intracranial hemor rhage. After platelet transfusion, craniotomy for hemato ma evacuation is then performed. An algorithm for varia tions of this theme in idiopathic thrombocytopenic purpu ra has been designed to assist the surgeon and to avoid complications 1161. Similarly, the most crucial factor in the management of hemorrhage in a patient with hemophilia is the coopera tive interaction between hematologist and surgeon. The hematologist must establish the diagnosis of the clotting disorder, assay the factor level and. where applicable -
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Cerebral Hemorrhage Associated with a Preexistent Neoplasm Cerebral neoplasms are far more common in children than are events of spontaneous hemorrhage. Therefore one must maintain a skeptical attitude when viewing a child's CT scan which shows only parenchymal clot. Does this represent an isolated hemorrhagic stroke or did the bleed occur into a preexistent tumor? If one presumed the for mer then one might be inclined to allow the hematoma to resolve without further diagnostic intervention. Or. at the time of craniotomy, one might fail to biopsy appropriate tissues for tumor sampling. The following may assist with the distinction between the two conditions. (A) Preexis tent neurologic symptoms (including headache) are very rare in the child with a structural vascular cause for their stroke whereas there is often a suggestion of some prior neurologic mischief in the patient who has bled into a tumor. (B) The location of the hematoma (on CT scan) when it relates to a preexistent tumor tends to be in sites where tumors occur in children - centrum semiovale of hemispheres, brain stem parenchyma and in the lateral cerebellum or vermis. (C) The bleeding from a tumor with rare exceptions remains confined to the substance of the tumor, whereas that in association with an aneurysm is dispersed in addition through the subarachnoid space or into the adjacent ventricle when an AVM has bled. (D) It is unusual for an AVM hematoma to be surrounded by brain edema, whereas such may be detected around the clot of a tumor which has bled. (E) Additional nuances such as obvious feeding or draining vessels in an AVM or enhancing solid tissue may distinguish the primary vascu lar problem from the tumor, respectively, on the enhanced CT or MRI studies. (F) All of the tumor tissue may be de stroyed when some tumors bleed. Even so, if the surgeon is suspicious during the operation that the margins of the hematoma have an appearance out of keeping with an or dinary clot cavity, then tissue biopsy of the margins is mandatory.
Conclusions During the surgeon's first encounter with the child who has suffered a hemorrhagic stroke, the following should
be observed. ( I) Maintain an open mind as to the wide va riety of causes of brain hemorrhage in the child (table 1). (2) Assess the historical information with those potential causes in mind. (3) Request appropriate consultations when the information suggests a multisystem disorder. (4) Structure the neuroinvestigations around the acuity of the child’s illness, and in particular determine whether and when cerebral arteriography will be required. (5) Once the investigational data has suggested the most likely diagno sis, determine the goals of operative intervention, and. more importantly, when surgery should proceed. What are the risk and benefits of ‘early’ verus ‘late’ operation, and what else should be in place before surgery? (6) Regard less of the perceived success of the operative intervention, the case must be studied postoperatively with appropriate imaging - particularly arteriography for the child with an excised AVM.
References 1 Gold AP, Challenor YP Gilles PH. Hillel SP, Leviton A. Rolins HI. Solomon GE. Stein BM: Report of the Joint Committee for Stroke Facilities. IX. Strokes in children (part I). J Stroke 1973;4:835-858. 2 Humphreys RP Hockley AD. Freedman MH. Saunders EF: Man agement of intracerebal hemorrhage in idiopathic thrombocytope nic purpura. Report of four cases. J Neurosurg 1976;45:700-704. 3 Harwood-Nash DC. Fitz. CR: Neuroradioigoy in Infants and Chil dren. St. Louis. Mosby.1976. vol. 3. pp902-964. 4 Horowitz NH. Rizzoli J V: Postoperative Complications of Intracra nial Neurological Surgery . Baltimore. Williams & Wilkins. 1982, pp 182-235. 5 Humphreys RP: Intracranial arterial aneurysms: in Edwards MSB. Hoffman HJ (eds): Cerebral Vascular Disease in Children. Balti more. Williams & Wilkins. 1989. pp 247-254. 6 Cohen HCM. Tucker WS. Humphreys RP Perrin RG: Angiographically occult histologically verified cerebrovascular malformations. Neurosurgery 1982:10:7(M-714. 7 Kondziolka D. Humphreys RP Hoffman HJ. Hendrick EB. Drake JM: Arteriovenous malformations in the brain in children: A forty year experience with 132 cases. Can J Neurol Sei 1992:19:40-45. 8 Ondra SL. Troupp H. George ED. Schwab K: The natural history of symptomatic arteriovenous malformations of the brain: A 24-year follow-up assessment. J Neurosurg 1990:73:387-391. 9 Brown RD Jr. Wiebers DO. Forbes G. O'Fallon WM. Piepgras DG. Marsh WR. Maciunas RJ: The natural history of unruptured intracranial arteriovenous malformations. J Neurosurg 1988; 68:352-357. 10 Spetzler RF. Wilson CB. Weinstein P Mehdorn M. Townsend J. Tel les D: Normal perfusion pressure breakthrough theory. Clin Neuro surg 1977;25:651-672. 11 Leblanc R. Fcindel W. Ethier R: Epilepsy from cerebral arterio venous malformations. Can J Neurol Sei 1983:10:91-95. 12 Yell HS. Kashiwagi S. Tew JM. BergerTS: Surgical management of
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particularly for any patient who is to undergo major sur gery, identify the presence of inhibitor to the missing pro coagulant, a problem in about 10% of patients with hemo philia [ 16J. All of these initiatives are required before the surgeon acts.
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epilepsy associaled with cerebral arteriovenous malformations. J Neurosurg 1990;72:216-223. 13 Tranmer Bl. Humphreys RP. Chuang SH-C: Microsurgical recovery of a migrated balloon from the internal carotid artery of a child. Neurosurgery 1985; 16:381 -386. 14 Garner TB. Curling OD Jr, Kelly DL Jr, Laster DW: The natural history of intracranial venous angiomas. J Neurosurg 1991:75: 715-722. 15 Heafner MD. Duncan CC. Kier EL, Ment LR. Scott DT. Kolaski R. Sorgen C: Intraventricular hemorrhage in a term neonate secondary to a third ventricular AVM. Case report. J Neurosurg 1985:63: 640-643.
16 Crone KR. Humphreys RP: Hemophilia and other coagulopathies: in Section of Pediatric Neurosurgery. AANS (eds): Pediatric Neuro surgery. ed 2. Baltimore. Williams & Wilkins. 1989. pp 517-523.
Dr. Robin P. Humphreys Division of Neurosurgery The Hospital for Sick Children Rm. 1504. 555 University Avenue Toronto. Ont.. M5G 1X8 (Canada)
In the article ‘Pathophysiology of Isolated Lateral Ventriculomegaly in Shunted Myelodysplastic Children' by Berger M.S.. el al.. Pediatr Neurosurg 1990-91:16:301-304. figure 2c in plate I is upside down and should be rotated by 180°.
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Erratum
©1991-92 S. Karger AG. Basel 10 16-2291/9I -92/0173-0163 S 2.75/0
Complications of Hemorrhagic Stroke in Children Robin P. Humphreys Department of Surgery and Anatomy, University of Toronto, and Division of Neurosurgery. The Hospital for Sick Children. Toronto. Canada
Key Words. Stroke Pediatric • Complications • Arteriovenous malformations • Intracranial aneurysm • Coagulation disorders Abstract. The complications of hemorrhagic stroke in children begin first with one's failure to establish the correct diagnosis or from the lack of knowledge of attendant phenomena and second, from those events which occur before, during or because of the treatment provided for specific lesions. The fundamental principles of history gathering, clin ical evaluation and appropriate neuroimaging will direct safe, uncomplicated patient care. This paper will examine those complications which may arise during the treatment of pediatric aneurysm, arteriovenous malformation and venous angiomas, newborn intraventricular hemorrhage, and cerebral hemorrhage associated with either a preexistent coagulopathy or neoplasm.
The problem of stroke in children was put into perspec tive by the 1973 Report of the Joint Committee for Stroke Facilities [ 1]. Children can suffer either ischemic or he morrhagic cerebrovascular events but from causes which differ from such occurrences in adults. Hence several ce rebrovascular hemorrhagic events may happen in the pe diatric age group (table 1). The complications which may result from these conditions begin first with the failure to establish the correct diagnosis or from the lack of appreci ation of the attendant phenomena and second, from those which occur before, during or because of the treatment provided for specific lesions. This paper will examine the complications which may arise from some of the lesions capable of producing hem orrhage within the child’s nervous system.
Table 1. Causes of hemorrhagic stroke in childhood Structural abnormalities of the intracranial vasculature Arterial aneurysms Vascular malformations Venous and sinus occlusive disease Intraventricular/parenchymal hemorrhage in the newborn Germinal matrix/choroid plexus/AVM Hematological disorders Leukemia Thrombocytopenia Hemophilia Sickle cell disease Neoplasia Hemorrhage into preexistent neoplasm Substance abuse Amphetamines
While there are certain recognizable settings for the ap pearance of cerebrovascular disease in the adult, the warn ings of stroke in children are notable by their absence. With the exception of the vein of Galen malformation in the infant which presents with unexplained congestive heart failure, or the presence of another major system dis-
order capable of causing brain hemorrhage, most chil dren's strokes occur as a totally unexpected neurologic ictus. Furthermore, because of the relative rarity of pedi atric stroke, the clinician may be mislead into believing that the current neurologic event is due to a more common childhood malady.
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Complications Related to Diagnosis
Humphreys
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The Clinical Evaluation Most often the child with a cerebral hemorrhage is quite ill. The neurosurgeon is advised to seek expert pedi atric medical advice when the possibility of an associated major system abnormality exists. If an infant is also in heart failure from a high-flow intracranial arterial-venous fistula or the older child has a coincident coagulation dis turbance then such consultations can only provide infor mation which will assist in the best treatment path for the child |2|. Moreover, the neurosurgeon may have to stand aside while the cardiologist or hematologist initiates their treatment in order to make the rest of the operative care safe for the surgeon and child. For the neurosurgeon to begin treatment without full appreciation of the causes of the stroke may lead to troubling consequences. The Nature and Timing o f Neuroimaging The first computed tomographic (CT) scan will in most circumstances show blood in brain parenchyma, ventricu lar cavity and /or subarachnoid spaces. It must now be de cided whether additional neuroimaging is required and if so of what kind. For example, computed tomography is all that is required for the child who suffers an intracranial bleed in association with leukemia or another coagulopa thy. But if it cannot be determined whether the hemor rhage arose because of a structural abnormality of blood vessels or a preexistent tumor, then additional imaging is necessary. While magnetic resonance imaging (MRI) might provide new information, the safety and time taken to obtain such in a very ill child who requires respiratory support could preclude the study. If the CT scan suggests that an intracranial aneurysm or arteriovenous malfor mation (AVM) is responsible for the child's hemorrhage, then ‘aggressive and intensive angiographic study’ is necessary to understand ‘their morphology and charac
teristics’ [3J. The decision to proceed with urgent arte riography must be based on the acuteness of the child’s condition, and the timing and intentions of operative inter vention.
Complications Relating to Lesions The various lesions of particular interest to the surgeon which are capable of producing cerebral hemorrhage will be examined with regard to the complications which may result from their preoperative and surgical treatment. At tention will also be paid to complication avoidance. Intracranial Aneurysms The symptomatic intracranial aneurysm is so uncom mon in children that a discussion of the complications re lating to its care could not be as exhaustive as those for treatment of the adult problem. For the adult, the mortal ity and morbidity relating to the aneurysm depend on the condition of the patient at the time of surgery, the time span since the last subarachnoid hemorrhage (SAH). the nature of the procedure performed, and the experience and judgement of the surgeon [4]. The specific features which relate to the aneurysm which occurs in the child, and which in turn may influence the care given are [5] as fol lows. (A) The incidental, unruptured aneurysm is so ex traordinarily rare in children [3] that every effort should be taken to prove that such a suspected lesions is indeed an aneurysm. If so proven, then the aneurysm’s obliteration is recommended given the child's anticipated life span. (B) The congenital saccular aneurysm may not necessari ly be found nestled in the crotch of two vessels nor have a definable neck. The surgeon should expect unusual vascu lar anatomy with regard to the location of the aneurysm. (C) An unusual number are giant aneurysms, a fact which may not be appreciated from preoperative arteriography because of partial thrombosis within the sac. (D) At least 20% of children's intracranial aneurysms will have a my cotic or traumatic origin, and these possibilities must be kept in mind during treatment. For example, the mycotic aneurysm on occasion will spontaneously thrombose. (E) Most children declare their intracranial aneurysm with SAH. Unfortunately, as few as 15% will present in a good SAH grade. (F) The operative treatment of a child’s aneu rysm will on occasion require certain unorthodox or inno vative techniques for its obliteration. With these idiosyncrasies of the child's aneurysm in mind, the treating surgeon will have a little more advan tage with regard to the prevention of complications.
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The History Is Critical For the most part, the child’s past medical history is un varnished and can be quickly gathered. It is critical that the physician match the child’s present neurologic condi tion with the alleged events leading up to it as well as any other relevant past medical data. Accurate historical infor mation is necessary to guide the surgeon through the correct diagnostic and treatment paths. What is the rele vance of any of the omnipresent head injury mentioned in almost every child’s past history? A child found uncon scious on the floor is usually thought to have suffered an injury instead of a spontaneous intracranial hemorrhage. That attitude may prompt incorrect investigation and treatment.
Arteriovenous Malformations The special features of AVM management with regard to complication avoidance are the following. Angiographically Occult Lesions. Some vascular mal formations are angiographically ‘cryptic' and might there fore seem innocent [6|. These lesions usually lie within the middle cerebral artery territory but are not demonstrat ed on arteriography. They represent potential complica tions for two reasons: (a) an apparently simple operation for a clot or seizure focus may become a little more trying if a small tangle of vessels is encountered, and (b) even when an AVM is suspected and a hematoma removed, the location of the AVM vessels may be quite uncertain and their residual may trigger a subsequent delayed hemor rhage. Postoperative arteriography is mandatory in this circumstance. Whether to Operate? This question is not often faced by the surgeon who treats the child with a cerebral AVM as in the majority of children the lesion has bled and an op eration must proceed to evacuate hematoma and remove the malformation [7], But there will be a few cases where the malformation is deep, small and buried in critical tis sue (e.g. hypothalamus, or brain stem) and where it may be possible to remove clot, but not the nidus. For these children as well as the few who have had a single convul sion from a large rolandic region lesion, the decision to operate will be difficult indeed. Alternative therapies must be considered. The complications - hemorrhage and seizures - of the untreated arteriovenous malformation have been studied in some detail over the last several years. Recent reports for adults indicate that the rate of major rebleeding is 4% per year and the mortality 1% per year |8]. The combined rate of major morbidity and mortality is 2.7% per year. Naturally, figures are not available for children. But given that a greater number of children (79%) present with hem orrhage than do adults (62%), and that the mortality from the child’s AVM which bleeds is 25%. we have concluded on the basis of our studies that for a 10-year-old child with an AVM which has bled once, the chance of dying from SAH over the next 70 years is 20%. This compares with a risk of 29% mortality in adults over a 20-year period [91. Wherever possible, we recommend excision of the lesion to protect the child against future bleeding episodes. The Timing o f Surgery. AVM surgery is usually diffi cult, and should ideally be carried out under optimum con ditions. Complications arise when the case extends over many hours, and the operating team becomes fatigued. Troublesome bleeding within the malformation can be ex asperating, and the surgeon who is fatigued and impatient
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will run the risk of accelerating an annoying situation to one which borders on the dangerous. It is our advice that unless a life-threatening clot requires urgent evacuation, the definitive operation should wait for an arbitrary period of 2-7 days and then be carried out as a well-planned de liberate effort. The entire team can prepare their strategies, the artériographie studies be fully examined and most of all the surgeon be thoroughly rested. Locations o f AVM. The child's AVM is often small and awkwardly situated. Some thought to lie on the cerebral surface are instead buried just below it and have as their only sign an unusually straightened artery which takes an unexpected turn and disappears into a sulcus. If the sur geon is not aware of this possibility, then harm may come if random dissection proceeds. Complications may also arise if the surgeon does not properly plan the approach for the lesions which lie along the midline structures and are similarly hidden just below the cortex. In effect, the surgeon will be working around at least one right angle to circumscribe a lesion which for example is located in the medial right occipi tal lobe. Deep Choroidal Supply. The commonest complication arising during the management of the child’s AVM is one’s failure to recognize the choroidal contribution to the malformation. The posterior choroidal system in particu lar supplies many of these lesion and it can be responsible for deep bleeding in the AVM bed at a time when it was thought that the malformation otherwise had been ex cised. The residual nidus of the malformation is that part glued onto the choroid plexus. One’s discipline in this matter is not to consider the lesion totally removed until the ventricular cavity. CSF and choroid plexus have been visualized. The Single Draining Vein. All neurosurgeons are aware of the hazards which arise if the venous drainage to an AVM is sacrified before all of the arterial input has been obliterated. A conscious effort is thus made to protect at least one vein during the dissection about the malforma tion. This rule is paramount in the child as very frequent ly there is only one major draining vein from the entire le sion. Although there are frequently minor exit routes through the choroidal venous system, the surgeon should not rely upon those and instead protect the major superfi cial draining vein until the end of the case. The surgeon should not be disheartened if that vein remains ‘red’ until the very end even when all other deep connections have been severed. Characteristically there is a small artery which runs beneath the dilated vein and both structures are thus clipped and divided simultaneously.
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Complications of Hemorrhagic Stroke in Children
Residual Malformation/Recurrent Bleeding. The ex perienced surgeon usually knows whether total removal of a cerebral AVM has been achieved by the conclusion of the case. On the one hand a deliberate decision may have been made to stage the procedure, with a second attempt planned after an interval. There will be other times when the postoperative arteriogram (mandatory) shows resi dual malformation and a reoperation becomes necessary to excise the residual lesion. Such is also responsible for con tinued bleeding in the bed of the malformation, which tends to arise from tiny ‘coils’ of vessels lying within the adjacent brain white matter. These must be circumscribed and excised. Normal Perfusion Pressure Breakthrough. The phe nomenon of 'breakthrough' as originally described has not been encountered in our children [10]. That may repre sent the combination of the small size of many pediatric AVMs and the protection which children have with regard to their cerebral circulation. Ischemic symptoms alone with evidence of poor filling of the normal hemispheral branches because of the sump effect of the AVM are not characteristic features seen in children’s arteriograms. Neurologic Deficit. Children show a remarkable degree of recovery after treatment of their AVM and associated cerebral hemorrhage. What begins as a substantial neuro logic deficit improves dramatically after the malformation entangled in gliotic brain tissue is excised. With the intent of total removal of the lesion, we found that 27% of chil dren had a fixed neurologic deficit postoperatively |7|. This usually relates to the extent of the cerebral hemato ma. which is present preoperatively. Postoperative Seizures. A postoperative seizure disor der is not a common occurrence after removal of a child's AVM. Indeed, 70-73% of patients with a chronic seizure disturbance relating to cerebral AVM will be complete ly free of such events after surgical excision of the lesion 17, 11, 12]. There is however an 11% risk of postopera tive convulsions developing in children who did not have seizures preoperatively [71. The child with a large ce rebral hematoma is particularly liable to this complication. Complications o f Interventional Intravascular Proce dures. Complications from interventional procedures arise from emboli passing into normal arteries, or when bal loons or glue do not remain at the target [13], An addition al hazard from the latter technique occurs when the glue bonds the introductory catheter in situ. Venous Angiomas With more neuroimaging being performed for a varie ty of neurologic complaints, the venous angioma is more
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common than previously known. Recent studies have in dicated that many of these lesions have no associated symptoms [14|. However, in some instances, the lesion may be complicated by hemorrhage (distinctly uncom mon), seizures or transient focal deficits. The risk of these complications is low, and likely far less than the risks to be encountered if the lesion is excised [14]. These lesions run a benign course and the angioma represents physiological ly essential venous drainage from the brain. There have been experiences with the attempted resection of a venous angioma and associated hematoma, which have had disasterous outcomes. Intraventricular Hemorrhage in the Newborn The complication of note is the failure to recognize the cause of a spontaneous intraventricular hemorrhage which occurs in a full-term neonate. Such may be dismissed as a variant of a germinal plate hemorrhage, when instead in a few instances a structural vascular lesion is responsible [15]. A certain skepticism on the part of the clinician is re quired when assessing these babies and the case must be studied thoroughly with MRI and arteriography. If de fined, the lesion must be removed. Cerebral Hemorrhage Associated with Coagulopathy The cerebral hemorrhage which occurs in association with a coagulopathy may occur at the time of first diagno sis, or as a terminal event in a child whose blood dyscrasia has been under treatment for some time. To avoid the complications of recurrent or continued bleeding in the child with an otherwise benign coagulopathy the surgeon must seek expert hematological assistance so that the medical and surgical programs can be coordinated [2. 16|. For example, the child who has suffered an intracranial hemorrhage in association with idiopathic thrombocyto penic purpura must first have the diagnosis confirmed by bone marrow aspiration. Emergency splenectomy is next required in patients with subarachnoid or parenchymal hemorrhage who also show evidence of bleeding at other sites at the time of diagnosis of the intracranial hemor rhage. After platelet transfusion, craniotomy for hemato ma evacuation is then performed. An algorithm for varia tions of this theme in idiopathic thrombocytopenic purpu ra has been designed to assist the surgeon and to avoid complications 1161. Similarly, the most crucial factor in the management of hemorrhage in a patient with hemophilia is the coopera tive interaction between hematologist and surgeon. The hematologist must establish the diagnosis of the clotting disorder, assay the factor level and. where applicable -
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Cerebral Hemorrhage Associated with a Preexistent Neoplasm Cerebral neoplasms are far more common in children than are events of spontaneous hemorrhage. Therefore one must maintain a skeptical attitude when viewing a child's CT scan which shows only parenchymal clot. Does this represent an isolated hemorrhagic stroke or did the bleed occur into a preexistent tumor? If one presumed the for mer then one might be inclined to allow the hematoma to resolve without further diagnostic intervention. Or. at the time of craniotomy, one might fail to biopsy appropriate tissues for tumor sampling. The following may assist with the distinction between the two conditions. (A) Preexis tent neurologic symptoms (including headache) are very rare in the child with a structural vascular cause for their stroke whereas there is often a suggestion of some prior neurologic mischief in the patient who has bled into a tumor. (B) The location of the hematoma (on CT scan) when it relates to a preexistent tumor tends to be in sites where tumors occur in children - centrum semiovale of hemispheres, brain stem parenchyma and in the lateral cerebellum or vermis. (C) The bleeding from a tumor with rare exceptions remains confined to the substance of the tumor, whereas that in association with an aneurysm is dispersed in addition through the subarachnoid space or into the adjacent ventricle when an AVM has bled. (D) It is unusual for an AVM hematoma to be surrounded by brain edema, whereas such may be detected around the clot of a tumor which has bled. (E) Additional nuances such as obvious feeding or draining vessels in an AVM or enhancing solid tissue may distinguish the primary vascu lar problem from the tumor, respectively, on the enhanced CT or MRI studies. (F) All of the tumor tissue may be de stroyed when some tumors bleed. Even so, if the surgeon is suspicious during the operation that the margins of the hematoma have an appearance out of keeping with an or dinary clot cavity, then tissue biopsy of the margins is mandatory.
Conclusions During the surgeon's first encounter with the child who has suffered a hemorrhagic stroke, the following should
be observed. ( I) Maintain an open mind as to the wide va riety of causes of brain hemorrhage in the child (table 1). (2) Assess the historical information with those potential causes in mind. (3) Request appropriate consultations when the information suggests a multisystem disorder. (4) Structure the neuroinvestigations around the acuity of the child’s illness, and in particular determine whether and when cerebral arteriography will be required. (5) Once the investigational data has suggested the most likely diagno sis, determine the goals of operative intervention, and. more importantly, when surgery should proceed. What are the risk and benefits of ‘early’ verus ‘late’ operation, and what else should be in place before surgery? (6) Regard less of the perceived success of the operative intervention, the case must be studied postoperatively with appropriate imaging - particularly arteriography for the child with an excised AVM.
References 1 Gold AP, Challenor YP Gilles PH. Hillel SP, Leviton A. Rolins HI. Solomon GE. Stein BM: Report of the Joint Committee for Stroke Facilities. IX. Strokes in children (part I). J Stroke 1973;4:835-858. 2 Humphreys RP Hockley AD. Freedman MH. Saunders EF: Man agement of intracerebal hemorrhage in idiopathic thrombocytope nic purpura. Report of four cases. J Neurosurg 1976;45:700-704. 3 Harwood-Nash DC. Fitz. CR: Neuroradioigoy in Infants and Chil dren. St. Louis. Mosby.1976. vol. 3. pp902-964. 4 Horowitz NH. Rizzoli J V: Postoperative Complications of Intracra nial Neurological Surgery . Baltimore. Williams & Wilkins. 1982, pp 182-235. 5 Humphreys RP: Intracranial arterial aneurysms: in Edwards MSB. Hoffman HJ (eds): Cerebral Vascular Disease in Children. Balti more. Williams & Wilkins. 1989. pp 247-254. 6 Cohen HCM. Tucker WS. Humphreys RP Perrin RG: Angiographically occult histologically verified cerebrovascular malformations. Neurosurgery 1982:10:7(M-714. 7 Kondziolka D. Humphreys RP Hoffman HJ. Hendrick EB. Drake JM: Arteriovenous malformations in the brain in children: A forty year experience with 132 cases. Can J Neurol Sei 1992:19:40-45. 8 Ondra SL. Troupp H. George ED. Schwab K: The natural history of symptomatic arteriovenous malformations of the brain: A 24-year follow-up assessment. J Neurosurg 1990:73:387-391. 9 Brown RD Jr. Wiebers DO. Forbes G. O'Fallon WM. Piepgras DG. Marsh WR. Maciunas RJ: The natural history of unruptured intracranial arteriovenous malformations. J Neurosurg 1988; 68:352-357. 10 Spetzler RF. Wilson CB. Weinstein P Mehdorn M. Townsend J. Tel les D: Normal perfusion pressure breakthrough theory. Clin Neuro surg 1977;25:651-672. 11 Leblanc R. Fcindel W. Ethier R: Epilepsy from cerebral arterio venous malformations. Can J Neurol Sei 1983:10:91-95. 12 Yell HS. Kashiwagi S. Tew JM. BergerTS: Surgical management of
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particularly for any patient who is to undergo major sur gery, identify the presence of inhibitor to the missing pro coagulant, a problem in about 10% of patients with hemo philia [ 16J. All of these initiatives are required before the surgeon acts.
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epilepsy associaled with cerebral arteriovenous malformations. J Neurosurg 1990;72:216-223. 13 Tranmer Bl. Humphreys RP. Chuang SH-C: Microsurgical recovery of a migrated balloon from the internal carotid artery of a child. Neurosurgery 1985; 16:381 -386. 14 Garner TB. Curling OD Jr, Kelly DL Jr, Laster DW: The natural history of intracranial venous angiomas. J Neurosurg 1991:75: 715-722. 15 Heafner MD. Duncan CC. Kier EL, Ment LR. Scott DT. Kolaski R. Sorgen C: Intraventricular hemorrhage in a term neonate secondary to a third ventricular AVM. Case report. J Neurosurg 1985:63: 640-643.
16 Crone KR. Humphreys RP: Hemophilia and other coagulopathies: in Section of Pediatric Neurosurgery. AANS (eds): Pediatric Neuro surgery. ed 2. Baltimore. Williams & Wilkins. 1989. pp 517-523.
Dr. Robin P. Humphreys Division of Neurosurgery The Hospital for Sick Children Rm. 1504. 555 University Avenue Toronto. Ont.. M5G 1X8 (Canada)
In the article ‘Pathophysiology of Isolated Lateral Ventriculomegaly in Shunted Myelodysplastic Children' by Berger M.S.. el al.. Pediatr Neurosurg 1990-91:16:301-304. figure 2c in plate I is upside down and should be rotated by 180°.
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Erratum
