JStroke Cerebrovasc Dis 1991;1;146-151 © 1991 Demos Publications
Benign Brainstem Hemorrhage: A Brief Review Ashfaq Shuaib, M.D., F.R.C.P.(C)
Brainstem hemorrhage is usually associated with a poor prognosis. With the availability of cranial computed tomography (CT) in recent years, it has become apparent that some patients with hemorrhage in the brainstem may have milder symptoms and a better outcome. Although most such hemorrhages have been reported in the midbrain, benign hemorrhages have also been reported in the pons and medulla. This review summarizes reports in the literature with respect to the clinical features, diagnosis, and prognosis in patients with brainstem hemorrhage and a benign prognosis. My experience and review of the literature suggest that these hemorrhages are often missed until after cranial CT is performed, and etiology remains unknown in most cases. In patients with an arteriovenous malformation (AVM), angiographically visible or occult recurrences are frequent. In cases in which an etiology is not found, recovery is rapid and often complete or nearly complete, and recurrences are very rare. Key Words: Brainstem-s-Hemorrhages-Computed tomography.
Hemorrhages in the brainstem have in the past been almost uniformly associated with a poor prognosis. Rapid onset of coma, hyperventilation, pinpoint pupils, and brainstem signs are well-known symptoms of pontine hemorrhages that often lead to early death (1,2). With the advent of cranial computed tomography (CT), smaller nonfatal hemorrhages have increasingly been recognized in the pons, midbrain, and medulla (3). In most cases, the symptoms are suggestive of a brainstem lesion, but because of no decrease in the level of consciousness and mildness of symptoms, the diagnosis remains unsuspected until after cranial CT or magnetic resonance imaging (MRI) is performed. Recovery in most reported cases has been rapid, and, if one can exclude an arteriovenous malformation (AVM),recurrences are rare. The etiolFrom the Department of Medicine (Neurology), College of Medicine and Royal University Hospital, Saskatoon, Saskatchewan, Canada. Address correspondence and reprint requests to Dr. A. Shuaib at Department of Medicine (Neurology), College of Medicine and Royal University Hospital, Saskatoon, Saskatchewan, Canada S7N OXO. 146
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ogy remains unestablished, and prognosis is generallyexcellent. In this review, the clinical features, diagnosis, pathophysiology, and prognosis of brainstem hemorrhage with a benign outcome are presented. The hemorrhages are reviewed under the subtitles of pontine, midbrain, and medullary hemorrhages according to their decreasing order of frequency.
Pontine Hemorrhage Pontine hemorrhage most commonly results from rupture of a paramedian intraparenchymal blood vessel at the junction of the basis pontis and the tegmentum (1). These vessels have microaneurysms that usually develop secondary to long-standing hypertension. Most patients rapidly develop coma with small pupils and respiratory abnormalities. Abnormal horizontal eye movements and ocular bobbing are also sometimes seen. Prognosis in such cases is guarded. Hemorrhage in the basal region or the tegmentum is frequently smaller and may have a benign outcome. In Silverstein's series (2),22% of patients had
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basal or basal-tegmental hemorrhages. More recently, unexpected smaller hemorrhages with milder symptoms have been reported on cranial CT scans (3,4). Unilateral hematomas in these regions can be clinically indistinguishable from lacunar infarctions. Thus, patients with isolated syndromes such as ataxia -hemiparesis (5,6), dysarthria-clumsy hand (7), hemisensory deficits, and pure motor weakness (8) have been reported. Graveleau et a1.'s (9) patient presented with sudden-onset sensory disturbances. Examination showed a severe deficit in position and vibration sensation. Additionally, astereognosis and difficulty with two-point discrimination were also present. Pain and temperature sensation were noted to be norma1. MRI localized the hematoma to the medial lemniscus in the pons. In cases in which the hemorrhage extends into the tegmentum, which is frequently the case, an ipsilateral gaze paralysis or facial weakness may also be seen. Angiography is normal in most cases, and etiology remains uncertain. An occasional patient may show an AVM. Rarely, the hematoma may be secondary to mild trauma or cervical manipulation (10). Recovery begins early, usually within a week, and is nearly complete within 6 weeks (5,8). In Tuhrim's case (7L the patient was neurologically normal within 2 weeks. Repeat CT in most cases showed early and complete resolution of the hematomas. Recurrence, in the absence of an AVM, was reported in only one case (9). Hematomas with benign prognosis are more common in the lateral tegmentum (11). In cases with unilateral restricted hematomas, clinical evaluation usually shows predominantly ocular motor abnormalities. Involvement of other tegmental tracts such as the spinothalamic tract or the cerebellar fibers may result in sensory defects and ataxia. In cases with basal involvement, additional long tract motor abnormalities may also be seen. Caplan and Goodvin reported three patients with lateral tegmental hematomas and also reviewed the previously published literature (11). Symptoms in most cases included ipsilateral lateral gaze palsy, ipsilateral internuclear ophthalmoplegia, small reactive pupils, mild contralateral weakness, and severe contralateral sensory disturbances. Two of these patients died, and the third showed gradual recovery. The two patients reported by Kase et a1. had ocular abnormalities and contralateral sensory symptoms (12). Both cases had ocular bobbing. This was unilateral in one patient. Recovery was gradual but incomplete in both cases (12). Ocular bobbing was also present in the patient with pontine hemorrhage and subsequent recovery reported by Payne et a1. (13). Case 4 of Abe et aI. (14) presented with diplopia, vertigo, and facial
numbness. Episodes were recurrent, and, 12 years after onset of symptoms, the patient died from progressive neurological deficits. An AVMwas identified in the lateral tegmental region at autopsy. Finally, the patient with the mildest symptomatology was reported by Kellen et al. (15). This patient had isolated bilateral sixth nerve palsies and unilateral Horner's syndrome. The initial level of consciousness and the extent of brainstem involvement by the hematoma does not always predict prognosis. The patient reported by Lavi et al. (16) was somnolent and had bilateral flaccid quadriparesis and bilateral facial and ocular abductor paralysis. Over an 8-week follow-up period, recovery was complete without any intervention. Similarly, the level of consciousness or the exact size of the hematoma did not show consistent bearing on the outcome in the six patients with lateral tegmental hematomas reported by Del-Brutto et aI. (17). In their series, larger hematomas did not always lead to a poor prognosis, whereas a small hematoma located strategically led to severe d isability. As a general rule, however, larger hemorrhages would lead to more tissue destruction and thus more severe symptoms. In some cases, milder complaints can progress to more serious symptoms (18) or death (19). Recurrences are rare, can occasionally occur early, and may lead to new symptoms. This was seen in the patient reported by Graveleau et al. (9). Ten days after onset with isolated sensory deficits, the patient developed auditory hallucinosis and increased his neurological deficits. Cranial CT showed an increase in the size of the hematoma secondary to recurrence. Recurrences were frequent in the large series of Abe et aI. (14). This was especially prominent in the anglographically occult AVMs. Death can also result from pneumonia and be unrelated to the neurological problem (20). Finally, improvement and recovery has also been reported with surgical evacuation (21, 22). In the patients reported by Veerapen et a1., improvement was dramatic after evacuation of the hematomas (22).
Midbrain Hematomas Spontaneous midbrain hemorrhages until recently have been considered extremely rare. The first case was described by Scoville and Poppen in 1949 (23). They reported a 44-year-old woman who developed occipital headaches with right-sided sensory deficit, ataxia, and hyperreflexia. Eighteen months later, she developed bilateral third-nerve weakness followed 3 weeks later by right hemiplegia, an altered level of consciousness, bilateral ptosis, and seventh / STROKE CEREBROVASC DIS, VOL. 1, NO.3, 1991
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nerve palsy and complete loss of conjugate eye movements with associated pinpoint pupils. Craniotomy was performed for a presumed midbrain tumor. At craniotomy, surprisingly, a hematoma was identified and drained. She improved significantly postoperatively, and no new symptoms developed in a 6-year follow-up. The authors believed the patient to have sustained two hemorrhages, one at initial presentation and the second 18 months later. The next reports were published in 1978 by Torre et a1. (24) and Humphreys (25). In their patients, the diagnosis had not been initially considered. The patients had presented with headaches, an altered level of consciousness, and vomiting. Both underwent angiography, and this was normal in both cases. Surgical evacuation in both cases led to excellent recovery. An AVMwas found in the extracted hematoma in one patient (24). In over 20 patients reported since then, diagnosis has almost invariably been unsuspected until after CT is performed. Angiography was done in the majority or'cases and was normal in all. There were no deaths reported, and all patients were discharged from the hospital with minimal or insignificant deficits. In contrast to patients with pontine hematomas, hypertension was rarely reported with hematomas restricted to the midbrain (26-35). Neuro-ophthalmological involvement has been prominent in most cases reported to date. In Weisberg's report (29) of six patients, two had downward ocular deviation, and all patients had limited upward gaze. Pupils were unequal and unreactive to light in all cases. Ocular motor involvement was present in all three patients reported by Sand et a1. (30). One patient had Parinaud's syndrome, the second patient developed a vertical gaze palsy, skew deviation, and bilateral Horner's syndrome, and the third patient developed bilateral fourth nerve palsies and a unilateral Horner's syndrome. In Shuaib and Murphy's report (31), both patients showed prominent unilateral third nerve involvement with minimal other associated symptoms. Fingerote et a1. (33) reported five patients, and, again in all cases, neuro-ophthalmological involvement was prominent. Stern and Bernick's (26) patient had bilateral ptosis and unilateral inferior rectus weakness. Finally, Shuaib et a1.'s patient had mild headache and isolated unilateral unreactive pupil at presentation. This patient subsequently developed transient diplopia (32). The diverse neuro-ophthalmological manifestations can be explained by the location of the hematoma in the midbrain (36). Partial or complete' third nerve palsy can result from damage to the third nerve nucleus or its fascicle. In cases with nuclear involvement, there is bilateral superior rectus and levator palpebrae superioris dysfunction, since the innerva148
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tion to these muscles is predominantly crossed. Such lesions can be separated from damage to the fascicle. With fascicular involvement, muscle weakness is restricted to one eye only. Inferiorly placed lesions at the level of the inferior colliculus involve the fourth nerve and result in superior oblique weakness. Superiorlyplaced hematomas in the region of the posterior commissure and the superior colliculus result in Parinaud's syndrome. The associated motor, sensory, and cerebellar deficits result from damage to the long tracts passing through the midbrain. Similarly, involuntary movements can result from involvement of the red nucleus (36). Finally, two recent reports need to be reviewed due to their unusual presentation. One patient, reported by Ono and Inoue (28), developed cheiro-oral syndrome (sensory disturbance of the arms and around the mouth) that had not been previously observed with a midbrain lesion. Such symptoms are commonly associated with damage in the parietal lobe or the thalamus. Recovery was almost complete over a 10week follow-up. Mehler and Ragone (35) reported two patients with midbrain hemorrhages, one of whom had prominent behavioral deficit that consisted of severe retrograde amnesia. Neuro-ophthalmological signs suggestive of midbrain dysfunction were present in both cases. The second patient required a shunt for progressive hydrocephalus. The mechanism leading to midbrain hematomas has only rarely been documented to be an AVM, although such a malformation has frequently been suspected. In hypertensive individuals, rupture of an aneurysm of a small intraparenchymal branch of the superior cerebellar artery, similar to a rupture in the basal ganglion or the pons, is possible. Most reported cases, however, have normal blood pressure. In most cases of recovery without surgical intervention, the possibility of a venous, cavernous, or telangiectatic vascular abnormality cannot be excluded. At present, it would be fair to say that in most cases the diagnosis remains unestablished. Before concluding the section on midbrain hemorrhages, it is worth re-emphasizing that some patients can rapidly deteriorate secondary to acute hydrocephalus. This commonly results from aqueductal compression from the expanding hematoma. Shunt insertion relieves the obstruction and can often result in a dramatic reversal of symptoms (27).
Medullary Hemorrhage Hemorrhage in the medulla remains the least common type of brainstem hemorrhage (37-41). In most reported cases, there is extension of the hematoma
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into the caudal pons. It is also possible that the hematoma could begin in the caudal pons and dissect downward. Arseni and Stanciu (38) reported a 40year-old woman with a 6-month history of episodic vomiting and dizziness. Additionally, recurrent headaches were associated with ataxia and sensory disturbances. The final episode consisted of headache/ neck stiffness, and somnolence. Exploration of the fourth ventricle floor disclosed a hematoma. After evacuation, the patient showed improvement in the headaches and sensory symptoms. Recurrent symptoms suggested an AVM, although none was found in the hematoma. Cappa et al. (37) reported a 44-yearold patient with a sudden onset of vertigo and severe ataxia. Examination showed a left sixth and seventh nerve dysfunction, left-sided dysmetria, and impairment of sensation on the left side. Cranial CT showed a hematoma in the posterolateral brainstem lateral to the fourth ventricle. Although the paper was entitled "Brainstem Hemorrhage with Complete Recovery," the patient showed impaired sensory function and a left beating nystagmus at the final evaluation 1 month after the hemorrhage. The patient reported by Rousseaux et al. (39) showed severe "neurovegetative" status that improved after "surgical evacuation. Late deficits included tongue weakness, downbeating nystagmus/ ataxia, and autonomic dysfunction. Kempe's (40) patient presented with a lateral medullary syndrome/ and the diagnosis was made on surgical evacuation. I recently reported a patient who developed central respiratory arrest a few days after presenting with a medullary hemorrhage. With recovery, respiratory problems c1eared, and the patient was discharged after remaining on a ventilator for several weeks (41). It is important to watch for respiratory or cardiac dysfunction. This can develop early and may lead to sudden death. Likewise, the upper airway needs to be protected, since the loss of lower cranial nerve function can lead to serious aspiration pneumonia. Central hypoventilation developing after a medullary infarction carries a grave prognosis. As was seen in my patient, with reabsorption of the hematoma, respiratory function can be restored and thus should be treated aggressively. The etiology of the hematoma is unknown in most cases.
Discussion In recent years, there has been an increase in reports of milder brainstem hemorrhages. This most likely represents an improvement in diagnostic methods and not an increase in the incidence of small brainstem hematomas. Presently, small hemorrhages can easily be diagnosed with the aid of CT or MRI.
In many cases, the test is ordered for a suspected infarction/ and the hematoma is a surprising finding. The frequency of brainstem hemorrhage is at present difficult to determine. In one study, small midbrain hemorrhages were seen in 3 of 227 cases with intracerebral hematomas (34). Despite advances in imaging technology, the mechanism leading to the bleeding in most cases with small brainstem hematomas remains unestablished. Cranial CT or MRI can show the extent of the hematoma quite nicely. Angiography, whenever it has been done, has been normal. In recent reports, including our experience, repeat CT after the hemorrhage has reabsorbed is either normal or shows a small hypodensity with no enhancement so that the mechanism leading to the hemorrhage remains obscure. Several possibilities could be entertained to explain the hematomas. AVMs have occasionally been found in the removed surgical specimens. Such malformations classically cause recurrent hemorrhages until they are removed or result in the patient's death. Posterior fossa AVMs are rare. Recent experience has shown that very small AVMs can easily be detected by contrast CT or MRI (14). Abe et al. (14) separated their cases with brainstem AVM into two groups. In angiographically visible AVMs, most patients presented with progressive neurological symptoms or developed large hematomas with a grave prognosis. Angiographically occult AVMs, on the other hand, rarely presented with a progressive neurological deficit. Single or recurrent hemorrhages were seen in most cases, and associated symptoms were seldom apoplectic (14). Besides AVMs, other types of vascular malformations seen in the brain include telangiectasias and cavernous and venous malformations. In the brainstern, the most common site for these malformations is the pons. In McCormick and Nofzinger's report (42)/ 164 cases of posterior fossa vascular malformations were reviewed, and, of these, AVMs had the greatest tendency to bleed. Among the 12 brainstem angiomas that bled, 9 were AVMs, and 2 were venous angiomas. Most brainstem AVMs were seen in the pons, followed by the midbrain and the medulla. Similarly, telangiectasias and venous malformations were also most commonly seen in the pons. Unlike AVMs, however, these lesions only rarely bleed. None of the 27 telangiectasias in McCormick and Nofzinger's series (42) showed significant hemorrhage. Venous malformations may be present in 2% of autopsies as incidental findings. These or telangiectatic defects are alleged to be the underlying mechanism in most cases in which an exact etiology cannot be determined. Because of their small size, they may get completely destroyed within the hematomas and thus may not be found when looked for in the evacuated / STROKECEREBROVASC DIS, VOL. 1/ NO.3, 1991
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specimen. Since these lesions are common, found incidentally at autopsy, and seldom show signs of bleeding when examined, it is difficult to tie them in with spontaneous brainstern hematomas. These lesions thus may be responsible for only a small proportion of brainstem hematomas. Several other possibilities could also be responsible, either alone or in combination. Long-standing hypertension has been associated with the formation of microaneurysms in the intraparenchymal small blood vessels. These are commonly seen in the striatum and the cerebral cortex. Although the aneurysms commonly occur in patients with hypertension, they are not restricted to such a population. Dinsdale (1) has reviewed his experience with such lesions in the brainstem. Rupture of such aneurysms is believed to be the cause of the classic hypertensive hemorrhage with rapid development of coma and death. It is possible that a smaller hematoma from rupture of such lesions may result in milder symptoms. Early hemorrhagic transformation of an ischemic infarction is unlikely in patients with normal cardiac status and normal angiograms. Such a possibility, however, should be entertained in patients with severe vertebrobasilar atherosclerotic disease or another source for embolism. Under such circumstances, dramatic recovery would not be expected. Head trauma may result in brainstem hemorrhages. In most patients with hematomas secondary to head injury, the trauma is usually severe. Except for the patient with pontine hematoma resulting from cervical manipulation (10), prominent trauma has not been mentioned with published reports. Bleeding diathesis or bleeding into a neoplasm may be diagnosed with the help of associated history and investigations. The actual frequency of hemorrhage into a multiple sclerosis plaque is not known, but this may need to be considered in younger individuals. Unfortunately, in the end, after these later etiologies have been excluded, there still remains a large proportion of cases in which no cause can be found for the spontaneous brainstern hemorrhage. Whether these are the result of an occult AVM that gets destroyed as a result of the hemorrhage is difficult to prove. Is it possible to diagnose the hematoma without the assistance of CT or MRl? Before the advent of CT all reported cases of small brainstem hemorrhage were either diagnosed at surgery or after death. Subsequent to the wider availability ofCTand, more recently, MRl technology, almost all reported cases of brainstem hematomas were unsuspected until afterthese procedures were completed. Neurological effects of hemorrhage result from direct damage to brainstem nuclei and descending or 150
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ascending long tracts . The symptoms are no different from symptoms that result from damage to the same structures by other mechanisms such as multiple sclerosis, ischemia, or neoplasia. Diagnosis may especially be difficult in cases with very mild symptoms or if there is single tract involvement, such as isolated third nerve palsy, isolated pupillary defect, or isolated sixth nerve palsy (unilateral or bilateral). Common locations for the hematoma include the upper midbrain (third nerve palsy, Parinaud's syndrome, isolated vertical gaze palsies), lateral tegmental (pure motor or sensory syndromes), or basal pontine regions (sixth nerve or horizontal gaze abnormalities) . If such symptoms occur, a brainstem hematoma should be included in the differential diagnosis, especially in patients with no or few risk factors for cerebrovascular disease. In most cases with no evidence of an AVM, prognosis for complete or nearly complete recovery is good. Recovery begins almost immediately and is well under way within the first week. Most patients can be discharged within 2-3 weeks of the ictal event. Investigations other than the abnormal CT or MRI study are normal. Midbrain hematomas can cause obstruction to the cerebrospinal fluid pathway. This usually presents with a progressive decrease in the level of consciousness and can be effectively treated with a ventricular shunt operation. The role of surgery in evacuation of the hematoma is at present unclear. In the few reported cases in which the hematoma was evacuated, the patients seemed to do well, improvement being noticeable almost immediately after surgery. Most hematomas reabsorb without surgery and therefore should be carefully observed and evacuation left to neurosurgeons with expertise in the field. Lower pontine and medullary hematomas, by damaging the respiratory brainstern centers and the autonomic pathways, can lead to serious respiratory or cardiac abnormalities. In my patient with acute respiratory difficulties, these seemed to improve as the hematoma reabsorbed. Lower medullary hematomas can cause severe dysphagia and leave the upper airway unprotected. This may cause aspiration pneumonia. The hematomas usually completely reabsorb in 3-4 weeks, and recurrences are rare. In cases with recurrent hemorrhages, an AVM should be suspected. Prognosis in such cases may not be as favorable as those without an AVM.
References 1. Dinsdale HB. Spontaneous hematoma in the posterior 1 fossa. Arch Ne/lro/1964;10:98-115. 2. Silverstein A. Primary pontine hemorrhage. In: Vin-
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kens PJ, Bruyn GW, eds. Handbbo): of clinicai neurologq, vol 12. Amsterdam: North Holland, 1972:37-53. MulIer HR, Wuthrich R, Wiggli U, Eike M. The contribution of the CAT scan to the diagnosis of cerebellar and pontine lesions. Stroke 1975;6:467-75. Zuccarello M, lavicoli R, Pardatscherk K, et al. Primary brain-stem hematoma. Diagnosis and treatment. Acta Neurochir 1980;54:45-54. Schnapper RA. Pontine hemorrhage presenting as ataxia-hemiparesis. Stroke 1983;13:518 . Kabatake K, Shinohara Y. Ataxia hemiparesis in a patient with primary pontine hemorrhage. Stroke 1983; 14:762-4. Tuhrim S, Yang WC, Rubenowitz H, Weinberger J. Primary pontine hemorrhage and the dysarthria-clumsy hand syndrome. Neurology 1982;32: 1027-8. Gobernado JM, Fernandez DC, Molina AR, Gimeno A. Pure motor hemiparesis due to a lesion in the lower pons. Arch Neurol 1980;37:393. Graveleau Ph, Decroix JP, Sampson Y, Masson M, Cambier J. Deficit sensitif isole d'un hemicoorps par hematome du pont. Rev NeuroI1986;142:788-90. Morel Maroger A, Metzger J, Dardeur 0, Verger JB. Les hematomes benins du tronc cerebral chez les hydertendus arterieles. Rev NeuroI1982;138:435-7. Caplan LR, Goodvin JA. Lateral tegmental brain-stem hemorrhage. Neurology 1982;32 :252-60. Kase CS, Maulsby GO, Mohr JP. Partial pontine hemorrhage. Neurology 1980;3q:652-5. Payne HA, Maraurlla KR, Levinstone A, Heuler J, Tindal SA. Recovery from pontine hemorrhage. Auu Neurol 1978;4:455-8.
14. Abe M, KjelIberg RN, Adams RD. Clinical presentation of vascular malformations of the brain-stem: comparison of angiographically positive and negative types.
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15. KelIen RI, Burde RM, Hudges FJ, Roper-Hall G. Central bilateral six nerve palsies with unilateral Horner's syndrome. J cu« Neuro -oplltllaI1988;8:1,?9-84. 16. Lavi E, Rothman S, Reches A. Primary pontine hemorrhage with complete recovery. Arch Neurol 1981;38: 320. 17. Del-Brullo OH, Noboa CA, Barinagarrementeria F. Lateral tegmental pontine hemorrhages. A reappraisal of 3 cases. Stroke 1987;18:954-6. 18. Freidman W, Ammerman HH, Stanley M. Syndrome of the pontine tegmentum. Arch Neurol Psychiatry 1943; 50:462-71. 19. Case 36-1972. MGH c1inico-pathological conferences. N Eugl J M ed 1972;287:506-12.
20. Sands GH, Portnoy RK. Normal mental status despite bilateral pontine tegmental hematoma. J Neuro11988; 233:200-1. 21. Koos WT, Sunder-Plassman M, Salah S. Successful removal of a large pontine hematoma. J Neurosurg 1969; 31:690-4. 22. Veerapen RJ,Sbeith lA, O'Laoire S. Surgical treatment
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of cryptic AVM's and associated hematomas in the brainstem and the spinal cord. J Neurosurg 1986;65: 188-93. Scoville WB, Poppen JL Intra-peduncular hematoma of the brainstem. Arch Neurol Psychiatry 1949;61:68894. Torre EL,Delitala A, Sorano V. Hematoma of the quadrigeminal plate. J Neurosurg 1978;49:610-3. Humphreys RP. Computerized tomographic definition of mesencephalic hematoma with evacuation through pedunculotomy. J Neurosurg 1978;49:74952. Stern LZ, Bernick C. Spontaneous isolated mesencephalic hemorrhage. Neurology 1986;36:1627. Duward QJ, Barnell HJM, Barr HWK. Presentation and management of mesencephalic hematoma. J Neurosurg 1982;56:123-7. Ono S, Inoue K. Cheiro-oral syndrome following mid brain hemorrhage. J NeuroI1985;232:304-6. Weisberg LA. Mesencephalic hemorrhage. Clinical and computed tomographic correlations. Neurology 1986;36:713-6. Sand J], Biller J, Corbell J], Adams HP, Dunn V. Partial mesencephalic hemorrhages. Neurology 1986;3:52933. Shuaib A, Murphy W. Mesenc ephalic hemorrhages and third nerve palsy. CT: J COlllput TOlllogr 1987;11: 385-8. Shuaib A, Lee MA, Israelian G. Mesencephalic hemorrhage and isolated pupillary deficit. JClinNeuro-ophihal 1989;9:47-9. . Fingerote R, Shuaib A, Brownell AKW. Mesencephalic hematomas. South Med J 1990;83:280-2. Roig C, Carvagal A, IlIa I, Escartinn A, Grau JM, Barraquer L Hemorragies mesencephaliques isolees. Rev NeuroI1982;138:53-61.
35. Mehler MF, Ragone PS. Primary sp ontaneous mesencephalic hemorrhage. Cau J Neurol Sci 1988;15: 435-8. 36. Carpenter MB. Core text of neuroanatomv. Baltimore: Williams & Wilkins, 1985. 37. Cappa SF, Riva M, Sterzi R, Canepari C, Delzenno GB. Brain-stem hemorrhage with complete recovery. J NeuroI1985;232:352-3.
38. Arseni C, Stanciu M. Primary hemorrhage of the brainstem. Acta Neurochir 1973;28 :323-30. 39. Rous seaux M, Griffie G, DhelIemmes P, Dupard T, Caron J. Hematoma bulbare postero-median d'evolution favorable. Rev NeuroI1988;144 :481-8. 40. Kempe LG. Surgical removal of intra-medulIary hemorrhage stimulating WalIenburg's syndrome.
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Benign Brainstem Hemorrhage: A Brief Review Ashfaq Shuaib, M.D., F.R.C.P.(C)
Brainstem hemorrhage is usually associated with a poor prognosis. With the availability of cranial computed tomography (CT) in recent years, it has become apparent that some patients with hemorrhage in the brainstem may have milder symptoms and a better outcome. Although most such hemorrhages have been reported in the midbrain, benign hemorrhages have also been reported in the pons and medulla. This review summarizes reports in the literature with respect to the clinical features, diagnosis, and prognosis in patients with brainstem hemorrhage and a benign prognosis. My experience and review of the literature suggest that these hemorrhages are often missed until after cranial CT is performed, and etiology remains unknown in most cases. In patients with an arteriovenous malformation (AVM), angiographically visible or occult recurrences are frequent. In cases in which an etiology is not found, recovery is rapid and often complete or nearly complete, and recurrences are very rare. Key Words: Brainstem-s-Hemorrhages-Computed tomography.
Hemorrhages in the brainstem have in the past been almost uniformly associated with a poor prognosis. Rapid onset of coma, hyperventilation, pinpoint pupils, and brainstem signs are well-known symptoms of pontine hemorrhages that often lead to early death (1,2). With the advent of cranial computed tomography (CT), smaller nonfatal hemorrhages have increasingly been recognized in the pons, midbrain, and medulla (3). In most cases, the symptoms are suggestive of a brainstem lesion, but because of no decrease in the level of consciousness and mildness of symptoms, the diagnosis remains unsuspected until after cranial CT or magnetic resonance imaging (MRI) is performed. Recovery in most reported cases has been rapid, and, if one can exclude an arteriovenous malformation (AVM),recurrences are rare. The etiolFrom the Department of Medicine (Neurology), College of Medicine and Royal University Hospital, Saskatoon, Saskatchewan, Canada. Address correspondence and reprint requests to Dr. A. Shuaib at Department of Medicine (Neurology), College of Medicine and Royal University Hospital, Saskatoon, Saskatchewan, Canada S7N OXO. 146
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ogy remains unestablished, and prognosis is generallyexcellent. In this review, the clinical features, diagnosis, pathophysiology, and prognosis of brainstem hemorrhage with a benign outcome are presented. The hemorrhages are reviewed under the subtitles of pontine, midbrain, and medullary hemorrhages according to their decreasing order of frequency.
Pontine Hemorrhage Pontine hemorrhage most commonly results from rupture of a paramedian intraparenchymal blood vessel at the junction of the basis pontis and the tegmentum (1). These vessels have microaneurysms that usually develop secondary to long-standing hypertension. Most patients rapidly develop coma with small pupils and respiratory abnormalities. Abnormal horizontal eye movements and ocular bobbing are also sometimes seen. Prognosis in such cases is guarded. Hemorrhage in the basal region or the tegmentum is frequently smaller and may have a benign outcome. In Silverstein's series (2),22% of patients had
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basal or basal-tegmental hemorrhages. More recently, unexpected smaller hemorrhages with milder symptoms have been reported on cranial CT scans (3,4). Unilateral hematomas in these regions can be clinically indistinguishable from lacunar infarctions. Thus, patients with isolated syndromes such as ataxia -hemiparesis (5,6), dysarthria-clumsy hand (7), hemisensory deficits, and pure motor weakness (8) have been reported. Graveleau et a1.'s (9) patient presented with sudden-onset sensory disturbances. Examination showed a severe deficit in position and vibration sensation. Additionally, astereognosis and difficulty with two-point discrimination were also present. Pain and temperature sensation were noted to be norma1. MRI localized the hematoma to the medial lemniscus in the pons. In cases in which the hemorrhage extends into the tegmentum, which is frequently the case, an ipsilateral gaze paralysis or facial weakness may also be seen. Angiography is normal in most cases, and etiology remains uncertain. An occasional patient may show an AVM. Rarely, the hematoma may be secondary to mild trauma or cervical manipulation (10). Recovery begins early, usually within a week, and is nearly complete within 6 weeks (5,8). In Tuhrim's case (7L the patient was neurologically normal within 2 weeks. Repeat CT in most cases showed early and complete resolution of the hematomas. Recurrence, in the absence of an AVM, was reported in only one case (9). Hematomas with benign prognosis are more common in the lateral tegmentum (11). In cases with unilateral restricted hematomas, clinical evaluation usually shows predominantly ocular motor abnormalities. Involvement of other tegmental tracts such as the spinothalamic tract or the cerebellar fibers may result in sensory defects and ataxia. In cases with basal involvement, additional long tract motor abnormalities may also be seen. Caplan and Goodvin reported three patients with lateral tegmental hematomas and also reviewed the previously published literature (11). Symptoms in most cases included ipsilateral lateral gaze palsy, ipsilateral internuclear ophthalmoplegia, small reactive pupils, mild contralateral weakness, and severe contralateral sensory disturbances. Two of these patients died, and the third showed gradual recovery. The two patients reported by Kase et a1. had ocular abnormalities and contralateral sensory symptoms (12). Both cases had ocular bobbing. This was unilateral in one patient. Recovery was gradual but incomplete in both cases (12). Ocular bobbing was also present in the patient with pontine hemorrhage and subsequent recovery reported by Payne et a1. (13). Case 4 of Abe et aI. (14) presented with diplopia, vertigo, and facial
numbness. Episodes were recurrent, and, 12 years after onset of symptoms, the patient died from progressive neurological deficits. An AVMwas identified in the lateral tegmental region at autopsy. Finally, the patient with the mildest symptomatology was reported by Kellen et al. (15). This patient had isolated bilateral sixth nerve palsies and unilateral Horner's syndrome. The initial level of consciousness and the extent of brainstem involvement by the hematoma does not always predict prognosis. The patient reported by Lavi et al. (16) was somnolent and had bilateral flaccid quadriparesis and bilateral facial and ocular abductor paralysis. Over an 8-week follow-up period, recovery was complete without any intervention. Similarly, the level of consciousness or the exact size of the hematoma did not show consistent bearing on the outcome in the six patients with lateral tegmental hematomas reported by Del-Brutto et aI. (17). In their series, larger hematomas did not always lead to a poor prognosis, whereas a small hematoma located strategically led to severe d isability. As a general rule, however, larger hemorrhages would lead to more tissue destruction and thus more severe symptoms. In some cases, milder complaints can progress to more serious symptoms (18) or death (19). Recurrences are rare, can occasionally occur early, and may lead to new symptoms. This was seen in the patient reported by Graveleau et al. (9). Ten days after onset with isolated sensory deficits, the patient developed auditory hallucinosis and increased his neurological deficits. Cranial CT showed an increase in the size of the hematoma secondary to recurrence. Recurrences were frequent in the large series of Abe et aI. (14). This was especially prominent in the anglographically occult AVMs. Death can also result from pneumonia and be unrelated to the neurological problem (20). Finally, improvement and recovery has also been reported with surgical evacuation (21, 22). In the patients reported by Veerapen et a1., improvement was dramatic after evacuation of the hematomas (22).
Midbrain Hematomas Spontaneous midbrain hemorrhages until recently have been considered extremely rare. The first case was described by Scoville and Poppen in 1949 (23). They reported a 44-year-old woman who developed occipital headaches with right-sided sensory deficit, ataxia, and hyperreflexia. Eighteen months later, she developed bilateral third-nerve weakness followed 3 weeks later by right hemiplegia, an altered level of consciousness, bilateral ptosis, and seventh / STROKE CEREBROVASC DIS, VOL. 1, NO.3, 1991
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nerve palsy and complete loss of conjugate eye movements with associated pinpoint pupils. Craniotomy was performed for a presumed midbrain tumor. At craniotomy, surprisingly, a hematoma was identified and drained. She improved significantly postoperatively, and no new symptoms developed in a 6-year follow-up. The authors believed the patient to have sustained two hemorrhages, one at initial presentation and the second 18 months later. The next reports were published in 1978 by Torre et a1. (24) and Humphreys (25). In their patients, the diagnosis had not been initially considered. The patients had presented with headaches, an altered level of consciousness, and vomiting. Both underwent angiography, and this was normal in both cases. Surgical evacuation in both cases led to excellent recovery. An AVMwas found in the extracted hematoma in one patient (24). In over 20 patients reported since then, diagnosis has almost invariably been unsuspected until after CT is performed. Angiography was done in the majority or'cases and was normal in all. There were no deaths reported, and all patients were discharged from the hospital with minimal or insignificant deficits. In contrast to patients with pontine hematomas, hypertension was rarely reported with hematomas restricted to the midbrain (26-35). Neuro-ophthalmological involvement has been prominent in most cases reported to date. In Weisberg's report (29) of six patients, two had downward ocular deviation, and all patients had limited upward gaze. Pupils were unequal and unreactive to light in all cases. Ocular motor involvement was present in all three patients reported by Sand et a1. (30). One patient had Parinaud's syndrome, the second patient developed a vertical gaze palsy, skew deviation, and bilateral Horner's syndrome, and the third patient developed bilateral fourth nerve palsies and a unilateral Horner's syndrome. In Shuaib and Murphy's report (31), both patients showed prominent unilateral third nerve involvement with minimal other associated symptoms. Fingerote et a1. (33) reported five patients, and, again in all cases, neuro-ophthalmological involvement was prominent. Stern and Bernick's (26) patient had bilateral ptosis and unilateral inferior rectus weakness. Finally, Shuaib et a1.'s patient had mild headache and isolated unilateral unreactive pupil at presentation. This patient subsequently developed transient diplopia (32). The diverse neuro-ophthalmological manifestations can be explained by the location of the hematoma in the midbrain (36). Partial or complete' third nerve palsy can result from damage to the third nerve nucleus or its fascicle. In cases with nuclear involvement, there is bilateral superior rectus and levator palpebrae superioris dysfunction, since the innerva148
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tion to these muscles is predominantly crossed. Such lesions can be separated from damage to the fascicle. With fascicular involvement, muscle weakness is restricted to one eye only. Inferiorly placed lesions at the level of the inferior colliculus involve the fourth nerve and result in superior oblique weakness. Superiorlyplaced hematomas in the region of the posterior commissure and the superior colliculus result in Parinaud's syndrome. The associated motor, sensory, and cerebellar deficits result from damage to the long tracts passing through the midbrain. Similarly, involuntary movements can result from involvement of the red nucleus (36). Finally, two recent reports need to be reviewed due to their unusual presentation. One patient, reported by Ono and Inoue (28), developed cheiro-oral syndrome (sensory disturbance of the arms and around the mouth) that had not been previously observed with a midbrain lesion. Such symptoms are commonly associated with damage in the parietal lobe or the thalamus. Recovery was almost complete over a 10week follow-up. Mehler and Ragone (35) reported two patients with midbrain hemorrhages, one of whom had prominent behavioral deficit that consisted of severe retrograde amnesia. Neuro-ophthalmological signs suggestive of midbrain dysfunction were present in both cases. The second patient required a shunt for progressive hydrocephalus. The mechanism leading to midbrain hematomas has only rarely been documented to be an AVM, although such a malformation has frequently been suspected. In hypertensive individuals, rupture of an aneurysm of a small intraparenchymal branch of the superior cerebellar artery, similar to a rupture in the basal ganglion or the pons, is possible. Most reported cases, however, have normal blood pressure. In most cases of recovery without surgical intervention, the possibility of a venous, cavernous, or telangiectatic vascular abnormality cannot be excluded. At present, it would be fair to say that in most cases the diagnosis remains unestablished. Before concluding the section on midbrain hemorrhages, it is worth re-emphasizing that some patients can rapidly deteriorate secondary to acute hydrocephalus. This commonly results from aqueductal compression from the expanding hematoma. Shunt insertion relieves the obstruction and can often result in a dramatic reversal of symptoms (27).
Medullary Hemorrhage Hemorrhage in the medulla remains the least common type of brainstem hemorrhage (37-41). In most reported cases, there is extension of the hematoma
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into the caudal pons. It is also possible that the hematoma could begin in the caudal pons and dissect downward. Arseni and Stanciu (38) reported a 40year-old woman with a 6-month history of episodic vomiting and dizziness. Additionally, recurrent headaches were associated with ataxia and sensory disturbances. The final episode consisted of headache/ neck stiffness, and somnolence. Exploration of the fourth ventricle floor disclosed a hematoma. After evacuation, the patient showed improvement in the headaches and sensory symptoms. Recurrent symptoms suggested an AVM, although none was found in the hematoma. Cappa et al. (37) reported a 44-yearold patient with a sudden onset of vertigo and severe ataxia. Examination showed a left sixth and seventh nerve dysfunction, left-sided dysmetria, and impairment of sensation on the left side. Cranial CT showed a hematoma in the posterolateral brainstem lateral to the fourth ventricle. Although the paper was entitled "Brainstem Hemorrhage with Complete Recovery," the patient showed impaired sensory function and a left beating nystagmus at the final evaluation 1 month after the hemorrhage. The patient reported by Rousseaux et al. (39) showed severe "neurovegetative" status that improved after "surgical evacuation. Late deficits included tongue weakness, downbeating nystagmus/ ataxia, and autonomic dysfunction. Kempe's (40) patient presented with a lateral medullary syndrome/ and the diagnosis was made on surgical evacuation. I recently reported a patient who developed central respiratory arrest a few days after presenting with a medullary hemorrhage. With recovery, respiratory problems c1eared, and the patient was discharged after remaining on a ventilator for several weeks (41). It is important to watch for respiratory or cardiac dysfunction. This can develop early and may lead to sudden death. Likewise, the upper airway needs to be protected, since the loss of lower cranial nerve function can lead to serious aspiration pneumonia. Central hypoventilation developing after a medullary infarction carries a grave prognosis. As was seen in my patient, with reabsorption of the hematoma, respiratory function can be restored and thus should be treated aggressively. The etiology of the hematoma is unknown in most cases.
Discussion In recent years, there has been an increase in reports of milder brainstem hemorrhages. This most likely represents an improvement in diagnostic methods and not an increase in the incidence of small brainstem hematomas. Presently, small hemorrhages can easily be diagnosed with the aid of CT or MRI.
In many cases, the test is ordered for a suspected infarction/ and the hematoma is a surprising finding. The frequency of brainstem hemorrhage is at present difficult to determine. In one study, small midbrain hemorrhages were seen in 3 of 227 cases with intracerebral hematomas (34). Despite advances in imaging technology, the mechanism leading to the bleeding in most cases with small brainstem hematomas remains unestablished. Cranial CT or MRI can show the extent of the hematoma quite nicely. Angiography, whenever it has been done, has been normal. In recent reports, including our experience, repeat CT after the hemorrhage has reabsorbed is either normal or shows a small hypodensity with no enhancement so that the mechanism leading to the hemorrhage remains obscure. Several possibilities could be entertained to explain the hematomas. AVMs have occasionally been found in the removed surgical specimens. Such malformations classically cause recurrent hemorrhages until they are removed or result in the patient's death. Posterior fossa AVMs are rare. Recent experience has shown that very small AVMs can easily be detected by contrast CT or MRI (14). Abe et al. (14) separated their cases with brainstem AVM into two groups. In angiographically visible AVMs, most patients presented with progressive neurological symptoms or developed large hematomas with a grave prognosis. Angiographically occult AVMs, on the other hand, rarely presented with a progressive neurological deficit. Single or recurrent hemorrhages were seen in most cases, and associated symptoms were seldom apoplectic (14). Besides AVMs, other types of vascular malformations seen in the brain include telangiectasias and cavernous and venous malformations. In the brainstern, the most common site for these malformations is the pons. In McCormick and Nofzinger's report (42)/ 164 cases of posterior fossa vascular malformations were reviewed, and, of these, AVMs had the greatest tendency to bleed. Among the 12 brainstem angiomas that bled, 9 were AVMs, and 2 were venous angiomas. Most brainstem AVMs were seen in the pons, followed by the midbrain and the medulla. Similarly, telangiectasias and venous malformations were also most commonly seen in the pons. Unlike AVMs, however, these lesions only rarely bleed. None of the 27 telangiectasias in McCormick and Nofzinger's series (42) showed significant hemorrhage. Venous malformations may be present in 2% of autopsies as incidental findings. These or telangiectatic defects are alleged to be the underlying mechanism in most cases in which an exact etiology cannot be determined. Because of their small size, they may get completely destroyed within the hematomas and thus may not be found when looked for in the evacuated / STROKECEREBROVASC DIS, VOL. 1/ NO.3, 1991
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specimen. Since these lesions are common, found incidentally at autopsy, and seldom show signs of bleeding when examined, it is difficult to tie them in with spontaneous brainstern hematomas. These lesions thus may be responsible for only a small proportion of brainstem hematomas. Several other possibilities could also be responsible, either alone or in combination. Long-standing hypertension has been associated with the formation of microaneurysms in the intraparenchymal small blood vessels. These are commonly seen in the striatum and the cerebral cortex. Although the aneurysms commonly occur in patients with hypertension, they are not restricted to such a population. Dinsdale (1) has reviewed his experience with such lesions in the brainstem. Rupture of such aneurysms is believed to be the cause of the classic hypertensive hemorrhage with rapid development of coma and death. It is possible that a smaller hematoma from rupture of such lesions may result in milder symptoms. Early hemorrhagic transformation of an ischemic infarction is unlikely in patients with normal cardiac status and normal angiograms. Such a possibility, however, should be entertained in patients with severe vertebrobasilar atherosclerotic disease or another source for embolism. Under such circumstances, dramatic recovery would not be expected. Head trauma may result in brainstem hemorrhages. In most patients with hematomas secondary to head injury, the trauma is usually severe. Except for the patient with pontine hematoma resulting from cervical manipulation (10), prominent trauma has not been mentioned with published reports. Bleeding diathesis or bleeding into a neoplasm may be diagnosed with the help of associated history and investigations. The actual frequency of hemorrhage into a multiple sclerosis plaque is not known, but this may need to be considered in younger individuals. Unfortunately, in the end, after these later etiologies have been excluded, there still remains a large proportion of cases in which no cause can be found for the spontaneous brainstern hemorrhage. Whether these are the result of an occult AVM that gets destroyed as a result of the hemorrhage is difficult to prove. Is it possible to diagnose the hematoma without the assistance of CT or MRl? Before the advent of CT all reported cases of small brainstem hemorrhage were either diagnosed at surgery or after death. Subsequent to the wider availability ofCTand, more recently, MRl technology, almost all reported cases of brainstem hematomas were unsuspected until afterthese procedures were completed. Neurological effects of hemorrhage result from direct damage to brainstem nuclei and descending or 150
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ascending long tracts . The symptoms are no different from symptoms that result from damage to the same structures by other mechanisms such as multiple sclerosis, ischemia, or neoplasia. Diagnosis may especially be difficult in cases with very mild symptoms or if there is single tract involvement, such as isolated third nerve palsy, isolated pupillary defect, or isolated sixth nerve palsy (unilateral or bilateral). Common locations for the hematoma include the upper midbrain (third nerve palsy, Parinaud's syndrome, isolated vertical gaze palsies), lateral tegmental (pure motor or sensory syndromes), or basal pontine regions (sixth nerve or horizontal gaze abnormalities) . If such symptoms occur, a brainstem hematoma should be included in the differential diagnosis, especially in patients with no or few risk factors for cerebrovascular disease. In most cases with no evidence of an AVM, prognosis for complete or nearly complete recovery is good. Recovery begins almost immediately and is well under way within the first week. Most patients can be discharged within 2-3 weeks of the ictal event. Investigations other than the abnormal CT or MRI study are normal. Midbrain hematomas can cause obstruction to the cerebrospinal fluid pathway. This usually presents with a progressive decrease in the level of consciousness and can be effectively treated with a ventricular shunt operation. The role of surgery in evacuation of the hematoma is at present unclear. In the few reported cases in which the hematoma was evacuated, the patients seemed to do well, improvement being noticeable almost immediately after surgery. Most hematomas reabsorb without surgery and therefore should be carefully observed and evacuation left to neurosurgeons with expertise in the field. Lower pontine and medullary hematomas, by damaging the respiratory brainstern centers and the autonomic pathways, can lead to serious respiratory or cardiac abnormalities. In my patient with acute respiratory difficulties, these seemed to improve as the hematoma reabsorbed. Lower medullary hematomas can cause severe dysphagia and leave the upper airway unprotected. This may cause aspiration pneumonia. The hematomas usually completely reabsorb in 3-4 weeks, and recurrences are rare. In cases with recurrent hemorrhages, an AVM should be suspected. Prognosis in such cases may not be as favorable as those without an AVM.
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