Outcome in patients with subarachnoid haemorrhage and negative angiography according to pattern of haemorrhage on computed tomography

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the BASF-AG on November 17, 1953. Am 14.

J Ind Med 1982; 3: 179-89.

Fingerhut MA, Halperin WE, Marlow DA, Piacitelli LA, Honchar PA, Sweeney MH, et al. Cancer mortality in workers exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin. N Engl J Med 1991; 199: 212-18.

15. Zober A, Messerer P, Huber P.

16.

17.

18.

19.

20.

21.

Thirty-four year mortality follow-up of BASF employees exposed to 2,3,7,8-TCDD after the 1953 accident. Int Arch Occ Environ Health 1990; 62: 139-57. Kaune A, Fiedler H, Hutzinger O. Dioxine und Furane—Quellen, Eintrag in die Umwelt und Aufnahme durch den Menschen (Literaturstudie). Lehrstuhl fur Ökologische Chemie und Geochemie der Universität, Bayreuth, 1990. Beck H, Eckart K, Mathar W, Wittkowski R. Levels of PCDD’s and PCDF’s in adipose tissue of occupationally exposed workers. Chemosphere 1989; 18: 507-16. Bond GG, McLaren EA, Lipps TE, Cook RR. Update of mortality among chemical workers with potential exposure to higher chlorinated dioxins. J Occup Med 1989; 31: 121-23. Zack JA, Gaffey WR. A mortality study of workers employed at the Monsanto Company plant in Nitro, West Virginia. Environ Sci Res 1983; 26: 575-91. Manz A, Berger J, Waltsgott H. Zur Frage des Berufskrebses bei Beschäftigten der Gasindustrie—Cohortenstudie. Forschungsbericht Nr. 352 der Bundesanstalt für Arbeitsschutz, Dortmund. Wirtschaftsverlag NW, Bremerhaven, 1983. Breslow NE, Day NE. Statistical methods in cancer research: vol II. The

design and analysis of cohort studies. IARC Sci Publ 1987; 82: 1-406. Höpker WW, Burkhardt HU. Validitätsuntersuchungen zur amtlichen Todesursachenstatistik. Verh D Ges Pathol 1984; 68: 431. 23. Kircher T, Nelson J, Burdo H. The autopsy as a measure of accuracy of the death certificate. N Engl J Med 1985; 313: 1263-69. 24. Johnson ES. Association between exposure to phenoxys/chlorophenols and soft-tissue sarcomas and malignant lymphomas. Fund Appl Toxicol 22.

1990; 14: 219-34. 25. Ott MG, Olson RA, Cook RR, Bond GG. Cohort mortality study of chemical worker with potential exposure to higher chlorinated dioxins. J Occup Med 1987; 29: 422-29. 26. Pitot HC, Goldsworthy T, Campbell HA, Poland A. Quantitative evaluation of the promotion by 2,3,7,8-tetrachlorodibenzo-p-dioxin of hepatocarcinogenesis from dimethylnitrosamine. Cancer Res 1980; 40: 2616-20. 27. Poland A, Palen D, Glover E. Tumour promotion by TCDD in skin of HRS/J hairless mice. Nature 1982; 300: 271-73. 28. Lynge E. A follow-up of cancer incidence among workers in manufacture of phenoxy herbicides in Denmark. Br J Cancer 1985; 52: 259-70. 29. Fitzgerald EF, Weinstein AL, Youngblood LG,. Standfast SJ, Melius JM. Health effects three years after potential exposure to the toxic contaminants of an electrical transformer fire. Arch Envir Health 1989; 44: 214-21. 30. Boyle CA, Decoufle P, O’Brian TR. Long-term health consequences of military service in Vietnam. Epidemiol Rev 1989; 11: 1-27.

Outcome in patients with subarachnoid haemorrhage and negative angiography according to pattern of haemorrhage on computed tomography

15% of patients with spontaneous subarachnoid haemorrhage have normal cerebral angiograms; they fare better than patients with demonstrated

rebleeding and cerebral still occur. In patients with a normal angiogram and accumulation of blood in the cisterns around the midbrain—"perimesencephalic nonaneurysmal haemorrhage"—outcome is excellent. aneurysms,

ischaemia

though

can

To test the hypothesis that rebleeding and disability in angiogram-negative subarachnoid haemorrhage might be limited to those with other patterns of haemorrhage on initial computed tomography (CT), complications and long-term outcome were studied in 113 patients with angiogram-negative subarachnoid haemorrhage, admitted between January, 1983, and July, 1990. All patients were investigated with thirdgeneration CT scans within 72 h of the event, and with cerebral angiography. The mean follow-up period was 45 (range 6-96) months. None of 77 patients with a perimesencephalic pattern of haemorrhage on CT died or was left disabled as a result of the haemorrhage (0% [95% confidence interval 0-5%]). Among the other 36 patients, who had a blood distribution on CT indistinguishable from that in proven aneurysmal bleeds, 4 had rebleeds and 9 died or were left disabled as result of the haemorrhage (25% [14-43%]). Thus, two distinct subsets of patients with

angiogram-negative subarachnoid haemorrhage

be recognised. Patients with a perimesencephalic pattern of haemorrhage have an excellent prognosis. Rebleeding, cerebral ischaemia, and residual disability occur exclusively in patients with aneurysmal patterns of haemorrhage on initial CT. Repeated angiography in search of an occult aneurysm is justified only in the patients with aneurysmal patterns. should

Introduction More than half of patients with aneurysmal rupture die or remain severely disabled.1 Blood in the basal cisterns on

computed tomography (CT) strongly suggests aneurysmal rupture,2 but the cause of the bleed remains uncertain until it is confirmed by cerebral angiography. Despite substantial improvements in imaging acquisition, angiography fails to show an aneurysm in 15% of patients with spontaneous subarachnoid haemorrhage.1.3-7 It is widely believed that patients with angiogram-negative subarachnoid haemorrhage have a more favourable prognosis than those with positive angiograms. Nevertheless, they may suffer fatal rebleeds and long-term disability.3’s,6.8-1O. ADDRESSES. University Departments of Neurology, Utrecht (G. J E. Rinkel, MD, E F M. Wijdicks, MD, Prof J. van Gijn, MD), and Rotterdam (D. Hasan, MD, Prof M Vermeulen, MD); University Department of Neurosurgery, Academic Medical Centre, Amsterdam (L M. Hageman, MD); and Departments of Neurology, St Elisabeth Hospital, Tilburg (G. E. M. Kienstra, MD), and De Wever Hospital, Heerlen, the Netherlands (C. L. Franke, MD). Correspondence to Dr Gabriel J. E. Rinkel, University Department of Neurology, Heidelberglaan 100, 3584 CX Utrecht, the Netherlands

965

In 1985

we

reported

the existence of

a

variant of

subarachnoid haemorrhage characterised by a normal angiogram and focal clots in the cisterns around the midbrain on CT, which we called perimesencephalic

non-aneurysmal haemorrhage.’1 In a small preliminary study the outcome for these patients was excellent.12 This finding prompted us to reconsider the whole group of subarachnoid angiogram-negative patients with in relation to the of haemorrhage patterns haemorrhage on initial CT scan. We postulated that patients with other than perimesencephalic patterns of haemorrhage in the basal cisterns might be susceptible to rebleeding, cerebral ischaemia, and residual disability. We describe here the outcome for a large series of patients with and without a perimesencephalic pattern of haemorrhage on CT. Patients and methods We studied a consecutive series of patients with subarachnoid haemorrhage and negative angiography, admitted between January, 1983, and July, 1990, to ten teaching hospitals in the Netherlands. This period was selected to include only patients investigated with third-generation CT scanners and to allow a minimum follow-up period of 6 months. 37 of the patients, with perimesencephalic haemorrhage only, were included in a preliminary follow-up study. 12 Inclusion criteria for this study were: third-generation CT scanning done within 72 h of the first symptoms with evidence of subarachnoid blood; and a selective four-vessel angiogram with oblique views, magnifications, and subtractions judged normal by both the radiologist and clinician (neurologist, neurosurgeon, or both).

Fig 2-Period of follow-up in 36 patients wih aneurysmal pattern and 77 patients with perimesencephalic pattern of haemorrhage on CT. Before evaluation of the outcome of the patients, all CT scans classified by one of us (G. J. E. R.). The amount of subarachnoid blood on CT was graded for each of the ten basal cisterns and fissures (anterior interhemispheric fissure, quadrigeminal cistern, the paired suprasellar cisterns, ambient cisterns, basal sylvian fissures, and lateral sylvian fissures), on a semiquantitative scale: 0 no blood; 1 = small amount of blood; 2 = moderately filled with blood; 3 completely filled with blood. The density of the clot was not measured. Clots that had expanded the original size of a cistern or fissue were graded as 3. The total amount of subarachnoid blood (sum score) was calculated by adding the ten scores; the sum could therefore range from 0 to 30." The criteria for a perimesencephalic pattern of haemorrhage were: centre of the bleeding located immediately anterior to the midbrain, with or without extension of blood to the anterior part of the ambient cistern or to the basal part of the sylvian fissure; no extension to the anterior interhemispheric fissure and no extension to the lateral sylvian fissue, except for a small amount of blood (grade 1); and absence of frank intraventricular haemorrhage.14 As a linear measurement of ventricular size, we used the bicaudate index, which is the width of the frontal horns at the levels of the caudate nuclei divided by the corresponding diameter of the brain. We converted the bicaudate index into a relative size by dividing the absolute values by the upper limit for age as described previously.15 The inhospital course of some of the patients with perimesencephalic haemorrhage has been described elsewhere. 16 The outcome was assessed according to the Glasgow outcome scale.17 Patients were interviewed by telephone, seen as outpatients, or visited at their homes. The interview included questions about recurrent episodes of sudden severe headache, quality of life, and level of performance. In a few cases the information was obtained through the general practitioner if he or she advised against contacting the patient. were

=

=

Results

Fig 1-Non-contrast-enhanced CT scans showing of haemorrhage on CT.

two patterns

Upper. perimesencephalic pattern of haemorrhage, with accumulation of subarachnoid blood in cistern around midbrain (interpeduncular, ambient, and suprasellar cisterns). Lower aneurysmal pattern of haemorrhage, with subarachnoid blood in cisterns around midbrain and also in anterior interhemispheric fissure and both sylvian fissures.

We studied 113 patients with angiogram-negative subarachnoid haemorrhage who met the inclusion criteria. The CT scan showed a perimesencephalic pattern of haemorrhage in 77 patients (fig 1). The cisternal blood distribution of the remaining 36 patients was indistinguishable from CT patterns in patients with a proven aneurysmal bleed (aneurysmal pattern, fig 1). In 2 of these patients the CT scan also showed an intracerebral haematoma. Angiography was repeated in 7 patients with a perimesencephalic pattern, and in 15 patients with an aneurysmal pattern of haemorrhage. The mean age was 51 years for both groups of patients. The mean period of follow-up was 45 (range 12-90) months in the perimesencephalic group and 44 (6-96) in the aneurysmal group (fig 2). No patient was lost to follow-up. The clinical and CT features of the two groups are listed in table i.

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TABLE I-CLINICAL AND CT SCAN FEATURES OF PATIENTS

Inhospital course in perimesencephalic non-aneurysmal haemorrhage 2 patients deteriorated owing to acute hydrocephalus. 1 of these patients18 completely recovered after ventricular shunting. The other improved spontaneously. No patient had a rebleed or delayed cerebral ischaemia. 1 patient became drowsy after angiography, which had not shown an examination he was disoriented and he had slight weakness of the left arm. The symptoms resolved within 4 h. A repeated CT scan a week after the episode was normal, but a magnetic resonance imaging scan 4 weeks later showed a right occipital infarct. aneurysm

or

vasopasm;

on

Inhospital course in aneurysmal pattern of haemorrhage 8 patients were drowsy or stuporous (Glasgow coma sum scores 7-12)19 on admission (table i), but all improved during the following days. In general, patients with aneurysmal patterns of haemorrhage had larger amounts of cisternal blood than patients with perimesencephalic haemorrhage, apart from the difference in distribution (table I). In most patients the blood had extravasated

Fig 3-Successive CT scans of a 54-year-old

woman

diffusely throughout the basal cisterns; a localised clot was found in the anterior interhemispheric fissure in 2 patients and in the lateral sylvian fissure in 5 patients. Frank intraventricular haemorrhage was found in 7 patients. 2 patients died from rebleeding-l on day 17 after a CT-proven rebleed and the other on day 7 after a sudden loss of consciousness and apnoea (permission for necropsy was not given). Another patient, with a pattern of haemorrhage that suggested middle cerebral artery aneurysm, had a CT-proven rebleed on day 21 (fig 3), after two technically satisfactory but normal angiograms. Exploratory craniotomy disclosed a middle cerebral artery aneurysm without evidence of thrombotic obliteration. She made a full recovery after the aneurysm was clipped. 1 patient had a CT-proven episode of cerebral ischaemia, with focal deficits and obtundation on day 15. She was disabled at discharge; there was some improvement in the following months but she remained handicapped. 5 patients deteriorated from acute hydrocephalus and were treated by ventricular shunting. 4 of these had initially been alert or only slightly drowsy. 2 of the 5 patients remained severely disabled. The early course of the other 27 patients was unremarkable.

Long-term follow-up in perimesencephalic non-aneurysmal haemorrhage No patient had a rebleed or reported sudden bouts of headache reminiscent of their haemorrhage. Persisting neurological deficits were not found. 2 patients died from cancer. 5 of the 77 patients did not resume their previous activities: 1 had a severe myocardial infarction 4 months after the haemorrhage; 1 underwent surgery for bronchial carcinoma; 1 had severe depression; and the other 2 patients were declared unfit by their employers’ medical advisers mainly because of fear of rebleeding. 15 patients mentioned non-specific headaches or slight forgetfulness 2-4 years after the bleed; these symptoms did not interfere with their work. Long-term follow-up in aneurysmal pattern of haemorrhage 1 patient probably rebled 6 months after haemorrhage. He suddenly complained of

the initial a

severe

headache, lost consciousnes, and died before he reached

hospital. Necropsy was not permitted. Another patient had a sudden, painless, and complete oculomotor palsy 2 years

with acute onset of

severe

headache followed

by neck stiffness.

21 days after initial episode, there was sudden aggravation of headache, resembling the initial bout Left: CT scan 12 h after initial onset of headache,with blood in basal cisterns and left sylvian fissure Centre CT scan 8 days after onset of symptoms shows resolution of cisternal blood with only a minute amount of blood in basal and peripheral part of left sylvian fissure Right CT scan 21 days after initial bout and 1 h after sudden aggravation of headache with increase of blood in left sylman fissure (arrow)

967

TABLE II-OUTCOME

after the haemorrhage. Two angiograms had been normal at the time of the haemorrhage. A third angiogram at the time of the oculomotor palsy showed a posterior communicating artery aneurysm. He made a full recovery after operation. 2 middle-aged patients lived in nursing homes, 3 and 5 years after the haemorrhage. In both, the clinical course had been complicated by acute hydrocephalus. 2 other patients lived at home but with severe intellectual deficits; they had to be cared for by relatives. 2 patients had not been able to resume their previous activities because of a mild disturbance of memory. Of the remaining patients, 1 had suffered two myocardial infarcts, 1 had been treated for major depression, and 2 patients reported a reduced level of performance because of frequent headaches and forgetfulness. The outcome of all patients is summarised in table 11. No patient with a perimesencephalic non-aneurysmal haemorrhage had a rebleed, and none died or was left disabled as a result of the haemorrhage (0% [95% confidence interval 4-5%]). By contrast, 4 of the 36 patients with aneurysmal patterns on CT had a rebleed, and 9 had died or were left disabled as a result of the haemorrhage

(25% [14-43%]). Discussion Our primary aim was to assess the outcome in a large series of patients with normal angiograms, with and without a perimesencephalic pattern of subarachnoid haemorrhage on CT scan. In previous follow-up studies these patterns of haemorrhage could not be distinguished because early CT scans were not done in the majority of the patients or those available used poor-resolution first-generation CT scanners.3-10 Moreover, in most studies of angiogramnegative subarachnoid haemorrhage without CT confirmation of the haemorrhage, xanthochromia of the cerebrospinal fluid was not measured3-9 and therefore these studies, which claimed good outcomes, may have included patients with traumatic lumbar punctures and thunderclap headaches, mimicking subarachnoid haemorrhage. 20 We found two subsets of patients with angiogramnegative subarachnoid haemorrhage, separated by the pattern of haemorrhage on CT and by outcome. The outcome was excellent in patients with local clots in the perimesencephalic cisterns on initial CT, whereas patients with a blood distribution indistinguishable from proven aneurysmal bleeds on CT suffered rebleeding, ischaemia, or persisting neurological deficits. It may be argued that part of the unfavourable course in patients with aneurysmal patterns of haemorrhage on CT could be explained by other indicators of poor outcome-for instance, the amount of subarachnoid blood or the presence of intraventricular blood.1,21,22 However, there is sufficient evidence that the risk of rebleeding, a major factor determining the difference in outcome between the two subsets of patients, is independent of the amount of subarachnoid blood on CT.23 In addition, this series was

patients with a good clinical grade on which was a prerequisite for angiographic admission, studies. We suspect that the outcome in patients with aneurysmal patterns of haemorrhage would have been worse if we had included patients who died before angiography could be carried out and in whom no aneurysm could be demonstrated at necropsy, or those with angiography at a later stage, after clinical improvement. The pronounced difference in outcome, within the group of patients with a negative angiogram, between the two patterns of haemorrhage suggests the existence of two distinct clinical entities. Patients with a perimesencephalic non-aneurysmal haemorrhage are in good clinical condition on admission, apart from their headache and occasional drowsiness. Most patients resumed their previous activities and none had suffered a rebleed. The only complication that may develop during the early clinical course is acute hydrocephalus, but even then the outcome is good. The benign clinical presentation and limited extent of the haemorrhage on CT suggests a small venous leakage of blood rather than a rupture under arterial pressure. So far we have been unable to determine the origin of the bleed in biased towards

perimesencephalic haemorrhage. Magnetic resonance imaging studies were normal,14 and because of the good outcome, no patient has yet come to necropsy. The higher frequency of rebleeding in the group of patients with aneurysmal patterns of haemorrhage suggests that in at least some patients an aneurysm escaped radiological detection. Apart from technical reasons, such as use of too few angiographic projections, this phenomenon may have several other explanations. Narrowing of vessels by vasospasm has been invoked in some cases,24 but repeated angiography after the period of vasospasm only occasionally reveals an aneurysm. Thrombosis of the aneurysmal stalk or the entire sac is another possible explanation for an aneurysm’s being missed on selective angiography.4,25 Microaneurysms too small to be detected on angiography have been suggested as a possible cause but have only rarely been found.6,26 Obliteration of the aneurysm by pressure of an adjacent haemotoma may also occur; 2 patients with a haematoma in the anterior interhemispheric tissue and with repeatedly normal angiograms have been described, in whom exploratory craniotomy disclosed a patent anterior communicating aneurysm 25 Among our 36 patients with aneurysmal patterns of haemorrhage on CT, vasospasm was rare and only 2 patients had haematomas on CT. From our series we could therefore not categorically support any of these explanations. As a rule the two patterns of subarachnoid haemorrhage can be reliably distinguished on CT. In an interobserver study among neuroradiologists we found that most patients with a perimesencephalic haemorrhage were correctly with identified, high interobserver agreement (kappa 0-87). We are, however, aware of 1 patient with a perimesencephalic pattern of haemorrhage who had a =

968

basilar artery aneurysm so we still recommend a single four-vessel angiogram to exclude a posterior circulation aneurysm.

This study was not designed to answer the question of which patients with an adequate normal angiogram should undergo repeat angiography. On the other hand, it seems that the management of patients with subarachnoid haemorrhage and a normal, technically satisfactory cerebral angiogram can be guided by our findings. Cerebral angiography still carries substantial morbidity and its inherent risks should preclude injudicious use. In two prospective studies, crude complication rates up to 7% have been reported, and transient neurological deficits occurred in 4% of the patients with subarachnoid haemorrhage.27.28 It has been suggested that ischaemic complications may be more frequent than previously appreciated, on the basis of a preliminary magnetic resonance study that found clinically silent infarcts after cerebral angiography, predominantly in the territory of the posterior circulation.29 Moreover, in 1 of our patients with a perimesencephalic haemorrhage,

angiography

was

complicated by

a

magnetic-resonance-

proven infarct. Nevertheless, given the risk of a later rebleed, we urge follow-up angiograms in patients with an of aneurysmal pattern haemorrhage on CT, although we found that even a second normal angiogram does not definitively exclude an aneurysm. Perhaps a third angiogram should be carried out after several months in this subgroup. Magnetic resonance angiography is a promising technique,30 but its value in detecting occult aneurysms has not yet been proved. Because no systematic study has shown a benefit of exploratory craniotomy in patients with repeatedly normal angiograms, we think this is indicated only in patients who have, and survive, a rebleed. By contrast, a policy of repeated angiography is untenable in perimesencephalic nonaneurysmal haemorrhage. The absence of rebleeding in our 77 patients with a perimesencephalic pattern of haemorrhage on CT does not justify repetition of vertebral angiography.

Similarly, patients with perimesencephalic haemorrhage should be explicitly told that their prognosis is excellent. It was unnecessary that 2 of our patients were declared unfit for work. In conclusion, this study provides evidence that potential rebleeding and disability in patients with subarachnoid haemorrhage and a normal angiogram is limited to those with an aneurysmal pattern of haemorrhage on CT and does not occur in patients with a localised clot in the with a cisterns. Patients perimesencephalic make perimesencephalic non-aneurysmal haemorrhage up two-thirds of all patients with angiogram-negative subarachnoid haemorrhage. Given the differences in outcome between these two groups, the use of the umbrella term "angiogram-negative subarachnoid haemorrhage" is no

longer justified.

We thank Dr P. J. A M. Brouwers, Dr J. Lodder, Dr E. A. C. M. Sanders, Dr J. T. J. Tans, and Dr A. R. Wintzen, for help in collecting patient data, Dr A. I. M. Heopelman and Dr A. Algra, for critical review of the paper and helpful suggestions; the departments of radiology of the University Hospitals in Utrecht, Rotterdam, Amsterdam, Leiden, and Maastricht and St Elisabeth Hospital in Tilburg, Ignatius Hospital in Breda, De Wever Hospital in Heerlen, and Medisch Spectrum Twente Hospital in Enschede, for carrying out all radiological procedures and allowing us to review the photographs; and Ms E. Budelman-Verschuren for secretarial help.

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