From the Instituto Nacional de Neurología y Neurocirugía,
Mexico City, Mexico.
Correspondence to Fernando Barinagarrementeria, MD, Stroke Clinic, Instituto Nacional de Neurología y Neurocirugía, Insurgentes Sur 3877, Tlalpan, 41269, Mexico City, Mexico. E-mail fbarinaga{at}compuserve.com
Methods—We evaluated 359 patients with neuroimaging evidence of
cerebral hemorrhage and selected 22 with RPCH.
Results—Five patients (23%) were older than 70 years at the
first cerebral hemorrhage. Mean ages at the first and second
hemorrhages were 60 and 63 years, respectively. Risk factors
included hypertension (86%), diabetes (27%), and tobacco and alcohol
use (each 14%). Hypocholesterolemia was demonstrated
in 35% of the patients. The most common pattern of recurrent bleeding
was ganglionic-ganglionic, mainly related to hypertension. Overall
mortality was 32%. Forty-one percent and 27% of patients,
respectively, had incapacitating and nonincapacitating sequelae; 2 of
the latter had RPCH with a lobar location. Ganglionic-ganglionic
hemorrhage was associated with a poor prognosis; otherwise,
this pattern was uncommon in patients with nonincapacitating sequelae.
Analysis of the control of risk factors, primarily hypertension
after the first cerebral hemorrhage, disclosed that 56% of
patients did not gain subsequent control.
Conclusions—Rebleeding after a first primary
intracerebral hemorrhage is not uncommon. The
main topographic pattern of bleeding, ganglionic-ganglionic, is likely
the result of hypertension; the less common lobar-lobar pattern
probably results from amyloid angiopathy.
In each case, age at the time of the first and second
hemorrhages, sex, risk factors, the location of each cerebral
hemorrhage, and the time period between initial and recurrent
cerebral hemorrhages were analyzed. Clinical outcome
was determined at hospital discharge as follows: (1) total recovery;
(2) the presence of mild sequelae, with which the patients could work,
although they might have mild complaints; (3) the presence of severe
sequelae, with which patients had physical limitations and serious
neurological symptoms that made them unable to engage in everyday
activities; and (4) death.
The locations of the first cerebral hemorrhages were as
follows: basal ganglia (putamen, caudate nucleus, thalamus) in 13
patients (59%), lobar region in 6 (27%), cerebellum in 2 (9%), and
brain stem in 1 (5%). During the follow-up period, 4 cases of RPCH
(18%) occurred in the ipsilateral structures and 18 (82%) in the
contralateral structures. The locations of the second cerebral
hemorrhages were the basal ganglia in 16 patients (73%) and
the lobar region in 6 (27%). The recurrence pattern in each
case is shown in Table 1
The mean age at which the first ganglionic hemorrhage
occurred was 57.8 years; the first lobar hemorrhage, 67 years;
recurrent ganglionic hemorrhages, 62 years; and recurrent lobar
hemorrhage, 65 years. The average time to recurrent bleeding
based on the location of the first cerebral hemorrhage was 39
months in the ganglionic region, 46 months in the lobar region, and 28
months in other locations. Eight patients (36%) had a
recurrence within the first year after the initial
hemorrhage. The pattern of recurrent bleeding is shown in Table 2
The overall mortality in this series was 32%. Nine patients (41%) had
incapacitating sequelae, and 6 (27%) had nonincapacitating sequelae (2
of these patients had a recurrent cerebral hemorrhage with a
lobar location). Ganglionic-ganglionic hemorrhage was
associated with 85% of the deaths and almost 50% of incapacitating
sequelae; otherwise, this pattern was uncommon in patients with
nonincapacitating sequelae.
Analysis of the control of risk factors, mainly hypertension
after the first cerebral hemorrhage, disclosed that in 12
patients (56%) there was no subsequent control of risk factors. Two
patients developed more than 2 cerebral hemorrhages (patients
18 and 19, Table 1
The mean patient age in our series was 63 years. The most common
risk factor was hypertension, which was present in almost 90% of
patients. The frequency of hypertension was 62% to 70% in the
European series12 13 and 100% in the Asian
series.11 14 15 16 This high frequency of
hypertension explains why the most common pattern of recurrence
was ganglionic-ganglionic. Because most hypertensive hemorrhage
occurs in the basal ganglia,22 it is reasonable
to attribute this bleeding location to hypertension. This pattern of
recurrence also was the most common in the Asian series. A
recurrent lobar-lobar pattern was present in only 18% of patients,
a frequency between those reported by European (58% and
45%)12 13 and Asian authors (0 to
7%).11 14 15 16
It is probable that a higher number of patients without
hypertension and recurrent lobar hemorrhage had amyloid
angiopathy as a cause of bleeding. Cerebral amyloid angiopathy is a
well-known cause of recurrent ICH.23 The
incidence of amyloid angiopathy characteristically increases with age.
The mean age of patients with ICH resulting from amyloid angiopathy in
most reported series is over 70 years.24 ICH
secondary to amyloid angiopathy is not associated with hypertension and
is usually lobar in distribution because amyloid angiopathy has a
predilection for the cortical arteries.24 This
finding can explain the higher frequency of lobar hemorrhage in
the series reported by Neau et al12 and Passero
et al,13 which included older patients. In the
present series, the mean age of the patients with a
ganglionic-ganglionic recurrence pattern was 60 years compared
with 70 years for those with the lobar-lobar recurrence
pattern. In all patients with hypertension, some of the primary or
recurrent hemorrhages involved the basal ganglia. In the series
of Passero et al,13 only 25% of patients with
the lobar-lobar recurrence pattern had hypertension.
The global mortality rate in our series was 32%, higher than in the
series reporting first cerebral hemorrhages (20 to
23%).25 26
The prognosis for patients with RPCH was worse than for those with
nonrecurrent bleeding. Only 27% of patients had good functional
recovery compared with 37% to 55% of patients with a first cerebral
hemorrhage.27 28 In the series of Neau et
al,12 two thirds of patients could walk after
RPCH. In the present series, recurrence with the
lobar-lobar pattern was associated with the best prognosis.
In conclusion, our study shows that rebleeding after a first primary
ICH is not an uncommon event. The main topographic pattern of bleeding,
ganglionic-ganglionic, is likely the result of hypertension; the less
common lobar-lobar pattern is probably the result of amyloid
angiopathy. The frequency and mechanisms of RPCH appear to be different
among Asian and Europeans, reflecting the similarities of the
present series to the Asian series.
Received April 6, 1998;
revision received May 26, 1998;
accepted May 26, 1998.
2.
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© 1998 American Heart Association, Inc.
Original Contributions
Recurrent Primary Cerebral Hemorrhage
Frequency, Mechanisms, and Prognosis
Abstract
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
Background and Purpose—The frequency
of recurrent primary cerebral hemorrhage (RPCH), mainly in
cases related to hypertension, has been considered low. This study
investigated the frequency, mechanisms, and prognosis of RPCH.
Key Words: cerebral hemorrhage • hypertension • amyloid • prognosis
Introduction
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
Nontraumatic cerebral
hemorrhage is an important cause of death and disability among
adults. Intracerebral hemorrhage (ICH) accounts
for approximately 10% of stroke cases.1 The
incidence of ICH is higher among individuals of Asian and
African-American descent.2 3 4 A recently
published study has also suggested a high frequency of cerebral
hemorrhage in the Ecuadoran population.5
The causes of ICH are multiple,6 and the
frequency of the various etiologies are age dependent. In people
younger than 45 years the most common cause is arteriovenous
malformation7 ; in individuals older than 70 years
it is amyloid angiopathy8 ; and in the
intermediate age groups hypertension is the primary
cause.9 The frequency of recurrence of
cerebral hemorrhage, mainly in those cases related to
hypertension, is considered very low10 ; however,
relevant information is scarce,11 12 13 14 15 16 17 primarily
from Asian countries11 15 16 and, less often,
from Europe.12 13 The goal of the present
study was to determine the frequency, mechanisms, and prognosis of
recurrent primary cerebral hemorrhage (RPCH).
Subjects and Methods
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
Between March 1989 and September 1997, of 1737 patients with
stroke we evaluated 497 (28.6%) patients with neuroimaging evidence of
cerebral hemorrhage. We excluded 22 patients with cerebral
hemorrhage that resulted from intracranial aneurysms,
arteriovenous malformations, bleeding diathesis, trauma, intracranial
brain tumor, and anticoagulant use. Among the remaining 475 patients,
83 (17%) died in the acute stage as a result of cerebral
hemorrhage, and 33 surviving patients were lost to follow-up.
Among the remaining 359 surviving patients, 31 (8.6%) had recurrent
cerebral hemorrhage and 9 were excluded because the
neuroimaging studies of the first cerebral hemorrhage were
unavailable for analysis. Twenty-two patients were considered
eligible for final analysis.
Results
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
We studied 22 patients (17 men [77%] and 5 women [23%]) with
RPCH. The mean age at the time of the first cerebral hemorrhage
was 60 years (range, 28 to 77 years); the mean age of the men was 58
years and that of the women was 64 years. Five (23%) patients were
older than 70 years at the time of the first cerebral
hemorrhage. The mean age at the time of the second
hemorrhage was 63 years (range, 28 to 84 years). The mean
interval between the first and second cerebral hemorrhages was
39 months (range, 1 month to 12 years). Risk factors included
hypertension in 19 patients (86%), diabetes in 6 (27%), tobacco use
in 3 (14%), and alcohol use in 3 (14%).
Hypocholesterolemia was demonstrated in 35% of the
patients. 
. During a mean
follow-up of 55 months, the recurrent stroke rate was 2/100 patients
per year.
View this table:
[in a new window]
Table 1. Patient Ages and Locations of First and Recurrent
Cerebral Hemorrhages ; the most common pattern was
ganglionic-ganglionic.
View this table:
[in a new window]
Table 2. Characteristics of Patterns of Recurrence 
).
Discussion
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
Compared with the extensive information regarding short-term
outcome in patients with cerebral hemorrhage, few reports have
documented the frequency of RPCH, which has been considered uncommon.
Douglas and Haerer10 did not find a case of
recurrence among 35 surviving patients with cerebral
hemorrhage. Similar results were published by Fieschi et
al,18 who analyzed the 1-year outcome in
69 patients. Neuropathological studies have estimated the incidence of
recurrent ICH as being higher than 14%.19 In 7
published clinical series,11 12 13 14 15 16 17 the frequency of
RPCH was an average of 3.8% (156 cases of RPCH among 4028 patients)
(Table 3). In the present series, the
frequency of RPCH was 6%, which is similar to findings reported by
Chen et al11 in Taiwan (5.3%) and Maruishi et
al15 in Japan (5.9%) and higher than those
reported by Lee et al14 in Korea (2.7%). The
frequency of cerebral hemorrhage as a cause of stroke in our
hospital registry was 28.6%, a number considerably higher than those
in stroke registries from countries such as the United States
(11%)1 and Switzerland
(11%),20 similar to those from Taiwan
(35%)21 and Korea
(32%),14 and lower than those reported in
Japan.2
View this table:
[in a new window]
Table 3. Series of Recurrent Primary Cerebral
Hemorrhage
Acknowledgments
We thank Carlos S. Kase, MD, Boston, Mass, for his suggestions
and helpful criticism of this article.
References
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
1.
Mohr JP, Caplan LR, Melski JW, Goldstein RJ,
Duncan GW, Kistler JP, Pessin MS, Bleich HL. The Harvard Cooperative
Stroke Registry: a prospective registry. Neurology. 1978;28:754–762.
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