Report on the Cooperative Study of Intracranial
Aneurysms and Subarachnoid Hemorrhage
SECTION III
Subarachnoid Hemorrhage Unrelated to Intracranial
Aneurysm and A-V Malformation*
A Study of Associated Diseases and Prognosis
HERBERT B. LOCKSLEY, M.D.; A. L. SAHS,M.D., AND RONALD SANDLER**
Introduction
PONTANEOUS subarachnoid hemorrhage
S is almost always a dramatic and fre-
quently a catastrophic event. This
m a y explain why subarachnoid hemorrhage
(SAH) in years past came to be elevated to
the status of a disease entity. Increasing
knowledge of the subject and improved diag-
nostic methods have made it possible to
recognize a number of disease processes
which may present as subarachnoid hemor-
rhage. This is an important advance since
treatment, prognosis and ultimately, preven-
tion, are dependent upon a specific diagnosis.
Statistics on the incidence of various
causes of SAH are difficult to acquire. In the
reports available, marked variations are en-
countered and appear to reflect differences in
methods of study and in selection of cases.
In this paper, the various diagnostic cate-
gories of SAH will be reviewed based on the
experience of the Cooperative Study in 5836
cases. Special attention will be given to the
groups of cases in which SAH is unrelated to
aneurysms and arteriovenous malformations.
(AVM).
Brief Review of the Literature
Symonds '24 delineated the four major
* Supported by the National Institute of Neurological
Diseases and Blindness of the United States Public
H e a l t h Service through grants to the Cooperative Study
of Intracranial Aneurysms and Subarachnoid Hemor-
rhage. For names of investigators and centers participat-
ing in this inter-institutional project, see "Contributors
and Centers" listed in Section I of the report by Sahs
el al. in Journal of Neurosurgery, 1966, 24 : 779-780.
** Central Registry of the Cooperative Study, Divi-
sion of Neurosurgery and Department of Neurology,
University of Iowa, Iowa City, Iowa.
1034
routes by which blood enters the subarach-
noid space in nontraumatic SAH: (1) An
effusion originating within the subdural
space m ay rupture the arachnoid membrane
and gain entrance to the subarachnoid space.
(2) A hemorrhage into the superficial parts of
the nervous system may break through the
pia m at er into the subarachnoid space. (3) A
deeply situated cerebral hemorrhage m ay
rupture into one of the ventricles, and thence
the blood may find its way into the subarach-
noid space. (4) T he hemorrhage m a y be
derived from one of the larger vessels lying in
the subarachnoid space itself.
In Walton's '53 series of 312 consecutive
cases of SAH bearing clinical and autopsy
diagnoses, but before angiography was in
general use, aneurysms were responsible for
65 (20 per cent), angiomas for 5 (1.6 per cent),
unusual causes for 16 (5 per cent) and the
remaining cases were largely unknown (63
per cent). Walton '55, in another analysis of
etiology, excluded cases with primary intra-
cerebral hemorrhage with extension into the
subarachnoid space. I t would seem desirable
to continue to include these cases because of
the clinical difficulty of distinguishing hy-
pertensive-arteriosclerotic parenchymal hem-
orrhage from those due to aneurysm, AVN[,
and others.
The role of intracranial aneurysm in SAII
has been dealt with extensively in writings
by D a n d y '44, H a m b y '52, Walton '56, Mc-
Kissock et al. '58, '59, Fields and Sahs '65,
and Pool and Potts '65. Although saccular
aneurysms are the most common cause of
subarachnoid hemorrhage, a number of other
conditions must also be considered. This is at
variance with some early reports, e.g., Ayer
'34, which considered spontaneous subarach-
 Unrelated Subarachnoid Hemorrhage 1035
TABLE 10
Non-Traumatic Subarachnoid Hemorrhage

D a t a from D a t a from D a t a from D a t a from

Courville, Odom et al. McKissock Levy
'37 '52 et al. '59 '60

Aneurysm 16 15% 102 32% 1183 56% 64 39%

Hypertension-Arteriosclerosis 32 30% 43 14% . . . .
Intracerebral H e m a t o m a -- -- 8 8% ~78 18% -- --
Arteriovenous Malformation -- -- ~0 6% 183 9~o ~3 14~o
Embolism 11 10% . . . . . .
Eelampsia 4 4% . . . . . .
Infection 9 8% . . . . . .
Venous T h r o m b o s i s 5 5% . . . . . .
Epilepsy o 2% . . . . . .
Blood Dyserasia 1 1% . . . . . .
Tumor 3 3% . . . . . .
Miscellaneous 4 4% . . . . 1 0.7%
Cause U n k n o w n s 19% 143 45% 47~ ~2% 76 47%

107 100% 816 100% 2116 100% 164 100%

noid hemorrhage practically synonymous erature by M c D o n a l d and K o r b '39 wherein

with r u p t u r e d intracranial aneurysms.
Courville '37 found 107 cases of nontrau-
matic subarachnoid hemorrhage as the cause
of death in a series of 15,000 routine autop-
sies and listed the causes. Odom et al. '52
analyzed the incidence of various causes of
SAH in 316 cases studied mostly b y clinical
means. Odom et al. noted t h a t in 143 cases
the etiology of the hemorrhage was not found.
L e v y '60 reported on 164 cases of SAH all of
which had been studied by bilateral carotid
angiography. H e also mentioned the difficulty
of determining the cause of hemorrhage in
cases without demonstrable aneurysm or
AVM. P e r t i n e n t data from these four series
are summarized in Table 10.
Arteriovenous malformations rank well
down the list of causes of SAH. In the series
of 781 cases of SAH reported b y McKissock
and Paine '59, there were 36 cases of AVM
(5 per cent). Small " c r y p t i c " angiomas have
been described b y Margolis et al. '51 and
Crawford and Russell '56 lying in the walls of
cerebral hematomas. These were brought to
light b y careful dissection and pathologic
s t u d y in cases of otherwise obscure etiology.
M y c o t i c aneurysms still occur occasionally
(Barker '54; R o a c h and D r a k e '65). T h e re-
ported incidence of mycotic aneurysms in the
series of 191 patients surveyed by R o a c h and
D r a k e '65 was ~.6 per cent, a great reduction
in recent years when compared with the
1,1~5 aneurysm cases collected from the lit-
the incidence of mycotic a n e u r y s m s was 12.2
per cent.
Syphilis appears to play an inconsequen-
tial role at the present time, a l t h o u g h it was
reported as responsible for 5.6 per cent of
the aneurysms surveyed b y M c D o n a l d and
Korb '39.
The various causes of massive intracere-
bral hemorrhage have been fairly well docu-
mented because the high d e a t h rate fre-
quently permits clinicopathological correla-
tion. Russell '54 surveyed 461 a u t o p s y cases
of massive cerebral h e m o r r h a g e in the Lon-
don Hospital from 1912 to 1952 and found 50
per cent related to hypertension. H e r cases
are listed in Table 11.
In the series of 244 cases of p r i m a r y intra-
cerebral hemorrhage reported b y M c K i s s o c k
et al. '59, subarachnoid h e m o r r h a g e was
present in 80 per cent. T h e y indicated t h a t
large intracerebral hemorrhages m a y occur
without evidence of bleeding into the sub-
arachnoid space. H y l a n d '61 s t a t e d t h a t cere-
brovascular disease with h y p e r t e n s i o n is the
most common cause of intracranial hemor-
rhage. Mutlu et al. '63 reported on the clini-
cal and pathological correlations in 222 cases
of massive cerebral h e m o r r h a g e (accom-
panied by SAH in 86 per cent). H y p e r t e n s i o n
and arteriosclerosis accounted for 60 per cent
of their cases (Table 11).
A great variety of unusual causes of spon-
taneous subarachnoid h e m o r r h a g e h a v e been