AJDRAJNR - American Journal of Neuroradiology

This Article
Right arrow Abstract Freely available
Right arrow Figures Only
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via CrossRef
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Given, C. A.
Right arrow Articles by Williams, D. W.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Given, C. A., II
Right arrow Articles by Williams, D. W., III

Case Report
BRAIN

Pseudo-Subarachnoid Hemorrhage: A Potential Imaging Pitfall Associated with Diffuse Cerebral Edema

Curtis A. Given, IIa, Jonathan H. Burdettea, Allen D. Elstera and Daniel W. Williams, IIIa

a From the Departments of Neuroradiology (C.A.G., J.H.B., D.W.W.) and Radiology (A.D.E.), Wake Forest University Baptist Medical Center, Winston-Salem, NC

Address reprint requests to Curtis A. Given II, MD, University of Kentucky, Department of Radiology, Room HX-311C, 800 Rose Street, Lexington, KY 40536


    Abstract
 TOP
 Abstract
 Introduction
 Case Reports
 Discussion
 Conclusion
 References
 
Summary: We report CT findings in seven patients with diffuse cerebral edema and increased attenuation in the basilar cisterns resembling subarachnoid hemorrhage. On the basis of autopsy (three cases) and lumbar puncture (four cases) findings, true subarachnoid hemorrhage was reasonably excluded. Pathophysiologic changes that occur with diffuse cerebral edema are explored, with proposed explanations for the appearance of a pseudo-subarachnoid hemorrhage.


    Introduction
 TOP
 Abstract
 Introduction
 Case Reports
 Discussion
 Conclusion
 References
 
Increased attenuation of the basal cisterns and subarachnoid spaces on CT scans is a characteristic finding of acute subarachnoid hemorrhage (SAH). Several radiographic mimics of SAH have been reported, including pyogenic leptomeningitis, CT appearance of intrathecally administered contrast material, and leakage of high-dose intravenous contrast medium into the subarachnoid spaces (16). Together, these CT mimics of SAH have been called pseudo-SAH (57).

The pseudo-SAH appearance may also be seen in patients with acute neurologic deficits in whom evidence of diffuse cerebral edema is present at CT examination. In this report, we describe seven patients with pseudo-SAH hemorrhage associated with diffuse cerebral edema. We also review the literature, investigate the pathophysiology behind its appearance, and discuss imaging findings that aid in its recognition and its distinction from true SAH.


    Case Reports
 TOP
 Abstract
 Introduction
 Case Reports
 Discussion
 Conclusion
 References
 
We retrospectively reviewed the clinical, laboratory, and pathology-autopsy reports in seven patients without trauma (Table). Diffuse cerebral edema and increased attenuation of the subarachnoid spaces was noted on CT scans. Nonenhanced head CT scans were obtained in all cases, and one of the patients (case 1) was also examined with a contrast-enhanced study. In each case, the attenuation within the basal cisterns mimicked that of SAH (Figs 1A, 2A). The patients were aged 8 months to 37 years and included four male and three female patients. The time from their clinical deterioration (usually during intubation) to the CT examination varied widely, ranging from approximately 2 hours before deterioration (case 4) to approximately 33 hours after resuscitation (case 2). Attenuation values within the basal cisterns were obtainable in three of the patients (cases 5–7). Two of the patients (cases 6 and 7) had undergone prior examinations, with images available for comparison. These permitted quantification of the observed decrease in attenuation within the deep gray matter structures. True SAH was excluded by means of either autopsy (three cases) or lumbar puncture (four cases).


View this table:
[in this window]
[in a new window]
 
Summary of clinical and imaging findings

 



View larger version (90K):
[in this window]
[in a new window]
 
FIG 1. Case 1. Axial nonenhanced CT images through the basal cisterns.

A, Image obtained before contrast enhancement reveals abnormally increased attenuation within the basal cisterns (arrows).

B, The basal cisterns (arrowheads) are enhancing after the intravenous administration of contrast material.



View larger version (92K):
[in this window]
[in a new window]
 
FIG 2. Case 6. Axial nonenhanced CT images through the basal cisterns.

A, Image reveals effacement of and increased attenuation within the basal cisterns (arrowheads).

B, The findings were not present on the prior image obtained approximately 3 days earlier.

CT scans in each of the seven patients displayed increased attenuation of the subarachnoid spaces in the basal cisterns (mimicking SAH), as well as signs of diffuse cerebral edema (Figs 1 and 2). Signs of cerebral edema included the following: effacement of the basal cisterns and cortical sulci (seven patients), compression or mass effect or both on the fourth ventricle (six patients), and poor gray matter—white matter differentiation (four patients). One patient (case 1) had an additional finding of abnormal enhancement within the basal cisterns after the intravenous administration of contrast material (Fig 1B). None of the patients had evidence of hemorrhage or increased attenuation within the ventricular system or the superficial sulci. When obtainable, the attenuation values within the basal cisterns ranged from 21 to 40 HU, with mean values of 29–33 HU (Table). In the two cases with prior CT examinations (cases 6 and 7), the mean attenuation value of the deep gray matter (thalami) decreased by 12.5% and 6.5%, respectively, with the development of the pseudo-SAH appearance. The CT findings were prospectively interpreted as demonstrating pseudo-SAH in five of the cases, with aneurysmal-type SAH suggested in the remaining two cases. Six of the patients subsequently died, and one patient (case 3) fully recovered after surgical intervention.


    Discussion
 TOP
 Abstract
 Introduction
 Case Reports
 Discussion
 Conclusion
 References
 
The pseudo-SAH appearance within the basal cisterns, in conjunction with diffuse cerebral edema, has received only limited attention in the medical literature. Avrahami et al (7) noted pseudo-SAH in a case series of comatose patients (without trauma), and pseudo-SAH was the subject of a case report by Al-Yamany et al (6). Others (3, 4) have noted increased attenuation of the falx and tentorium in association with cerebral edema, but they made no mention of increased attenuation within the basal cisterns.

To explain the origin of pseudo-SAH in association with cerebral edema, we considered the proposed causes of pseudo-SAH in other diseases. In cases of meningitis, toxins elaborated by the offending organism lead to breakdown of the blood-brain barrier (BBB) (2). The resultant BBB disruption allows proteinaceous material to leak into the subarachnoid space (2, 8). However, CSF protein concentrations are sufficiently elevated to cause appreciable changes in CSF attenuation only in the most severe cases of meningitis (2, 9). Breakdown of the BBB and vasogenic edema usually accompany diffuse cerebral edema (1012). During the acute phases of cerebral injury, vasogenic edema is predominately cleared by means of CSF resorption (10, 13, 14). While the CSF protein content may be elevated in cases of cerebral edema (and other pathologic entities), this elevation has a negligible effect on the CSF attenuation value at CT examination (9). Any increase in the CSF protein content would not contribute significantly to the pseudo-SAH appearance observed in cases of cerebral edema. Some have postulated that other factors, such as edema within the adjacent cortex, elevated intracranial pressure with venous distention, or purulent material within the subarachnoid spaces contribute to the pseudo-SAH appearance (6, 7).

The increase in intracranial pressure and the brain swelling that accompany cerebral edema narrow the subarachnoid spaces and displace CSF. The increased intracranial pressure causes engorgement and dilatation of the superficial (pial) venous structures (1518). The resultant subarachnoid spaces become relatively devoid of the hypoattenuated CSF and fill with a larger fraction of meninges and blood vessels than in the normal state, potentially increasing their CT attenuation. The pooling of contrast agent within these distended venous structures may have accounted for the abnormal enhancement observed within the basal cisterns in one of our cases (Fig 1B). Avrahami et al (7) observed a similar pattern of contrast enhancement within the basal cisterns in patients with cerebral edema.

With development of cerebral edema, the attenuation of the brain parenchyma decreases concurrently (12, 19). The attenuation value of normal gray matter varies with patient age. Normal values of around 33 HU are observed in adults (20, 21). Prior CT scans were available in two of our cases. These permitted us to eliminate age-associated variation and to calculate the decrease in attenuation within the parenchyma in these cases of pseudo-SAH. In cases 6 and 7, attenuation within the thalami decreased by 12.5% and 6.5%, respectively, with development of edema and the pseudo-SAH appearance. This decrease in attenuation is indicative of cerebral edema and likely contributes to the pseudo-SAH appearance by increasing the conspicuity of the distended vasculature within the basal cisterns.

We were able to measure attenuation values within the basal cisterns in three of our patients (cases 5–7), with mean values ranging from 29 to 33 HU (Table). These values were well below the expected attenuation of clot within the basal cisterns in patients with SAH, in whom attenuation values typically range from 60 to70 HU (2224). These lower attenuation values, in association with signs of diffuse cerebral edema, should permit the prospective recognition of pseudo-SAH and obviate more invasive testing.


    Conclusion
 TOP
 Abstract
 Introduction
 Case Reports
 Discussion
 Conclusion
 References
 
A false appearance of SAH, or pseudo-SAH, may be seen on CT scans in cases of marked cerebral edema. A plausible explanation for this appearance includes a combination of displacement of hypoattenuated CSF, distention of the superficial vasculature, and edema within the adjacent cortex. Although an increase in the CSF protein content may be seen in cases of cerebral edema, this is unlikely to contribute to the pseudo-SAH appearance. Attenuation values within the basal cisterns in cases of pseudo-SAH are much lower than those observed in cases of true acute SAH. Radiologists should be aware of this potential mimic of SAH when evaluating patients with diffuse cerebral edema.


    References
 TOP
 Abstract
 Introduction
 Case Reports
 Discussion
 Conclusion
 References
 

  1. Eckel T, Breiter SN, Lee HM. Subarachnoid contrast enhancement after spinal angiography mimicking diffuse subarachnoid hemorrhage. AJR Am J Roentgenol1998; 170 :503 –505[Free Full Text]

  2. Mendelsohn D, Moss ML, Chason DP, Muphree S, Casey S. Acute purulent leptomeningitis mimicking subarachnoid hemorrhage on CT. J Comput Assist Tomogr1994; 18 :126 –128[Medline]

  3. Osborn AG, Anderson RE, Wing DS. The false falx sign. Radiology1980; 134 :421 –425[Abstract/Free Full Text]

  4. Spiegel M, Fox AJ, Vinuela F, Pelz DM. Increased density of tentorium and falx: a false positive CT sign of subarachnoid hemorrhage. Can Assoc Radiol J1986; 37 :243 –247[Medline]

  5. Osborn AG. Diagnostic Neuroradiology. St Louis, Mo: Mosby-Year Book, Inc.;1994 :212

  6. Al-Yamany M, Deck J, Bernstein M. Pseudo-subarachnoid hemorrhage: a rare neuroimaging pitfall. Can J Neurol Sci1999; 26 :57 –59[Medline]

  7. Avrahami E, Katz R, Rabin A, Friedman V. CT diagnosis of non-traumatic subarachnoid hemorrhage in patients with brain edema. Eur J Radiol1998; 28 :222 –225[Medline]

  8. Prockop LD, Fishman RA. Experimental pneumococcal meningitis. Arch Neurol19 :449 –463

  9. Norman D, Price D, Boyd D, Fishman R, Newton TH. Quantitative aspects of computed tomography of the blood and cerebrospinal fluid. Radiology1997; 123 :335 –338[Abstract]

  10. Klatzo I. Disturbances of the blood-brain barrier in cerebrovascular disorders. Acta Neuropathol (Berl)1983 :suppl 8 :81 –88

  11. Weisberg L, Greenberg J, Stazio A. Computed tomographic findings in brain swelling. Comput Med Imaging Graph1990; 14 :263 –268[Medline]

  12. Rieth KG, Fujiwara K, Di Chiro G, et al. Serial measurements of CT attenuation and specific gravity in experimental cerebral edema. Radiology1980; 135 :343 –348[Abstract/Free Full Text]

  13. Marmarou A, Hochwald G, Nakamura T, Tanaka K, Weaver J, Dunbar J. Brain edema resolution by CSF pathways and brain vasculature in cats. Am J Physiol1994; 267(2 pt 2) :H514 –H520[Abstract/Free Full Text]

  14. Mei Liu H, Sturner WQ. Extravasation of plasma proteins in brain trauma. Forensic Sci Int1988; 38 :285 –295[Medline]

  15. Wolff HG, Forbes HS. The cerebral circulation: observations of the pial circulation during changes in intracranial pressure. Arch Neurol Psychiatr1928; 20 :1035 –1047

  16. Yada K, Nakagawa Y, Tsuru M. Circulatory disturbance of the venous system during experimental intracranial hypertension. J Neurosurg1973; 39 :723 –729[Medline]

  17. Schmidek HH, Ludwig MA, Kapp JP. The cerebral venous system. Neurosurgery1985; 17 :663 –678[Medline]

  18. Osterholm JL. Reaction of the cerebral venous sinus system to acute intracranial hypertension. J Neurosurg1970; 32 :654 –659[Medline]

  19. Clasen RA, Huckman MS, Von Roenn KA, Pandolfi S, Laing I, Lobick J A correlative study of computed tomography and histology in human and experimental vasogenic cerebral edema. J Comput Assist Tomogr1981; 5 :313 –327[Medline]

  20. Cala LA, Thickbroom GW, Black JL, Collins DW, Mastaglia FL. Brain density and cerebrospinal fluid space size: CT of normal volunteers. AJNR Am J Neuroradiol1981; 2 :41 –47[Abstract]

  21. Boris P, Bundgaard F, Olsen A. The CT (Hounsfield unit) number of brain tissue in healthy infants: a new reliable method for detection of possible degenerative disease. Childs Nerv Syst1987; 3 :175 –177[Medline]

  22. Ohkawa M, Masatada T, Toyama Y, et al. CT angiography with helical CT in assessment of acute stage of subarachnoid hemorrhage. Radiat Med1998; 16 :91 –97[Medline]

  23. Mizoi K, Yoshimoto T, Fujiwara S, Sugawara T, Takahashi A, Koshu K. Prevention of vasospasm by clot removal and intrathecal bolus injection of tissue-type plasminogen activator: preliminary report. Neurosurgery1991; 28 :807 –812[Medline]

  24. Fujita S. Computed tomographic grading with Hounsfield number related to delayed vasospasm in cases of ruptured cerebral aneurysm. Neurosurgery1985; 17 :609 –612[Medline]

Received February 5, 2002; accepted after revision July 1, 2003.




This article has been cited by other articles:


Home page
Am. J. Neuroradiol.Home page
H. Yuzawa, S. Higano, S. Mugikura, A. Umetsu, T. Murata, A. Nakagawa, A. Koyama, and S. Takahashi
Pseudo-Subarachnoid Hemorrhage Found in Patients with Postresuscitation Encephalopathy: Characteristics of CT Findings and Clinical Importance
AJNR Am. J. Neuroradiol., September 1, 2008; 29(8): 1544 - 1549.
[Abstract] [Full Text] [PDF]


Home page
NeurologyHome page
W. I. Schievink, M. M. Maya, J. Tourje, and F. G. Moser
Pseudo-subarachnoid hemorrhage: A CT-finding in spontaneous intracranial hypotension
Neurology, July 12, 2005; 65(1): 135 - 137.
[Abstract] [Full Text] [PDF]


Home page
NEJMHome page
E. Jenwitheesuk, A. C. Jackson, V. Lapierre, P. Tiberghien, A. Srinivasan, M. Kuehnert, and C. Rupprecht
Transmission of Rabies from an Organ Donor
N. Engl. J. Med., June 16, 2005; 352(24): 2551 - 2552.
[Full Text] [PDF]


Home page
Am. J. Neuroradiol.Home page
M. Silberstein and C. A. Given II
Diagnosis of Pseudosubarachnoid Hemorrhage
AJNR Am. J. Neuroradiol., August 1, 2003; 24(7): 1492 - 1492.
[Full Text] [PDF]


This Article
Right arrow Abstract Freely available
Right arrow Figures Only
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via CrossRef
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Given, C. A.
Right arrow Articles by Williams, D. W.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Given, C. A., II
Right arrow Articles by Williams, D. W., III