- Email: [email protected]
Should Patients Be Counseled About Possible Recurrence of Perimesencephalic Subarachnoid Hemorrhage?
Case Report
Should Patients Be Counseled About Possible Recurrence of Perimesencephalic Subarachnoid Hemorrhage? Ajay Malhotra1, Xiao Wu1, Riddhi Borse3, Charles C. Matouk1,2, Ketan Bulsara2
Key words Angiography - CTA - MRI - Perimesencephalic subarachnoid hemorrhage - Recurrence -
Abbreviations and Acronyms BVR: Basal vein of Rosenthal CT: Computed tomography CTA: Computed tomography angiography MRI: Magnetic resonance imaging pSAH: Perimesencephalic subarachnoid hemorrhage SAH: Subarachnoid hemorrhage
- BACKGROUND:
Isolated perimesencephalic subarachnoid hemorrhage (pSAH) is a distinct subtype of subarachnoid hemorrhage (SAH) seen in 5% of patients with SAH, with a relatively benign natural course and good outcome compared with diffuse, aneurysmal SAH. Traditionally, the prognosis of pSAH is believed to be excellent compared with aneurysmal SAH, with no risk of recurrent hemorrhage after long-term follow-up. We describe a case of pSAH in which the patient had a recurrent perimesencephalic bleed 8 years after the initial episode. There are 5 previous reports of recurrent pSAH in existing literature.
- CASE
To whom correspondence should be addressed: Ajay Malhotra, M.D. [E-mail: [email protected]]
REPORT: A patient in sixth decade of life with no history of trauma presented in 2006 with acute-onset, severe headache, and “off-balance” gait. The patient was diagnosed with pSAH on the basis of computed tomography angiography and digital subtraction angiography. The patient was discharged, and follow-up computed tomography angiography over the next 2 years revealed no underlying vascular anomaly. The patient presented in 2014 with sudden onset of headache, similar to the previous episode with no new neurologic signs. Patient had repeated imaging over the succeeding 2 years, which were all negative for new blood or source of subarachnoid bleed.
Citation: World Neurosurg. (2016) 94:580.e17-580.e22. http://dx.doi.org/10.1016/j.wneu.2016.07.112
- REVIEW
From the Departments of 1Radiology and Biomedical Imaging and 2Neurosurgery, Yale School of Medicine, New Haven, Connecticut, USA; and 3Topiwala National Medical College, Mumbai, India
Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2016 Elsevier Inc. All rights reserved.
AND DISCUSSION: There are only a couple of case reports of recurrent pSAH, some of which were defined questionably. We review the reported cases and discuss the imaging results and outcome. Considering the rarity, low risks of complications, as well as the good outcome even after recurrence, we do not recommend routinely counseling patients about possibility of recurrence of pSAH.
INTRODUCTION Isolated perimesencephalic subarachnoid hemorrhage (pSAH) is a distinct subtype of subarachnoid hemorrhage (SAH) seen in 5% of patients with SAH, with a relatively benign natural course and good outcome compared with diffuse, aneurysmal SAH.1-3 Initial angiographic imaging is essential in pSAH to detect aneurysms, because 10% of posterior circulation aneurysms can present with a pSAH pattern.4-6 Initial computed tomography angiography (CTA) has been shown to be reliable in the exclusion of aneurysms in patients meeting the strict imaging and clinical criteria of pSAH, with limited utility of repeat follow-up imaging.7,8 Hydrocephalus and symptomatic vasospasm are much less common with pSAH relative to aneurysmal SAH.9 Other reported complications, including acute seizures, hyponatremia, and cardiac complications including arrhythmias, are also uncommon.10 Traditionally, the prognosis
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of pSAH is believed to be excellent compared with aneurysmal SAH, with no risk of recurrent hemorrhage after longterm follow-up.2,11-13 We describe a case of pSAH in which patient had a recurrent perimesencephalic bleed 8 years after the initial episode. There are 5 previous reports of recurrent pSAH in existing literature, 4 of which occurred in a relatively short time frame after the initial bleed (5 days to 31 months) and the most recent report a recurrent bleed that occurred 12 years after the initial episode.14-18 We review these cases to assess the risk factors linked with the recurrence of pSAH and the outcome of recurrent bleed in the reported cases. CASE REPORT A patient in sixth decade of life with no history of trauma presented in 2006 with
acute-onset, severe headache and “offbalance” gait. The patient had a history of hypertension and diabetes on treatment. On clinical examination, the patient had mild anisocoria but reactive pupils. No other focal neurologic signs were elicited. Initial noncontrast computed tomography (CT) showed hyperdense blood in the prepontine and interpeduncular cistern extending to the left quadrigeminal cistern with a tiny amount layering in the fourth ventricle (Figures 1 and 2). The hemorrhagic component in the inferior third and fourth ventricles was probably attributable to sedimentation phenomenon because the greatest density of blood was within the interpeduncular cistern. CTA and 6 vessel-selective injections digital subtraction angiography performed at presentation were negative for any
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2016.07.112
CASE REPORT AJAY MALHOTRA ET AL.
ADVISING PATIENTS OF POSSIBLE RECURRENCE OF PSAH
Figure 1. Initial noncontrast computed tomography of the head (A and B) shows hyperdense blood in the prepontine and ambient cistern. (C) Computed tomography angiography does
vascular source of the subarachnoid blood (Figures 3 and 4). Magnetic resonance imaging (MRI) of the brain and cervical spine performed at day 3 did not reveal the source of SAH, either. The patient was discharged home after an uneventful recovery and neurologic function at baseline. Follow-up CTAs during the next 2 years revealed no underlying vascular anomaly. The patient presented in 2014 with sudden-onset headache (6/10), similar to the previous episode with no new neurologic symptoms. Since 2006, the patient had developed coronary artery disease and had myocardial infarction
not show any intracranial aneurysm or vascular lesion. A prominent left posterior communicating artery is seen with hypoplastic P1 segment.
status postangioplasty and stenting, on aspirin 81 mg. Noncontrast CT showed subarachnoid blood confined anterior to the brainstem, and cerebrospinal fluid analysis showed blood in 4/4 tubes (Figure 5). CTA, MRI/magnetic resonance angiography, and digital subtraction angiography at presentation were all negative for vascular source of SAH. The patient had a repeat CTA at 1 week, and 2 CTAs and 1 MRI during the next 2 years, all of which were negative for new blood or source of subarachnoid bleed. At 2-year followup, the patient remains neurologically at baseline and has not had any
Figure 2. Brain magnetic resonance imaging performed on Day 3. (A) Axial fluid-attenuated inversion recovery and (B) T1-weighted images show hyperintense signal in the perimesencephalic cisterns corresponding to the previously
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recurrence of further episodes of similar headache/SAH. DISCUSSION There are only a couple of case reports of recurrent pSAH. Schwartz and Solomon12 reviewed the literature in 1996 and found no cases of rebleeding in 169 patients after a follow-up of 8e51 months. The first reported case of recurrent pSAH was in 2000 by Marquardt et al.,15 where the recurrent bleed occurred 31 months after the initial episode. A summary table of the 5 previously reported studies is presented in Table 1.14-18
seen hyperdense blood. (C) Magnetic resonance imaging of the cervical spine, sagittal gradient echo image shows blood in the prepontine cistern, but no underlying structural abnormality was identified.
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ADVISING PATIENTS OF POSSIBLE RECURRENCE OF PSAH
Figure 3. Cerebral conventional angiogram. (A) Right internal carotid artery injection, right anterior oblique (RAO) projection. (B) Left internal carotid artery injection, RAO projection. (C) Right vertebral artery injection, frontal projection. (D) Left vertebral artery injection, frontal projection. No vascular etiology for subarachnoid hemorrhage was identified.
In 2009 Reynolds et al.17 questioned the 3 previously reported cases of recurrent pSAH and added a case of definite recurrent pSAH to 1 “probable” and 2 “possible” reported cases. They raised
concern for confirmation of pSAH on the initial bleed in case of the case reported by Marquardt et al.15 The cases reported by Ildan et al.14 and van der Worp et al.18 died after the recurrent bleed and did
Figure 4. Images (A) and (B) show the venous phases of right internal carotid artery injection and left internal carotid artery injection injections. Basal vein of Rosenthal (BVR) variant type C is shown on the right (arrow in B) with BVR draining into the transverse sinus and BVR type B on the left (arrow in A) with BVR draining anteriorly into the uncal vein and posteriorly into the Galenic system.
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not undergo any repeat vascular imaging or autopsy. Ildan et al.14 reported that the repeat CT scan of the patient with rebleed suggested aneurysmal SAH, which raises questions about the validity of these cases being true perimesencephalic rebleeds. In addition to our case, we found only 1 additional definite case in which both SAH episodes were true, documented cases of recurrent, idiopathic pSAH many years after the initial bleed (8 and 12 years, respectively).16 Multiple imaging studies performed in our patient did not reveal a vascular etiology for the pSAH. Similarly, Rahme and Vyas16 also could not find an underlying structural lesion despite head CTA, cerebral and cervical spinal angiography, and MRI of the brain and spine. They reported a neurologically favorable outcome, with the patient discharged home, but did not have longer follow-up. We present a 2-year follow-up after the recurrent bleed, with multiple imaging studies remaining negative and patient remaining at neurologic baseline. Several risk factors of pSAH have been suggested, such as smoking, female sex, and younger age, with hypertension as the only risk factor consistently present in different studies.19,20 Although the etiology of pSAH remains elusive, multiple hypothesis have been suggested, including venous bleed caused by tear in the basal vein of Rosenthal (BVR) or its tributaries, unrecognized vertebrobasilar dissections, rupture of arterial perforators, or radiographically occult aneurysms or vascular malformations.8,21-23 The long interval period of many years in these 2 cases excludes the possibility of deficient hemostasis being the cause of bleed. The first 4 reported cases of rebleed occurred after shorter intervals (5 days to 21 months), and inadequate hemostasis after the first bleeding episode has been invoked as a possible explanation in those cases.17,18 Van der Worp et al.18 reported a case of recurrent pSAH 3 days after starting treatment with intravenous heparin for acute coronary syndrome, and they postulated that anticoagulant therapy may have resulted in dissolution of clot in a ruptured vein at the tentorial edge, thereby resulting in recurrent hemorrhage. Unfortunately, the patient died the same day due to ventricular
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2016.07.112
CASE REPORT AJAY MALHOTRA ET AL.
ADVISING PATIENTS OF POSSIBLE RECURRENCE OF PSAH
anterior to the medulla. (A, B) Axial CT and (C) Sagittal reformats.
Figure 5. Noncontrast computed tomography shows hyperdense blood in the prepontine cistern extending inferiorly
fibrillation, and no follow-up imaging could be obtained. There was no antithrombotic use in the other reported case by Rahme et al.,16 where the rebleed happened after many years. Other vascular causes of pSAH that have been hypothesized are ruptured capillary telangiectasias or perforating arteries, and unrecognized vertebrobasilar dissections, aneurysms, or vascular malformations.16 Repeat imaging was not performed in 2 of the pSAH rebleed cases, and thus, a small vascular lesion causing the bleed theoretically could have been missed.14,18 However, recurrent bleed happening after so many years and the fact that repeated imaging did not reveal any vascular cause in both cases where rebleed happened after many years make these causes unlikely.
Although the yield of repeated imaging in patients with pSAH is questionable, even recent literature advocates follow-up imaging.24,25 Catheter angiography has been postulated to be better than CTA and often is used in the evaluation for pSAH. Its routine use, however, remains questionable.5,26 The utility of MRI also has been questioned, with relatively low diagnostic yield.27 Although no definite precipitating cause was identified in the case by Reynolds et al.,17 the patient had engaged in exertional activity before both events. None of the other reported cases had a similar history. Song et al.28 found physical actions, including breath holding during coughing, shouting, and ejaculation, in 30% instances of nonaneurysmal SAH in their series,
Table 1. Summary of Previously Reported Cases Study
Time to Postulated Recurrence Antithrombotics Risk Factor
Outcome
Rahme and Vyas, 201516
12 years
No antithrombotics
Primitive venous drainage
Discharged home
Reynolds et al., 201117
5 months
Aspirin 81 mg
Exertional activity
Discharged with no neurologic deficits; complete resolution at 1 year
Van der Worp et al., 200918
5 days
Antithrombotic
Ildan et al., 200214
Early rebleed
Marquardt et al., 31 months 200015
Died Died after rebleed Discharged without neurologic deficits
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leading them to reinforce the hypothesis that intracranial venous congestion caused by straining in patients with anomalous venous drainage might tear a vein fixed to a dural sinus. Primitive variants of the venous anatomy, with the BVR draining directly into the dural sinuses rather than into the Vein of Galen, have been found to have a greater prevalence in patients with pSAH.28-31 Song et al.28 found bilateral primitive venous drainage (type C) in 13% of patients with idiopathic SAH, compared with 2% of patients with aneurysmal SAH. Sabatino et al.32 found BVR variant B to be more prevalent in idiopathic patients compared with controls, with BVR draining anteriorly into the uncal vein and posteriorly into the Galenic system. The greater incidence of variant venous anatomy has led to the hypothesis that the etiology of pSAH might be stretching and tearing of the BVR or its tributaries. Our patient had primitive variant (type C) on the right and type B on the left. The patient described by Rahme et al.,16 who had a rebleed after many years, had bilateral type C variant. Unfortunately, the other reported cases of pSAH rebleeds do not mention the venous anatomy or variations in their patients. Some authors have not found an association between variant venous drainage and pSAH.33 Although anomalous venous drainage may be more common in patients with pSAH, its role in the counseling of patients
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with pSAH regarding risk of rebleed is of uncertain significance. These variants in venous anatomy are much more common than the reported incidence of recurrent pSAH, and patients with pSAH frequently have bilateral normal venous drainage.28,32,34 Given the extreme rarity, Rahme et al.16 also postulated pure randomness being the explanation of recurrent pSAH. pSAH has been shown to have an annual incidence of 0.5 per 100,000 in population-based study. With an 80-year life expectancy, the life-time risk of recurrent pSAH would be 79 per billion.16 Given only the few reported cases in literature, this is not totally inconceivable. On the basis of their case and review, Reynolds et al.17 advocated that patients with pSAH should be counseled as to the low, but real, possibility of recurrence. Of all the cases reported so far, clinical follow-up is unfortunately available only in Reynolds et al.,17 where the patient at 1 year after rebleed had complete resolution of symptoms and had no neurologic deficits. Two cases died soon after the rebleed, and 2 mention the patient being discharged home with no neurologic deficits. Our patient has a 2-year followup after the rebleed and continues to be at neurologic baseline. Although there may be a remote possibility of recurrence of pSAH, angiographic imaging remains negative for a vascular etiology, and the outcome may not be adversely affected after the rebleed. Long-term outcomes after recurrent pSAH are not available and need further studies. Although there is a possibility that some cases of recurrent pSAH may have gone unreported, given the current evidence, it may not warrant a change in the patient’s lifestyle. REFERENCES 1. van Gijn J, van Dongen KJ, Vermeulen M, Hijdra A. Perimesencephalic hemorrhage: a nonaneurysmal and benign form of subarachnoid hemorrhage. Neurology. 1985;35:493-497.
ADVISING PATIENTS OF POSSIBLE RECURRENCE OF PSAH
4. Alen JF, Lagares A, Lobato RD, Gomez PA, Rivas JJ, Ramos A. Comparison between perimesencephalic nonaneurysmal subarachnoid hemorrhage and subarachnoid hemorrhage caused by posterior circulation aneurysms. J Neurosurg. 2003;98:529-535.
19. Flaherty ML, Haverbusch M, Kissela B, Kleindorfer D, Schneider A, Sekar P, et al. Perimesencephalic subarachnoid hemorrhage: incidence, risk factors, and outcome. J Stroke Cerebrovasc Dis. 2005;14:267-271.
5. Topcuoglu MA, Ogilvy CS, Carter BS, Buonanno FS, Koroshetz WJ, Singhal AB. Subarachnoid hemorrhage without evident cause on initial angiography studies: diagnostic yield of subsequent angiography and other neuroimaging tests. J Neurosurg. 2003;98:1235-1240.
20. Kleinpeter G, Lehr S. Characterization of risk factor differences in perimesencephalic subarachnoid hemorrhage. Minim Invasive Neurosurg. 2003;46:142-148.
6. Urbach H, Zentner J, Solymosi L. The need for repeat angiography in subarachnoid haemorrhage. Neuroradiology. 1998;40:6-10. 7. Kalra VB, Wu X, Matouk CC, Malhotra A. Use of follow-up imaging in isolated perimesencephalic subarachnoid hemorrhage: a meta-analysis. Stroke. 2015;46:401-406. 8. Rinkel GJ, Wijdicks EF, Vermeulen M, Ramos LM, Tanghe HL, Hasan D, et al. Nonaneurysmal perimesencephalic subarachnoid hemorrhage: CT and MR patterns that differ from aneurysmal rupture. AJNR Am J Neuroradiol. 1991;12:829-834. 9. Rinkel GJ, Wijdicks EF, Vermeulen M, Hasan D, Brouwers PJ, van Gijn J. The clinical course of perimesencephalic nonaneurysmal subarachnoid hemorrhage. Ann Neurol. 1991;29:463-468. 10. Sprenker C, Patel J, Camporesi E, Vasan R, Van Loveren H, Chen H, et al. Medical and neurologic complications of the current management strategy of angiographically negative nontraumatic subarachnoid hemorrhage patients. J Crit Care. 2015; 30:216.e7-216.e11. 11. Greebe P, Rinkel GJ. Life expectancy after perimesencephalic subarachnoid hemorrhage. Stroke. 2007;38:1222-1224. 12. Schwartz TH, Solomon RA. Perimesencephalic nonaneurysmal subarachnoid hemorrhage: review of the literature. Neurosurgery. 1996;39:433-440 [discussion: 440]. 13. van Gijn J, Kerr RS, Rinkel GJ. Subarachnoid haemorrhage. Lancet. 2007;369:306-318. 14. Ildan F, Tuna M, Erman T, Gocer AI, Cetinalp E. Prognosis and prognostic factors in nonaneurysmal perimesencephalic hemorrhage: a follow-up study in 29 patients. Surg Neurol. 2002; 57:160-165 [discussion: 65-66]. 15. Marquardt G, Niebauer T, Schick U, Lorenz R. Long term follow up after perimesencephalic subarachnoid haemorrhage. J Neurol Neurosurg Psychiatry. 2000;69:127-130. 16. Rahme R, Vyas NA. Recurrent perimesencephalic subarachnoid hemorrhage after 12 years: missed diagnosis, vulnerable anatomy, or random events? World Neurosurg. 2015;84:2076.e7-2076.e11.
2. Rinkel GJ, Wijdicks EF, Hasan D, Kienstra GE, Franke CL, Hageman LM, et al. Outcome in patients with subarachnoid haemorrhage and negative angiography according to pattern of haemorrhage on computed tomography. Lancet. 1991;338:964-968.
17. Reynolds MR, Blackburn SL, Zipfel GJ. Recurrent idiopathic perimesencephalic subarachnoid hemorrhage. J Neurosurg. 2011;115:612-616.
3. Van Calenbergh F, Plets C, Goffin J, Velghe L. Nonaneurysmal subarachnoid hemorrhage: prevalence of perimesencephalic hemorrhage in a consecutive series. Surg Neurol. 1993;39:320-323.
18. van der Worp HB, Fonville S, Ramos LM, Rinkel GJ. Recurrent perimesencephalic subarachnoid hemorrhage during antithrombotic therapy. Neurocrit Care. 2009;10:209-212.
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21. Schievink WI, Wijdicks EF. Origin of pretruncal nonaneurysmal subarachnoid hemorrhage: ruptured vein, perforating artery, or intramural hematoma? Mayo Clin Proc. 2000;75:1169-1173. 22. Alexander MS, Dias PS, Uttley D. Spontaneous subarachnoid hemorrhage and negative cerebral panangiography. Review of 140 cases. J Neurosurg. 1986;64:537-542. 23. Cioffi F, Pasqualin A, Cavazzani P, Da Pian R. Subarachnoid haemorrhage of unknown origin: clinical and tomographical aspects. Acta Neurochir (Wien). 1989;97:31-39. 24. Heit JJ, Pastena GT, Nogueira RG, Yoo AJ, LeslieMazwi TM, Hirsch JA, et al. Cerebral angiography for evaluation of patients with ct angiogramnegative subarachnoid hemorrhage: an 11-year experience. AJNR Am J Neuroradiol. 2016;37:297-304. 25. Wu X, Kalra VB, Forman HP, Matouk CC, Mongelluzzo G, Liu R, et al. Regarding “Cerebral Angiography for Evaluation of Patients with CT Angiogram-Negative Subarachnoid Hemorrhage: An 11-Year Experience”. AJNR Am J Neuroradiol. 2016;37:E52-E53. 26. Ruigrok YM, Rinkel GJ, Buskens E, Velthuis BK, van Gijn J. Perimesencephalic hemorrhage and CT angiography: a decision analysis. Stroke. 2000;31: 2976-2983. 27. Maslehaty H, Petridis AK, Barth H, Mehdorn HM. Diagnostic value of magnetic resonance imaging in perimesencephalic and nonperimesencephalic subarachnoid hemorrhage of unknown origin. J Neurosurg. 2011;114:1003-1007. 28. Song JH, Yeon JY, Kim KH, Jeon P, Kim JS, Hong SC. Angiographic analysis of venous drainage and a variant basal vein of Rosenthal in spontaneous idiopathic subarachnoid hemorrhage. J Clin Neurosci. 2010;17:1386-1390. 29. van der Schaaf IC, Velthuis BK, Gouw A, Rinkel GJ. Venous drainage in perimesencephalic hemorrhage. Stroke. 2004;35:1614-1618. 30. Watanabe A, Hirano K, Kamada M, Imamura K, Ishii N, Sekihara Y, et al. Perimesencephalic nonaneurysmal subarachnoid haemorrhage and variations in the veins. Neuroradiology. 2002;44: 319-325. 31. Yamakawa H, Ohe N, Yano H, Yoshimura S, Iwama T. Venous drainage patterns in perimesencephalic nonaneurysmal subarachnoid hemorrhage. Clin Neurol Neurosurg. 2008;110:587-591. 32. Sabatino G, Della Pepa GM, Scerrati A, Maira G, Rollo M, Albanese A, et al. Anatomical variants of the basal vein of Rosenthal: prevalence in idiopathic subarachnoid hemorrhage. Acta Neurochir (Wien). 2014;156:45-51.
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CASE REPORT AJAY MALHOTRA ET AL.
33. Daenekindt T, Wilms G, Thijs V, Demaerel P, Van Calenbergh F. Variants of the basal vein of Rosenthal and perimesencephalic nonaneurysmal hemorrhage. Surg Neurol. 2008;69:526-529 [discussion: 529]. 34. Alen JF, Lagares A, Campollo J, Ballenilla F, Kaen A, Nunez AP, et al. Idiopathic subarachnoid hemorrhage and venous drainage: are they
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related? Neurosurgery. 2008;63:1106-1111 [discussion: 11-12].
Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
WORLD NEUROSURGERY 94: 580.e17-580.e22, OCTOBER 2016
Received 23 June 2016; accepted 30 July 2016 Citation: World Neurosurg. (2016) 94:580.e17-580.e22. http://dx.doi.org/10.1016/j.wneu.2016.07.112 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2016 Elsevier Inc. All rights reserved.
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Should Patients Be Counseled About Possible Recurrence of Perimesencephalic Subarachnoid Hemorrhage? Ajay Malhotra1, Xiao Wu1, Riddhi Borse3, Charles C. Matouk1,2, Ketan Bulsara2
Key words Angiography - CTA - MRI - Perimesencephalic subarachnoid hemorrhage - Recurrence -
Abbreviations and Acronyms BVR: Basal vein of Rosenthal CT: Computed tomography CTA: Computed tomography angiography MRI: Magnetic resonance imaging pSAH: Perimesencephalic subarachnoid hemorrhage SAH: Subarachnoid hemorrhage
- BACKGROUND:
Isolated perimesencephalic subarachnoid hemorrhage (pSAH) is a distinct subtype of subarachnoid hemorrhage (SAH) seen in 5% of patients with SAH, with a relatively benign natural course and good outcome compared with diffuse, aneurysmal SAH. Traditionally, the prognosis of pSAH is believed to be excellent compared with aneurysmal SAH, with no risk of recurrent hemorrhage after long-term follow-up. We describe a case of pSAH in which the patient had a recurrent perimesencephalic bleed 8 years after the initial episode. There are 5 previous reports of recurrent pSAH in existing literature.
- CASE
To whom correspondence should be addressed: Ajay Malhotra, M.D. [E-mail: [email protected]]
REPORT: A patient in sixth decade of life with no history of trauma presented in 2006 with acute-onset, severe headache, and “off-balance” gait. The patient was diagnosed with pSAH on the basis of computed tomography angiography and digital subtraction angiography. The patient was discharged, and follow-up computed tomography angiography over the next 2 years revealed no underlying vascular anomaly. The patient presented in 2014 with sudden onset of headache, similar to the previous episode with no new neurologic signs. Patient had repeated imaging over the succeeding 2 years, which were all negative for new blood or source of subarachnoid bleed.
Citation: World Neurosurg. (2016) 94:580.e17-580.e22. http://dx.doi.org/10.1016/j.wneu.2016.07.112
- REVIEW
From the Departments of 1Radiology and Biomedical Imaging and 2Neurosurgery, Yale School of Medicine, New Haven, Connecticut, USA; and 3Topiwala National Medical College, Mumbai, India
Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2016 Elsevier Inc. All rights reserved.
AND DISCUSSION: There are only a couple of case reports of recurrent pSAH, some of which were defined questionably. We review the reported cases and discuss the imaging results and outcome. Considering the rarity, low risks of complications, as well as the good outcome even after recurrence, we do not recommend routinely counseling patients about possibility of recurrence of pSAH.
INTRODUCTION Isolated perimesencephalic subarachnoid hemorrhage (pSAH) is a distinct subtype of subarachnoid hemorrhage (SAH) seen in 5% of patients with SAH, with a relatively benign natural course and good outcome compared with diffuse, aneurysmal SAH.1-3 Initial angiographic imaging is essential in pSAH to detect aneurysms, because 10% of posterior circulation aneurysms can present with a pSAH pattern.4-6 Initial computed tomography angiography (CTA) has been shown to be reliable in the exclusion of aneurysms in patients meeting the strict imaging and clinical criteria of pSAH, with limited utility of repeat follow-up imaging.7,8 Hydrocephalus and symptomatic vasospasm are much less common with pSAH relative to aneurysmal SAH.9 Other reported complications, including acute seizures, hyponatremia, and cardiac complications including arrhythmias, are also uncommon.10 Traditionally, the prognosis
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of pSAH is believed to be excellent compared with aneurysmal SAH, with no risk of recurrent hemorrhage after longterm follow-up.2,11-13 We describe a case of pSAH in which patient had a recurrent perimesencephalic bleed 8 years after the initial episode. There are 5 previous reports of recurrent pSAH in existing literature, 4 of which occurred in a relatively short time frame after the initial bleed (5 days to 31 months) and the most recent report a recurrent bleed that occurred 12 years after the initial episode.14-18 We review these cases to assess the risk factors linked with the recurrence of pSAH and the outcome of recurrent bleed in the reported cases. CASE REPORT A patient in sixth decade of life with no history of trauma presented in 2006 with
acute-onset, severe headache and “offbalance” gait. The patient had a history of hypertension and diabetes on treatment. On clinical examination, the patient had mild anisocoria but reactive pupils. No other focal neurologic signs were elicited. Initial noncontrast computed tomography (CT) showed hyperdense blood in the prepontine and interpeduncular cistern extending to the left quadrigeminal cistern with a tiny amount layering in the fourth ventricle (Figures 1 and 2). The hemorrhagic component in the inferior third and fourth ventricles was probably attributable to sedimentation phenomenon because the greatest density of blood was within the interpeduncular cistern. CTA and 6 vessel-selective injections digital subtraction angiography performed at presentation were negative for any
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2016.07.112
CASE REPORT AJAY MALHOTRA ET AL.
ADVISING PATIENTS OF POSSIBLE RECURRENCE OF PSAH
Figure 1. Initial noncontrast computed tomography of the head (A and B) shows hyperdense blood in the prepontine and ambient cistern. (C) Computed tomography angiography does
vascular source of the subarachnoid blood (Figures 3 and 4). Magnetic resonance imaging (MRI) of the brain and cervical spine performed at day 3 did not reveal the source of SAH, either. The patient was discharged home after an uneventful recovery and neurologic function at baseline. Follow-up CTAs during the next 2 years revealed no underlying vascular anomaly. The patient presented in 2014 with sudden-onset headache (6/10), similar to the previous episode with no new neurologic symptoms. Since 2006, the patient had developed coronary artery disease and had myocardial infarction
not show any intracranial aneurysm or vascular lesion. A prominent left posterior communicating artery is seen with hypoplastic P1 segment.
status postangioplasty and stenting, on aspirin 81 mg. Noncontrast CT showed subarachnoid blood confined anterior to the brainstem, and cerebrospinal fluid analysis showed blood in 4/4 tubes (Figure 5). CTA, MRI/magnetic resonance angiography, and digital subtraction angiography at presentation were all negative for vascular source of SAH. The patient had a repeat CTA at 1 week, and 2 CTAs and 1 MRI during the next 2 years, all of which were negative for new blood or source of subarachnoid bleed. At 2-year followup, the patient remains neurologically at baseline and has not had any
Figure 2. Brain magnetic resonance imaging performed on Day 3. (A) Axial fluid-attenuated inversion recovery and (B) T1-weighted images show hyperintense signal in the perimesencephalic cisterns corresponding to the previously
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recurrence of further episodes of similar headache/SAH. DISCUSSION There are only a couple of case reports of recurrent pSAH. Schwartz and Solomon12 reviewed the literature in 1996 and found no cases of rebleeding in 169 patients after a follow-up of 8e51 months. The first reported case of recurrent pSAH was in 2000 by Marquardt et al.,15 where the recurrent bleed occurred 31 months after the initial episode. A summary table of the 5 previously reported studies is presented in Table 1.14-18
seen hyperdense blood. (C) Magnetic resonance imaging of the cervical spine, sagittal gradient echo image shows blood in the prepontine cistern, but no underlying structural abnormality was identified.
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Figure 3. Cerebral conventional angiogram. (A) Right internal carotid artery injection, right anterior oblique (RAO) projection. (B) Left internal carotid artery injection, RAO projection. (C) Right vertebral artery injection, frontal projection. (D) Left vertebral artery injection, frontal projection. No vascular etiology for subarachnoid hemorrhage was identified.
In 2009 Reynolds et al.17 questioned the 3 previously reported cases of recurrent pSAH and added a case of definite recurrent pSAH to 1 “probable” and 2 “possible” reported cases. They raised
concern for confirmation of pSAH on the initial bleed in case of the case reported by Marquardt et al.15 The cases reported by Ildan et al.14 and van der Worp et al.18 died after the recurrent bleed and did
Figure 4. Images (A) and (B) show the venous phases of right internal carotid artery injection and left internal carotid artery injection injections. Basal vein of Rosenthal (BVR) variant type C is shown on the right (arrow in B) with BVR draining into the transverse sinus and BVR type B on the left (arrow in A) with BVR draining anteriorly into the uncal vein and posteriorly into the Galenic system.
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not undergo any repeat vascular imaging or autopsy. Ildan et al.14 reported that the repeat CT scan of the patient with rebleed suggested aneurysmal SAH, which raises questions about the validity of these cases being true perimesencephalic rebleeds. In addition to our case, we found only 1 additional definite case in which both SAH episodes were true, documented cases of recurrent, idiopathic pSAH many years after the initial bleed (8 and 12 years, respectively).16 Multiple imaging studies performed in our patient did not reveal a vascular etiology for the pSAH. Similarly, Rahme and Vyas16 also could not find an underlying structural lesion despite head CTA, cerebral and cervical spinal angiography, and MRI of the brain and spine. They reported a neurologically favorable outcome, with the patient discharged home, but did not have longer follow-up. We present a 2-year follow-up after the recurrent bleed, with multiple imaging studies remaining negative and patient remaining at neurologic baseline. Several risk factors of pSAH have been suggested, such as smoking, female sex, and younger age, with hypertension as the only risk factor consistently present in different studies.19,20 Although the etiology of pSAH remains elusive, multiple hypothesis have been suggested, including venous bleed caused by tear in the basal vein of Rosenthal (BVR) or its tributaries, unrecognized vertebrobasilar dissections, rupture of arterial perforators, or radiographically occult aneurysms or vascular malformations.8,21-23 The long interval period of many years in these 2 cases excludes the possibility of deficient hemostasis being the cause of bleed. The first 4 reported cases of rebleed occurred after shorter intervals (5 days to 21 months), and inadequate hemostasis after the first bleeding episode has been invoked as a possible explanation in those cases.17,18 Van der Worp et al.18 reported a case of recurrent pSAH 3 days after starting treatment with intravenous heparin for acute coronary syndrome, and they postulated that anticoagulant therapy may have resulted in dissolution of clot in a ruptured vein at the tentorial edge, thereby resulting in recurrent hemorrhage. Unfortunately, the patient died the same day due to ventricular
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anterior to the medulla. (A, B) Axial CT and (C) Sagittal reformats.
Figure 5. Noncontrast computed tomography shows hyperdense blood in the prepontine cistern extending inferiorly
fibrillation, and no follow-up imaging could be obtained. There was no antithrombotic use in the other reported case by Rahme et al.,16 where the rebleed happened after many years. Other vascular causes of pSAH that have been hypothesized are ruptured capillary telangiectasias or perforating arteries, and unrecognized vertebrobasilar dissections, aneurysms, or vascular malformations.16 Repeat imaging was not performed in 2 of the pSAH rebleed cases, and thus, a small vascular lesion causing the bleed theoretically could have been missed.14,18 However, recurrent bleed happening after so many years and the fact that repeated imaging did not reveal any vascular cause in both cases where rebleed happened after many years make these causes unlikely.
Although the yield of repeated imaging in patients with pSAH is questionable, even recent literature advocates follow-up imaging.24,25 Catheter angiography has been postulated to be better than CTA and often is used in the evaluation for pSAH. Its routine use, however, remains questionable.5,26 The utility of MRI also has been questioned, with relatively low diagnostic yield.27 Although no definite precipitating cause was identified in the case by Reynolds et al.,17 the patient had engaged in exertional activity before both events. None of the other reported cases had a similar history. Song et al.28 found physical actions, including breath holding during coughing, shouting, and ejaculation, in 30% instances of nonaneurysmal SAH in their series,
Table 1. Summary of Previously Reported Cases Study
Time to Postulated Recurrence Antithrombotics Risk Factor
Outcome
Rahme and Vyas, 201516
12 years
No antithrombotics
Primitive venous drainage
Discharged home
Reynolds et al., 201117
5 months
Aspirin 81 mg
Exertional activity
Discharged with no neurologic deficits; complete resolution at 1 year
Van der Worp et al., 200918
5 days
Antithrombotic
Ildan et al., 200214
Early rebleed
Marquardt et al., 31 months 200015
Died Died after rebleed Discharged without neurologic deficits
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leading them to reinforce the hypothesis that intracranial venous congestion caused by straining in patients with anomalous venous drainage might tear a vein fixed to a dural sinus. Primitive variants of the venous anatomy, with the BVR draining directly into the dural sinuses rather than into the Vein of Galen, have been found to have a greater prevalence in patients with pSAH.28-31 Song et al.28 found bilateral primitive venous drainage (type C) in 13% of patients with idiopathic SAH, compared with 2% of patients with aneurysmal SAH. Sabatino et al.32 found BVR variant B to be more prevalent in idiopathic patients compared with controls, with BVR draining anteriorly into the uncal vein and posteriorly into the Galenic system. The greater incidence of variant venous anatomy has led to the hypothesis that the etiology of pSAH might be stretching and tearing of the BVR or its tributaries. Our patient had primitive variant (type C) on the right and type B on the left. The patient described by Rahme et al.,16 who had a rebleed after many years, had bilateral type C variant. Unfortunately, the other reported cases of pSAH rebleeds do not mention the venous anatomy or variations in their patients. Some authors have not found an association between variant venous drainage and pSAH.33 Although anomalous venous drainage may be more common in patients with pSAH, its role in the counseling of patients
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with pSAH regarding risk of rebleed is of uncertain significance. These variants in venous anatomy are much more common than the reported incidence of recurrent pSAH, and patients with pSAH frequently have bilateral normal venous drainage.28,32,34 Given the extreme rarity, Rahme et al.16 also postulated pure randomness being the explanation of recurrent pSAH. pSAH has been shown to have an annual incidence of 0.5 per 100,000 in population-based study. With an 80-year life expectancy, the life-time risk of recurrent pSAH would be 79 per billion.16 Given only the few reported cases in literature, this is not totally inconceivable. On the basis of their case and review, Reynolds et al.17 advocated that patients with pSAH should be counseled as to the low, but real, possibility of recurrence. Of all the cases reported so far, clinical follow-up is unfortunately available only in Reynolds et al.,17 where the patient at 1 year after rebleed had complete resolution of symptoms and had no neurologic deficits. Two cases died soon after the rebleed, and 2 mention the patient being discharged home with no neurologic deficits. Our patient has a 2-year followup after the rebleed and continues to be at neurologic baseline. Although there may be a remote possibility of recurrence of pSAH, angiographic imaging remains negative for a vascular etiology, and the outcome may not be adversely affected after the rebleed. Long-term outcomes after recurrent pSAH are not available and need further studies. Although there is a possibility that some cases of recurrent pSAH may have gone unreported, given the current evidence, it may not warrant a change in the patient’s lifestyle. REFERENCES 1. van Gijn J, van Dongen KJ, Vermeulen M, Hijdra A. Perimesencephalic hemorrhage: a nonaneurysmal and benign form of subarachnoid hemorrhage. Neurology. 1985;35:493-497.
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4. Alen JF, Lagares A, Lobato RD, Gomez PA, Rivas JJ, Ramos A. Comparison between perimesencephalic nonaneurysmal subarachnoid hemorrhage and subarachnoid hemorrhage caused by posterior circulation aneurysms. J Neurosurg. 2003;98:529-535.
19. Flaherty ML, Haverbusch M, Kissela B, Kleindorfer D, Schneider A, Sekar P, et al. Perimesencephalic subarachnoid hemorrhage: incidence, risk factors, and outcome. J Stroke Cerebrovasc Dis. 2005;14:267-271.
5. Topcuoglu MA, Ogilvy CS, Carter BS, Buonanno FS, Koroshetz WJ, Singhal AB. Subarachnoid hemorrhage without evident cause on initial angiography studies: diagnostic yield of subsequent angiography and other neuroimaging tests. J Neurosurg. 2003;98:1235-1240.
20. Kleinpeter G, Lehr S. Characterization of risk factor differences in perimesencephalic subarachnoid hemorrhage. Minim Invasive Neurosurg. 2003;46:142-148.
6. Urbach H, Zentner J, Solymosi L. The need for repeat angiography in subarachnoid haemorrhage. Neuroradiology. 1998;40:6-10. 7. Kalra VB, Wu X, Matouk CC, Malhotra A. Use of follow-up imaging in isolated perimesencephalic subarachnoid hemorrhage: a meta-analysis. Stroke. 2015;46:401-406. 8. Rinkel GJ, Wijdicks EF, Vermeulen M, Ramos LM, Tanghe HL, Hasan D, et al. Nonaneurysmal perimesencephalic subarachnoid hemorrhage: CT and MR patterns that differ from aneurysmal rupture. AJNR Am J Neuroradiol. 1991;12:829-834. 9. Rinkel GJ, Wijdicks EF, Vermeulen M, Hasan D, Brouwers PJ, van Gijn J. The clinical course of perimesencephalic nonaneurysmal subarachnoid hemorrhage. Ann Neurol. 1991;29:463-468. 10. Sprenker C, Patel J, Camporesi E, Vasan R, Van Loveren H, Chen H, et al. Medical and neurologic complications of the current management strategy of angiographically negative nontraumatic subarachnoid hemorrhage patients. J Crit Care. 2015; 30:216.e7-216.e11. 11. Greebe P, Rinkel GJ. Life expectancy after perimesencephalic subarachnoid hemorrhage. Stroke. 2007;38:1222-1224. 12. Schwartz TH, Solomon RA. Perimesencephalic nonaneurysmal subarachnoid hemorrhage: review of the literature. Neurosurgery. 1996;39:433-440 [discussion: 440]. 13. van Gijn J, Kerr RS, Rinkel GJ. Subarachnoid haemorrhage. Lancet. 2007;369:306-318. 14. Ildan F, Tuna M, Erman T, Gocer AI, Cetinalp E. Prognosis and prognostic factors in nonaneurysmal perimesencephalic hemorrhage: a follow-up study in 29 patients. Surg Neurol. 2002; 57:160-165 [discussion: 65-66]. 15. Marquardt G, Niebauer T, Schick U, Lorenz R. Long term follow up after perimesencephalic subarachnoid haemorrhage. J Neurol Neurosurg Psychiatry. 2000;69:127-130. 16. Rahme R, Vyas NA. Recurrent perimesencephalic subarachnoid hemorrhage after 12 years: missed diagnosis, vulnerable anatomy, or random events? World Neurosurg. 2015;84:2076.e7-2076.e11.
2. Rinkel GJ, Wijdicks EF, Hasan D, Kienstra GE, Franke CL, Hageman LM, et al. Outcome in patients with subarachnoid haemorrhage and negative angiography according to pattern of haemorrhage on computed tomography. Lancet. 1991;338:964-968.
17. Reynolds MR, Blackburn SL, Zipfel GJ. Recurrent idiopathic perimesencephalic subarachnoid hemorrhage. J Neurosurg. 2011;115:612-616.
3. Van Calenbergh F, Plets C, Goffin J, Velghe L. Nonaneurysmal subarachnoid hemorrhage: prevalence of perimesencephalic hemorrhage in a consecutive series. Surg Neurol. 1993;39:320-323.
18. van der Worp HB, Fonville S, Ramos LM, Rinkel GJ. Recurrent perimesencephalic subarachnoid hemorrhage during antithrombotic therapy. Neurocrit Care. 2009;10:209-212.
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21. Schievink WI, Wijdicks EF. Origin of pretruncal nonaneurysmal subarachnoid hemorrhage: ruptured vein, perforating artery, or intramural hematoma? Mayo Clin Proc. 2000;75:1169-1173. 22. Alexander MS, Dias PS, Uttley D. Spontaneous subarachnoid hemorrhage and negative cerebral panangiography. Review of 140 cases. J Neurosurg. 1986;64:537-542. 23. Cioffi F, Pasqualin A, Cavazzani P, Da Pian R. Subarachnoid haemorrhage of unknown origin: clinical and tomographical aspects. Acta Neurochir (Wien). 1989;97:31-39. 24. Heit JJ, Pastena GT, Nogueira RG, Yoo AJ, LeslieMazwi TM, Hirsch JA, et al. Cerebral angiography for evaluation of patients with ct angiogramnegative subarachnoid hemorrhage: an 11-year experience. AJNR Am J Neuroradiol. 2016;37:297-304. 25. Wu X, Kalra VB, Forman HP, Matouk CC, Mongelluzzo G, Liu R, et al. Regarding “Cerebral Angiography for Evaluation of Patients with CT Angiogram-Negative Subarachnoid Hemorrhage: An 11-Year Experience”. AJNR Am J Neuroradiol. 2016;37:E52-E53. 26. Ruigrok YM, Rinkel GJ, Buskens E, Velthuis BK, van Gijn J. Perimesencephalic hemorrhage and CT angiography: a decision analysis. Stroke. 2000;31: 2976-2983. 27. Maslehaty H, Petridis AK, Barth H, Mehdorn HM. Diagnostic value of magnetic resonance imaging in perimesencephalic and nonperimesencephalic subarachnoid hemorrhage of unknown origin. J Neurosurg. 2011;114:1003-1007. 28. Song JH, Yeon JY, Kim KH, Jeon P, Kim JS, Hong SC. Angiographic analysis of venous drainage and a variant basal vein of Rosenthal in spontaneous idiopathic subarachnoid hemorrhage. J Clin Neurosci. 2010;17:1386-1390. 29. van der Schaaf IC, Velthuis BK, Gouw A, Rinkel GJ. Venous drainage in perimesencephalic hemorrhage. Stroke. 2004;35:1614-1618. 30. Watanabe A, Hirano K, Kamada M, Imamura K, Ishii N, Sekihara Y, et al. Perimesencephalic nonaneurysmal subarachnoid haemorrhage and variations in the veins. Neuroradiology. 2002;44: 319-325. 31. Yamakawa H, Ohe N, Yano H, Yoshimura S, Iwama T. Venous drainage patterns in perimesencephalic nonaneurysmal subarachnoid hemorrhage. Clin Neurol Neurosurg. 2008;110:587-591. 32. Sabatino G, Della Pepa GM, Scerrati A, Maira G, Rollo M, Albanese A, et al. Anatomical variants of the basal vein of Rosenthal: prevalence in idiopathic subarachnoid hemorrhage. Acta Neurochir (Wien). 2014;156:45-51.
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33. Daenekindt T, Wilms G, Thijs V, Demaerel P, Van Calenbergh F. Variants of the basal vein of Rosenthal and perimesencephalic nonaneurysmal hemorrhage. Surg Neurol. 2008;69:526-529 [discussion: 529]. 34. Alen JF, Lagares A, Campollo J, Ballenilla F, Kaen A, Nunez AP, et al. Idiopathic subarachnoid hemorrhage and venous drainage: are they
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related? Neurosurgery. 2008;63:1106-1111 [discussion: 11-12].
Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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Received 23 June 2016; accepted 30 July 2016 Citation: World Neurosurg. (2016) 94:580.e17-580.e22. http://dx.doi.org/10.1016/j.wneu.2016.07.112 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2016 Elsevier Inc. All rights reserved.
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