Skip to main content

Advertisement

SpringerLink
Log in

Subarachnoid hemorrhage and negative angiography: clinical course and long-term follow-up

  • Original Article
  • Published:
Neurosurgical Review Aims and scope Submit manuscript

Abstract

The aim of this study was to investigate the long-term natural history of nontraumatic angiogram-negative subarachnoid hemorrhage with typical pretruncal (P-SAH) and diffuse (D-SAH) pattern of hemorrhage. A retrospective review of 102 patients who experienced angiographically negative SAH at our institution was undertaken (11.6% of 882 spontaneous SAH). Follow-ups were obtained at 7.9 to 16 years. In the D-SAH group, 11 patients (13.9%) out of 79 had an aneurysm, and four (5.1%) had rebleeding episodes. In the P-SAH group, the second angiography was negative in all of the 23 cases, and no rebleeding episodes were recorded. The long-term follow-up confirms that P-SAH is a benign disease. A second angiography could not be necessary. D-SAH is probably due to an aneurysm that thrombose early after the bleeding. At short-term follow-up, the sack could frequently recanalize and rebleed, whereas a late follow-up shows that rebleeding is very rare.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Alén JF, Lagares A, Lobato RD, Gómez PA, Rivas JJ, Ramos A (2003) Comparison between perimesencephalic nonaneurysmal subarachnoid hemorrhage and subarachnoid hemorrhage caused by posterior circulation aneurysms. J Neurosurg 98:529–535

    Article  PubMed  Google Scholar 

  2. Alexander MS, Dias PS, Uttley D (1986) Spontaneous subarachnoid hemorrhage and negative cerebral panangiography. Review of 140 cases. J Neurosurg 64:537–542

    Article  PubMed  CAS  Google Scholar 

  3. Bradac GB, Bergui M, Ferrio M, Fontanella M, Stura G (1997) False-negative angiograms in subarachnoid haemorrhage due to intracranial aneurysms. Neuroradiology 39:772–776

    Article  PubMed  CAS  Google Scholar 

  4. Cioffi F, Pasqualin A, Cavazzani P, Da Pian R (1989) Subarachnoid haemorrhage of unknown origin: clinical and tomographical aspects. Acta Neurochir 97:31–39

    Article  CAS  Google Scholar 

  5. Cossandi C, Griva F, Fontanella M, Zullo N, Bergui M, Bradac GB, Pagni CA (2000) Calloso-marginal artery aneurysm missed by three angiographic studies. Acta Neurochir 142:1315–1316

    Article  CAS  Google Scholar 

  6. Duong H, Melancon D, Tampieri D, Ethier R (1996) The negative angiogram in subarachnoid haemorrhage. Neuroradiology 38:15–19

    Article  PubMed  CAS  Google Scholar 

  7. Fisher CM, Kistler JP, Davis JM (1980) Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery 16:1–9

    Article  Google Scholar 

  8. Fontanella M, Perozzo P, Ursone R, Garbossa D, Bergui M (2003) Neuropsychological assessment after microsurgical cliping or endovascular treatment for anterior communicating artery aneurysm. Acta Neurochir 145:867–872

    Article  CAS  Google Scholar 

  9. Fontanella M, Valfrè W, Benech F, Carlino C, Garbossa D, Ferrio M, Perez R, Berardino M, Bradac GB, Ducati A (2008) Vasospasm after SAH due to aneurysm rupture of the anterior circle of Willis: value of TCD monitoring. Neurol Res 30:256–261

    Article  PubMed  Google Scholar 

  10. Forster DM, Steiner L, Hakanson S, Bergvall U (1978) The value of repeat pan-angiography in cases of unexplained subarachnoid haemorrhage. J Neurosurg 48:712–716

    Article  PubMed  CAS  Google Scholar 

  11. Gascón P, Ley TJ, Toltzis RJ, Bonow RO (1983) Spontaneous subarachnoid hemorrhage simulating acute transmural myocardial infarction. Am Heart J 105:511–513

    Article  PubMed  Google Scholar 

  12. Giombini S, Bruzzone MG, Pluchino F (1988) Subarachnoid hemorrhage of unexplained cause. Neurosurgery 22:313–316

    Article  PubMed  CAS  Google Scholar 

  13. Hui FK, Tumialán LM, Tanaka T, Cawley CM, Zhang YJ (2009) Clinical differences between angiographically negative, diffuse subarachnoid hemorrhage and perimesencephalic subarachnoid hemorrhage. Neurocrit Care 11:64–70

    Article  PubMed  Google Scholar 

  14. Hunt WE, Hess RM (1968) Surgical risk as related to time of intervention in the repair of intracranial aneurysms. J Neurosurg 28:14–20

    Article  PubMed  CAS  Google Scholar 

  15. Hurley TR, Balandrin J (1997) Perimesencephalic nonaneurysmal subarachnoid hemorrhage: review of the literature. Neurosurgery 40:885

    Article  PubMed  CAS  Google Scholar 

  16. Iwanaga H, Wakai S, Ochiai C, Narita J, Inoh S, Nagai M (1990) Ruptured cerebral aneurysm missed by initial angiographic study. Neurosurgery 27:45–51

    Article  PubMed  CAS  Google Scholar 

  17. Jafar JJ, Weiner HL (1993) Surgery for angiographically occult cerebral aneurysms. J Neurosurg 79:674–679

    Article  PubMed  CAS  Google Scholar 

  18. Jung JY, Kim YB, Lee JW, Huh SK, Lee KC (2006) Spontaneous subarachnoid haemorrhage with negative initial angiography: a review of 143 cases. J Clin Neurosci 13:1011–1017

    Article  PubMed  Google Scholar 

  19. Kitahara T, Ohwada T, Tokiwa K, Kurata A, Miyasaka Y, Yada K, Kan S (1993) Clinical study in patients with perimesenscephalic subarachnoid haemorrhage of unknown etiology. No Shinkei Geka 21:903–908

    PubMed  CAS  Google Scholar 

  20. Pinto AN, Ferro JM, Canhao P, Campos J (1993) How often is a perimesencephalic subarachnoid haemorrhage CT pattern caused by ruptured aneurysms? Acta Neurochir 124:79–81

    Article  CAS  Google Scholar 

  21. Rijnkel GJ, van Gijn J, Wijdicks EF (1993) Subarachnoid hemorrhage without detectable aneurysm. A review of the causes. Stroke 24:1403–1409

    Article  Google Scholar 

  22. Rijnkel GJ, Wijdicks EF, Vermeulen M, Hageman LM, Tans JT, van Gijn J (1990) Outcome in perimesencephalic (nonaneurysmal) subarachnoid hemorrhage: a follow-up study in 37 patients. Neurology 40:1130–1132

    Google Scholar 

  23. Rijnkel GJ, Wijdicks EF, Vermeulen M, Hasan D, Brouwers PJ, van Gijn J (1991) The clinical course of perimesencephalic nonaneurysmal subarachnoid hemorrhage. Ann Neurol 29:463–468

    Article  Google Scholar 

  24. Rijnkel GJ, Wijdicks EF, Vermeulen M, Ramos LM, Tanghe HL, Hasan D, Meiners LC, van Gijn J (1991) Nonaneurysmal perimesencephalic subarachnoid hemorrhage: CT and MR patterns that differ from aneurysmal rupture. AJNR Am J Neuroradiol 12:829–834

    Google Scholar 

  25. Ronkanien A, Hernesniemi J (1992) Subarachnoid haemorrhage of unknown aetiology. Acta Neurochir 119:29–34

    Article  Google Scholar 

  26. Rogg JM, Smeaton S, Doberstein C, Goldstein JH, Tung GA, Haas RA (1999) Assesment of the value of MR imaging for examining patients with angiographically negative subarachnoid hemorrhage. Am J Roentgenol 172:201–206

    CAS  Google Scholar 

  27. Schievnik WI, Wijdicks EF (1997) Pretruncal subarachnoid hemorrhage: an anatomically correct description of the perimesencephalic subarachnoid hemorrhage. Stroke 28:2572

    Google Scholar 

  28. Schievnik WI, Wijdicks EF, Piepgras DG, Nichols DA, Ebersold MJ (1994) Perimesencephalic subarachnoid hemorrhage. Additional perspectives from four cases. Stroke 25:1507–1511

    Article  Google Scholar 

  29. Schwartz TH, Mayer SA (2000) Quadrigeminal variant of perimesencephalic nonaneurysmal subarachnoid hemorrhage. Neurosurgery 46:584–588

    Article  PubMed  CAS  Google Scholar 

  30. Schwartz TH, Solomon RA (1996) Perimesencephalic nonaneurysmal subarachnoid hemorrhage: review of the literature. Neurosurgery 39:433–440

    PubMed  CAS  Google Scholar 

  31. Tatter SB, Crowell RM, Ogilvy CS (1995) Aneurysmal and microaneurysmal “angiogram-negative” subarachnoid hemorrhage. Neurosurgery 37:48–55

    Article  PubMed  CAS  Google Scholar 

  32. Topcuoglu MA, Ogilvy CS, Carter BS, Buonanno FS, Koroshetz WJ, Singhal AB (2003) Subarachnoid hemorrhage without evident cause on initial angiography studies: diagnostic yield of subsequent angiography and other neuroimaging tests. J Neurosurg 98:1235–1240

    Article  PubMed  Google Scholar 

  33. van der Worp HB, Fonville S, Ramos LM, Rinkel GJ (2009) Recurrent perimesencephalic subarachnoid hemorrhage during antitrombotic therapy. Neurocrit Care 10:209–212

    Article  PubMed  Google Scholar 

  34. Velthuis BK, Rinkel GJ, Ramos LM, Witkamp TD, van Leeuwen MS (1999) Perimesencephalic hemorrhage. Exclusion of vertebrobasilar aneurysms with CT angiography. Stroke 30:1103–1109

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Neurosurgery, Department of Neuroscience, University of Torino, Via Cherasco 15, 10126, Torino, Italy

    Marco Fontanella, Pier Paolo Panciani, Chiara Benevello, Diego Garbossa, Christian Carlino, Federico Griva & Alessandro Ducati

  2. Division of Neurology, Department of Neuroscience, University of Torino, Torino, Italy

    Innocenzo Rainero & Walter Valfrè

  3. Department of Neurosurgery, University Hospital Geneva, Geneva, Switzerland

    Bawarjan Schatlo

  4. Division of Neuroradiology, Department of Neuroscience, University of Torino, Torino, Italy

    Gianni Boris Bradac

Authors
  1. Marco Fontanella
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Innocenzo Rainero
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pier Paolo Panciani
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bawarjan Schatlo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chiara Benevello
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Diego Garbossa
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Christian Carlino
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Walter Valfrè
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Federico Griva
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Gianni Boris Bradac
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Alessandro Ducati
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marco Fontanella.

Additional information

Comments

Deanna Sasaki-Adams, Saint Louis, USA

The manuscript entitled, “Subarachnoid Hemorrhage and Negative Angiography: Clinical Course and Long-term Follow-up” submitted by Dr. Fontanella et al. seeks to evaluate radiographic and clinical characteristics that differentiate between diffuse and perimesencephalic angiographically negative subarachnoid hemorrhage. It has been customary in many institutions to perform two to three angiograms in these patients to confirm no aneurysmal origin of the subarachnoid hemorrhage. Fontanella et al. have demonstrated that a second angiogram may not be necessary in those patients whose initial CT scan shows blood limited to the area just anterior to the midbrain without significant extension into the interhemispheric fissures or ambient cisterns. In a retrospective review of 79 patients with angiogram negative for underlying aneurysm, 23 patients were defined as having a characteristic pattern in the perimesencephalic region as opposed to a more diffuse pattern of hemorrhage. None of those patients labeled with perimesencephalic hemorrhage alone were found to have a lesion upon repeat angiography, and all demonstrated a benign clinical course. The data suggest that a repeat arteriogram in a select group of patients may not be necessary. The present study supports what many neurosurgeons have found to be true anecdotally and will add to our armamentarium when dealing with these often challenging scenarios in an evidence-driven and cost-effective manner.

Giuseppe Lanzino, Emanuela Crobeddu, Rochester, MN, USA

Fontanella and coworkers retrospectively analyzed a consecutive series of patients with subarachnoid hemorrhage (SAH) and no evidence of aneurysm on first catheter angiography. Patients were followed for a mean of 10.6 years. Two groups are considered: patients with “classic” pretruncal SAH (23 patients) and those with a diffuse pattern suggestive of aneurysm rupture (72 patients). Patients underwent a “second look” angiography between day 11 and day 20 after SAH. In patients with diffuse SAH, the second angiogram revealed an aneurysm in nine out of 72 (12.5%), and four patients in this group suffered a rebleeding before a definitive diagnosis of the aneurysm. Angiography-negative SAH continues to be not an uncommon diagnosis among patients with nontraumatic SAH despite sophisticated and ever improving diagnostic imaging.

Patients with a classic pattern of pretruncal hemorrhage share other clinical characteristics, namely good clinical “appearance” on presentation, a relatively benign course (even though they can occasionally suffer from vasospasm and hydrocephalus), and a uniformly good outcome. We agree with the authors that in patients with a “classic” pattern a high-quality six-vessel angiogram suffices and no repeat imaging studies are necessary. Patients with a diffuse, “true” aneurysmal pattern continue to represent a challenge. It has been our experience that with modern 3D angiography capabilities, these patients are less common than a few decades ago. In these patients, careful search of an offending underlying vascular cause is imperative given the risk of rebleeding. We routinely perform a “second look” catheter angiography in this group. The timing of the repeat angiogram in this situation is controversial. However, this study suggests that another catheter angiography should probably be performed 1 week after presentation since the four rebleedings observed occurred between days 3 and 17.

We have noticed that more and more patients with angiography-negative SAH fall within a third category: the “pretruncal plus” pattern. In this category, the epicenter of the bleeding is still in the area of the interpeduncular cistern, but the subarachnoid blood extends beyond the confines considered “classic” for the pretruncal type such as the distal sylvian fissure and the distal two thirds of the interhemispheric fissure. We have noted (a finding corroborated by others) that often these patients are on antiplatelet or anticoagulation therapy. Therefore, it is conceiveable that in some of these cases, the bleeding originates from the same source which gives rise to the “classic” pretruncal pattern, but the blood burden may be increased by the pharmacological effects of the antiplatelet/anticoagulant treatment allowing for extension beyond the boundaries of the pretruncal type. In these patients, we perform a “second look” catheter angiography only selectively and often consider a noninvasive method instead. Future research will likely further characterize this specific subgroup.

One final word about the use of axial imaging studies such as MRI of the brain and cervical spine. These have been traditionally recommended to rule out possible, less common causes of SAH such as cavernous malformations or the sporadic tumor (usually ependymoma or schwannoma). For the past 9 years, we have been doing axial imaging of the brain and the cervical spine routinely in patients with angiography-negative SAH, but in accordance with Fontanella and coworkers’ findings, we have not found these studies useful. We now consider MRI of the brain and cervical spine only selectively in those patients with atypical features or when symptom onset clearly suggests a possible upper spinal origin of the bleed (i.e., sudden, severe pain starting in the spine, and then migrating upward).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fontanella, M., Rainero, I., Panciani, P.P. et al. Subarachnoid hemorrhage and negative angiography: clinical course and long-term follow-up. Neurosurg Rev 34, 477–484 (2011). https://doi.org/10.1007/s10143-011-0323-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10143-011-0323-8

Keywords

Search

Navigation