Letter to the Editor: Arteriovenous malformations and radiosurgery

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To The Editor: I read with interest the recent paper on the outcomes after stereotactic radiosurgery (SRS) for patients with unruptured intracranial arteriovenous malformations (AVMs)4 (Ding D, Yen CP, Xu Z, et al: Radiosurgery for patients with unruptured intracranial arteriovenous malformations. Clinical article. J Neurosurg 118: 958–966, May 2013).

This study provides useful information in the discussion of one of the most controversial topics in cerebral AVM management, which is, should patients with an unruptured AVM be observed or should they undergo treatment to eliminate the malformation and reduce the risk of future intracranial hemorrhages.19 As mentioned by the authors, a randomized trial of unruptured brain arteriovenous malformations (ARUBA) was funded by the National Institute of Neurological Disorders (U01 NS051483) and began enrolling patients in April 2007. This trial is designed to compare the risks of observation versus those of prophylactic intervention for patients diagnosed with unruptured intracranial AVM. Exclusion criteria for the ARUBA trial, in addition to prior bleeding, include age less than 18 years, prior AVM treatment, presence of multiple AVMs, and a modified Rankin Score (mRS) ≥ 2. The primary end points of the ARUBA trial are the combined risk of death or stroke and risk of clinical impairment, defined as an mRS ≥ 2. The ARUBA trial has been criticized for a number of reasons, including the intended follow-up period after randomization (planned, 5–10 years), which is considered insufficient for a disorder that is commonly diagnosed in patients with life expectancies of 30 years or more.2,11

Ding and colleagues from the University of Virginia report the outcomes of single-fraction SRS in a large cohort of patients (n = 444) with unruptured AVM (median clinical follow-up, 74 months).4 The mean AVM volume was 4.2 cm3; the median margin dose was 20 Gy. Of note, 122 patients (27.4%) underwent pre-SRS embolization and 20 patients (4.5%) had prior microsurgery. Overall, the authors reported a cumulative AVM obliteration rate of 62% after one or more SRS procedures. Clinical deterioration was noted in 30 patients (6.8%). The most frequent cause of neurologic decline was post-SRS bleeding. The authors concluded that SRS provided a reasonable benefit-to-risk ratio and recommended treatment for younger patients, patients with larger-volume AVMs, and patients with a higher radiosurgery-based AVM score (RBAS).13 We recently published the outcomes of 174 patients with unruptured AVM having SRS at our center from 1990 to 2005 using the same eligibility criteria and outcome measures as the ARUBA trial (median follow-up, 64 months).16 In our series, the obliteration rate after one or more procedures was 79%. Overall, the risk of hemorrhagic stroke or death was 10% at 5 years and 12% at 10 years. The risk of patients' having clinical impairment (mRS ≥ 2) was 8% at 5 years and 12% at 10 years. Larger AVM volume was associated with an increased risk of stroke resulting in death or clinical impairment after SRS. The 10-year risk of mRS ≥ 2 for patients with an RBAS ≤ 1.50 was 2% in comparison with 18% for patients with an RBAS > 1.50. Thus, like Ding et al., we found that SRS was a safe and effective option for patients with unruptured intracranial AVM, especially if they were younger, with many years of risk for AVM hemorrhage.

I was surprised to see the authors refer to the “Pittsburgh radiosurgery-based AVM score” throughout this paper. In contrast to the Spetzler-Martin grading system, which was designed to predict outcomes after AVM resection,18 the RBAS was developed by the Mayo Clinic in collaboration with the University of Pittsburgh over a period of 15 years as a method to specifically predict outcomes after AVM SRS.13,14 Since its publication in 2002, 5 years after I left the University of Pittsburgh and joined the Department of Neurological Surgery at the Mayo Clinic, the original and modified versions of the RBAS have been cited more than 175 times. This grading scale has been shown to be valid after not only Gamma Knife SRS,1 but also after LINAC-based and Cyber Knife procedures.3,17 To the best of my knowledge, only one publication erroneously referred to Pittsburgh as the origin of this grading scale in its abstract.20 In fact, the University of Pittsburgh group did not use this misnomer in its recent six-part opus on AVM radiosurgery published last year in the Journal of Neurosurgery,5–10 and Dr. Lunsford himself, in a commentary on an article by Pollock et al., has referred to it as “the Mayo Clinic's proposed AVM grading system.”15 Proper citation of appropriate references lies at the heart of intellectual exchange, as it allows scholars to give credit to other scholars for their hard work and their ideas. Also, proper citation provides a guide for readers who are interested in learning more about a topic. The history of the development and testing of the RBAS has recently been published.12

Disclosure

The author reports no conflict of interest.

References

  • 1

    Andrade-Souza YMZadeh GRamani MScora DTsao MNSchwartz ML: Testing the radiosurgery-based arteriovenous malformation score and the modified Spetzler-Martin grading system to predict radiosurgical outcome. J Neurosurg 103:6426482005

    • Search Google Scholar
    • Export Citation
  • 2

    Cockroft KMJayaraman MVAmin-Hanjani SDerdeyn CPMcDougall CGWilson JA: A perfect storm: how a randomized trial of unruptured brain arteriovenous malformations' (ARUBA's) trial design challenges notions of external validity. Stroke 43:197919812012

    • Search Google Scholar
    • Export Citation
  • 3

    Colombo FCavedon CCasentini LFrancescon PCausin FPinna V: Early results of CyberKnife radiosurgery for arteriovenous malformations. Clinical article. J Neurosurg 111:8078192009

    • Search Google Scholar
    • Export Citation
  • 4

    Ding DYen CPXu ZStarke RMSheehan JP: Radiosurgery for patients with unruptured intracranial arteriovenous malformations. Clinical article. J Neurosurg 118:9589662013

    • Search Google Scholar
    • Export Citation
  • 5

    Kano HKondziolka DFlickinger JCYang HCFlannery TJAwan NR: Stereotactic radiosurgery for arteriovenous malformations, Part 2: management of pediatric patients. Clinical article. J Neurosurg Pediatr 9:1102012

    • Search Google Scholar
    • Export Citation
  • 6

    Kano HKondziolka DFlickinger JCYang HCFlannery TJAwan NR: Stereotactic radiosurgery for arteriovenous malformations, Part 3: outcome predictors and risks after repeat radiosurgery. Clinical article. J Neurosurg 116:21322012

    • Search Google Scholar
    • Export Citation
  • 7

    Kano HKondziolka DFlickinger JCYang HCFlannery TJNiranjan A: Stereotactic radiosurgery for arteriovenous malformations, Part 4: management of basal ganglia and thalamus arteriovenous malformations. Clinical article. J Neurosurg 116:33432012

    • Search Google Scholar
    • Export Citation
  • 8

    Kano HKondziolka DFlickinger JCYang HCFlannery TJNiranjan A: Stereotactic radiosurgery for arteriovenous malformations, Part 5: management of brainstem arteriovenous malformations. Clinical article. J Neurosurg 116:44532012

    • Search Google Scholar
    • Export Citation
  • 9

    Kano HKondziolka DFlickinger JCPark KJParry PVYang HC: Stereotactic radiosurgery for arteriovenous malformations, Part 6: multistaged volumetric management of large arteriovenous malformations. Clinical article. J Neurosurg 116:54652012

    • Search Google Scholar
    • Export Citation
  • 10

    Kano HLunsford LDFlickinger JCYang HCFlannery TJAwan NR: Stereotactic radiosurgery for arteriovenous malformations, Part 1: management of Spetzler-Martin Grade I and II arteriovenous malformations. Clinical article. J Neurosurg 116:11202012

    • Search Google Scholar
    • Export Citation
  • 11

    Mathiesen T: Arguments against the proposed randomised trial (ARUBA). Neuroradiology 50:4694712008

  • 12

    Pollock BEDevelopment and testing of a radiosurgery-based arteriovenous malformation grading system. Niranjan AKano HLunsford LD: Gamma Knife Radiosurgery for Brain Vascular Malformations BaselKarger2013. 27:5866

    • Search Google Scholar
    • Export Citation
  • 13

    Pollock BEFlickinger JC: Modification of the radiosurgery-based arteriovenous malformation grading system. Neurosurgery 63:2392432008

    • Search Google Scholar
    • Export Citation
  • 14

    Pollock BEFlickinger JC: A proposed radiosurgery-based grading system for arteriovenous malformations. J Neurosurg 96:79852002

  • 15

    Pollock BEGorman DACoffey RJ: Patient outcomes after arteriovenous malformation management: results based on a 5- to 14-year follow-up study. Neurosurgery 52:129112972003

    • Search Google Scholar
    • Export Citation
  • 16

    Pollock BELink MJBrown RD: The risk of stroke or clinical impairment after stereotactic radiosurgery for ARUBA-eligible patients. Stroke 44:4374412013

    • Search Google Scholar
    • Export Citation
  • 17

    Raffa SJChi YYBova FJFriedman WA: Validation of the radiosurgery-based arteriovenous malformation score in a large linear accelerator radiosurgery experience. J Neurosurg 111:8328392009

    • Search Google Scholar
    • Export Citation
  • 18

    Spetzler RFMartin NA: A proposed grading system for arteriovenous malformations. J Neurosurg 65:4764831986

  • 19

    Stapf CMohr JPChoi JHHartmann AMast H: Invasive treatment of unruptured brain arteriovenous malformations is experimental therapy. Curr Opin Neurol 19:63682006

    • Search Google Scholar
    • Export Citation
  • 20

    Wegner REOysul KPollock BESirin SKondziolka DNiranjan A: A modified radiosurgery-based arteriovenous malformation grading scale and correlation with outcomes. Int J Radiat Oncol Biol Phys 79:114711502011

    • Search Google Scholar
    • Export Citation
Keywords:

Response

We thank Dr. Pollock for his letter regarding our article. We agree that there is a favorable benefit-to-risk ratio for radiosurgery in selected cohorts of patients with unruptured AVM. In particular, those patients who are younger and whose AVMs exhibit features indicating a greater likelihood of rupture over time are likely to benefit from radiosurgery.

Regarding the name of the radiosurgery scale cited in our paper, we utilized the name noted in the recent peer-reviewed journal article published by Dr. Pollock and colleagues in which it was referred to as the Pittsburgh modified radiosurgery-based AVM grading scale.5 The modified radiosurgery-based AVM system (RBAS) was derived from 220 AVM patients treated with radiosurgery at the University of Pittsburgh from 1987 to 1992 and subsequently tested in a cohort of 247 patients treated at the Mayo Clinic from 1990 to 2001.1 The system has been revised over the years, and it was the modified radiosurgery-based arteriovenous malformation grading scale outlined in the publication by Wegner et al. (2011) that we utilized in our study.2,3,5 The modified scale has been validated by a number of centers, and we have also done so in our current study. We have recently developed a new AVM grading system that we believe will prove simpler to use, as it does not involve an algebraic equation, but this new system appears no less reliable.4 The Radiosurgery AVM scale was derived from a series of 1012 AVM patients.4

Dr. Pollock's contributions to the development of the RBAS and stereotactic radiosurgery as a whole are substantial. We appreciate his insight into the derivation of AVM grading schemes for radiosurgery and his seminal contribution to the same.1–3,5

References

  • 1

    Pollock BEFlickinger JC: Modification of the radiosurgery-based arteriovenous malformation grading system. Neurosurgery 63:2392432008

    • Search Google Scholar
    • Export Citation
  • 2

    Pollock BEFlickinger JC: A proposed radiosurgery-based grading system for arteriovenous malformatons. J Neurosurg 96:79852002

  • 3

    Pollock BEFlickinger JCLunsford LDMaitz AKondziolka DThe Pittsburgh Arteriovenous Malformation Radiosurgery (PAR) Grading Scale. Kondziolka D: Radiosurgery 1997. BaselKarger2:137146

    • Search Google Scholar
    • Export Citation
  • 4

    Starke RMYen CPDing DSheehan JP: A practical grading scale for predicting outcome after radiosurgery for arteriovenous malformations: analysis of 1012 treated patients. Clinical article. J Neurosurg (in press)2013

    • Search Google Scholar
    • Export Citation
  • 5

    Wegner REOysul KPollock BESirin SKondziolka DNiranjan A: A modified radiosurgery-based arteriovenous malformation grading scale and its correlation with outcomes. Int J Radiat Oncol Biol Phys 79:114711502011

    • Search Google Scholar
    • Export Citation

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Article Information

Contributor Notes

Please include this information when citing this paper: published online June 28, 2013; DOI: 10.3171/2013.4.JNS13746.
Headings
References
  • 1

    Andrade-Souza YMZadeh GRamani MScora DTsao MNSchwartz ML: Testing the radiosurgery-based arteriovenous malformation score and the modified Spetzler-Martin grading system to predict radiosurgical outcome. J Neurosurg 103:6426482005

    • Search Google Scholar
    • Export Citation
  • 2

    Cockroft KMJayaraman MVAmin-Hanjani SDerdeyn CPMcDougall CGWilson JA: A perfect storm: how a randomized trial of unruptured brain arteriovenous malformations' (ARUBA's) trial design challenges notions of external validity. Stroke 43:197919812012

    • Search Google Scholar
    • Export Citation
  • 3

    Colombo FCavedon CCasentini LFrancescon PCausin FPinna V: Early results of CyberKnife radiosurgery for arteriovenous malformations. Clinical article. J Neurosurg 111:8078192009

    • Search Google Scholar
    • Export Citation
  • 4

    Ding DYen CPXu ZStarke RMSheehan JP: Radiosurgery for patients with unruptured intracranial arteriovenous malformations. Clinical article. J Neurosurg 118:9589662013

    • Search Google Scholar
    • Export Citation
  • 5

    Kano HKondziolka DFlickinger JCYang HCFlannery TJAwan NR: Stereotactic radiosurgery for arteriovenous malformations, Part 2: management of pediatric patients. Clinical article. J Neurosurg Pediatr 9:1102012

    • Search Google Scholar
    • Export Citation
  • 6

    Kano HKondziolka DFlickinger JCYang HCFlannery TJAwan NR: Stereotactic radiosurgery for arteriovenous malformations, Part 3: outcome predictors and risks after repeat radiosurgery. Clinical article. J Neurosurg 116:21322012

    • Search Google Scholar
    • Export Citation
  • 7

    Kano HKondziolka DFlickinger JCYang HCFlannery TJNiranjan A: Stereotactic radiosurgery for arteriovenous malformations, Part 4: management of basal ganglia and thalamus arteriovenous malformations. Clinical article. J Neurosurg 116:33432012

    • Search Google Scholar
    • Export Citation
  • 8

    Kano HKondziolka DFlickinger JCYang HCFlannery TJNiranjan A: Stereotactic radiosurgery for arteriovenous malformations, Part 5: management of brainstem arteriovenous malformations. Clinical article. J Neurosurg 116:44532012

    • Search Google Scholar
    • Export Citation
  • 9

    Kano HKondziolka DFlickinger JCPark KJParry PVYang HC: Stereotactic radiosurgery for arteriovenous malformations, Part 6: multistaged volumetric management of large arteriovenous malformations. Clinical article. J Neurosurg 116:54652012

    • Search Google Scholar
    • Export Citation
  • 10

    Kano HLunsford LDFlickinger JCYang HCFlannery TJAwan NR: Stereotactic radiosurgery for arteriovenous malformations, Part 1: management of Spetzler-Martin Grade I and II arteriovenous malformations. Clinical article. J Neurosurg 116:11202012

    • Search Google Scholar
    • Export Citation
  • 11

    Mathiesen T: Arguments against the proposed randomised trial (ARUBA). Neuroradiology 50:4694712008

  • 12

    Pollock BEDevelopment and testing of a radiosurgery-based arteriovenous malformation grading system. Niranjan AKano HLunsford LD: Gamma Knife Radiosurgery for Brain Vascular Malformations BaselKarger2013. 27:5866

    • Search Google Scholar
    • Export Citation
  • 13

    Pollock BEFlickinger JC: Modification of the radiosurgery-based arteriovenous malformation grading system. Neurosurgery 63:2392432008

    • Search Google Scholar
    • Export Citation
  • 14

    Pollock BEFlickinger JC: A proposed radiosurgery-based grading system for arteriovenous malformations. J Neurosurg 96:79852002

  • 15

    Pollock BEGorman DACoffey RJ: Patient outcomes after arteriovenous malformation management: results based on a 5- to 14-year follow-up study. Neurosurgery 52:129112972003

    • Search Google Scholar
    • Export Citation
  • 16

    Pollock BELink MJBrown RD: The risk of stroke or clinical impairment after stereotactic radiosurgery for ARUBA-eligible patients. Stroke 44:4374412013

    • Search Google Scholar
    • Export Citation
  • 17

    Raffa SJChi YYBova FJFriedman WA: Validation of the radiosurgery-based arteriovenous malformation score in a large linear accelerator radiosurgery experience. J Neurosurg 111:8328392009

    • Search Google Scholar
    • Export Citation
  • 18

    Spetzler RFMartin NA: A proposed grading system for arteriovenous malformations. J Neurosurg 65:4764831986

  • 19

    Stapf CMohr JPChoi JHHartmann AMast H: Invasive treatment of unruptured brain arteriovenous malformations is experimental therapy. Curr Opin Neurol 19:63682006

    • Search Google Scholar
    • Export Citation
  • 20

    Wegner REOysul KPollock BESirin SKondziolka DNiranjan A: A modified radiosurgery-based arteriovenous malformation grading scale and correlation with outcomes. Int J Radiat Oncol Biol Phys 79:114711502011

    • Search Google Scholar
    • Export Citation
  • 1

    Pollock BEFlickinger JC: Modification of the radiosurgery-based arteriovenous malformation grading system. Neurosurgery 63:2392432008

    • Search Google Scholar
    • Export Citation
  • 2

    Pollock BEFlickinger JC: A proposed radiosurgery-based grading system for arteriovenous malformatons. J Neurosurg 96:79852002

  • 3

    Pollock BEFlickinger JCLunsford LDMaitz AKondziolka DThe Pittsburgh Arteriovenous Malformation Radiosurgery (PAR) Grading Scale. Kondziolka D: Radiosurgery 1997. BaselKarger2:137146

    • Search Google Scholar
    • Export Citation
  • 4

    Starke RMYen CPDing DSheehan JP: A practical grading scale for predicting outcome after radiosurgery for arteriovenous malformations: analysis of 1012 treated patients. Clinical article. J Neurosurg (in press)2013

    • Search Google Scholar
    • Export Citation
  • 5

    Wegner REOysul KPollock BESirin SKondziolka DNiranjan A: A modified radiosurgery-based arteriovenous malformation grading scale and its correlation with outcomes. Int J Radiat Oncol Biol Phys 79:114711502011

    • Search Google Scholar
    • Export Citation
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