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Stereotactic Radiosurgical Procedures for Arteriovenous Malformations of the Brain

1995; Elsevier BV; Volume: 70; Issue: 3 Linguagem: Inglês

10.4065/70.3.305

1942-5546

L. Dade Lunsford,

Intracerebral and Subarachnoid Hemorrhage Research

Patients throughout the world have benefited from a resurgence of interest in new management strategies for arteriovenous malformations (AVMs) of the brain. Improved knowledge is based on a better understanding of the natural history of untreated vascular malformations and the response of AVMs to treatment, advanced neurodiagnostic imaging tools such as magnetic resonance imaging (MRI), superselective angiographic techniques that can disclose the vascular angioarchitecture, advances in microsurgical techniques, staged endovascular embolizations, and stereotactic radiosurgical procedures. All these advances have had a positive effect on outcomes for a large group of patients with AVMs. Since 1971, more than 5,000 patients worldwide have received radiosurgical treatment with the gamma knife. Several thousand more have undergone particle beam irradiation, and an unknown number (certainly in the thousands) have been treated by linear accelerator technology. Stereotactic radiosurgical surgical treatment is a minimally invasive and effective alternative to surgical removal of an AVM. Although it was originally advocated for high-risk AVMs (for example, Spetzler-Martin grade III or VI), increasingly patients and their referring physicians have opted for radiosurgical rather than microsurgical treatment, even in patients with small or less critically located AVMs.1Pollock BE Lunsford LD Kondziolka D Maitz A Flickinger JC Patient outcomes after stereotactic radio-surgery for “operable” arteriovenous malformations.Neurosurgery. 1994; 35: 1-7Crossref PubMed Scopus (148) Google Scholar Except in elderly persons or patients with concomitant medical illnesses that seriously limit their potential survival, most patients with AVMs should undergo a definitive procedure designed to obliterate the lesion, to eliminate the risk of fatal hemorrhage, to ameliorate symptoms, and to restore the patient to a normal, productive lifestyle and full working capacity. As with any new technique or alternative treatment strategy, stereotactic radiosurgical procedures are variously viewed as a valuable therapeutic option, a potentially useful adjunct, or a serious economic threat to the well-being of patients and their neurosurgeons. Mayo Clinic Experience.—The article by Coffey and associates in this issue of the Mayo Clinic Proceedings (pages 214 to 222) is a useful addition to the burgeoning literature on the role of stereotactic radiosurgical treatment.2Altschuler EM Lunsford LD Coffey RJ Bissonette DJ Flickinger JC Gamma knife radiosurgery for intracranial arteriovenous malformations in childhood and adolescence.Pediatr Neurosci. 1989; 15: 53-61Crossref PubMed Scopus (65) Google Scholar, 3Kondziolka D Lunsford LD Flickinger JC Intra-parenchymal brain stem radiosurgery.Neurosurg Clin North Am. 1993 Jul; 4: 469-479PubMed Google Scholar, 4Lunsford LD Kondziolka D Flickinger JC Bissonette DJ Jungreis CA Maitz AH et al.Stereotactic radiosurgery for arteriovenous malformations of the brain.J Neurosurg. 1991; 75: 512-524Crossref PubMed Scopus (553) Google Scholar From tentative beginnings in 1971, the number of peer-reviewed reports related to outcomes after radiosurgical procedures has steadily climbed, and most have sought to maintain a judicious balance in reporting both the risks and the benefits. The results from a variety of centers have been consistent. Angiographic complete obliteration rates range from 70 to 88%.1Pollock BE Lunsford LD Kondziolka D Maitz A Flickinger JC Patient outcomes after stereotactic radio-surgery for “operable” arteriovenous malformations.Neurosurgery. 1994; 35: 1-7Crossref PubMed Scopus (148) Google Scholar, 4Lunsford LD Kondziolka D Flickinger JC Bissonette DJ Jungreis CA Maitz AH et al.Stereotactic radiosurgery for arteriovenous malformations of the brain.J Neurosurg. 1991; 75: 512-524Crossref PubMed Scopus (553) Google Scholar, 5Steiner L Lindquist C Cail W Karlsson B Steiner M Microsurgery and radiosurgery in brain arteriovenous malformations [editorial].J Neurosurg. 1993; 79: 647-652Crossref PubMed Scopus (63) Google Scholar The Mayo Clinic experience is reported by a dedicated team of experts who had thoroughly reviewed each case to select an appropriate therapy. Multidisciplinary input from vascular neurosurgeons, neurologic surgeons with expertise in radiosurgical techniques, radiation oncologists, and medical physicists is necessary. Such an approach is likely to improve the selection of patients and the results. The Mayo Clinic protocol required that specific doses be calculated on the basis of AVM volume measured during the procedure itself. In general, such dose prescriptions were consistent with those used at other centers and were based on radiobiologic concerns previously outlined by others.6Flickinger JC An integrated logistic formula for prediction of complications from radiosurgery.Int J Radiat Oncol Biol Phys. 1989; 17: 879-885Abstract Full Text PDF PubMed Scopus (210) Google Scholar, 7Flickinger JC Lunsford LD Wu A Maitz AH Kalend AM Treatment planning for gamma knife radiosurgery with multiple isoccnters.Int J Radiat Oncol Biol Phys. 1990; 18: 1495-1501Abstract Full Text PDF PubMed Scopus (106) Google Scholar, 8Flickinger JC Lunsford LD Kondziolka D Maitz AH Epstein AH Simons SR et al.Radiosurgery and brain tolerance: an analysis of neurodiagnostic imaging changes after gamma knife radiosurgery for arteriovenous malformations.Int J Radiat Oncol Biol Phys. 1992; 23: 19-26Abstract Full Text PDF PubMed Scopus (140) Google Scholar The central thesis of the report by Coffey and coworkers is that AVM obliteration after radiosurgical treatment may be unrelated to the single-fraction radiation dose given to the margin of the AVM. At the Mayo Clinic, the radiation dose was decreased for larger volume AVMs, but administered doses did not differ widely. University of Pittsburgh Experience.—At the University of Pittsburgh, my colleagues and I use similar criteria for selection of patients, intraoperative stereotactic angiography, and MRI dose prescriptions based on an estimated 3% risk of delayed radiation injury to the surrounding brain.6Flickinger JC An integrated logistic formula for prediction of complications from radiosurgery.Int J Radiat Oncol Biol Phys. 1989; 17: 879-885Abstract Full Text PDF PubMed Scopus (210) Google Scholar, 7Flickinger JC Lunsford LD Wu A Maitz AH Kalend AM Treatment planning for gamma knife radiosurgery with multiple isoccnters.Int J Radiat Oncol Biol Phys. 1990; 18: 1495-1501Abstract Full Text PDF PubMed Scopus (106) Google Scholar A recent summary of our results (Table 1) indicates that, at 2 to 3 years after radiosurgical treatment, smaller volume AVMs (those less than 1 cm3) have a high rate of obliteration (88%), whereas large AVMs (more than 10 cm3) have a reduced likelihood of total obliteration (40%) (after a single procedure).Table 1Obliteration of Arteiovenous Malformations by 3 Years After Stereotactic Radiosurgical Treatment: University of Pittsburgh Experience in 185 Patients, 1987 Through 1992*AVM = arteriovenous malfomation.AVM volume (cm3)No. of patientsObliterationNo changeComplete†No evidence of residual AVM at time of follow-up angiography 2 to 3 years after radiosurgical intervention.Subtotal‡Persistent early draining vein or small residual AVM.No.%No.%No.%<14136885120…1–483668017200…4.1–1051326319370…10104405§Second procedure recommended.50110* AVM = arteriovenous malfomation.† No evidence of residual AVM at time of follow-up angiography 2 to 3 years after radiosurgical intervention.‡ Persistent early draining vein or small residual AVM.§ Second procedure recommended. Open table in a new tab What explanation can be offered for the discrepancy between our results and those of Coffey and associates? For very small vascular malformations, we have used a higher dose to the margin (25 Gy at the 50% isodose; 50-Gy maximal dose). For the much larger vascular malformations, we have prescribed an even lower dose at the AVM margin than Coffey and colleagues did. Our results indicated that, at the end of 3 years, more than 80% of patients will have complete obliteration of smaller volume AVMs (those less than 25 mm in average diameter). For the larger volume vascular malformations, we now advocate a prospective staged radiosurgical approach parallel to the staged microsurgical procedures recommended by others.9Hamilton MG Spetzlcr RF The prospective application of a grading system for arteriovenous malformations.Neurosurgery. 1994; 34: 2-6Crossref PubMed Scopus (298) Google Scholar For example, at radiosurgical centers, an average of two or three operations per patient may be necessary to eradicate a large-volume AVM. Similarly, a staged procedure recommended. radiosurgical procedure can be performed by dose staging (treating the entire volume of the AVM with a reduced tolerable dose to the brain) or volume staging (treating separate volumes of the AVM with a higher dose). The optimal staging interval is unclear and may be as brief as 1 day. We have elected to wait between 3 and 6 months for prospectively staged procedures. We recommend this approach because in our 3-year review of large AVMs that were subsequently treated by staging of the A VM, we achieved AVM obliteration in an additional 70 to 80% of patients. Although some large A VMs may be obliterated by a single lower dose procedure, the number is probably minimal and the patient may remain at risk of bleeding during the latency interval until the AVM is completely obliterated. Predictive Features.-Several factors probably contribute to the successful radiosurgical obliteration of AVMs. VMs. Most of those factors are not addressed in the current report by Coffey and coworkers but should continue to be analyzed in larger series so that not only can the likelihood of obliteration be predicted but also the chances of complications during the latency interval can be estimated. The following factors may influence the rate of obliteration: (1) the vol ume.10Spetzler RF Martin NA A proposed grading system for arteriovenous malformations.J Neurosurg. 1986; 65: 476-483Crossref PubMed Scopus (1745) Google Scholar (2) the site of involvement, (3) the presence or absence of associated aneurysms in the circle of Willis or flowrelated aneurysms proximal to the AVM, (4) the number and adequacy of venous outflow channels, (5) the compactness or amount of flow through the nidus itself, and (6) the presence or absence of deep venous drainage (similar to the risk predictions described for microsurgical series).10Spetzler RF Martin NA A proposed grading system for arteriovenous malformations.J Neurosurg. 1986; 65: 476-483Crossref PubMed Scopus (1745) Google Scholar These features may help predict the risk of complications such as bleeding during the latency interval. For example, if an angiogram demonstrates an AVM with intranidal or flowrelated aneurysms, venous outflow restriction, and easy accessibility in the brain, surgical resection would be preferred. Alternatively, a patient with a similarly located AVM without restricted venous outflow or associated aneurysms may be at low risk for rupture during the latency interval after radiosurgical treatment. My colleagues and I have early evidence that protection from radiosurgical effects may not always be totally related to the angiographic appearance of the AVM. We recently reviewed our series of patients who had hemorrhages from A most of which occurred during the first year after a radiosurgical procedure. Perhaps small-volume AVMs have an annual natural history bleeding risk greater than the 2 to 4% frequency quoted.11Sisti MB Kader A Stein BM Microsurgery for 67 intracranial arteriovenous malformations less than 3 cm in diameter.J Neurosurg. 1993; 79: 653-660Crossref PubMed Scopus (132) Google Scholar, 12Spetzler RF Hargraves RW McCormick PW Zabramski JM Flom RA Zimmerman RS Relationship of perfusion pressure and size to risk of hemorrhage from arteriovenous malformations.J Neurosurg. 1992; 76: 918-923Crossref PubMed Scopus (321) Google Scholar Dur ing the latency interval after radiosurgical treatment, the risk may be 6% per year; the risk may be less than 1% after the first year and reaches 0% at the time of obliteration.1Pollock BE Lunsford LD Kondziolka D Maitz A Flickinger JC Patient outcomes after stereotactic radio-surgery for “operable” arteriovenous malformations.Neurosurgery. 1994; 35: 1-7Crossref PubMed Scopus (148) Google Scholar Thus, the risk of bleeding may be decreased or eliminated after a period of 1 year has elapsed. These features necessitate a larger patient database and a longer duration of follow-up to facilitate rational selection of an appropriate treatment option by both surgeons and their patients. Angiographic Assessment.—We certainly agree that angiography is essential for performance of AVM outcome studies. In our experience, MRI has approximately an 80% positive correlation-that is, an 80% possibility exists that angiography will confirm obliteration of an AVM that MRI suggests is obliterated. We do not re-treat a patient with an incompletely obliterated AVM until a period of 3 years has elapsed. Fewer and fewer patients have further obliteration of an AVM beyond a 3- or 4-year observation interval. Retreatment is associated with a significant further likelihood of obliteration. Delayed hemorrhage in those patients selected for re-treatment has been rare. Additional Important Data.—Three additional pieces of information would have been valuable in the otherwise excellent report by Coffey and associates. First, consistent with the current emphasis on outcome studies in general, an understanding of the patient's functional status and employment status would have been desirable. Deficiency in reporting these features has also been frequently noted in descriptions of results from microsurgical centers. Such outcome criteria provide a concrete balance to our usual neurologic outcome scales; sometimes we are too optimistic in our assessments. “Good” outcomes do not always translate into a patient's full return to an active lifestyle and normal employment. Second, at a center of neurovascular surgical excellence such as the Mayo Clinic, some indication of the percentage of patients at the Mayo Clinic who were selected for or opted for radiosurgical rather than microsurgical treatment would have been useful. At our center, we have noted a distinct radiosurgical trend during the past 7 years; 90% of our patients have had radiosurgical rather than microsurgical procedures. Third, a more detailed evaluation of the role of embolization before radiosurgical intervention would have been helpful. Permanent volume reduction of an AVM by staged embolizations may enhance the likelihood of eventual radiosurgical obliteration.13Dawson III, RC Tarr RW Hecht ST Jungreis CA Lunsford LD Coffey R et al.Treatment of arteriovenous malformations of the brain with combined embolization and stereotactic radiosurgery: results after 1 and 2 years.AJNR Am J Neuroradiol. 1990; 11: 857-864PubMed Google Scholar, 14Jungreis CA Lunsford LD Barker D Angiographic complications during stereotactic radiosurgery for cerebral arteriovenous malformations.AJNR Am J Neuroradiol. 1992; 13: 946-948PubMed Google Scholar Conclusion.—As more refined outcome analyses are developed because of a better understanding of the risk-to-benefit ratio based on the aforementioned factors, the relative roles of the various management techniques for AVMs may change again. In the meantime, neurologic surgeons, radiation oncologists, patients, and their referring physicians should be gratified by the addition of the stereotactic radiosurgical option for treatment of AVMs. VMs.