From: Subject: Bevacizumab for recurrent malignant gliomas: Efficacy, toxicity, and patterns of recurrence -- Norden et al. 70 (10): 779 -- Neurology Date: Thu, 17 Jun 2010 19:01:26 +0200 MIME-Version: 1.0 Content-Type: multipart/related; type="text/html"; boundary="----=_NextPart_000_0000_01CB0E4F.7C61CAA0" X-MimeOLE: Produced By Microsoft MimeOLE V6.00.2900.5931 This is a multi-part message in MIME format. ------=_NextPart_000_0000_01CB0E4F.7C61CAA0 Content-Type: text/html; charset="Windows-1252" Content-Transfer-Encoding: quoted-printable Content-Location: http://www.neurology.org/cgi/content/full/70/10/779?ijkey=8155c39c4654d1f18c818d4162957d03a099856a Bevacizumab for recurrent malignant gliomas: = Efficacy, toxicity, and patterns of recurrence -- Norden et al. 70 (10): = 779 -- Neurology
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NEUROLOGY 2008;70:779-787
=A9 2008 American = Academy of=20 Neurology

Bevacizumab for recurrent malignant gliomas

Efficacy, toxicity, and patterns of recurrence=20
3D"Formula=20

A. D. Norden, MD, G. S. = Young,=20 MD, K. Setayesh, MA, A. Muzikansky, = MA,=20 R. Klufas, MD, G. L. Ross, MD, A. = S.=20 Ciampa, NP, L. G. Ebbeling, BA, B. Levy, = BA, J. Drappatz, MD, S. Kesari, MD, = PhD=20 and P. Y. Wen, MD

From the Division of Cancer Neurology (A.D.N., = A.S.C.,=20 L.G.E., B.L., J.D., S.K., P.Y.W.), Department of Neurology, = Brigham and=20 Women's Hospital and Center For Neuro-Oncology, = Dana-Farber/Brigham and=20 Women's Cancer Center and Harvard Medical School; Brigham and = Women's=20 Hospital Department of Radiology and Harvard Medical School = (G.S.Y., K.S.,=20 R.K., G.L.R.); and Massachusetts General Hospital Biostatistics = Center=20 (A.M.), Boston.

Address correspondence and reprint requests to = Dr Norden,=20 Dana-Farber/Brigham and Women's Cancer Center and Harvard Medical = School,=20 SW430B, 44 Binney St., Boston, MA 02115 anorden{at}partners.org


  =20 Abstract.
Top.
3D"Abstract.
METHODS
RESULTS
DISCUSSION
REFERENCES
 
<= B>Background:=20 Bevacizumab, a humanized monoclonal antibody against=20 vascular endothelial growth factor, may have activity in=20 recurrent malignant gliomas. At recurrence some = patients appear=20 to develop nonenhancing infiltrating disease rather = than=20 enhancing tumor.

Methods: We retrospectively reviewed 55 consecutive=20 patients with recurrent malignant gliomas who received=20 bevacizumab and chemotherapy to determine efficacy, = toxicity,=20 and patterns of recurrence. Using a blinded, = standardized=20 imaging review and quantitative volumetric analysis, = the=20 recurrence patterns of patients treated with = bevacizumab were=20 compared to recurrence patterns of 19 patients treated = with=20 chemotherapy alone.

Results: A total of 2.3% of patients had a complete=20 response, 31.8% partial response, 29.5% minimal = response, and=20 29.5% had stable disease. Median time to radiographic=20 progression was 19.3 weeks. Six-month progression-free = survival=20 (PFS) was 42% for patients with glioblastoma and 32% = for=20 patients with anaplastic glioma. In 23 patients who = progressed=20 on their initial therapy, bevacizumab was continued and = the=20 concurrent chemotherapy agent changed. In no case did = the=20 change produce a radiographic response, but two = patients had=20 prolonged PFS of 20 and 31 weeks. Recurrence pattern = analysis=20 identified a significant increase in the volume of = infiltrative=20 tumor relative to enhancing tumor in bevacizumab=20 responders.

Conclusions: Combination therapy with bevacizumab and=20 chemotherapy is well-tolerated and active against = recurrent=20 malignant gliomas. At recurrence, continuing = bevacizumab and=20 changing the chemotherapy agent provided long-term = disease=20 control only in a small subset of patients. Bevacizumab = may=20 alter the recurrence pattern of malignant gliomas by=20 suppressing enhancing tumor recurrence more effectively = than it=20 suppresses nonenhancing, infiltrative tumor = growth.

Abbreviations: AA =3D anaplastic = astrocytoma;=20 AG =3D anaplastic glioma; CR =3D complete response; = GBM =3D=20 glioblastoma; EIAED =3D enzyme-inducing antiepileptic drug; = FLAIR =3D fluid-attenuated inversion recovery; KPS = =3D Karnofsky=20 Performance Status; MR =3D minimal response; PFS =3D = progression-free survival; PR =3D partial response; = rFPR =3D=20 relative FLAIR progression ratio; rNTR =3D relative = nonenhancing=20 tumor ratio; T1W =3D T1-weighted; VEGF =3D vascular = endothelial=20 growth factor.

Despite recent therapeutic advances, malignant gliomas are = associated=20 with a strikingly poor prognosis. Median survival is 14.6=20 months among patients with newly diagnosed glioblastoma = (GBM)=20 who receive optimal therapy with surgery, radiation, = and=20 chemotherapy.1=20 For patients with anaplastic astrocytoma (AA), median = survival=20 is in the range of 2 to 3 years.2,3=20 Recurrent malignant glioma confers a dismal prognosis, = with=20 median survival of 25 weeks for patients with GBM and = 47 weeks=20 for patients with AA. Less than 15% of recurrent tumors = show a=20 radiographic response to chemotherapy, and the 6-month=20 progression-free survival (6M-PFS) for GBM is only 15 = to=20 21%.4=20 There is a clear need for more effective = therapies.

As the molecular pathogenesis of malignant gliomas is = elucidated,=20 novel therapeutic targets are emerging. Vascular = endothelial=20 growth factor (VEGF) is a critical mediator of new blood = vessel=20 formation, or angiogenesis, within gliomas.5,6=20 Robust angiogenesis is required for the growth of many = human=20 cancers,7,8=20 including malignant gliomas.9=20 VEGF secreted by glioma cells acts by paracrine = mechanisms upon=20 endothelial cells in the vicinity of the tumor, = resulting in=20 endothelial cell proliferation, survival, and migration.10=20 The level of VEGF expression in gliomas correlates with = blood=20 vessel density, degree of malignancy, and prognosis.11,12=20

Bevacizumab is a humanized monoclonal antibody against = VEGF=20 that has proven efficacy against metastatic colon = cancer13=20 and nonsmall cell lung cancer14=20 when administered in conjunction with traditional=20 chemotherapeutics. The published experience with = bevacizumab=20 and chemotherapy for recurrent malignant gliomas is=20 encouraging, with radiographic response rates of at least=20 5015=9617=20 and median PFS of 24 weeks.17=20 In the first reported cohort of 29 patients with = recurrent=20 malignant gliomas treated with bevacizumab and = irinotecan,=20 there were 3 complete responses (CRs) and 16 partial = responses=20 (PRs).15=20 Among 14 evaluable patients treated with bevacizumab = and a=20 variety of chemotherapeutic agents, 7 PRs and 3 = patients with=20 stable disease were observed.16=20 More recently, 32 patients treated with bevacizumab and = irinotecan had an overall response rate of 63%.18=20 6M-PFS was 30% for patients with GBM and 56% for = patients with=20 anaplastic glioma (AG). This compares favorably with = the=20 results from the MD Anderson database of 8 negative = trials in=20 which the 6M-PFS for GBM was 15% and 31% for AG.4=20 There is also evidence that VEGF receptor inhibitors = may have=20 activity.19=20 In a recent phase II study of the pan-VEGF receptor = inhibitor=20 AZD2171 in recurrent GBMs, the radiographic response = rate was=20 approximately 50%, and 6M-PFS was 27%.19,20=20

In our initial experience treating patients with malignant = glioma=20 with bevacizumab, a larger than expected number of = patients=20 developed diffuse infiltrating disease at the time of = tumor=20 progression. This appeared as diffuse hyperintensity on=20 T2-weighted fluid-attenuated inversion recovery (FLAIR) = MRI=20 sequences, rather than abnormal gadolinium enhancement. = Since=20 recurrence within 2 to 4 cm of the tumor margin is = observed in=20 the majority of patients treated with radiation and = cytotoxic=20 chemotherapy,21,22=20 we hypothesized that bevacizumab treatment effectively = controls=20 local tumor growth but either fails to control or actually=20 promotes distant and diffuse recurrences. A plausible = mechanism=20 for this hypothesis comes from animal model data which = suggest=20 that VEGF-induced angiogenesis blockade facilitates = co-option=20 of the normal vasculature and tumor invasion.23,24=20

We sought to confirm the subjective impression of = increased=20 infiltrative disease using volumetric MRI measurements. If=20 bevacizumab treatment promotes diffuse tumor = infiltration,=20 bevacizumab-treated patients with recurrent malignant = gliomas=20 should have larger volumes of FLAIR hyperintense, = nonenhancing=20 tumor than control patients treated with cytotoxic = chemotherapy=20 alone. Since bevacizumab appears to control local tumor = growth,=20 bevacizumab-treated patients would be expected to have = smaller=20 volumes of local enhancing tumor compared with = controls. In=20 addition, if increased infiltrative disease is a result = of the=20 anti-angiogenic effect of bevacizumab, nonenhancing = tumor=20 infiltration should be even more apparent in patients = with=20 bevacizumab who respond to treatment than nonresponders. = To=20 test these hypotheses, we reviewed our experience with = bevacizumab=20 in combination with conventional chemotherapy for heavily=20 pretreated patients with recurrent malignant gliomas. = We=20 designed a blinded, standardized imaging review to = allow an=20 unbiased comparison of recurrence patterns in=20 bevacizumab-treated patients to patients treated with=20 traditional cytotoxic chemotherapy alone.


  =20 METHODS
Top.
Abstract.
3D"METHODS
RESULTS
DISCUSSION
REFERENCES
 
W= e=20 performed a retrospective chart review of 55 consecutive=20 patients with histologic diagnoses of malignant gliomas = who=20 were treated with bevacizumab (Avastin) and a conventional=20 chemotherapy agent between June 2005 and March 2007. = All=20 patients had prior treatment with radiotherapy and=20 temozolomide, and most with at least one additional=20 chemotherapeutic. There was no limit on the number of = prior=20 therapies. Except for one patient who received 5 mg/kg, = patients received bevacizumab 10 mg/kg every 2 weeks. A = total=20 of 47 patients received irinotecan (125 mg/m2 = every=20 2 weeks for patients not on enzyme-inducing antiepileptic = drugs=20 [EIAEDs] and 340 mg/m2 every 2 weeks for patients on=20 EIAEDs), 6 patients received carboplatin (AUC of = 5=966), one=20 patient received carmustine (200 mg/m2 every = 6=20 weeks), and one patient received temozolomide (150 to = 200=20 mg/m2 for 5 days every 4 weeks). Adverse = events were=20 graded based on the Common Terminology Criteria for = Adverse=20 Events v3.0. The Kaplan-Meier method was used to = estimate=20 survival functions, and statistical comparisons between = groups=20 were evaluated with the log-rank test.

To determine the pattern of recurrence in patients treated = with=20 conventional cytotoxic chemotherapy, we evaluated 19 = patients=20 enrolled in three phase II clinical trials of cytotoxic=20 chemotherapy for recurrent malignant gliomas. Control = patients=20 were selected on the basis of available MRI scan data, = as=20 described below. Seven patients were enrolled in a = phase II=20 trial of temozolomide (150 mg/m2/day for 5 = days=20 every 4 weeks) and irinotecan (200 mg/m2 = every 2=20 weeks for patients not on EIAEDs and 500 mg/m2 = for=20 patients on EIAEDs) (North American Brain Tumor Consortium=20 protocol 99-07). Eleven patients were enrolled in a phase = II=20 trial of gimatecan (1 mg/m2/day for 5 days every = 4 weeks)=20 (Dana-Farber Cancer Institute protocol 05-291). One = patient was=20 enrolled in a phase II trial of edotecarin (13 to 15=20 mg/m2 every 3 weeks) (Dana-Farber Cancer = Institute=20 protocol 03-205).

Subjects were included in the imaging analysis if = acceptable=20 digital MRI data could be retrieved for scans performed = within=20 2 weeks prior to initiating therapy and at least every 8 = weeks=20 thereafter until progression. Interpretable FLAIR and=20 post-gadolinium T1-weighted (T1W) sequences were = required for=20 each time point. By these criteria, 44 = bevacizumab-treated=20 patients were included and 11 patients were excluded. = In 26=20 cases, T1W and FLAIR images were reviewed independently = by=20 three neuroradiologists to detect evidence of distant = tumor=20 recurrence and to qualitatively assess interval changes = and=20 recurrence patterns. The neuroradiologists were blind = to=20 patient identity, scan date, and treatment. In 18 = cases, scans=20 were reviewed by one author. Using a standard approach, = the=20 largest cross-sectional and perpendicular diameters of=20 enhancing tumor on each gadolinium-enhanced T1W image were=20 measured. These measurements were multiplied to determine = the=20 largest cross-sectional tumor area. In order to = quantitatively=20 assess diffuse tumor recurrence, similar measurements of=20 nonenhancing tumor were made on FLAIR sequences. = Radiographic=20 response was defined by the Macdonald Criteria, in = which CR=20 represents complete disappearance of all measurable = disease, PR=20 represents a 50% or greater decrease in largest = cross-sectional=20 tumor area, and progressive disease represents a 25% or = greater=20 increase in largest cross-sectional tumor area or = appearance of=20 a new lesion.25=20 We defined minimal response (MR) as a 25 to 49% decrease = in=20 largest cross-sectional tumor area. All other conditions = were=20 classified as stable disease. Stability or improvement on = FLAIR=20 sequences was required for classification as a response = (CR,=20 PR, or MR). Additionally, a subject must have been taking = the=20 same or decreased dose of corticosteroids and have had a = stable=20 or improved neurologic examination. When progressive = disease=20 was detected, scans were classified on the basis of = recurrence=20 pattern. Scans found to have new foci of enhancement = distant=20 from the original area of enhancing tumor were classified = as=20 distant recurrence (figure=20 1). When increased enhancement developed in = contiguity with=20 the original tumor mass, the scan was classified as = local=20 recurrence (figure=20 2). If the local tumor mass remained stable but = there was=20 at least a 25% increase in area of abnormal FLAIR=20 hyperintensity, the scan was classified as diffuse recurrence = (figure=20 3). The significance of the difference in recurrence=20 patterns between control and bevacizumab-treated patients = was=20 evaluated using Fisher exact test.



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  		Figure 1 Distant = recurrence=20 in a patient with recurrent malignant glioma treated = with=20 bevacizumab and irinotecan

Post-gadolinium T1-weighted MRI scan before = treatment with=20 bevacizumab and irinotecan (A). After 4 weeks of = treatment,=20 there is reduction in the intensity of enhancement = (B). After=20 5 months of treatment, the intensity and size of = enhancement=20 has reduced sufficiently to achieve a partial response = (C).=20 After 7 months of treatment, a new area of enhancement = inferior to the original tumor has appeared, = consistent with a=20 distant recurrence (D). =

 = ;


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  		Figure 2 Local = recurrence in=20 a patient with recurrent malignant glioma treated with = bevacizumab and irinotecan

Post-gadolinium T1-weighted MRI scan before = treatment with=20 bevacizumab and irinotecan (A). After 4 weeks of = treatment,=20 there is reduction in the size and intensity of = enhancement=20 sufficient to achieve a minor response (B). After 5 = months of=20 treatment, the size and intensity of enhancement at = the=20 location of the original abnormality has increased=20 substantially, consistent with a local recurrence (C). =

 = ;


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  		Figure 3 Diffuse = recurrence=20 in a patient with recurrent malignant glioma treated = with=20 bevacizumab and irinotecan

Post-gadolinium T1-weighted (A) and FLAIR (D) MRI = scans=20 before treatment with bevacizumab and irinotecan. = After 6=20 weeks of treatment, there is reduction in the size and = intensity of enhancement sufficient to achieve a = partial=20 response (B). Abnormal FLAIR hyperintensity is = proportionately=20 reduced (E). After 6 months of treatment with = bevacizumab and=20 irinotecan, there has been further reduction in = enhancement=20 (C), yet the extent of abnormal FLAIR hyperintensity = has=20 increased markedly, suggesting nonenhancing tumor = infiltration=20 (F). =

 = ;

In addition, quantitative volumetric analysis using = off-line=20 post-processing software (ITK-Snap) was performed under = the=20 supervision of the principal neuroradiologist by manually=20 segmenting areas of abnormal enhancement and FLAIR=20 hyperintensity. Cystic and necrotic portions of tumor = were=20 excluded, and regions of heterogeneous enhancement = considered=20 likely to be tumor were included in the segmentation = volumes.=20 Total volumes were calculated by multiplying voxel size = by the=20 number of pixels in the segmented region of interest = using=20 MRIcro and MATLAB software to produce estimates of = total volume=20 of abnormal enhancement and FLAIR hyperintensity. =

In order to quantitatively assess the hypothesis that = bevacizumab=20 alters the pattern of recurrence, we calculated a relative=20 nonenhancing tumor ratio (rNTR), defined as the ratio = of the=20 volume of abnormal FLAIR hyperintensity (infiltrative = tumor) to=20 the volume of abnormal gadolinium enhancement for each = patient=20 in the control and bevacizumab groups. rNTR = calculations were=20 based on the progression MRI available for each = patient. We=20 also calculated a relative FLAIR progression ratio = (rFPR),=20 defined as the ratio of the volume of abnormal FLAIR=20 hyperintensity at the time of progression to the volume = of=20 abnormal FLAIR hyperintensity on the baseline study. = Wilcoxon=20 two-sample tests were used to evaluate the significance = of rNTR=20 and rFPR differences between the following patient groups, = as=20 defined by consensus interpretations using Macdonald = Criteria:=20 bevacizumab responders, bevacizumab nonresponders, control=20 responders, and control nonresponders. Single-tailed = tests were=20 used because the chief study hypothesis predicted the = direction=20 of rNTR and rFPR differences.


  =20 RESULTS
Top.
Abstract.
METHODS
3D"RESULTS
DISCUSSION
REFERENCES
 
<= EM>Patient=20 population. We studied 55 patients (32 men, 23 women) (table=20 1). Thirty-three had GBM, 21 had AG, and 1 had a = high-grade=20 glioma. Median age was 50 years (range 23 to 71), and = median=20 Karnofsky Performance Status (KPS) was 80 (range 50 to = 100).=20 The median number of prior chemotherapy treatments was = 2 (range=20 0 to 6). Fourteen patients had prior therapy with=20 anti-angiogenic agents including thalidomide, = lenalidomide,=20 imatinib, enzastaurin, sorafenib, or AZD2171. Median = follow-up=20 time was 27.6 weeks.


View this=20 table:
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  		Table 1 Patient=20 characteristics =

 = ;

Response assessment. One patient (2.3%) achieved CR. A = total=20 of 31.8% of patients achieved PR and 29.5% MR. A total = of 29.5%=20 had stable disease. Only 3 patients (6.8%) had = progressive=20 disease at the first follow-up MRI. The median time to=20 radiographic progression was 19.3 weeks. Overall 6M-PFS = was 39%=20 and 6M-OS 65%. Median PFS was 23.9 weeks (95% CI: 17.7, = 28.3=20 weeks) and median OS 35.7 weeks (95% CI: 27.7, 61.4 = weeks). For=20 GBM patients, 6M-PFS was 42% and for AG patients 32% = (p=20 =3D 0.81). Among patients who achieved radiographic = response,=20 6M-PFS was 52%. For nonresponders, 6M-PFS was 19% = (p =3D=20 0.11). Patients who had been previously treated with=20 anti-angiogenic therapies had a 6M-PFS of 40%, while patients = who had received only cytotoxic chemotherapy had a 6M-PFS = of=20 39% (p =3D 0.89). With bevacizumab treatment, steroid = dose=20 decreased in 33% of patients, remained stable in 53%, = and=20 increased in 14%.

Treatment at progression. In 23 patients who = progressed on=20 their initial therapy, bevacizumab was continued and = the=20 concurrent chemotherapy agent changed. In 17 cases, = irinotecan=20 was changed to carboplatin. In one case each, = irinotecan was=20 changed to etoposide, lomustine, or carmustine. = Carboplatin was=20 changed to erlotinib in one case and to etoposide in = another.=20 In a single case, carmustine was changed to irinotecan. = In=20 seven cases, the chemotherapy agent was changed a second = time,=20 and in two cases, a third time. Third and fourth line=20 chemotherapy options included carmustine, lomustine,=20 carboplatin, etoposide, temozolomide, and erlotinib = with either=20 carboplatin or sirolimus. In no case did the change = from one=20 chemotherapy agent to another produce a radiographic = response.=20 Among the 23 patients whose chemotherapy was changed = while the=20 patients remained on bevacizumab, the median time to=20 radiographic progression was only 7 weeks. However, in = 2 cases,=20 patients achieved prolonged clinical stability after a = change=20 in the chemotherapy agent. One patient who was changed = from=20 irinotecan to carboplatin and then temozolomide was = stable for=20 31 weeks from the time of the first chemotherapy = change.=20 Another patient who was changed from irinotecan to = carmustine=20 and then carboplatin was stable for 20 weeks. In both = cases,=20 chemotherapy was changed because the clinician detected = possible radiographic progression at the point of care. = On=20 quantitative review, no radiographic progression had=20 occurred.

Anticoagulation and bevacizumab. Eleven patients = received=20 anticoagulation during treatment with bevacizumab for = venous=20 thromboembolic disease. Most patients received = low-molecular=20 weight heparin. One patient who developed = heparin-induced=20 thrombocytopenia received fondaparinux, and one patient = who had=20 a pulmonary embolism before initiating bevacizumab = therapy=20 received warfarin. Apart from one patient who had epistaxis, = no=20 bleeding was observed among the anticoagulated patients. =

Toxicity. Common adverse effects such as bone marrow=20 suppression and nausea were attributable to the = concurrently=20 administered chemotherapy agent rather than to = bevacizumab (table=20 2). Fatigue was frequently reported as well. Nine = patients=20 experienced hemorrhage, and all of these events were = Grade 1 or=20 2, primarily epistaxis or other mucosal bleeding. Two = patients=20 developed asymptomatic brain hemorrhages that were = detected on=20 routine neuroimaging. One patient experienced = spontaneous Grade=20 4 colon perforation that necessitated emergent surgery. = Grade 1=20 proteinuria was detected in a single patient. Five = Grade 3 or 4=20 thromboembolic complications occurred. Four patients = were found=20 to have pulmonary emboli, and one developed a superior=20 mesenteric vein thrombosis. There were two cases of = impaired=20 craniotomy wound healing.


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  		Table 2 Adverse = effects=20 attributed to bevacizumab =

 = ;

Progression patterns. Blind reading and Macdonald = Criteria=20 measurements of 26 bevacizumab-treated patients = demonstrated 16=20 local recurrences, 4 diffuse recurrences, and 4 distant = recurrences (table=20 3). The remaining 2 patients did not have = radiographic=20 evidence of progression at the time of publication. = Among the=20 19 control patients, 13 experienced local recurrence, 3 = diffuse, and one distant. Two patients did not = experience=20 radiographic progression. The likelihood of diffuse or = distant=20 recurrence was higher in bevacizumab-treated patients = than in=20 controls (31% vs 21%, p =3D 0.48). The majority of = diffuse=20 or distant recurrences in bevacizumab-treated patients = (6/8,=20 75%) occurred in subjects who achieved at least a minor=20 radiographic response.


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  		Table 3 Recurrence = patterns=20 as a function of treatment group =

 = ;

Volumetric analysis. The average rNTR was higher in = the=20 bevacizumab group than the control group (5.3 vs 4.7, = p=20 =3D 0.10). The rNTR was also higher among bevacizumab = responders=20 than bevacizumab nonresponders (7.1 vs 2.4, p = =3D 0.02; figure=20 4) and higher among bevacizumab responders than=20 conventional chemotherapy responders (7.1 vs 3.5, = p =3D=20 0.48). A small subgroup (3 of 26) of the bevacizumab = responders=20 had strikingly elevated rNTR of greater than 20 (23.8, = 22.1,=20 3D{infty}).=20 A single control patient had an rNTR greater than 10 = (18.3),=20 but no conventional chemotherapy patient or bevacizumab=20 nonresponder had an rNTR greater than 20. rFPR values were=20 similar for the bevacizumab and control groups (1.9 vs = 2.1,=20 p =3D 0.43) and for bevacizumab responders and=20 nonresponders (1.8 vs 1.9, p =3D 0.08). =



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  		Figure 4 Relative=20 nonenhancing tumor ratio (rNTR) and relative = fluid-attenuated=20 inversion recovery (FLAIR) progression ratio (rFPR) = for=20 bevacizumab-treated patients

rNTR, defined as the ratio of the volume of = abnormal FLAIR=20 hyperintensity to the volume of abnormal gadolinium=20 enhancement, is greater among radiographic responders = than=20 nonresponders (*p =3D 0.02). rFPR, defined as = the ratio=20 of the abnormal FLAIR hyperintensity volume at the = time of=20 progression to the abnormal FLAIR hyperintensity = volume on the=20 baseline MRI, does not differ based on radiographic = response. =

 = ;


  =20 DISCUSSION
Top.
Abstract.
METHODS
RESULTS
3D"DISCUSSION
REFERENCES
 
T= hese=20 data confirm that combination therapy with bevacizumab = and=20 chemotherapy is active against recurrent malignant gliomas,=20 even in the setting of extensive pretreatment. Because the=20 prognosis associated with recurrent malignant gliomas = is=20 exceedingly poor, a treatment that produces disease=20 stabilization may provide substantial benefit. We found = a=20 radiographic response rate of 34.1% (CR + PR) and a=20 radiographic disease control rate (CR + PR + MR + = stable=20 disease) of 93.2%. This compares favorably to = historical data=20 from 375 patients with recurrent malignant gliomas = enrolled in=20 phase II clinical trials in which radiographic response = rate=20 was 14% and the radiographic disease control rate was=20 39%.4=20 The patients in this study were heavily pretreated = (median of 2=20 prior therapies; range 0 to 6), and 14 patients had = received=20 previous treatment with anti-angiogenic therapies.=20 Additionally, patients had a KPS score as low as 50, which=20 would have excluded them from most malignant glioma = clinical=20 trials. Despite these factors, our data are comparable = to=20 results from a recent phase II clinical trial of = bevacizumab=20 with irinotecan chemotherapy for recurrent malignant = glioma=20 which found a radiographic response rate of 63% and = 6M-PFS of=20 38%.18=20

At recurrence, continuing bevacizumab and changing the=20 chemotherapy agent provided long-term disease control = only in 2=20 patients (9.5%) who remained progression-free for 20 to = 31=20 weeks. In these patients, however, the PFS was longer = than is=20 typically observed in patients with recurrent malignant = gliomas. This suggests a possible synergistic effect = between=20 chemotherapy and bevacizumab that may be specific to = the=20 chemotherapy agent. At present, the optimal = chemotherapy agent=20 to combine with bevacizumab is unclear. A recently = completed=20 multicenter randomized phase II trial of bevacizumab = with or=20 without irinotecan for recurrent malignant gliomas will = determine whether the combination is more effective = than=20 bevacizumab alone.

Overall, bevacizumab therapy was well-tolerated. Most side = effects=20 were attributable to the concurrently administered = chemotherapy=20 agent. The extent to which bevacizumab contributed to = fatigue=20 is difficult to determine because fatigue is common among=20 patients with malignant gliomas. Despite concerns about = serious=20 or life-threatening bleeding in patients treated with=20 bevacizumab,26=20 we observed only minor hemorrhages. Two patients = experienced=20 asymptomatic intratumoral hemorrhages that were = detected on=20 routine MRI scans. Bleeding was not problematic among = 11=20 patients who received anticoagulant medications, which = suggests=20 that such medications may be used safely in patients = with=20 malignant gliomas during bevacizumab therapy. Five=20 thromboembolic complications occurred during therapy. = Because=20 patients with malignant gliomas are at high risk for=20 thromboembolism regardless of therapy,27=20 the additional risk conferred by bevacizumab is = unclear.=20

An important advantage of bevacizumab may be its ability = to=20 decrease peritumoral edema and function as a=20 corticosteroid-sparing agent. In this study, 33% of = patients=20 had reduction in their steroid dose after receiving=20 bevacizumab, potentially reducing steroid-related=20 complications. Our findings are consistent with the = results of=20 a recent phase II trial of AZD2171, an oral pan VEGF = receptor=20 tyrosine kinase inhibitor, for recurrent GBM. AZD2171 = treatment=20 resulted in a rapid and sustained anti-edema effect = that was=20 associated with reduced steroid dose in 11 of 11=20 patients.19=20

Preclinical data suggest that glioma cells may co-opt = existing=20 cerebral vasculature as an alternative to = angiogenesis.6=20 This mechanism appears to be particularly important = when=20 VEGF-mediated angiogenesis is blocked. In a murine = model,=20 treatment with the VEGF receptor antibody DC101 = promoted=20 satellite tumor formation with invasion along cerebral = blood=20 vessels.23=20 Similar findings have been observed in rat gliomas = treated with=20 an anti-VEGF antibody.24=20 If this phenomenon occurs in humans, it could represent = an=20 important limitation to anti-angiogenic therapy.28=20 In patients who have been treated with bevacizumab and=20 chemotherapy, we have observed cases in which the = volume and=20 intensity of contrast enhancement remain nearly stable = while=20 the volume and degree of abnormal FLAIR hyperintensity = increase=20 substantially (figure=20 3). In this study we were unable to demonstrate a=20 significant difference in the pattern of recurrence = between=20 bevacizumab-treated and control patients, although = there was a=20 trend toward more diffuse or distant recurrences in the = bevacizumab group, particularly among subjects who = achieved at=20 least a minor radiographic response. The failure to = detect a=20 difference in recurrence patterns between the two = groups may be=20 due in part to the relatively small number of patients = in this=20 study. In addition, abnormal FLAIR hyperintensity may = reflect=20 not only infiltrating tumor, but also peritumoral = edema.29=20 Since bevacizumab reduces peritumoral edema, abnormal = FLAIR=20 hyperintensity in the bevacizumab-treated group may primarily = reflect infiltrating tumor, while abnormal FLAIR = hyperintensity=20 in the chemotherapy-treated group likely reflects a = combination=20 of infiltrating tumor and peritumoral edema. This = phenomenon=20 may have reduced the difference in abnormal FLAIR=20 hyperintensity between the groups. Definitive = differentiation=20 between infiltrating tumor, edema, gliosis, and other = causes of=20 abnormal FLAIR hyperintensity such as treatment-related = leukoencephalopathy in bevacizumab-treated patients = will=20 require histopathologic analysis that may only be = possible in=20 an autopsy study. However, because increased abnormal = FLAIR=20 hyperintensity after bevacizumab treatment is often = associated=20 with clinical worsening that is not highly = steroid-responsive,=20 it most likely reflects infiltrating tumor. It is also = possible=20 that the addition of chemotherapy to the = bevacizumab-treated=20 group may have reduced the extent of tumor = infiltration. The=20 difference between the two groups may have been more = evident if=20 bevacizumab alone was used in the treatment group. =

A quantitative volumetric analysis was used to calculate = rNTR=20 and rFPR for patients in both groups. Although there was = not=20 a significant difference between rNTR values for all=20 bevacizumab-treated and control patients, a trend = toward=20 increased rNTR in bevacizumab-treated patients was = detected.=20 This suggests that there may be a greater relative = volume of=20 nonenhancing tumor in bevacizumab-treated patients.=20 Intriguingly, the rNTR was significantly greater in = bevacizumab=20 responders than nonresponders, and there was a trend = toward=20 elevated rNTR in bevacizumab responders compared to control=20 responders.

The observation that rNTR is higher among bevacizumab = responders=20 than nonresponders or control responders raises the = possibility=20 that bevacizumab's pro-invasion effect is directly related = to=20 its anti-angiogenic effect. The absence of a measurable=20 difference in the rFPR data between bevacizumab = responders and=20 nonresponders implies that nonenhancing, infiltrative = tumor=20 progresses at a similar rate in the two groups. = Therefore, the=20 difference in rNTR between the bevacizumab responders = and=20 nonresponders is likely due to differences in the = volume of=20 abnormal gadolinium enhancement (ratio denominator). = Taken=20 together, our results suggest that the apparent = promotion of=20 diffuse recurrence by bevacizumab therapy represents a=20 combination of increased suppression of local enhancing = tumor=20 recurrence with decreased suppression of nonenhancing,=20 infiltrative tumor progression. An alternative = explanation is=20 that bevacizumab therapy results in a significant = reduction in=20 tumor capillary permeability without producing a true=20 anti-tumor effect. By this mechanism, enhancing tumor = on MRI=20 scans could be converted into nonenhancing tumor, thus = giving=20 the false impression of increased infiltrative tumor.=20 Ktrans is a surrogate marker of vascular = permeability=20 that can be obtained from dynamic contrast-enhanced = MRI. In a=20 recent study, AZD2171 treatment resulted in prolonged=20 Ktrans suppression.19=20 Though anti-angiogenic therapies produce dramatic = radiographic=20 changes in malignant glioma patients, a definitive=20 demonstration of potent anti-tumor efficacy remains to = be=20 published. Larger, prospective studies are needed to = address=20 this issue.

It is intriguing that a small number of bevacizumab = responders=20 (3/16, 18.8%) had markedly elevated rNTR, substantially = greater=20 than other patients in the study. These patients may be = members=20 of a distinct subgroup of patients with malignant glioma = who=20 are at high risk for nonenhancing tumor progression during=20 anti-angiogenic therapy. Correlation with tumor = genotypes may=20 identify a molecular substrate that explains this = observation.=20 Such correlations are critically important in that they = may=20 elucidate novel therapeutic targets and suggest = genotypic=20 subgroups that warrant anti-invasion or other specific=20 therapies.

Our study was limited by small patient numbers and by its=20 retrospective nature. Additionally, some of the = patients had=20 received previous anti-angiogenic therapy. This may = have=20 reduced the likelihood of detecting increased invasion = during=20 bevacizumab therapy since tumor cells in these patients = may=20 have assumed a maximally invasive phenotype prior to = initiation=20 of bevacizumab. Even without previous exposure to=20 anti-angiogenic therapy, gliomas become increasingly=20 infiltrative with more advanced stages of disease.30=20 In addition, segmentation of nonenhancing signal = abnormality on=20 FLAIR MRI sequences is challenging because the = distinction=20 between normal brain tissue and areas of abnormal FLAIR = hyperintensity may be subtle, and threshold and = window-level=20 selection are subjective. Since scans were reviewed in = a=20 blinded fashion that eliminates any systematic bias, = this seems=20 unlikely to account for our results. The failure to = detect a=20 significant difference between all patients treated = with=20 bevacizumab and all patients treated with conventional=20 chemotherapy is likely due to small sample size with = dilution=20 of the effect observed in responders by inclusion of=20 nonresponders. A larger, prospective volumetric MRI study = of=20 progression patterns with histopathologic correlation in=20 bevacizumab-treated patients with malignant gliomas is=20 indicated.

*These authors contributed = equally to this=20 work.

Supported by the Amos E. Wasgatt Brain Tumor Research = Fund.

Disclosure: P.Y. Wen receives research support from=20 Genentech, Inc. The other authors report no conflicts = of=20 interest.

Received July 2, 2007. Accepted in final form September = 18,=20 2007.


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A. K. = Lucio-Eterovic, Y. Piao,=20 and J. F. de Groot
Mediators of Glioblastoma = Resistance=20 and Invasion during Antivascular Endothelial Growth Factor=20 Therapy
Clin. Cancer Res., = July 15, 2009;=20 15(14): 4589 - 4599.
[Abstract]=20 [Full=20 Text] [PD= F]=20
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Recurrent=20 Glioblastoma Multiforme: ADC Histogram Analysis Predicts = Response to=20 Bevacizumab Treatment1
Radiology,=20 July 1, 2009; 252(1): 182 - 189.
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M. J. van den Bent, = M. A.=20 Vogelbaum, P. Y. Wen, D. R. Macdonald, and S. M.=20 Chang
End Point Assessment in Gliomas: Novel = Treatments=20 Limit Usefulness of Classical Macdonald's = Criteria
J.=20 Clin. Oncol., June 20, 2009; 27(18): 2905 - 2908. =
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Y. Piao, L. Lu, and = J. de=20 Groot
AMPA receptors promote perivascular glioma = invasion=20 via {beta}1 integrin-dependent adhesion to the extracellular = matrix
Neuro Oncology, June 1, 2009; = 11(3):=20 260 - 273.
[Abstract]=20 [Full=20 Text] [P= DF]=20
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Angiogenesis as a=20 Therapeutic Target in Malignant = Gliomas
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[Abstract]=20 [Full=20 Text] [PDF= ]=20
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W. S. Kamoun, C. D. = Ley, C. T.=20 Farrar, A. M. Duyverman, J. Lahdenranta, D. A. Lacorre, T. = T.=20 Batchelor, E. di Tomaso, D. G. Duda, L. L. Munn, et=20 al.
Edema Control by Cediranib, a Vascular=20 Endothelial Growth Factor Receptor-Targeted Kinase = Inhibitor,=20 Prolongs Survival Despite Persistent Brain Tumor Growth in=20 Mice
J. Clin. Oncol., May 20, 2009; = 27(15):=20 2542 - 2552.
[Abstrac= t]=20 [Full=20 Text] [PDF]=20
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Bevacizumab and irinotecan for recurrent = oligodendroglial tumors
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[Abstra= ct]=20 [Full=20 Text] [PDF]=20
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K. Jahnke, L. L. = Muldoon, C. G.=20 Varallyay, S. J. Lewin, D. F. Kraemer, and E. A.=20 Neuwelt
Bevacizumab and carboplatin increase = survival and=20 asymptomatic tumor volume in a glioma = model
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[Abstract]=20 [Full=20 Text] [P= DF]=20
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M. C. Chamberlain, = M. M.=20 Mrugala, A. D. Norden, G. S. Young, and P. Y.=20 Wen
BEVACIZUMAB FOR RECURRENT MALIGNANT GLIOMAS:=20 EFFICACY, TOXICITY, AND PATTERNS OF=20 RECURRENCE
Neurology, = February 24, 2009;=20 72(8): 772 - 774.
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3D""=20=20 		3D""=20
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Dasatinib-induced = autophagy is=20 enhanced in combination with temozolomide in = glioma
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W. K. A. = Yung
Moving=20 Toward the Next Steps in Angiogenesis = Therapy?
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J. Ma and D. J.=20 Waxman
Combination of antiangiogenesis with = chemotherapy=20 for more effective cancer treatment
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D. H. Garfield and = A.=20 Hercbergs
Fewer Dollars, More = Sense
J. Clin.=20 Oncol., November 10, 2008; 26(32): 5304 - 5305. =
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E. S. Paulson and = K. M.=20 Schmainda
Comparison of Dynamic = Susceptibility-weighted=20 Contrast-enhanced MR Methods: Recommendations for Measuring = Relative=20 Cerebral Blood Volume in Brain Tumors
Radiology, = November 1, 2008; 249(2): 601 - 613.
[Ab= stract]=20 [Full=20 Text] [PDF]=20
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M. Weller and W. K. = A.=20 Yung
Bevacizumab -- News from the Fast=20 Lane?
Neuro Oncology, October 1, 2008; = 10(5):=20 647 - 647.
[Full=20 Text] [P= DF]=20
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W. B. Pope, J. H. = Chen, J.=20 Dong, M. R. J. Carlson, A. Perlina, T. F. Cloughesy, L. M. = Liau, P.=20 S. Mischel, P. Nghiemphu, A. Lai, et=20 al.
Relationship between Gene Expression and = Enhancement in Glioblastoma Multiforme: Exploratory DNA = Microarray=20 Analysis
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[Abstract]=20 [Full=20 Text] [PDF]=20
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L. W Buie and J.=20 Valgus
Bevacizumab: A Treatment Option for = Recurrent=20 Glioblastoma Multiforme
Ann. Pharmacother.,=20 October 1, 2008; 42(10): 1486 - 1490.
[Abstra= ct]=20 [Full=20 Text] [PDF]=20
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A. Idbaih, F. = Ducray, M. Sierra=20 Del Rio, K. Hoang-Xuan, and J.-Y. = Delattre
Therapeutic=20 Application of Noncytotoxic Molecular Targeted Therapy in = Gliomas:=20 Growth Factor Receptors and Angiogenesis=20 Inhibitors
Oncologist, = September 1, 2008;=20 13(9): 978 - 992.
[Abstract]=20 [Full=20 Text] [PDF= ]=20
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New Brain = Tumor=20 Therapies, New Recurrence Patterns
Journal Watch = Neurology, May 6, 2008; 2008(506): 1 - 1.
[Full=20 Text]
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E. T. Wong and S.=20 Brem
Antiangiogenesis Treatment for Glioblastoma=20 Multiforme: Challenges and Opportunities
J Natl = Compr=20 Canc Netw, May 1, 2008; 6(5): 515 - 522.
[Abstract]=20 [PDF]=20
3D""=20=20 		3D""=20

Correspondence:

Read = all Correspondence

Bevacizumab for recurrent malignant gliomas: = Efficacy,=20 toxicity, and patterns of recurrence=20
Marc C. Chamberlain=20
Neurology Online, 4 Jun 2008 [Full=20 text]=20
Bevacizumab for recurrent malignant gliomas: = Efficacy,=20 toxicity, and patterns of recurrence=20
Maciej M. Mrugala=20
Neurology Online, 4 Jun 2008 [Full=20 text]=20
Reply from the Authors=20
Andrew D Norden, et al.=20
Neurology Online, 4 Jun 2008 [Full=20 text]

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Verdana, Geneva, sans-serif } #LeftNavigation UL { PADDING-LEFT: 20px; LIST-STYLE-IMAGE: = url(../images/Left_Column_Bullet.gif); MARGIN: 5px 0px 15px } #LeftNavigation UL LI.active { LIST-STYLE-IMAGE: url(../images/Left_Column_Bullet_Active.gif) } #LeftNavigation UL LI:hover { LIST-STYLE-IMAGE: url(../images/Left_Column_Bullet_Active.gif) } #LeftNavigation UL LI A { COLOR: #000; TEXT-DECORATION: none } #LeftNavigation UL LI A:hover { TEXT-DECORATION: underline } #LeftNavigation UL.RSSFeeds { LIST-STYLE-IMAGE: url(../images/RSS_Bullet_Icon.gif) } #LeftNavigation UL.RSSFeeds LI.active { LIST-STYLE-IMAGE: url(../images/RSS_Bullet_Icon.gif) } #LeftNavigation UL.RSSFeeds LI:hover { LIST-STYLE-IMAGE: url(../images/RSS_Bullet_Icon.gif) } #RedundantNavigation UL { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: = 0px; PADDING-TOP: 0px } #RedundantNavigation UL LI { PADDING-RIGHT: 5px; DISPLAY: inline; PADDING-LEFT: 5px; PADDING-BOTTOM: = 0px; PADDING-TOP: 0px } #AAN_Logo { RIGHT: 20px; BACKGROUND-IMAGE: url(../images/AAN_Logo.gif); WIDTH: = 147px; BOTTOM: 35px; POSITION: absolute; HEIGHT: 49px } #AAN_Logo IMG { DISPLAY: none } #AAN_Press_Logo { MARGIN-TOP: 20px; TEXT-ALIGN: center } #AAN_Link { FONT-SIZE: 10px; RIGHT: 20px; MARGIN-LEFT: 34px; COLOR: #fff; POSITION: = absolute; TOP: 55px } #AAN_Link A { COLOR: #fff } #SiteCopyright { MARGIN-TOP: 10px } #SiteCredits { MARGIN-TOP: 20px } #AdSpaceTop { MARGIN-BOTTOM: 10px; WIDTH: 880px; TEXT-ALIGN: center } #AdSpaceTop .advertisement { MARGIN: 0px auto; WIDTH: 560px; HEIGHT: 60px } #AdSpaceRight { PADDING-LEFT: 10px; FLOAT: right; PADDING-TOP: 0px; HEIGHT: auto; = TEXT-ALIGN: center } #AdSpaceRight .advertisement { MARGIN-BOTTOM: 20px; WIDTH: 120px; HEIGHT: 325px } } #SiteCloumnCenter TABLE TD { WHITE-SPACE: normal } TABLE#search-results-table { WIDTH: 880px } TABLE#search-results-table TABLE { WIDTH: 100% } @media Print =20 { .noprint { DISPLAY: none } #UserIdentity { DISPLAY: none } #AdSpaceTop { DISPLAY: none } #AdSpaceRight { DISPLAY: none } #QuickSearch { DISPLAY: none } #subline { DISPLAY: none } #MainNavigation { DISPLAY: none } #RedundantNavigation { DISPLAY: none } TD#SiteCloumnLeft { DISPLAY: none } BODY { FONT-SIZE: 10pt } #MainSiteHeader { MARGIN-BOTTOM: 24pt } #SiteTitle { FONT-SIZE: 24pt; FONT-STYLE: italic; FONT-FAMILY: "Times New Roman", = Georgia, Times, serif } #SiteTitle SUP { FONT-SIZE: 12pt } #SiteTagline { MARGIN-TOP: 4pt; FONT-SIZE: 6pt; TEXT-TRANSFORM: uppercase; WIDTH: = 200pt; COLOR: #999 } #AAN_Logo { FLOAT: right } #AAN_Logo IMG { WIDTH: 1.5in; HEIGHT: 0.5in } #AAN_Link { DISPLAY: none; FONT-SIZE: 10px } TD#SiteCloumnCenter { VERTICAL-ALIGN: top; WIDTH: auto } TD#SiteCloumnRight { VERTICAL-ALIGN: top; WIDTH: 191px } DIV#SiteCloumnCenter { MARGIN-TOP: 10px; WIDTH: 100% } DIV#SiteCloumnRight { FONT-SIZE: 80%; MARGIN-LEFT: 10px; WIDTH: 181px } } ------=_NextPart_000_0000_01CB0E4F.7C61CAA0 Content-Type: application/octet-stream Content-Transfer-Encoding: quoted-printable Content-Location: http://www.neurology.org/master.js // JavaScript Document var QuickSearch =3D Object(); QuickSearch.FieldArray =3D Array(2); QuickSearch.FieldArray[0] =3D Array(); QuickSearch.FieldArray[0]['id'] =3D 'QuickSearchKeyword'; QuickSearch.FieldArray[0]['default'] =3D 'keyword'; QuickSearch.FieldArray[1] =3D Array(); QuickSearch.FieldArray[1]['id'] =3D 'QuickSearchAuthor'; QuickSearch.FieldArray[1]['default'] =3D 'author'; QuickSearch.FieldArray[2] =3D Array(); QuickSearch.FieldArray[2]['id'] =3D 'QuickSearchYear'; QuickSearch.FieldArray[2]['default'] =3D 'year'; QuickSearch.FieldArray[3] =3D Array(); QuickSearch.FieldArray[3]['id'] =3D 'QuickSearchVolume'; QuickSearch.FieldArray[3]['default'] =3D 'volume'; QuickSearch.FieldArray[4] =3D Array(); QuickSearch.FieldArray[4]['id'] =3D 'QuickSearchPage'; QuickSearch.FieldArray[4]['default'] =3D 'page'; QuickSearch.setDefaultText =3D function(field){ var elm =3D = document.getElementById(QuickSearch.FieldArray[field]['id']); elm.value =3D QuickSearch.FieldArray[field]['default']; elm.style.color =3D '#AAAAAA'; } QuickSearch.setEditorText =3D function(field){ var elm =3D = document.getElementById(QuickSearch.FieldArray[field]['id']); elm.value =3D ''; elm.style.color =3D '#333333'; } QuickSearch.focusEvent =3D function(field) { var elm =3D = document.getElementById(QuickSearch.FieldArray[field]['id']); if(elm.value =3D=3D QuickSearch.FieldArray[field]['default']){ QuickSearch.setEditorText(field); } } QuickSearch.blurEvent =3D function(field){ var elm =3D = document.getElementById(QuickSearch.FieldArray[field]['id']); if(elm.value =3D=3D QuickSearch.FieldArray[field]['default'] || = elm.value =3D=3D ''){ QuickSearch.setDefaultText(field); } } QuickSearch.loadEvent =3D function(){ for(var i=3D0; i.=0A= =0A= by Andrew Gregory=0A= http://www.scss.com.au/family/andrew/webdesign/xmlhttprequest/=0A= =0A= This work is licensed under the Creative Commons Attribution License. To = view a=0A= copy of this license, visit = http://creativecommons.org/licenses/by-sa/2.5/ or=0A= send a letter to Creative Commons, 559 Nathan Abbott Way, Stanford, = California=0A= 94305, USA.=0A= =0A= Attribution: Leave my name and web address in this script intact.=0A= =0A= Not Supported in Opera=0A= ----------------------=0A= * user/password authentication=0A= * responseXML data member=0A= =0A= Not Fully Supported in Opera=0A= ----------------------------=0A= * async requests=0A= * abort()=0A= * getAllResponseHeaders(), getAllResponseHeader(header)=0A= =0A= */=0A= // IE support=0A= if (window.ActiveXObject && !window.XMLHttpRequest) {=0A= window.XMLHttpRequest =3D function() {=0A= var msxmls =3D new Array(=0A= 'Msxml2.XMLHTTP.5.0',=0A= 'Msxml2.XMLHTTP.4.0',=0A= 'Msxml2.XMLHTTP.3.0',=0A= 'Msxml2.XMLHTTP',=0A= 'Microsoft.XMLHTTP');=0A= for (var i =3D 0; i < msxmls.length; i++) {=0A= try {=0A= return new ActiveXObject(msxmls[i]);=0A= } catch (e) {=0A= }=0A= }=0A= return null;=0A= };=0A= }=0A= // Gecko support=0A= /* ;-) */=0A= // Opera support=0A= if (window.opera && !window.XMLHttpRequest) {=0A= window.XMLHttpRequest =3D function() {=0A= this.readyState =3D 0; // = 0=3Duninitialized,1=3Dloading,2=3Dloaded,3=3Dinteractive,4=3Dcomplete=0A= this.status =3D 0; // HTTP status codes=0A= this.statusText =3D '';=0A= this._headers =3D [];=0A= this._aborted =3D false;=0A= this._async =3D true;=0A= this._defaultCharset =3D 'ISO-8859-1';=0A= this._getCharset =3D function() {=0A= var charset =3D _defaultCharset;=0A= var contentType =3D = this.getResponseHeader('Content-type').toUpperCase();=0A= val =3D contentType.indexOf('CHARSET=3D');=0A= if (val !=3D -1) {=0A= charset =3D contentType.substring(val);=0A= }=0A= val =3D charset.indexOf(';');=0A= if (val !=3D -1) {=0A= charset =3D charset.substring(0, val);=0A= }=0A= val =3D charset.indexOf(',');=0A= if (val !=3D -1) {=0A= charset =3D charset.substring(0, val);=0A= }=0A= return charset;=0A= };=0A= this.abort =3D function() {=0A= this._aborted =3D true;=0A= };=0A= this.getAllResponseHeaders =3D function() {=0A= return this.getAllResponseHeader('*');=0A= };=0A= this.getAllResponseHeader =3D function(header) {=0A= var ret =3D '';=0A= for (var i =3D 0; i < this._headers.length; i++) {=0A= if (header =3D=3D '*' || this._headers[i].h =3D=3D header) {=0A= ret +=3D this._headers[i].h + ': ' + this._headers[i].v + '\n';=0A= }=0A= }=0A= return ret;=0A= };=0A= this.getResponseHeader =3D function(header) {=0A= var ret =3D getAllResponseHeader(header);=0A= var i =3D ret.indexOf('\n');=0A= if (i !=3D -1) {=0A= ret =3D ret.substring(0, i);=0A= }=0A= return ret;=0A= };=0A= this.setRequestHeader =3D function(header, value) {=0A= this._headers[this._headers.length] =3D {h:header, v:value};=0A= };=0A= this.open =3D function(method, url, async, user, password) {=0A= this.method =3D method;=0A= this.url =3D url;=0A= this._async =3D true;=0A= this._aborted =3D false;=0A= this._headers =3D [];=0A= if (arguments.length >=3D 3) {=0A= this._async =3D async;=0A= }=0A= if (arguments.length > 3) {=0A= opera.postError('XMLHttpRequest.open() - user/password not = supported');=0A= }=0A= this.readyState =3D 1;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= };=0A= this.send =3D function(data) {=0A= if (!navigator.javaEnabled()) {=0A= alert("XMLHttpRequest.send() - Java must be installed and = enabled.");=0A= return;=0A= }=0A= if (this._async) {=0A= setTimeout(this._sendasync, 0, this, data);=0A= // this is not really asynchronous and won't execute until the = current=0A= // execution context ends=0A= } else {=0A= this._sendsync(data);=0A= }=0A= }=0A= this._sendasync =3D function(req, data) {=0A= if (!req._aborted) {=0A= req._sendsync(data);=0A= }=0A= };=0A= this._sendsync =3D function(data) {=0A= this.readyState =3D 2;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= // open connection=0A= var url =3D new java.net.URL(new = java.net.URL(window.location.href), this.url);=0A= var conn =3D url.openConnection();=0A= for (var i =3D 0; i < this._headers.length; i++) {=0A= conn.setRequestProperty(this._headers[i].h, this._headers[i].v);=0A= }=0A= this._headers =3D [];=0A= if (this.method =3D=3D 'POST') {=0A= // POST data=0A= conn.setDoOutput(true);=0A= var wr =3D new = java.io.OutputStreamWriter(conn.getOutputStream(), this._getCharset());=0A= wr.write(data);=0A= wr.flush();=0A= wr.close();=0A= }=0A= // read response headers=0A= // NOTE: the getHeaderField() methods always return nulls for me :(=0A= var gotContentEncoding =3D false;=0A= var gotContentLength =3D false;=0A= var gotContentType =3D false;=0A= var gotDate =3D false;=0A= var gotExpiration =3D false;=0A= var gotLastModified =3D false;=0A= for (var i =3D 0; ; i++) {=0A= var hdrName =3D conn.getHeaderFieldKey(i);=0A= var hdrValue =3D conn.getHeaderField(i);=0A= if (hdrName =3D=3D null && hdrValue =3D=3D null) {=0A= break;=0A= }=0A= if (hdrName !=3D null) {=0A= this._headers[this._headers.length] =3D {h:hdrName, = v:hdrValue};=0A= switch (hdrName.toLowerCase()) {=0A= case 'content-encoding': gotContentEncoding =3D true; break;=0A= case 'content-length' : gotContentLength =3D true; break;=0A= case 'content-type' : gotContentType =3D true; break;=0A= case 'date' : gotDate =3D true; break;=0A= case 'expires' : gotExpiration =3D true; break;=0A= case 'last-modified' : gotLastModified =3D true; break;=0A= }=0A= }=0A= }=0A= // try to fill in any missing header information=0A= var val;=0A= val =3D conn.getContentEncoding();=0A= if (val !=3D null && !gotContentEncoding) = this._headers[this._headers.length] =3D {h:'Content-encoding', v:val};=0A= val =3D conn.getContentLength();=0A= if (val !=3D -1 && !gotContentLength) = this._headers[this._headers.length] =3D {h:'Content-length', v:val};=0A= val =3D conn.getContentType();=0A= if (val !=3D null && !gotContentType) = this._headers[this._headers.length] =3D {h:'Content-type', v:val};=0A= val =3D conn.getDate();=0A= if (val !=3D 0 && !gotDate) this._headers[this._headers.length] = =3D {h:'Date', v:(new Date(val)).toUTCString()};=0A= val =3D conn.getExpiration();=0A= if (val !=3D 0 && !gotExpiration) = this._headers[this._headers.length] =3D {h:'Expires', v:(new = Date(val)).toUTCString()};=0A= val =3D conn.getLastModified();=0A= if (val !=3D 0 && !gotLastModified) = this._headers[this._headers.length] =3D {h:'Last-modified', v:(new = Date(val)).toUTCString()};=0A= // read response data=0A= var reqdata =3D '';=0A= var stream =3D conn.getInputStream();=0A= if (stream) {=0A= var reader =3D new java.io.BufferedReader(new = java.io.InputStreamReader(stream, this._getCharset()));=0A= var line;=0A= while ((line =3D reader.readLine()) !=3D null) {=0A= if (this.readyState =3D=3D 2) {=0A= this.readyState =3D 3;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= }=0A= reqdata +=3D line + '\n';=0A= }=0A= reader.close();=0A= this.status =3D 200;=0A= this.statusText =3D 'OK';=0A= this.responseText =3D reqdata;=0A= this.readyState =3D 4;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= if (this.onload) {=0A= this.onload();=0A= }=0A= } else {=0A= // error=0A= this.status =3D 404;=0A= this.statusText =3D 'Not Found';=0A= this.responseText =3D '';=0A= this.readyState =3D 4;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= if (this.onerror) {=0A= this.onerror();=0A= }=0A= }=0A= };=0A= };=0A= }=0A= // ActiveXObject emulation=0A= if (!window.ActiveXObject && window.XMLHttpRequest) {=0A= window.ActiveXObject =3D function(type) {=0A= switch (type.toLowerCase()) {=0A= case 'microsoft.xmlhttp':=0A= case 'msxml2.xmlhttp':=0A= case 'msxml2.xmlhttp.3.0':=0A= case 'msxml2.xmlhttp.4.0':=0A= case 'msxml2.xmlhttp.5.0':=0A= return new XMLHttpRequest();=0A= }=0A= return null;=0A= };=0A= }=0A= ------=_NextPart_000_0000_01CB0E4F.7C61CAA0 Content-Type: application/octet-stream Content-Transfer-Encoding: quoted-printable Content-Location: http://www.neurology.org/javascript/ajax/utility.js /************************************************************************= *****=0A= * javascript/ajax/utility.js=0A= *=0A= * Utility functions for working with XMLHttpRequest data.=0A= *=0A= * Copyright 2006 Board of Trustees of the Leland Stanford Junior = University.=0A= = *************************************************************************= ***/=0A= =0A= /*=0A= * Copy XML nodes into an HTMLElement. This effectively=0A= * clones XML markup which uses XHTML naming conventions=0A= * into an HTML DOM.=0A= */=0A= function copy_xml_to_html(src, dst) {=0A= if (src.nodeType =3D=3D 1) { /* Node.ELEMENT_NODE */=0A= var e =3D document.createElement(src.nodeName);=0A= for (var i =3D 0; i < src.childNodes.length; i++) {=0A= copy_xml_to_html(src.childNodes[i], e);=0A= }=0A= for (var i =3D 0; i < src.attributes.length; i++) {=0A= var n =3D src.attributes[i].name;=0A= var v =3D unescape_xml_string(src.attributes[i].value); =0A= e.setAttribute(n, v);=0A= if (n =3D=3D "class") {=0A= e.className =3D v;=0A= }=0A= else if (n =3D=3D "style") {=0A= set_css_style(v, e, "");=0A= }=0A= }=0A= dst.appendChild(e);=0A= }=0A= else if (src.nodeType =3D=3D 3) { /* Node.TEXT_NODE */=0A= dst.appendChild(document.createTextNode(src.nodeValue));=0A= }=0A= }=0A= =0A= /* =0A= * It is unclear that this is the right thing to be calling=0A= * from copy_xml_to_html, but it appears that Safari decides=0A= * to convert & to the NCR #, and then encodes that=0A= * NCR to &%26%2338;. So, I'm going to treat the DOM Attr=0A= * value as a plain string, and run our XML string input=0A= * through the decoding routine below.=0A= */=0A= function unescape_xml_string(s) {=0A= return s.replace(/'/g, "'")=0A= .replace(/'/g, "'")=0A= .replace(/"/g, "\"")=0A= .replace(/"/g, "\"")=0A= .replace(/>/g, ">")=0A= .replace(/>/g, ">")=0A= .replace(/</g, "<")=0A= .replace(/</g, "<")=0A= .replace(/&/g, "&")=0A= .replace(/&/g, "&");=0A= }=0A= =0A= /*=0A= * Parse set of CSS rules and apply them to an element.=0A= * This is quite horrifying, but I'm unable to determine=0A= * how else to handle this with IE 6. FireFox and other=0A= * sane browsers let you simply set the style attribute=0A= * or use e.style.setProperty(rule, value, priority),=0A= * IE 6 appears to have neither of these capabilities..=0A= */=0A= function set_css_style(css, e, priority) {=0A= var rules =3D css.split(";");=0A= for (var i =3D 0; i < rules.length; i++) {=0A= var nvpair =3D rules[i].split(":");=0A= if (nvpair.length =3D=3D 2) {=0A= try {=0A= var name =3D nvpair[0]; /* style attribute */=0A= var value =3D nvpair[1]; /* attribute value */=0A= =0A= /*=0A= * For each possible style attribute, set the=0A= * appropriate style property in the element.=0A= */=0A= if (name =3D=3D "background") {=0A= e.style.background =3D value;=0A= }=0A= else if (name =3D=3D "background-attachment") {=0A= e.style.backgroundAttachment =3D value;=0A= }=0A= else if (name =3D=3D "background-color") {=0A= e.style.backgroundColor =3D value;=0A= }=0A= else if (name =3D=3D "background-image") {=0A= e.style.backgroundImage =3D value;=0A= }=0A= else 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quoted-printable Content-Location: http://www.neurology.org/javascript/entrez/callback.js /************************************************************************= *****=0A= * javascript/entrez/callback.js=0A= *=0A= * Entrez Linking callback to populate content box.=0A= *=0A= * Copyright 2006 Board of Trustees of the Leland Stanford Junior = University.=0A= = *************************************************************************= ***/=0A= =0A= /*=0A= * Execute callback to fill content box with Entrez Linking information.=0A= */=0A= function entrez_callback(pmid, callback_url) {=0A= /*=0A= * MSIE 5.5 and below have issues with the JavaScript=0A= * used for Entrez Linking. 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_rsEvent.arguments[1] = : _rsCG;=0A= (new Image(1,1)).src =3D _rsRecordFactory(_rsClickUrl, _rsNewCG);=0A= }=0A= =0A= function _rsLinkTrack(_rsClickUrl) {=0A= =0A= var _rsNewCG =3D _rsLinkTrack.arguments.length > 1 ? = _rsLinkTrack.arguments[1] : _rsCG;=0A= var _rsClickImg =3D new Image(1,1);=0A= _rsClickImg.src =3D _rsRecordFactory(_rsClickUrl, _rsNewCG);=0A= _rsPause(_rsTC);=0A= }=0A= =0A= var _rsClickDst;=0A= function _rsClick(_rsClickUrl) {=0A= var _rsNewCG =3D _rsClick.arguments.length > 1 ? = _rsClick.arguments[1] : _rsCG;=0A= var _rsClickImg =3D new Image(1,1);=0A= _rsClickImg.src =3D _rsRecordFactory(_rsClickUrl, _rsNewCG);=0A= _rsClickDst =3D _rsClickUrl;=0A= setTimeout("window.location =3D _rsClickDst", _rsTC);=0A= }=0A= =0A= function _rsVerInfo(str, ct) {=0A= var p =3D 0;=0A= var sp =3D 0;=0A= for(var i=3D0;i=3D0;i++) { sp=3Dp+1; p =3D str.indexOf('.', sp); = }=0A= if(p>0) {=0A= var v =3D str.substring(sp, p).match(/\d+$/);=0A= return v ? v : 0;=0A= } else {=0A= return 0;=0A= }=0A= }=0A= =0A= function _rsPluginDetect() {=0A= var _rsPlugins =3D [];=0A= var _rsMT =3D navigator.mimeTypes; // -1 indicates unknown=0A= if(_rsMT && _rsMT.length > 0) {=0A= var k;=0A= if(_rsPLfl=3D=3D1) {=0A= _rsPlugins['FL']=3D-1;=0A= k =3D 'application/x-shockwave-flash';=0A= if(_rsMT[k] && _rsMT[k].enabledPlugin) {=0A= _rsPlugins['FL'] =3D _rsVerInfo(_rsMT[k].enabledPlugin.description, = 1);=0A= }=0A= }=0A= if(_rsPLqt=3D=3D1) {=0A= _rsPlugins['QT']=3D-1;=0A= k =3D 'video/quicktime';=0A= if(_rsMT[k] && _rsMT[k].enabledPlugin) {=0A= _rsPlugins['QT'] =3D _rsVerInfo(_rsMT[k].enabledPlugin.name, 1);=0A= }=0A= }=0A= if(_rsPLre=3D=3D1) {=0A= _rsPlugins['RE']=3D-1;=0A= k =3D 'audio/x-pn-realaudio-plugin';=0A= if(_rsMT[k] && _rsMT[k].enabledPlugin) {=0A= _rsPlugins['RE'] =3D 0;=0A= }=0A= }=0A= if(_rsPLwm=3D=3D1) {=0A= _rsPlugins['QT']=3D-1;=0A= var rt =3D true;=0A= if(window.GeckoActiveXObject) {=0A= try {=0A= var p =3D new GeckoActiveXObject("WMPlayer.OCX.7");=0A= _rsPlugins['WM'] =3D _rsVerInfo(p.versionInfo, 1);=0A= rt =3D false;=0A= } catch(e) {}=0A= } =0A= if(rt) {=0A= k =3D 'application/x-mplayer2';=0A= if(_rsMT[k] && _rsMT[k].enabledPlugin) {=0A= _rsPlugins['WM'] =3D 0;=0A= }=0A= }=0A= =0A= }=0A= if(_rsPLjj=3D=3D1) {=0A= _rsPlugins['JJ']=3D-1;=0A= k =3D 'application/x-java-applet';=0A= if(_rsMT[k] && _rsMT[k].enabledPlugin) {=0A= var v =3D _rsVerInfo(_rsMT[k].enabledPlugin.description, 2);=0A= _rsPlugins['JJ'] =3D (v =3D=3D 0 ? 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= 'image' : 'text';=0A= _rsCLSendIt(_rsCU, _rsALink.href, _rsALink.tagName.toLowerCase(), = _rsName, _rsALink.innerHTML);=0A= }=0A= function _rsCLSendForm(_rsInput) {=0A= if(_rsInput.form =3D=3D undefined || _rsInput.form.action =3D=3D = undefined) {=0A= return;=0A= }=0A= =0A= if (_rsInput.type =3D=3D 'image') {=0A= var _rsValue =3D _rsInput.src;=0A= }=0A= else if (_rsInput.tagName =3D=3D 'BUTTON') {=0A= var _rsValue =3D = _rsInput.innerHTML.replace(/^\s+|\s+$/g, '').replace(/\s+/g, ' ');=0A= if (_rsValue =3D=3D "") _rsValue =3D _rsInput.value;=0A= }=0A= else {=0A= var _rsValue =3D _rsInput.value;=0A= }=0A= =0A= _rsCLSendIt(_rsCU, _rsInput.form.action, = _rsInput.form.tagName.toLowerCase(), _rsInput.type.toLowerCase(), = _rsValue);=0A= }=0A= function _rsCLCatchIt(e) {=0A= var _rsCurr =3D e ? e.target : window.event.srcElement;=0A= if ((_rsCurr.tagName =3D=3D 'INPUT' || _rsCurr.tagName =3D=3D 'BUTTON')=0A= && (_rsCurr.type =3D=3D 'image' || _rsCurr.type =3D=3D 'submit' || = _rsCurr.type =3D=3D 'button')) {=0A= _rsCLSendForm(_rsCurr);=0A= }=0A= else=0A= {=0A= do {=0A= if ((_rsCurr.tagName =3D=3D 'A') && (_rsCurr.href.length > 0)) {=0A= _rsCLSendALink(_rsCurr);=0A= break;=0A= }=0A= _rsCurr =3D _rsCurr.parentNode;=0A= } while (_rsCurr !=3D null && _rsCurr.tagName !=3D 'BODY')=0A= }=0A= }=0A= =0A= function _rsCLRegisterIt() {=0A= if(!document.getElementById) {=0A= return;=0A= }=0A= var _rsOld =3D document.body.onclick;=0A= if(_rsOld) {=0A= document.body.onclick =3D function (e) {=0A= _rsCLCatchIt(e);=0A= _rsOld(e);=0A= }=0A= }=0A= else {=0A= document.body.onclick =3D _rsCLCatchIt;=0A= }=0A= }=0A= =0A= // main=0A= if((_rsSE)&&(random() <=3D _rsSM)) {=0A= var _rsIM=3D'<\/scr'+'ipt>';=0A= document.write(_rsIM);=0A= }=0A= else {=0A= rsCi();=0A= }=0A= if(_rsCL=3D=3D1) {=0A= _rsCLRegisterIt();=0A= }=0A= ------=_NextPart_000_0000_01CB0E4F.7C61CAA0--