From: Subject: Relationship of glioblastoma multiforme to neural stem cell regions predicts invasive and multifocal tumor phenotype -- Lim et al. 9 (4): 424 -- Neuro-Oncology Date: Mon, 21 Jan 2008 19:49:04 +0100 MIME-Version: 1.0 Content-Type: multipart/related; type="text/html"; boundary="----=_NextPart_000_0011_01C85C66.AD46FF70" X-MimeOLE: Produced By Microsoft MimeOLE V6.00.2900.3198 This is a multi-part message in MIME format. ------=_NextPart_000_0011_01C85C66.AD46FF70 Content-Type: text/html; charset="iso-8859-1" Content-Transfer-Encoding: quoted-printable Content-Location: http://neuro-oncology.dukejournals.org/cgi/content/full/9/4/424? Relationship of glioblastoma multiforme to neural = stem cell regions predicts invasive and multifocal tumor phenotype -- = Lim et al. 9 (4): 424 -- Neuro-Oncology
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First published on=20 July 10, 2007
This version was = published on=20 October 1, 2007
Neuro Oncol 2007 9(4):424-429; = DOI:10.1215/15228517-2007-023=20
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Basic and Translational = Investigations

Relationship of glioblastoma multiforme to neural stem cell regions = predicts=20 invasive and multifocal tumor phenotype

Daniel = A.=20 Lim, Soonmee Cha, Mary C. Mayo, = Mei-Hsiu=20 Chen, Evren Keles, Scott VandenBerg and = Mitchel S. Berger

Departments of Neurological Surgery (D.A.L., S.C., = E.K.,=20 M.S.B.), Radiology (S.C., M.C.M., M.-H.C.), and Neuropathology (S.V.),=20 University of California, San Francisco, San Francisco, CA 94143, = USA=20

Address correspondence to Daniel A. Lim or Mitchel S. = Berger,=20 Department of Neurological Surgery, University of California, San = Francisco, 505=20 Parnassus St., M779, Box 0112, San Francisco, CA 94143, USA (limd{at}neurosurg.ucsf.edu or bergerm{at}neurosurg.ucsf.edu ).


3D"   =20 Abstract
Top
3D"Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
N= eural=20 stem cells with astrocyte-like characteristics exist in the = human=20 brain subventricular zone (SVZ), and these cells may give = rise to=20 glioblastoma multiforme (GBM). We therefore analyzed MRI = features of=20 GBMs in specific relation to the SVZ. We reviewed the = preoperative=20 and serial postoperative MR images of 53 patients with newly=20 diagnosed GBM. The spatial relationship of the = contrast-enhancing=20 lesion (CEL) with the SVZ and cortex was determined = preoperatively.=20 Classification was as follows: group I, CEL contacting SVZ = and=20 infiltrating cortex; group II, CEL contacting SVZ but not = involving=20 cortex; group III, CEL not contacting SVZ but involving = cortex; and=20 group IV, CEL neither contacting SVZ nor infiltrating cortex. = Patients with group I GBMs (n =3D 16) were most likely = to have=20 multifocal disease at diagnosis (9 patients, 56%, p = =3D 0.001).=20 In contrast, group IV GBMs (n =3D 14) were never = multifocal.=20 Group II (n =3D 14) and group III (n =3D 9) = GBMs were=20 multifocal in 11% and 29% of cases, respectively. Group I = GBMs always=20 had tumor recurrences noncontiguous with the initial = lesion(s), while=20 group IV GBM recurrences were always bordering the primary = lesion.=20 Group I GBMs may be most related to SVZ stem cells; these = tumors were=20 in intimate contact with the SVZ, were most likely to be = multifocal=20 at diagnosis, and recurred at great distances to the initial=20 lesion(s). In contrast, group IV GBMs were always solitary = lesions;=20 these may arise from non-SVZ, white matter glial progenitors. = Our MRI-based classification of GBMs may further our=20 understanding of GBM histogenesis and help predict tumor = recurrence=20 pattern.

Key Words: glioblastoma multiforme (GBM) =95 MRI =95 = neural stem=20 cell =95 subventricular zone (SVZ) =95 tumor stem cell


3D"   =20 Introduction
Top
Abstract
3D"Introduction
Materials and Methods
Results
Discussion
References
 
<= B>Recent=20 studies demonstrate that glioblastoma multiforme (GBM) = contains a=20 subpopulation of cancer cells with stem cell characteristics,=20 including self-renewal and multipotentiality; these cancer = stem=20 cells can propagate tumors in vivo.1-4=20 The adult human brain harbors astrocyte-like neural stem = cells within=20 the subventricular zone (SVZ), which is located just under = the=20 ependyma of the brain ventricles5,6=20 (Fig.=20 1A). In animal models, gliomas=97including GBM=97can be = induced from=20 SVZ cells.7-9=20 These accumulating data have thus given rebirth to the notion = that=20 human gliomas may arise from SVZ neural stem cells (reviewed = in Sanai=20 et al.10),=20 an idea that was first suggested in the first half of the = 20th=20 century.11-13=20



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  = 		Fig. 1. (A) Neural stem cells = (red=20 circles) are found in the walls of the adult brain = ventricles=20 (blue). An axial section (black trapezoid) is indicated on = this=20 cartoon, representing the approximate level of section of = the MR=20 images shown. (B) Multiple hypotheses of brain tumor origin: = subventricular zone (SVZ) stem cells (S, red) normally = self-renew=20 and produce progenitor cells (light green, glial [g]; light = blue,=20 neuronal [n]), which then progress through a developmental = lineage=20 (e.g., g1 3D"-"=20 src=3D"http://neuro-oncology.dukejournals.org/math/rarr.gif" = border=3D0>=20 g2...) and differentiate into mature neurons (N, = dark=20 blue) or glia (G, dark green). g1 and = n1 cells=20 are highly migratory progenitors, directly descendent of SVZ = stem=20 cells. g2 and n2 cells represent less=20 migratory local progenitors. theories include the following: = (1)=20 stem cells become dysregulated and give rise to glioma cells = (t,=20 orange); (2) highly migratory progenitor cells are the=20 tumor-initiating cells; (3) local progenitors with limited = migration=20 give rise to the tumor; and (4) mature glial cells = dedifferentiate=20 to produce tumor cells. (C) Schematic of the different = groups of=20 glioblastoma multiforme (GBM) lesions based on MRI patterns. = (D-G)=20 Axial postcontrast t1-weighted MR images of representative = examples=20 for each group (I-IV) in this classification system. (D) For = this=20 group I GBM, note that the contrast-enhancing lesion (CEL) = extends=20 from the atrium SVZ to the pia. Interestingly, despite the = large=20 size, this GBM exerts relatively little mass effect. (E) = Group II:=20 SVZ-contacting tumor that does not involve the cortex. (F) = Group=20 III: the CEL is invading the cortex, reaching the pia, but = does not=20 touch the SVZ. (G) Group IV: these lesions "respect" both = the SVZ=20 and cortex; the CEL mass tends to displace brain matter = rather than=20 directly invade the cortex and reach the ventricle wall. =

 = ;
GBM=20 is a pathologically and clinically heterogeneous disease. = While some=20 GBMs may arise from transformed SVZ stem cells, other gliomas = may be=20 initiated by neoplastic transformation of non-SVZ progenitor = cells or=20 mature glial cells that have undergone dedifferentiation14=20 (Fig.=20 1B). Identifying a subset of GBMs that are related to = tumor stem=20 cells in the SVZ would have significant therapeutic=20 implications:15=20 stem-cell-derived GBM may need treatment that attends to both = the=20 primary lesion(s) and the SVZ. To better understand the = histogenetic=20 and clinical heterogeneity of GBM, we developed an MRI-based=20 classification of GBMs based on their involvement of the SVZ = and=20 cortex.

We identified a subset of GBMs that are more likely to be SVZ = stem=20 cell - related based on the spatial relationship of the tumor = to the=20 SVZ, involvement of cortex, multifocality, and recurrence = pattern.=20 Another GBM subset is more likely related to non-SVZ = progenitor cells=20 or dedifferentiated glial cells. This study provides MRI = evidence=20 suggesting a relationship between a subset of GBMs and tumor = stem=20 cells in the SVZ.


3D"   =20 Materials and Methods
Top
Abstract
Introduction
3D"Materials and = Methods
Results
Discussion
References
 
W= e studied=20 53 consecutive patients with newly diagnosed GBM who = underwent=20 preoperative, immediately postoperative (within 48 h after = surgery),=20 and subsequent follow-up MR images as a part of a brain tumor = imaging=20 research study (SPORE project grant). Informed consent for=20 participation in this study was obtained from each patient in = accordance to institutional protocol. The medical records of = all 53=20 patients were reviewed.

All patients underwent the same preoperative MRI protocol, which = consisted of a three-plane localizer sequence (8.5/1.6 ms = [TR/TE]),=20 an axial fluid-attenuated inversion-recovery (FLAIR) sequence = (10,000/148/2,200 [TR/TE/TI]), an axial fast spin-echo = T2-weighted=20 sequence (3,000/102, echo train length 16, matrix 256 x 196), axial = diffusion-weighted imaging=20 (10,000/99, b =3D 1,000 s/mm2), and a postcontrast = three-dimensional spoiled gradient-recalled acquisition in = the steady=20 state (SPGR; 34/8) T1-weighted sequence. Postoperatively, we = obtained=20 additional postcontrast imaging in the coronal and axial = planes.=20

A neuroradiologist (S.C.) and MRI research assistant (M.C.M.)=20 reviewed each tumor for the following on preoperative = imaging:=20 distance of contrast-enhancing lesion (CEL) to nearest = ventricle,=20 infiltration of CEL into cortex, volume of CEL, and = anatomical=20 location of the primary (largest volume) CEL. Multifocal = disease=20 at initial diagnosis was recognized by the presence of CELs = or=20 nonenhancing FLAIR lesions not typical of nonspecific white = matter=20 disease and suspicious for tumor that were noncontiguous with = the=20 primary CEL. Distances and volumes were measured with qBrain = (Medis=20 Medical Imaging, Leesburg, VA, USA). Tumor recurrence, = determined=20 based on contrast-enhanced T1-weighted MR images, was defined = as a=20 new or progressive increase in CEL, within the initial = surgical=20 resection site and/or in a remote location. Statistical = analyses were=20 performed using SAS version 9.1 (SAS Institute Inc., Cary, = NC, USA).=20 The likelihood ratio test of independence was used to = evaluate the=20 incidence rate of multifocal GBM among groups. Assuming there = is a=20 natural ordering in severity among groups (group I is more = severe=20 than group II, group II is more severe than group III, etc.), = the=20 Cochran-Armitage trend test was used to assess the = association=20 between the incidence rate and group order. To assess the=20 contribution of individual variables (SVZ contact, cortical=20 involvement, patient age, and tumor volume) to the incidence = of=20 multifocal GBM, we performed both univariate and multivariate = analyses, as described in Results.


3D"   =20 Results
Top
Abstract
Introduction
Materials and Methods
3D"Results
Discussion
References
 
G= BMs were=20 classified preoperatively into four groups by the spatial=20 relationship of the CEL with the SVZ and cortex as follows: = group I,=20 CEL contacting SVZ and infiltrating cortex; group II, CEL = contacting=20 SVZ but not involving cortex; group III, CEL not contacting = SVZ but=20 involving cortex; and group IV, CEL neither contacting SVZ = nor=20 infiltrating cortex (Fig.=20 1C-G). Table=20 1 lists patient demographics and tumor MRI = characteristics.=20


View = this=20 table:
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  = 		Table 1. Patient = demographics and=20 MRI characteristics of glioblastoma multiforme (GBM) in = groups I-IV =

 = ;

Multifocal GBM is suggestive of a more invasive and migratory=20 tumor phenotype, a feature more common to stem-cell-derived=20 cancer.16=20 We therefore examined the incidence of multifocal GBM among = the four=20 groups defined above. Patients with group I GBMs had the = highest=20 frequency of multifocal disease (Fig.=20 2A-C) at initial diagnosis (9 of 16 patients, 56%). In = contrast,=20 patients with group IV tumors did not have multifocal = disease.=20 Patients with group II and III GBMs had multifocal disease in = 11%=20 and 29% of cases, respectively. There was a significant=20 difference in the incidence of multifocal GBM among the four = groups=20 (p =3D 0.001, likelihood ratio test of independence). = In=20 addition, the results of Cochran-Armitage exact trend test = indicated=20 that the incidence of multifocal GBM was highest for group I = and=20 lowest for group IV (two-sided test, p =3D 0.002). =



View = larger=20 version (49K):
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  = 		Fig. 2. (A-C) Axial postcontrast = t1-weighted MR images of the same patient showing an example = of=20 group I multifocal glioblastoma multiforme (GBM). the=20 contrast-enhancing lesion (CEL) contacts the posterior = temporal horn=20 subventricular zone (SVZ) in A. Rostrally, there are at = least three=20 separate lesions in B and two in C, including one in the=20 contralateral hemisphere (orange asterisk). (D and E) = Recurrence of=20 group I GBM in distant SVZ location. (D) Preoperative axial=20 postcontrast t1-weighted MR images of a patient with group I = GBM.=20 this patient did not have multifocal disease preoperatively. = (E)=20 Fifteen months postoperatively, there was an enhancing mass = lesion=20 in the SVZ of the contralateral frontal horn (orange = arrowhead)=20 consistent with tumor recurrence. In addition, there is = subependymal=20 enhancement bilaterally. No abnormal subarachnoid = enhancement was=20 found in this or other images of this patient. (F-H) = Integration of=20 GBM cell-of-origin data from animal models with human MRI = data. (F)=20 P53-, NF1- SVZ astrocytes give rise to = group=20 I- and group II-like GBMs in the mouse. this coronal = schematic shows=20 an example of a group I tumor (red) extending from the SVZ = to the=20 pia. (G) A schematic of human group I and II GBMs in a = similar=20 coronal plane. (H) Model of group I and group IV GBM = subtypes. At=20 diagnosis, group I GBMs were often multifocal (9 of 16, = 56%),=20 possibly from the migration of tumor-initiating cells from = either=20 the SVZ or tumor mass. After resection, group I GBM always = recurred=20 at locations noncontiguous with the initial lesion(s). = Distant,=20 recurrent lesions may arise from tumor cells migrating from = the SVZ=20 through the parenchyma (solid arrow) or along the SVZ itself = (dotted=20 arrows). the cell of origin of group I GBMs may reside in or = near=20 the SVZ, and tumor cells derived from SVZ neural stem cells = may have=20 a greater migratory potential than those of group IV. Group = IV GBMs=20 occurred only as solitary lesions, and group IV GBM = recurrences were=20 always contiguous with the resection cavity. Group IV GBMs = may arise=20 from non-SVZ progenitor cells that have a limited migration=20 potential. =

 = ;
The=20 contribution of individual variables (SVZ contact, cortical=20 involvement, patient age, and tumor volume) was investigated = by=20 both univariate and multivariate analysis. Univariate analysis = showed=20 that only SVZ contact (p =3D 0.04) and cortical involvement=20 (p =3D 0.01) are significantly associated with = multifocality.=20 Multivariate analysis was conducted using a stepwise = selection=20 with 0.1 significance level to enter the model and 0.1 = significance=20 level for staying in the model, and the resulting model = included=20 both SVZ contact and cortical involvement.

Follow-up MRI was available for 11 of 16 group I patients = (follow-up=20 period of 5-23 months) and 13 of 14 group IV GBM patients = (follow-up=20 period of 3-38 months). For the 11 evaluable group I GBM = patients,=20 tumors recurred in all cases, and CELs were always found in=20 locations noncontiguous with the primary lesion(s), in = addition=20 to recurrence at the resection cavity (Fig.=20 2D,E). Nine of these 11 patients had CELs in distant SVZ=20 locations (contralateral in two cases), and two had CELs in=20 noncontiguous brain parenchyma (contralateral in one case). = For the=20 13 evaluable group IV GBM patients, 10 had tumor recurrence=20 contiguous with the resection cavity, and none had any = evidence of=20 noncontiguous tumor.


3D"   =20 Discussion
Top
Abstract
Introduction
Materials and Methods
Results
3D"Discussion
References
 
O= ur=20 results show that GBMs contacting the SVZ and involving the = cortex=20 (group I) were most likely to be multifocal at the time of = initial=20 diagnosis and were more likely to have recurrent tumor at = locations=20 distant to the initial lesion. GBMs not involving either the = SVZ or=20 the cortex (group IV) were not multifocal at diagnosis and = always=20 recurred within 2 cm of the resection margin.

Group I GBMs may be most closely related to SVZ neural stem = cells.=20 The physical association of malignant glioma with the SVZ has = led=20 neuropathologists to suggest that these tumors arise from = this region=20 of the brain.11-13=20 This hypothesis is supported by the results of animal model=20 experiments involving viral or carcinogen transformation of = SVZ cells=20 and resultant tumor formation.10=20 Recently, Zhu et al.9=20 demonstrated that p53 inactivation cooperates with NF1 loss = to induce=20 GBM formation from mouse SVZ astrocytes; intriguingly, these=20 SVZ-derived tumors usually contact the SVZ and infiltrate the = cortex=20 like human group I GBMs (Fig.=20 2F,G).

The multifocality at diagnosis and recurrence pattern of group = I=20 GBMs suggest that the cell of origin of this tumor type is = highly=20 migratory and invasive (see Fig.=20 2H). Neural stem cells express matrix metalloproteinases=20 (MMPs)=97proteolytic enzymes implicated in tumor cell = metastasis=97and=20 although the adult brain as a whole does not express MMPs, = gliomas=20 overexpress certain MMPs, leading to increased invasiveness = (reviewed=20 in Yong et al.17).=20 It is possible that gliomas arising from stem cells maintain = neural=20 stem cell MMP expression. The SVZ region, or niche, may also = be=20 highly permissive for both tumor growth and cellular = migration,=20 allowing tumor stem cells and their progeny to rapidly = proliferate=20 and migrate under the ependyma.

In this study, group IV GBMs occurred as solitary lesions and=20 recurred only around the resection cavity of the initial = tumor,=20 suggesting that these tumor cells are less migratory than = their=20 group I counterparts. Group IV GBMs were not intimately = associated=20 with the SVZ (and often displaced the SVZ away with their = mass),=20 suggesting that these tumors arise from non-SVZ progenitor = cells.=20 Progenitor cells expressing the chondroitin sulfate = proteoglycan=20 NG2 (neuronal/glial 2) are found throughout adult human = brain.18=20 In the mouse, NG2+ progenitor cells from non-SVZ = regions=20 have a very limited migration potential, whereas = NG2+=20 cells from the SVZ migrate long distances.19=20

The distinguishing characteristic between group I and group = II=20 tumors in this study is cortical invasion. What might account = for the=20 presence or absence of this phenotype? In their analysis of=20 asymptomatic mice with early GBMs arising from p53-,=20 NF1- astrocytes, Zhu et al.9=20 demonstrate that not all SVZ-associated gliomas infiltrate = the=20 cortex. Perhaps the difference between the two = classifications is=20 simply a temporal consequence: Some human group II GBMs are = simply=20 group I GBMs that have yet to reach the cortex at the time of = imaging. Alternatively, it is possible that some group II = GBMs are=20 derived from later-lineage cells with less migration/invasion = potential.

Zhu et al.9=20 additionally describe mice with gross GBM lesions = noncontiguous with=20 the SVZ; in these mice, microscopic cellular abnormalities = are=20 present in the SVZ. This pattern of microscopic SVZ cellular=20 abnormality and distant GBM mass lesion(s) is suggestive of a = mechanism in which SVZ tumor stem cells produce migratory = tumorigenic=20 daughter cells; these daughter cells take up residence in = locations=20 distant from the SVZ, where they then proliferate to form a = mass.=20 This migratory tumor progenitor cell hypothesis15=20 may account for the MRI findings of group III tumors: SVZ = cellular=20 abnormalities may be below the threshold of detection by MRI, = but the distant mass lesions arising from migratory = tumorigenic=20 daughter cells are easily apparent on typical MRI sequences.=20 Postmortem analysis of patients with group III GBM would be=20 useful to investigate this hypothesis.

Our results do not directly address whether GBMs can arise from=20 the SVZ. It is likely that for GBM there will be different = cells=20 of origin, each with different clinical and pathological=20 presentations. Because it will be difficult to directly = determine the=20 cell of origin in humans, it is important to draw parallels=20 between animal model data and actual human disease. Our = findings=20 suggest a testable hypothesis for animal models of glioma, = that=20 tumors from NG2+ SVZ cells are more invasive and = migratory=20 than tumors induced from NG2+ non-SVZ progenitors. = Group I=20 GBM may be enriched for CD133+ tumor stem cells in = comparison to group IV GBM. It will also be valuable to = compare the=20 genomic profile of tumors in the different GBM groups to = understand=20 their different biological behaviors (e.g., cortical = infiltration=20 between group I and II) on a molecular level, as well as to = make=20 comparisons to human neural stem cells.

There is great interest in classifying GBMs for prognosis. = Currently,=20 age and KPS are the two most significant prognostic = factors.20=20 Gene expression profiling holds promise for GBM = classification;21=20 however, transcriptional profiling is not performed = routinely.=20 In contrast, nearly all patients with GBM are diagnosed and=20 followed with MRI. Classifying GBMs based on their MRI = features=20 may allow a practical yet powerful tool for the assessment of = patient prognosis and treatment decisions.

Despite advances in surgery, radiotherapy, chemotherapy, and=20 immunotherapy, the median survival for GBM has remained = between=20 9 and 12 months.22=20 The potential of SVZ neural stem cells to divide = asymmetrically=20 combined with the migratory potential of SVZ-derived neural=20 progenitors may contribute to the treatment-resistant nature = of=20 GBM.15=20 Based on our preliminary results, it is possible that = patients who=20 present with group I GBM lesions will benefit from radiation = therapy=20 that includes distant SVZ locations. Perhaps group IV GBM = lesions=20 would be the most amenable to regional therapy (e.g.,=20 convection-enhanced delivery of immunotoxins), given that = this group=20 of tumors recurs only locally. Follow-up studies will be = required to=20 conclusively address the clinical value of MRI for assessing = GBM SVZ=20 and/or cortical involvement, but the preliminary results = presented=20 here appear promising for this type of tumor analysis. =

Received for publication September 1, 2006. Accepted for publication = January=20 4, 2007.


3D"   =20 References
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
3D"References
&nb= sp;

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Opera = requires=0A= the Sun Java Runtime Environment .=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_0011_01C85C66.AD46FF70 Content-Type: application/octet-stream Content-Transfer-Encoding: quoted-printable Content-Location: http://neuro-oncology.dukejournals.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 if (name =3D=3D "background-position") {=0A= e.style.backgroundPosition =3D value;=0A= }=0A= else if (name =3D=3D "background-position-x") {=0A= e.style.backgroundPositionX =3D value;=0A= }=0A= else if (name =3D=3D "background-position-y") {=0A= e.style.backgroundPositionY =3D value;=0A= }=0A= else if (name =3D=3D "background-repeat") {=0A= e.style.backgroundRepeat =3D value;=0A= }=0A= else if (name =3D=3D "behavior") {=0A= e.style.behavior =3D value;=0A= }=0A= else if (name =3D=3D "border") {=0A= e.style.border =3D value;=0A= }=0A= else if (name =3D=3D "border-bottom") {=0A= e.style.borderBottom =3D value;=0A= }=0A= else if (name =3D=3D "border-bottom-color") {=0A= e.style.borderBottomColor =3D value;=0A= }=0A= else if (name =3D=3D "border-bottom-style") {=0A= e.style.borderBottomStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-bottom-width") {=0A= e.style.borderBottomWidth =3D value;=0A= }=0A= else if (name =3D=3D "border-collapse") {=0A= e.style.borderCollapse =3D value;=0A= }=0A= else if (name =3D=3D "border-color") {=0A= e.style.borderColor =3D value;=0A= }=0A= else if (name =3D=3D "border-left") {=0A= e.style.borderLeft =3D value;=0A= }=0A= else if (name =3D=3D "border-left-color") {=0A= e.style.borderLeftColor =3D value;=0A= }=0A= else if (name =3D=3D "border-left-style") {=0A= e.style.borderLeftStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-left-width") {=0A= e.style.borderLeftWidth =3D value;=0A= }=0A= else if (name =3D=3D "border-right") {=0A= e.style.borderRight =3D value;=0A= }=0A= else if (name =3D=3D "border-right-color") {=0A= e.style.borderRightColor =3D value;=0A= }=0A= else if (name =3D=3D "border-right-style") {=0A= e.style.borderRightStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-right-width") {=0A= e.style.borderRightWidth =3D value;=0A= }=0A= else if (name =3D=3D "border-style") {=0A= e.style.borderStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-top") {=0A= e.style.borderTop =3D value;=0A= }=0A= else if (name =3D=3D "border-top-color") {=0A= e.style.borderTopColor =3D value;=0A= }=0A= else if (name =3D=3D "border-top-style") {=0A= e.style.borderTopStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-top-width") {=0A= e.style.borderTopWidth =3D value;=0A= }=0A= else if (name =3D=3D "border-width") {=0A= e.style.borderWidth =3D value;=0A= }=0A= else if (name =3D=3D "bottom") {=0A= e.style.bottom =3D value;=0A= }=0A= else if (name =3D=3D "clear") {=0A= e.style.clear =3D value;=0A= }=0A= else if (name =3D=3D "clip") {=0A= e.style.clip =3D value;=0A= }=0A= else if (name =3D=3D "color") {=0A= e.style.color =3D value;=0A= }=0A= else if (name =3D=3D "cssText") {=0A= e.style.Sets =3D value;=0A= }=0A= else if (name =3D=3D "cursor") {=0A= e.style.cursor =3D value;=0A= }=0A= else if (name =3D=3D "direction") {=0A= e.style.direction =3D value;=0A= }=0A= else if (name =3D=3D "display") {=0A= e.style.display =3D value;=0A= }=0A= else if (name =3D=3D "font") {=0A= e.style.font =3D value;=0A= }=0A= else if (name =3D=3D "font-family") {=0A= e.style.fontFamily =3D value;=0A= }=0A= else if (name =3D=3D "font-size") {=0A= e.style.fontSize =3D value;=0A= }=0A= else if (name =3D=3D "font-style") {=0A= e.style.fontStyle =3D value;=0A= }=0A= else if (name =3D=3D "font-variant") {=0A= e.style.fontVariant =3D value;=0A= }=0A= else if (name =3D=3D "font-weight") {=0A= e.style.fontWeight =3D value;=0A= }=0A= else if (name =3D=3D "height") {=0A= e.style.height =3D value;=0A= }=0A= else if (name =3D=3D "ime-mode") {=0A= e.style.imeMode =3D value;=0A= }=0A= else if (name =3D=3D "layout-flow") {=0A= e.style.layoutFlow =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid") {=0A= e.style.layoutGrid =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid-char") {=0A= e.style.layoutGridChar =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid-line") {=0A= e.style.layoutGridLine =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid-mode") {=0A= e.style.layoutGridMode =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid-type") {=0A= e.style.layoutGridType =3D value;=0A= }=0A= else if (name =3D=3D "left") {=0A= e.style.left =3D value;=0A= }=0A= else if (name =3D=3D "letter-spacing") {=0A= e.style.letterSpacing =3D value;=0A= }=0A= else if (name =3D=3D "line-break") {=0A= e.style.lineBreak =3D value;=0A= }=0A= else if (name =3D=3D "line-height") {=0A= e.style.lineHeight =3D value;=0A= }=0A= else if (name =3D=3D "list-style") {=0A= e.style.listStyle =3D value;=0A= }=0A= else if (name =3D=3D "list-style-image") {=0A= e.style.listStyleImage =3D value;=0A= }=0A= else if (name =3D=3D "list-style-position") {=0A= e.style.listStylePosition =3D value;=0A= }=0A= else if (name =3D=3D "list-style-type") {=0A= e.style.listStyleType =3D value;=0A= }=0A= else if (name =3D=3D "margin") {=0A= e.style.margin =3D value;=0A= }=0A= else if (name =3D=3D "margin-bottom") {=0A= e.style.marginBottom =3D value;=0A= }=0A= else if (name =3D=3D "margin-left") {=0A= e.style.marginLeft =3D value;=0A= }=0A= else if (name =3D=3D "margin-right") {=0A= e.style.marginRight =3D value;=0A= }=0A= else if (name =3D=3D "margin-top") {=0A= e.style.marginTop =3D value;=0A= }=0A= else if (name =3D=3D "min-height") {=0A= e.style.minHeight =3D value;=0A= }=0A= else if (name =3D=3D "overflow") {=0A= e.style.overflow =3D value;=0A= }=0A= else if (name =3D=3D "overflow-x") {=0A= e.style.overflowX =3D value;=0A= }=0A= else if (name =3D=3D "overflow-y") {=0A= e.style.overflowY =3D value;=0A= }=0A= else if (name =3D=3D "padding") {=0A= e.style.padding =3D value;=0A= }=0A= else if (name =3D=3D "padding-bottom") {=0A= e.style.paddingBottom =3D value;=0A= }=0A= else if (name =3D=3D "padding-left") {=0A= e.style.paddingLeft =3D value;=0A= }=0A= else if (name =3D=3D "padding-right") {=0A= e.style.paddingRight =3D value;=0A= }=0A= else if (name =3D=3D "padding-top") {=0A= e.style.paddingTop =3D value;=0A= }=0A= else if (name =3D=3D "page-break-after") {=0A= e.style.pageBreakAfter =3D value;=0A= }=0A= else if (name =3D=3D "page-break-before") {=0A= e.style.pageBreakBefore =3D value;=0A= }=0A= else if (name =3D=3D "pixelBottom") {=0A= e.style.pixelBottom =3D value;=0A= }=0A= else if (name =3D=3D "pixelHeight") {=0A= e.style.pixelHeight =3D value;=0A= }=0A= else if (name =3D=3D "pixelLeft") {=0A= e.style.pixelLeft =3D value;=0A= }=0A= else if (name =3D=3D "pixelRight") {=0A= e.style.pixelRight =3D value;=0A= }=0A= else if (name =3D=3D "pixelTop") {=0A= e.style.pixelTop =3D value;=0A= }=0A= else if (name =3D=3D "pixelWidth") {=0A= e.style.pixelWidth =3D value;=0A= }=0A= else if (name =3D=3D "posBottom") {=0A= e.style.posBottom =3D value;=0A= }=0A= else if (name =3D=3D "posHeight") {=0A= e.style.posHeight =3D value;=0A= }=0A= else if (name =3D=3D "position") {=0A= e.style.position =3D value;=0A= }=0A= else if (name =3D=3D "posLeft") {=0A= e.style.posLeft =3D value;=0A= }=0A= else if (name =3D=3D "posRight") {=0A= e.style.posRight =3D value;=0A= }=0A= else if (name =3D=3D "posTop") {=0A= 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quoted-printable Content-Location: http://neuro-oncology.dukejournals.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. For now we have to disable=0A= * the callback until we can track down a proper fix=0A= * (or everybody sanely upgrades to version 6 or 7!).=0A= */=0A= if (navigator) {=0A= var appname =3D navigator.appName;=0A= if (appname =3D=3D "Microsoft Internet Explorer") {=0A= var userAgent =3D navigator["userAgent"];=0A= var s =3D "MSIE ";=0A= var n =3D -1; =0A= if ((n =3D userAgent.indexOf(s)) !=3D -1) {=0A= var v =3D parseFloat(userAgent.substring(n+s.length));=0A= if (v < 6) {=0A= return;=0A= }=0A= }=0A= }=0A= }=0A= =0A= /*=0A= * Acquire table row element to update, initiate callback=0A= * to update table with Entrez Links.=0A= */=0A= var tr =3D document.getElementById('entrez_callback_'+pmid);=0A= if (!tr) {=0A= return;=0A= }=0A= var req =3D new XMLHttpRequest();=0A= if (!req) {=0A= return;=0A= }=0A= req.onreadystatechange =3D function() {=0A= if (req.readyState =3D=3D 4 && (req.status =3D=3D 200 || req.status = =3D=3D 304)) {=0A= var src =3D req.responseXML.documentElement;=0A= var dst =3D document.createDocumentFragment();=0A= for (var i =3D 0; i < src.childNodes.length; i++) {=0A= copy_xml_to_html(src.childNodes[i], dst);=0A= }=0A= var tbl =3D tr.parentNode;=0A= tbl.replaceChild(dst, tr);=0A= }=0A= }=0A= req.open('GET', callback_url, true);=0A= req.send(null);=0A= }=0A= ------=_NextPart_000_0011_01C85C66.AD46FF70--