Association between Tumor Acidity and Hypervascularity in Human Gliomas Using pH-Weighted Amine Chemical Exchange Saturation Transfer Echo-Planar Imaging and Dynamic Susceptibility Contrast Perfusion MRI at 3T

REFERENCES

1. 1.↵
   2. Ostrom QT,
   3. Gittleman H,
   4. Liao P, et al

   . CBTRUS Statistical Report: primary brain and other central nervous system tumors diagnosed in the United States in 2010–2014. Neuro Oncol 2017;19:v1–88 doi:10.1093/neuonc/nox158 pmid:29117289

   CrossRefPubMed
2. 2.↵
   2. Warburg OH,
   3. Dickens F

   , Kaiser Wilhelm Institute for Biology. The Metabolism of Tumours: Investigations from the Kaiser Wilhelm Institute for Biology, Berlin-Dahlem. London: Arnold Constable & Co; 1930
3. 3.↵
   2. Gatenby RA,
   3. Gillies RJ

   . Why do cancers have high aerobic glycolysis? Nat Rev Cancer 2004;4:891–99 doi:10.1038/nrc1478 pmid:15516961

   CrossRefPubMedWeb of Science
4. 4.↵
   2. Morita T,
   3. Nagaki T,
   4. Fukuda I, et al

   . Clastogenicity of low pH to various cultured mammalian cells. Mut Res 1992;268:297–305 doi:10.1016/0027-5107(92)90235-T pmid:1379335

   CrossRefPubMedWeb of Science
5. 5.↵
   2. Gatenby RA,
   3. Vincent TL

   . An evolutionary model of carcinogenesis. Cancer Res 2003;63:6212–20 pmid:14559806

   Abstract/FREE Full Text
6. 6.↵
   2. Martinez-Zaguilan R,
   3. Seftor EA,
   4. Seftor RE, et al

   . Acidic pH enhances the invasive behavior of human melanoma cells. Clin Exp Metastasis 1996;14:176–86 doi:10.1007/BF00121214 pmid:8605731

   CrossRefPubMedWeb of Science
7. 7.↵
   2. Turner GA

   . Increased release of tumour cells by collagenase at acid pH: a possible mechanism for metastasis. Experientia 1979;35:1657–58 doi:10.1007/BF01953252 pmid:42555

   CrossRefPubMed
8. 8.↵
   2. Russell SM,
   3. Elliott R,
   4. Forshaw D, et al

   . Glioma vascularity correlates with reduced patient survival and increased malignancy. Surg Neurol 2009;72:242–46; discussion 246–47 doi:10.1016/j.surneu.2008.11.012 pmid:19329156

   CrossRefPubMedWeb of Science
9. 9.↵
   2. Leon SP,
   3. Folkerth RD,
   4. Black PM

   . Microvessel density is a prognostic indicator for patients with astroglial brain tumors. Cancer 1996;77:362–72 doi:10.1002/(SICI)1097-0142(19960115)77:2<362::AID-CNCR20>3.0.CO;2-Z pmid:8625246

   CrossRefPubMedWeb of Science
10. 10.↵
    2. Wesseling P,
    3. van der Laak JA,
    4. Link M, et al

    . Quantitative analysis of microvascular changes in diffuse astrocytic neoplasms with increasing grade of malignancy. Hum Pathol 1998;29:352–58 doi:10.1016/S0046-8177(98)90115-0 pmid:9563784

    CrossRefPubMedWeb of Science
11. 11.↵
    2. Jain RK,
    3. di Tomaso E,
    4. Duda DG, et al

    . Angiogenesis in brain tumours. Nat Rev Neurosci 2007;8:610–22 pmid:17643088

    CrossRefPubMedWeb of Science
12. 12.↵
    2. Plate KH,
    3. Mennel HD

    . Vascular morphology and angiogenesis in glial tumors. Exp Toxicol Pathol 1995;47:89–94 doi:10.1016/S0940-2993(11)80292-7 pmid:7580112

    CrossRefPubMedWeb of Science
13. 13.↵
    2. Rampling R,
    3. Cruickshank G,
    4. Lewis AD, et al

    . Direct measurement of pO2 distribution and bioreductive enzymes in human malignant brain tumors. Int J Radiat Oncol Biol Phys 1994;29:427–31 doi:10.1016/0360-3016(94)90432-4 pmid:8005794

    CrossRefPubMedWeb of Science
14. 14.↵
    2. Harris RJ,
    3. Cloughesy TF,
    4. Liau LM, et al

    . Simulation, phantom validation, and clinical evaluation of fast pH-weighted molecular imaging using amine chemical exchange saturation transfer echo planar imaging (CEST-EPI) in glioma at 3 T. NMR Biomed 2016;29:1563–76 doi:10.1002/nbm.3611 pmid:27717216

    CrossRefPubMed
15. 15.↵
    2. Louis DN,
    3. Perry A,
    4. Reifenberger G, et al

    . The 2016 World Health Organization Classification of Tumors of the Central Nervous System: a summary. Acta Neuropathol 2016;131:803–20 doi:10.1007/s00401-016-1545-1 pmid:27157931

    CrossRefPubMed
16. 16.↵
    2. Ellingson BM,
    3. Bendszus M,
    4. Boxerman J, et al

    ; Jumpstarting Brain Tumor Drug Development Coalition Imaging Standardization Steering Committee. Consensus recommendations for a standardized brain tumor imaging protocol in clinical trials. Neuro Oncol 2015;17:1188–98 doi:10.1093/neuonc/nov095 pmid:26250565

    CrossRefPubMed
17. 17.↵
    2. Harris RJ,
    3. Yao J,
    4. Chakhoyan A, et al

    . Simultaneous pH-sensitive and oxygen-sensitive MRI of human gliomas at 3 T using multi-echo amine proton chemical exchange saturation transfer spin-and-gradient echo echo-planar imaging (CEST-SAGE-EPI). Magn Reson Med 2018;80:1962–78 doi:10.1002/mrm.27204 pmid:29626359

    CrossRefPubMed
18. 18.↵
    2. Yao J,
    3. Ruan D,
    4. Raymond C, et al

    . Improving B0 correction for pH-weighted amine proton chemical exchange saturation transfer (CEST) imaging by use of K-means clustering and Lorentzian estimation. Tomography 2018;4:123–37 doi:10.18383/j.tom.2018.00017 pmid:30320212

    CrossRefPubMed
19. 19.↵
    2. Ellingson BM,
    3. Kim HJ,
    4. Woodworth DC, et al

    . Recurrent glioblastoma treated with bevacizumab: contrast-enhanced T1-weighted subtraction maps improve tumor delineation and aid prediction of survival in a multicenter clinical trial. Radiology 2014;271:200–10 doi:10.1148/radiol.13131305 pmid:24475840

    CrossRefPubMedWeb of Science
20. 20.↵
    2. Raghunand N,
    3. Gatenby RA,
    4. Gillies RJ

    . Microenvironmental and cellular consequences of altered blood flow in tumours. Br J Radiol 2003;76(Spec No 1):S11–22 doi:10.1259/bjr/12913493 pmid:15456710

    Abstract/FREE Full Text
21. 21.↵
    2. Helmlinger G,
    3. Schell A,
    4. Dellian M, et al

    . Acid production in glycolysis-impaired tumors provides new insights into tumor metabolism. Clin Cancer Res 2002;8:1284–91 pmid:11948144

    Abstract/FREE Full Text
22. 22.↵
    2. Shi Q,
    3. Le X,
    4. Wang B, et al

    . Regulation of vascular endothelial growth factor expression by acidosis in human cancer cells. Oncogene 2001;20:3751–56 doi:10.1038/sj.onc.1204500 pmid:11439338

    CrossRefPubMedWeb of Science
23. 23.↵
    2. Griffiths L,
    3. Dachs GU,
    4. Bicknell R, et al

    . The influence of oxygen tension and pH on the expression of platelet-derived endothelial cell growth factor/thymidine phosphorylase in human breast tumor cells grown in vitro and in vivo. Cancer Res 1997;57:570–72 pmid:9044826

    Abstract/FREE Full Text
24. 24.↵
    2. Ellingson BM,
    3. Wen PY,
    4. Cloughesy TF

    . Evidence and context of use for contrast enhancement as a surrogate of disease burden and treatment response in malignant glioma. Neuro Oncol 2018;20:457–71 doi:10.1093/neuonc/nox193 pmid:29040703

    CrossRefPubMed
25. 25.↵
    2. da Ponte KF,
    3. Berro DH,
    4. Collet S, et al

    . In vivo relationship between hypoxia and angiogenesis in human glioblastoma: a multimodal imaging study. J Nucl Med 2017;58:1574–79 doi:10.2967/jnumed.116.188557 pmid:28596159

    Abstract/FREE Full Text
26. 26.↵
    2. Flynn JR,
    3. Wang L,
    4. Gillespie DL, et al

    . Hypoxia-regulated protein expression, patient characteristics, and preoperative imaging as predictors of survival in adults with glioblastoma multiforme. Cancer 2008;113:1032–42 doi:10.1002/cncr.23678 pmid:18618497

    CrossRefPubMedWeb of Science
27. 27.↵
    2. Helmlinger G,
    3. Yuan F,
    4. Dellian M, et al

    . Interstitial pH and pO2 gradients in solid tumors in vivo: high-resolution measurements reveal a lack of correlation. Nat Med 1997;3:177–82 doi:10.1038/nm0297-177 pmid:9018236

    CrossRefPubMedWeb of Science
28. 28.↵
    2. Patel AP,
    3. Tirosh I,
    4. Trombetta JJ, et al

    . Single-cell RNA-seq highlights intratumoral heterogeneity in primary glioblastoma. Science 2014;344:1396–401 doi:10.1126/science.1254257 pmid:24925914

    Abstract/FREE Full Text
29. 29.↵
    2. Sottoriva A,
    3. Spiteri I,
    4. Piccirillo SGM, et al

    . Intratumor heterogeneity in human glioblastoma reflects cancer evolutionary dynamics. Proc Natl Acad Sci U S A 2013;110:4009–14 doi:10.1073/pnas.1219747110 pmid:23412337

    Abstract/FREE Full Text
30. 30.↵
    2. Paech D,
    3. Windschuh J,
    4. Oberhollenzer J, et al

    . Assessing the predictability of IDH mutation and MGMT methylation status in glioma patients using relaxation-compensated multi-pool CEST MRI at 7.0 Tesla. Neuro Oncol 2018;20:1661–71 doi:10.1093/neuonc/noy073 pmid:29733378

    CrossRefPubMed
31. 31.↵
    2. Jiang S,
    3. Zou T,
    4. Eberhart CG, et al

    . Predicting IDH mutation status in grade II gliomas using amide proton transfer-weighted (APTw) MRI. Magn Reson Med 2017;78:1100–09 doi:10.1002/mrm.26820 pmid:28714279

    CrossRefPubMed
32. 32.↵
    2. Borodovsky A,
    3. Seltzer MJ,
    4. Riggins GJ

    . Altered cancer cell metabolism in gliomas with mutant IDH1 or IDH2. Curr Opin Oncol 2012;24:83–89 doi:10.1097/CCO.0b013e32834d816a pmid:22080945

    CrossRefPubMed
33. 33.↵
    2. Kickingereder P,
    3. Sahm F,
    4. Radbruch A, et al

    . IDH mutation status is associated with a distinct hypoxia/angiogenesis transcriptome signature which is non-invasively predictable with rCBV imaging in human glioma. Sci Rep 2015;5:16238 doi:10.1038/srep16238 pmid:26538165

    CrossRefPubMed
34. 34.↵
    2. Tietze A,
    3. Blicher J,
    4. Mikkelsen IK, et al

    . Assessment of ischemic penumbra in patients with hyperacute stroke using amide proton transfer (APT) chemical exchange saturation transfer (CEST) MRI. NMR Biomed 2014;27:163–74 doi:10.1002/nbm.3048 pmid:24288260

    CrossRefPubMedWeb of Science
35. 35.↵
    2. Xu X,
    3. Yadav NN,
    4. Knutsson L, et al

    . Dynamic glucose-enhanced (DGE) MRI: translation to human scanning and first results in glioma patients. Tomography 2015;1:105–14 doi:10.18383/j.tom.2015.00175 pmid:26779568

    CrossRefPubMed