Kinetic Modeling of Hyperpolarized Carbon-13 Pyruvate Metabolism in the Human Brain

Mammoli, Daniele; Carvajal, Lucas; Slater, James B.; Bok, Robert; Crane, Jason C.; Xu, Duan; Chang, Susan M.; Vigneron, Daniel B.; Gordon, Jeremy W.; Autry, Adam; Larson, Peder E. Z.; Li, Yan; Chen, Hsin-Yu; Chung, Brian T.; Shin, Peter; Criekinge, Mark Van

doi:10.1109/tmi.2019.2926437

Cited by 36 publications

(43 citation statements)

References 60 publications

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“…This resulted in dynamic profiles consistent with what is typically observed in human prostate, 8 and, therefore, more reliable pyruvate-to-lactate conversion rate k PL fits over the prostate, as shown in Figure 6B. The fitting error metric 30 also indicated that the error decreased and the accuracy increased after TRI. Diffusion images were unavailable for this study.…”

Section: Wsvd and Tri Improves Asnr By An Order Of Magnitude Or Morsupporting

confidence: 80%

“…The error metrics were calculated as previously described. 30 The pathophysiological information, such as the prostate biopsy results, are provided post hoc to correlate with the TRI-processed data and played no role in rank selection HP 13 C MRSI data that has spectral, spatial, and dynamic dimensions. Rather than being diagonal as in 2D SVD, the high-dimensional core tensor ( ∈ ℂ P×Q×S×R ) is a full tensor, meaning that each of its elements can take on a nonzero value.…”

Section: Why Tri Is More Appropriate Than Conventional Svd In Dynammentioning

confidence: 99%

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Tensor image enhancement and optimal multichannel receiver combination analyses for human hyperpolarized ¹³C MRSI

Chen

Autry

Brender

et al. 2020

Magnetic Resonance in Med

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Purpose With the initiation of human hyperpolarized 13C (HP‐13C) trials at multiple sites and the development of improved acquisition methods, there is an imminent need to maximally extract diagnostic information to facilitate clinical interpretation. This study aims to improve human HP‐13C MR spectroscopic imaging through means of Tensor Rank truncation‐Image enhancement (TRI) and optimal receiver combination (ORC). Methods A data‐driven processing framework for dynamic HP 13C MR spectroscopic imaging (MRSI) was developed. Using patient data sets acquired with both multichannel arrays and single‐element receivers from the brain, abdomen, and pelvis, we examined the theory and application of TRI, as well as 2 ORC techniques: whitened singular value decomposition (WSVD) and first‐point phasing. Optimal conditions for TRI were derived based on bias‐variance trade‐off. Results TRI and ORC techniques together provided a 63‐fold mean apparent signal‐to‐noise ratio (aSNR) gain for receiver arrays and a 31‐fold gain for single‐element configurations, which particularly improved quantification of the lower‐SNR‐[13C]bicarbonate and [1‐13C]alanine signals that were otherwise not detectable in many cases. Substantial SNR enhancements were observed for data sets that were acquired even with suboptimal experimental conditions, including delayed (114 s) injection (8× aSNR gain solely by TRI), or from challenging anatomy or geometry, as in the case of a pediatric patient with brainstem tumor (597× using combined TRI and WSVD). Improved correlation between elevated pyruvate‐to‐lactate conversion, biopsy‐confirmed cancer, and mp‐MRI lesions demonstrated that TRI recovered quantitative diagnostic information. Conclusion Overall, this combined approach was effective across imaging targets and receiver configurations and could greatly benefit ongoing and future HP 13C MRI research through major aSNR improvements.

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Section: Wsvd and Tri Improves Asnr By An Order Of Magnitude Or Morsupporting

confidence: 80%

Section: Why Tri Is More Appropriate Than Conventional Svd In Dynammentioning

confidence: 99%

Tensor image enhancement and optimal multichannel receiver combination analyses for human hyperpolarized ¹³C MRSI

Chen

Autry

Brender

et al. 2020

Magnetic Resonance in Med

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“…The total carbon SNR was 117 ± 126 in bone metastases (N = 4), and 85 ± 7 between liver involvements (N = 2). In general, the SNR in all cases was adequate for reliable k PL fitting (standard error metric σ kPL = 0.005 ± 0.003) [27].…”

Section: Hp 13 C-pyruvate Mri Detects High K Pl In Bone and Liver Metmentioning

confidence: 89%

Hyperpolarized 13C-pyruvate MRI detects real-time metabolic flux in prostate cancer metastases to bone and liver: a clinical feasibility study

Chen

Aggarwal

Bok

et al. 2019

Prostate Cancer Prostatic Dis

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ARTICLE Clinical ResearchHyperpolarized 13 C-pyruvate MRI detects real-time metabolic flux in prostate cancer metastases to bone and liver: a clinical feasibility study Abstract Background Hyperpolarized (HP) 13 C-pyruvate MRI is a stable-isotope molecular imaging modality that provides real-time assessment of the rate of metabolism through glycolytic pathways in human prostate cancer. Heretofore this imaging modality has been successfully utilized in prostate cancer only in localized disease. This pilot clinical study investigated the feasibility and imaging performance of HP 13 C-pyruvate MR metabolic imaging in prostate cancer patients with metastases to the bone and/or viscera. Methods Six patients who had metastatic castration-resistant prostate cancer were recruited. Carbon-13 MR examination were conducted on a clinical 3T MRI following injection of 250 mM hyperpolarized 13 C-pyruvate, where pyruvate-to-lactate conversion rate (k PL ) was calculated. Paired metastatic tumor biopsy was performed with histopathological and RNA-seq analyses.Results We observed a high rate of glycolytic metabolism in prostate cancer metastases, with a mean k PL value of 0.020 ± 0.006 (s −1 ) and 0.026 ± 0.000 (s −1 ) in bone (N = 4) and liver (N = 2) metastases, respectively. Overall, high k PL showed concordance with biopsy-confirmed high-grade prostate cancer including neuroendocrine differentiation in one case. Interval decrease of k PL from 0.026 at baseline to 0.015 (s −1 ) was observed in a liver metastasis 2 months after the initiation of taxane plus platinum chemotherapy. RNA-seq found higher levels of the lactate dehydrogenase isoform A (Ldha,15.7 ± 0.7) expression relative to the dominant isoform of pyruvate dehydrogenase (Pdha1, 12.8 ± 0.9).Conclusions HP 13 C-pyruvate MRI can detect real-time glycolytic metabolism within prostate cancer metastases, and can measure changes in quantitative k PL values following treatment response at early time points. This first feasibility study supports future clinical studies of HP 13 C-pyruvate MRI in the setting of advanced prostate cancer.

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“…Following the emergence of dissolution dynamic nuclear polarization (d‐DNP), 1 which significantly enhances carbon‐13 signal in labeled compounds, and the subsequent demonstration of rapid noninvasive imaging of metabolic conversion via magnetic resonance, 2 there has been a substantial expansion of applications for this technology. In short order, the field has moved from animal studies into clinical trials investigating human prostate, 3 brain, 4–6 kidney 7 and liver 8 cancer and metastasis, along with deviations in cardiac metabolism 9 . Given the ongoing efforts towards leveraging hyperpolarized carbon‐13 (HP‐ 13 C) MRI at more than 15 institutions worldwide, the importance of robust acquisition, processing and quantitation that provides reproducible findings is starting to be recognized.…”

Section: Introductionmentioning

confidence: 99%

Hyperpolarized ¹³C MRI data acquisition and analysis in prostate and brain at University of California, San Francisco

et al. 2020

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Based on the expanding set of applications for hyperpolarized carbon-13 (HP-13 C) MRI, this work aims to communicate standardized methodology implemented at the University of California, San Francisco, as a primer for conducting reproducible metabolic imaging studies of the prostate and brain. Current state-of-the-art HP-13 C acquisition, data processing/reconstruction and kinetic modeling approaches utilized in patient studies are presented together with the rationale underpinning their usage. Organized around spectroscopic and imaging-based methods, this guide provides an extensible framework for handling a variety of HP-13 C applications, which derives from two examples with dynamic acquisitions: 3D echo-planar spectroscopic imaging of the human prostate and frequency-specific 2D multislice echo-planar imaging of the human brain. Details of sequence-specific parameters and processing techniques contained in these examples should enable investigators to effectively tailor studies around individual-use cases. Given the importance of clinical integration in improving the utility of HP exams, practical aspects of standardizing data formats for reconstruction, analysis and visualization are also addressed alongside open-source software packages that enhance institutional interoperability and validation of methodology. To facilitate the adoption and further development of this methodology, example datasets and analysis pipelines have been made available in the supporting information.

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Kinetic Modeling of Hyperpolarized Carbon-13 Pyruvate Metabolism in the Human Brain

Cited by 36 publications

References 60 publications

Tensor image enhancement and optimal multichannel receiver combination analyses for human hyperpolarized ¹³C MRSI

Tensor image enhancement and optimal multichannel receiver combination analyses for human hyperpolarized ¹³C MRSI

Hyperpolarized 13C-pyruvate MRI detects real-time metabolic flux in prostate cancer metastases to bone and liver: a clinical feasibility study

Hyperpolarized ¹³C MRI data acquisition and analysis in prostate and brain at University of California, San Francisco

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Kinetic Modeling of Hyperpolarized Carbon-13 Pyruvate Metabolism in the Human Brain

Cited by 36 publications

References 60 publications

Tensor image enhancement and optimal multichannel receiver combination analyses for human hyperpolarized 13C MRSI

Tensor image enhancement and optimal multichannel receiver combination analyses for human hyperpolarized 13C MRSI

Hyperpolarized 13C-pyruvate MRI detects real-time metabolic flux in prostate cancer metastases to bone and liver: a clinical feasibility study

Hyperpolarized 13C MRI data acquisition and analysis in prostate and brain at University of California, San Francisco

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Tensor image enhancement and optimal multichannel receiver combination analyses for human hyperpolarized ¹³C MRSI

Tensor image enhancement and optimal multichannel receiver combination analyses for human hyperpolarized ¹³C MRSI

Hyperpolarized ¹³C MRI data acquisition and analysis in prostate and brain at University of California, San Francisco