Hyperpolarized [1-13C]-pyruvate MRS evaluates immune potential and predicts response to radiotherapy in cervical cancer

IF 3.7 Q1 RADIOLOGY, NUCLEAR MEDICINE & MEDICAL IMAGING
Gigin Lin, Ching-Yi Hsieh, Ying-Chieh Lai, Chun-Chieh Wang, Yenpo Lin, Kuan-Ying Lu, Wen-Yen Chai, Albert P. Chen, Tzu-Chen Yen, Shu-Hang Ng, Chyong-Huey Lai
{"title":"Hyperpolarized [1-13C]-pyruvate MRS evaluates immune potential and predicts response to radiotherapy in cervical cancer","authors":"Gigin Lin, Ching-Yi Hsieh, Ying-Chieh Lai, Chun-Chieh Wang, Yenpo Lin, Kuan-Ying Lu, Wen-Yen Chai, Albert P. Chen, Tzu-Chen Yen, Shu-Hang Ng, Chyong-Huey Lai","doi":"10.1186/s41747-024-00445-1","DOIUrl":null,"url":null,"abstract":"<h3 data-test=\"abstract-sub-heading\">Background</h3><p>Monitoring pyruvate metabolism in the spleen is important for assessing immune activity and achieving successful radiotherapy for cervical cancer due to the significance of the abscopal effect. We aimed to explore the feasibility of utilizing hyperpolarized (HP) [1-<sup>13</sup>C]-pyruvate magnetic resonance imaging (MRI) and magnetic resonance spectroscopy (MRS) to evaluate pyruvate metabolism in the human spleen, with the aim of identifying potential candidates for radiotherapy in cervical cancer.</p><h3 data-test=\"abstract-sub-heading\">Methods</h3><p>This prospective study recruited six female patients with cervical cancer (median age 55 years; range 39–60) evaluated using HP [1-<sup>13</sup>C]-pyruvate MRI/MRS at baseline and 2 weeks after radiotherapy. Proton (<sup>1</sup>H) diffusion-weighted MRI was performed in parallel to estimate splenic cellularity. The primary outcome was defined as tumor response to radiotherapy. The Student <i>t</i>-test was used for comparing <sup>13</sup>C data between the groups.</p><h3 data-test=\"abstract-sub-heading\">Results</h3><p>The splenic HP [1-<sup>13</sup>C]-lactate-to-total carbon (tC) ratio was 5.6-fold lower in the responders than in the non-responders at baseline (<i>p</i> = 0.009). The splenic [1-<sup>13</sup>C]-lactate-to-tC ratio revealed a 1.7-fold increase (<i>p</i> = 0.415) and the splenic [1-<sup>13</sup>C]-alanine-to-tC ratio revealed a 1.8-fold increase after radiotherapy (<i>p</i> = 0.482). The blood leukocyte differential count revealed an increased proportion of neutrophils two weeks following treatment, indicating enhanced immune activity (<i>p</i> = 0.013). The splenic apparent diffusion coefficient values between the groups were not significantly different.</p><h3 data-test=\"abstract-sub-heading\">Conclusions</h3><p>This exploratory study revealed the feasibility of HP [1-<sup>13</sup>C]-pyruvate MRS of the spleen for evaluating baseline immune potential, which was associated with clinical outcomes of cervical cancer after radiotherapy.</p><h3 data-test=\"abstract-sub-heading\">Trial registration</h3><p>ClinicalTrials.gov NCT04951921, registered 7 July 2021.</p><h3 data-test=\"abstract-sub-heading\">Relevance statement</h3><p>This prospective study revealed the feasibility of using HP <sup>13</sup>C MRI/MRS for assessing pyruvate metabolism of the spleen to evaluate the patients’ immune potential that is associated with radiotherapeutic clinical outcomes in cervical cancer.</p><h3 data-test=\"abstract-sub-heading\">Key points</h3><p>• Effective radiotherapy induces abscopal effect via altering immune metabolism.</p><p>• Hyperpolarized <sup>13</sup>C MRS evaluates patients’ immune potential non-invasively.</p><p>• Pyruvate-to-lactate conversion in the spleen is elevated following radiotherapy.</p><h3 data-test=\"abstract-sub-heading\">Graphical Abstract</h3>\n","PeriodicalId":36926,"journal":{"name":"European Radiology Experimental","volume":"43 1","pages":""},"PeriodicalIF":3.7000,"publicationDate":"2024-04-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"European Radiology Experimental","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.1186/s41747-024-00445-1","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"RADIOLOGY, NUCLEAR MEDICINE & MEDICAL IMAGING","Score":null,"Total":0}
引用次数: 0

Abstract

Background

Monitoring pyruvate metabolism in the spleen is important for assessing immune activity and achieving successful radiotherapy for cervical cancer due to the significance of the abscopal effect. We aimed to explore the feasibility of utilizing hyperpolarized (HP) [1-13C]-pyruvate magnetic resonance imaging (MRI) and magnetic resonance spectroscopy (MRS) to evaluate pyruvate metabolism in the human spleen, with the aim of identifying potential candidates for radiotherapy in cervical cancer.

Methods

This prospective study recruited six female patients with cervical cancer (median age 55 years; range 39–60) evaluated using HP [1-13C]-pyruvate MRI/MRS at baseline and 2 weeks after radiotherapy. Proton (1H) diffusion-weighted MRI was performed in parallel to estimate splenic cellularity. The primary outcome was defined as tumor response to radiotherapy. The Student t-test was used for comparing 13C data between the groups.

Results

The splenic HP [1-13C]-lactate-to-total carbon (tC) ratio was 5.6-fold lower in the responders than in the non-responders at baseline (p = 0.009). The splenic [1-13C]-lactate-to-tC ratio revealed a 1.7-fold increase (p = 0.415) and the splenic [1-13C]-alanine-to-tC ratio revealed a 1.8-fold increase after radiotherapy (p = 0.482). The blood leukocyte differential count revealed an increased proportion of neutrophils two weeks following treatment, indicating enhanced immune activity (p = 0.013). The splenic apparent diffusion coefficient values between the groups were not significantly different.

Conclusions

This exploratory study revealed the feasibility of HP [1-13C]-pyruvate MRS of the spleen for evaluating baseline immune potential, which was associated with clinical outcomes of cervical cancer after radiotherapy.

Trial registration

ClinicalTrials.gov NCT04951921, registered 7 July 2021.

Relevance statement

This prospective study revealed the feasibility of using HP 13C MRI/MRS for assessing pyruvate metabolism of the spleen to evaluate the patients’ immune potential that is associated with radiotherapeutic clinical outcomes in cervical cancer.

Key points

• Effective radiotherapy induces abscopal effect via altering immune metabolism.

• Hyperpolarized 13C MRS evaluates patients’ immune potential non-invasively.

• Pyruvate-to-lactate conversion in the spleen is elevated following radiotherapy.

Graphical Abstract

Abstract Image

超极化[1-13C]-丙酮酸 MRS 评估免疫潜能并预测宫颈癌放疗反应
背景由于腹水效应的重要性,监测脾脏的丙酮酸代谢对于评估免疫活性和成功进行宫颈癌放疗非常重要。我们旨在探索利用超极化(HP)[1-13C]-丙酮酸磁共振成像(MRI)和磁共振波谱(MRS)评估人体脾脏中丙酮酸代谢的可行性,以确定宫颈癌放疗的潜在候选者。方法这项前瞻性研究招募了六名女性宫颈癌患者(中位年龄 55 岁;39-60 岁不等),在基线和放疗后两周使用 HP [1-13C]- 丙酮酸 MRI/MRS 进行评估。质子(1H)弥散加权 MRI 同时进行,以评估脾脏细胞度。主要结果定义为肿瘤对放疗的反应。结果有反应者的脾脏HP [1-13C]-乳酸与总碳(tC)的比值是基线时无反应者的5.6倍(P = 0.009)。放疗后,脾脏[1-13C]-乳酸与总碳的比值增加了 1.7 倍(p = 0.415),脾脏[1-13C]-丙氨酸与总碳的比值增加了 1.8 倍(p = 0.482)。血液白细胞差计数显示,治疗两周后中性粒细胞比例增加,表明免疫活性增强(p = 0.013)。结论这项探索性研究揭示了用 HP [1-13C]- 丙酮酸 MRS 评估脾脏基线免疫潜能的可行性,而基线免疫潜能与宫颈癌放疗后的临床疗效相关。相关性声明该前瞻性研究揭示了使用HP 13C MRI/MRS评估脾脏丙酮酸代谢以评估患者免疫潜能的可行性,而免疫潜能与宫颈癌放疗后的临床疗效相关。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
European Radiology Experimental
European Radiology Experimental Medicine-Radiology, Nuclear Medicine and Imaging
CiteScore
6.70
自引率
2.60%
发文量
56
审稿时长
18 weeks
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信