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Divergent white matter changes in patients with nasopharyngeal carcinoma post-radiotherapy with different outcomes: a potential biomarker for prediction of radiation necrosis

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A Correction to this article was published on 19 August 2022

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Abstract

Objectives

To investigate the effects of standard radiotherapy on temporal white matter (WM) and its relationship with radiation necrosis (RN) in patients with nasopharyngeal carcinoma (NPC), and to determine the predictive value of WM volume alterations at the early stage for RN occurrence at the late-delay stage.

Methods

Seventy-four treatment-naive NPC patients treated with standard radiotherapy were longitudinally followed up for 36 months. Structural MRIs were collected at multiple time points during the first year post-radiotherapy. Longitudinal structural images were processed using FreeSurfer. Linear mixed models were used to delineate divergent trajectories of temporal WM changes between patients who developed RN and who did not. Four machine learning methods were used to construct predictive models for RN with temporal WM volume alterations at early-stage.

Results

The superior temporal gyrus (STG) had divergent atrophy trajectories in NPC patients with different outcomes (RN vs. NRN) post-radiotherapy. Patients with RN showed more rapid atrophy than those with NRN. A predictive model constructed with temporal WM volume alterations at early-stage post-radiotherapy had good performance for RN; the areas under the curve (AUC) were 0.879 and 0.806 at 1–3 months and 6 months post-radiotherapy, respectively. Moreover, the predictive model constructed with absolute temporal volume at 1–3 months post-radiotherapy also presented good performance; the AUC was 0.842, which was verified by another independent dataset (AUC = 0.773).

Conclusions

NPC patients with RN had more sharp atrophy in the STG than those with NRN. Temporal WM volume at early-stage post-radiotherapy may serve as an in vivo biomarker to identify and predict RN occurrence.

Key Points

• The STG had divergent atrophy trajectories in NPC patients with different outcomes (RN vs. NRN) post-radiotherapy.

• Although both groups exhibited time-dependent atrophy in the STG, the patients with RN showed a more rapid volume decrease than those with NRN.

• Temporal WM volume alteration (or absolute volume) at the early stage could predict RN occurrence at the late-delay stage after radiotherapy.

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Change history

Abbreviations

AJCC:

American Joint Committee on Cancer

AUC:

Area under the curve

BANKSSTS:

Banks of the superior temporal sulcus

DKI:

Diffusion kurtosis imaging

FUS:

Fusiform

GM:

Gray matter

IMRT:

Intensity-modulated radiation therapy

ITG:

Inferior temporal gyrus

KNN:

k-nearest neighbors

LMM:

Linear mixed model

LR:

Logistic regression

MRI:

Magnetic resonance imaging

MTG:

Middle temporal gyrus

NPC:

Nasopharyngeal carcinoma

PHG:

Parahippocampal gyrus

RF:

Random forest

RN:

Radiation-induced temporal lobe necrosis

ROC:

Receiver operating characteristic

RT:

Radiotherapy

RTLI:

Radiation-induced temporal lobe injury

SMG:

Supramarginal gyrus

STG:

Superior temporal gyrus

SVM:

Support vector machine

TP:

Temporal pole

TTG:

Transverse temporal gyrus

WM:

White matter

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Acknowledgements

We thank LetPub (www.letpub.com) for its linguistic assistance during the preparation of this manuscript.

Funding

This work has received funding by grants from the Natural Scientific Foundation of China (grant numbers: 81401399, 81560283, and 81201084), the Guangdong Basic and Applied Basic Research Foundation (2019A1515011143, 2020A1515011332, and 2022A1515012503).

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Author notes

  1. Xiaoshan Lin and Zhipeng Li contributed equally to this work.

Authors and Affiliations

  1. Department of Radiology, Huazhong University of Science and Technology Union Shenzhen Hospital, Shenzhen, 518052, China

    Xiaoshan Lin, Shengli Chen & Yingwei Qiu

  2. Department of Medical Imaging, Sun Yat-sen University Cancer Center, State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangzhou, 510060, China

    Zhipeng Li, Yadi Yang, Haoqiang He & Xiaofei Lv

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  1. Xiaoshan Lin
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Correspondence to Xiaofei Lv or Yingwei Qiu.

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Guarantor

The scientific guarantor of this publication is Yingwei Qiu.

Conflict of interest

The authors of this manuscript declare no relationships with any companies, whose products or services may be related to the subject matter of the article.

Statistics and biometry

One of the authors (Yingwei Qiu) has significant statistical expertise.

Informed consent

Written informed consent was obtained from all subjects (patients) in this study.

Ethical approval

Sun Yat-sen University Cancer Center Institutional Review Board approval was obtained.

Study subjects or cohorts overlap

Sixty-one study subjects have been previously reported in our prior publication, title: Irradiation-related longitudinal white matter atrophy underlies cognitive impairment in patients with nasopharyngeal carcinoma, which is published in Brain Imaging and Behavior 15, 2426–2435 (2021). In our previous study, we tried to longitudinally investigate alterations in cerebral WM volume as a function of irradiation dose and time after standard radiotherapy in NPC patients. Based on our previous study, we further attempted to elucidate the divergent change trajectories of temporal WM volume in NPC patients with different outcomes (RN or no RN), and to determine whether WM volume alterations at early stage could predict RN occurrence at late-delay stage.

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• prospective

• case-control study

• performed at one institution

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The original online version of this article was revised: The authors Xiaoshan Lin and Zhipeng Li are now referenced as equally contributing authors.

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Lin, X., Li, Z., Chen, S. et al. Divergent white matter changes in patients with nasopharyngeal carcinoma post-radiotherapy with different outcomes: a potential biomarker for prediction of radiation necrosis. Eur Radiol 32, 7036–7047 (2022). https://doi.org/10.1007/s00330-022-08907-z

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