Share:
Share this content in WeChat
X
Clinical Article
Surface-based morphological study on the relationship between cortical surface morphological changes and cancer-related fatigue changes in early chemotherapy for breast cancer
ZHOU Yanfei  LI Jing  FU Xiao  YUAN Wenjuan  WANG Hongzhi  YANG Lizhuang  LI Hai 

Cite this article as: ZHOU Y F, LI J, FU X, et al. Surface-based morphological study on the relationship between cortical surface morphological changes and cancer-related fatigue changes in early chemotherapy for breast cancer[J]. Chin J Magn Reson Imaging, 2024, 15(2): 48-55. DOI:10.12015/issn.1674-8034.2024.02.007.


[Abstract] Objective To study the early changes in cortical surface morphology in breast cancer patients in the early stage of chemotherapy and its relationship with cancer-related fatigue (CRF).Materials and Methods Twenty-five first-diagnosed female breast cancer patients were taken for neuropsychological tests such as Brief Fatigue Inventory (BFI), Hamilton Depression Scale (HAMD), and Hamilton Anxiety Scale (HAMA) and cranial magnetic resonance 3D-T1-weighted data acquisition before (within one week before the start of chemotherapy) and during (within two weeks of the end of the second cycle of chemotherapy) postoperative chemotherapy, respectively. Age-matched healthy women were recruited as a control group during the same period, and clinical information and magnetic resonance data were collected using the same assessed approach during the matched time intervals. Surface-based morphometry (SBM) was used to analyze the surface morphology of the cerebral cortex of all subjects using the computational anatomy toolbox 12 (CAT 12) in the statistical parametric mapping 12 (SPM 12) software, and SPSS 26.0 was used to analyze the correlation between brain areas with altered surface morphology of the cortex and longitudinal changes in CRF during chemotherapy in breast cancer patients.Results Compared with the pre-chemotherapy period, the differences in CRF, depression, and anxiety measurement scores of breast cancer patients in the early stage of chemotherapy were statistically significant (P<0.05). The values of cortical thickness, sulcal depth, fractal dimension, and gyrification index parameter of cortical surface morphology of breast cancer patients during chemotherapy changed compared with that of the pre-chemotherapy period. The differences were statistically significant (P<0.05): there was a reduction in cortical thickness in the parietal lobes (bilateral precuneus, right supramarginal, right postcentral) and occipital lobes (bilateral cuneus), a reduction in sulcus depth in the parietal lobes (bilateral inferiorparietal, right supramarginal and superiorparietal), the temporal lobes (right fusiform, superiortemporal and inferiortemporal), the occipital lobes (bilateral lateraloccipital, right cuneus, right pericalcarine), and a reduction in the number of fractal dimensions in the right frontal lobes (superiorfrontal, rostralmiddlefrontal and parsorbitalis), the right parietal lobes (supramarginal and inferiorparietal), and the left occipital lobes (lateraloccipital); The brain regions with increased parameter values were increased gyrification index in the left occipital lobe (lateraloccipital and cuneus), right parietal lobe (supramarginal, superiorparietal, and inferiorparietal), and right temporal lobe (middletemporal, inferiortemporal, and bankssts). Changes in the fractal dimension of the right rostralmiddlefrontal in the early phase of chemotherapy were negatively correlated with longitudinal changes in CRF compared with the pre-chemotherapy phase (r=-0.628, P=0.001).Conclusions Cortical surface morphology in breast cancer patients can undergo early changes during chemotherapy and associated with changes in CRF.
[Keywords] breast cancer;chemotherapy;cancer-related fatigue;cerebral cortex;magnetic resonance imaging

ZHOU Yanfei1, 2   LI Jing3   FU Xiao1, 2   YUAN Wenjuan2   WANG Hongzhi2   YANG Lizhuang1, 2   LI Hai1, 2*  

1 Department of Radiology, Hefei Cancer Hospital, Chinese Academy of Sciences, Hefei 230000, China

2 Institute of Health and Medical Technology, Hefei Institutes of Physical Science, Chinese Academy of Sciences, Hefei 230031, China

3 Breast Center, Hefei Cancer Hospital, Chinese Academy of Sciences, Hefei 230000, China

Corresponding author: LI H, E-mail: hli@cmpt.ac.cn

Conflicts of interest   None.

Received  2023-08-08
Accepted  2024-01-30
DOI: 10.12015/issn.1674-8034.2024.02.007
Cite this article as: ZHOU Y F, LI J, FU X, et al. Surface-based morphological study on the relationship between cortical surface morphological changes and cancer-related fatigue changes in early chemotherapy for breast cancer[J]. Chin J Magn Reson Imaging, 2024, 15(2): 48-55. DOI:10.12015/issn.1674-8034.2024.02.007.

[1]
SUNG H, FERLAY J, SIEGEL R L, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries[J]. CA Cancer J Clin, 2021, 71(3): 209-249. DOI: 10.3322/caac.21660.
[2]
AHLES T A, ROOT J C. Cognitive effects of cancer and cancer treatments[J/OL]. Annu Rev Clin Psychol, 2018, 14: 425-451 [2023-08-07]. https://pubmed.ncbi.nlm.nih.gov/29345974/. DOI: 10.1146/annurev-clinpsy-050817-084903.
[3]
LIU Y C, HUNG T T, KONARA MUDIYANSELAGE S P, et al. Beneficial exercises for cancer-related fatigue among women with breast cancer: a systematic review and network meta-analysis[J/OL]. Cancers, 2022, 15(1): 151 [2023-08-07]. https://pubmed.ncbi.nlm.nih.gov/36612147/. DOI: 10.3390/cancers15010151.
[4]
BERGER A M, MOONEY K, ALVAREZ-PEREZ A, et al. Cancer-related fatigue, version 2.2015[J]. J Natl Compr Canc Netw, 2015, 13(8): 1012-1039. DOI: 10.6004/jnccn.2015.0122.
[5]
PATRICK D L, FERKETICH S L, FRAME P S, et al. National Institutes of Health State-of-the-Science Conference Statement: symptom management in cancer: pain, depression, and fatigue, July 15-17, 2002[J]. J Natl Cancer Inst Monogr, 2004(32): 9-16. DOI: 10.1093/jncimonographs/djg014.
[6]
ARYA N, VAISH A, ZHAO K, et al. Neural mechanisms underlying breast cancer related fatigue: a systematic review of neuroimaging studies[J/OL]. Front Neurosci, 2021, 15: 735945 [2023-08-07]. https://pubmed.ncbi.nlm.nih.gov/34858127/. DOI: 10.3389/fnins.2021.735945.
[7]
BEKELE B M, LUIJENDIJK M, SCHAGEN S B, et al. Fatigue and resting-state functional brain networks in breast cancer patients treated with chemotherapy[J]. Breast Cancer Res Treat, 2021, 189(3): 787-796. DOI: 10.1007/s10549-021-06326-0.
[8]
ZICK S M, ZWICKEY H, WOOD L, et al. Preliminary differences in peripheral immune markers and brain metabolites between fatigued and non-fatigued breast cancer survivors: a pilot study[J]. Brain Imaging Behav, 2014, 8(4): 506-516. DOI: 10.1007/s11682-013-9270-z.
[9]
KESLER S R, KENT J S, O'HARA R. Prefrontal cortex and executive function impairments in primary breast cancer[J]. Arch Neurol, 2011, 68(11): 1447-1453. DOI: 10.1001/archneurol.2011.245.
[10]
MENNING S, DE RUITER M B, VELTMAN D J, et al. Multimodal MRI and cognitive function in patients with breast cancer prior to adjuvant treatment: the role of fatigue[J/OL]. Neuroimage Clin, 2015, 7: 547-554 [2023-08-07]. https://pubmed.ncbi.nlm.nih.gov/25844311/. DOI: 10.1016/j.nicl.2015.02.005.
[11]
AHLES T A, SAYKIN A J. Candidate mechanisms for chemotherapy-induced cognitive changes[J]. Nat Rev Cancer, 2007, 7(3): 192-201. DOI: 10.1038/nrc2073.
[12]
TAILLIBERT S, LE RHUN E, CHAMBERLAIN M C. Chemotherapy-related neurotoxicity[J/OL]. Curr Neurol Neurosci Rep, 2016, 16(9): 81 [2023-08-07]. https://pubmed.ncbi.nlm.nih.gov/27443648/. DOI: 10.1007/s11910-016-0686-x.
[13]
RUIZ-CASADO A, ÁLVAREZ-BUSTOS A, DE PEDRO C G, et al. Cancer-related fatigue in breast cancer survivors: a review[J]. Clin Breast Cancer, 2021, 21(1): 10-25. DOI: 10.1016/j.clbc.2020.07.011.
[14]
WANG L, ZHOU F Q. Research progress on neuroimaging biomarkers of chemotherapy-related cognitive impairment in breast cancer[J]. Chin J Magn Reson Imag, 2022, 13(2): 112-115. DOI: 10.12015/issn.1674-8034.2022.02.027.
[15]
LI X, CHEN H J, LV Y, et al. Diminished gray matter density mediates chemotherapy dosage-related cognitive impairment in breast cancer patients[J/OL]. Sci Rep, 2018, 8(1): 13801 [2023-08-07]. https://pubmed.ncbi.nlm.nih.gov/30218006/. DOI: 10.1038/s41598-018-32257-w.
[16]
LEPAGE C, SMITH A M, MOREAU J, et al. A prospective study of grey matter and cognitive function alterations in chemotherapy-treated breast cancer patients[J/OL]. Springerplus, 2014, 3: 444 [2023-08-07]. https://pubmed.ncbi.nlm.nih.gov/25184110/. DOI: 10.1186/2193-1801-3-444.
[17]
PERRIER J, VIARD A, LEVY C, et al. Longitudinal investigation of cognitive deficits in breast cancer patients and their gray matter correlates: impact of education level[J]. Brain Imaging Behav, 2020, 14(1): 226-241. DOI: 10.1007/s11682-018-9991-0.
[18]
RICCELLI R, TOSCHI N, NIGRO S, et al. Surface-based morphometry reveals the neuroanatomical basis of the five-factor model of personality[J]. Soc Cogn Affect Neurosci, 2017, 12(4): 671-684. DOI: 10.1093/scan/nsw175.
[19]
GHOSH A, KAUR S, SHAH R, et al. Surface-based brain morphometry in schizophrenia vs. cannabis-induced psychosis: a controlled comparison[J/OL]. J Psychiatr Res, 2022, 155: 286-294 [2023-08-07]. https://pubmed.ncbi.nlm.nih.gov/36170756/. DOI: 10.1016/j.jpsychires.2022.09.034.
[20]
MENNING S, DE RUITER M B, VELTMAN D J, et al. Changes in brain activation in breast cancer patients depend on cognitive domain and treatment type[J/OL]. PLoS One, 2017, 12(3): e0171724 [2023-08-07]. https://pubmed.ncbi.nlm.nih.gov/28267750/. DOI: 10.1371/journal.pone.0171724.
[21]
NASREDDINE Z S, PHILLIPS N A, BÉDIRIAN V, et al. The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment[J]. J Am Geriatr Soc, 2005, 53(4): 695-699. DOI: 10.1111/j.1532-5415.2005.53221.x.
[22]
The Committee of Rehabilitation and Palliative Care, China, The Committee of Tumor Support and Rehabilitation Therapy, Chinese Society of Clinical Oncology. China expert consensus on diagnosis and treatment of cancer-related fatigue[J]. Natl Med J China, 2022, 102(3): 180-189. DOI: 10.3760/cma.j.cn112137-20210811-01789.
[23]
LU W, WANG H, LIN Y X, et al. Psychological status of medical workforce during the COVID-19 pandemic: a cross-sectional study[J/OL]. Psychiatry Res, 2020, 288: 112936 [2023-08-07]. https://pubmed.ncbi.nlm.nih.gov/32276196/. DOI: 10.1016/j.psychres.2020.112936.
[24]
PARK J H, JUNG Y S, JUNG Y M, et al. The role of depression in the relationship between cognitive decline and quality of life among breast cancer patients[J]. Support Care Cancer, 2019, 27(7): 2707-2714. DOI: 10.1007/s00520-018-4546-x.
[25]
CHEN B T, YE N R, WONG C W, et al. Effects of chemotherapy on aging white matter microstructure: a longitudinal diffusion tensor imaging study[J]. J Geriatr Oncol, 2020, 11(2): 290-296. DOI: 10.1016/j.jgo.2019.09.016.
[26]
ZHANG J Y, ZHOU Y Q, FENG Z W, et al. Longitudinal trends in anxiety, depression, and quality of life during different intermittent periods of adjuvant breast cancer chemotherapy[J]. Cancer Nurs, 2018, 41(1): 62-68. DOI: 10.1097/NCC.0000000000000451.
[27]
SERVAES P, GIELISSEN M F, VERHAGEN S, et al. The course of severe fatigue in disease-free breast cancer patients: a longitudinal study[J]. Psychooncology, 2007, 16(9): 787-795. DOI: 10.1002/pon.1120.
[28]
FANN J R, THOMAS-RICH A M, KATON W J, et al. Major depression after breast cancer: a review of epidemiology and treatment[J]. Gen Hosp Psychiatry, 2008, 30(2): 112-126. DOI: 10.1016/j.genhosppsych.2007.10.008.
[29]
PANTONI L, MARZI C, POGGESI A, et al. Fractal dimension of cerebral white matter: a consistent feature for prediction of the cognitive performance in patients with small vessel disease and mild cognitive impairment[J/OL]. Neuroimage Clin, 2019, 24: 101990 [2023-08-07]. https://pubmed.ncbi.nlm.nih.gov/31491677/. DOI: 10.1016/j.nicl.2019.101990.
[30]
NIU R N, DU M Y, REN J, et al. Chemotherapy-induced grey matter abnormalities in cancer survivors: a voxel-wise neuroimaging meta-analysis[J]. Brain Imaging Behav, 2021, 15(4): 2215-2227. DOI: 10.1007/s11682-020-00402-7.
[31]
HAN Y, YANG Q L, ZHAO Y J, et al. Diffusion kurtosis imaging study on changes of brain microstructure and cognitive function in breast cancer survivors with chemotherapy[J]. Chin J Magn Reson Imag, 2022, 13(4): 111-114. DOI: 10.12015/issn.1674-8034.2022.04.021.
[32]
ZHOU X Y, TAN Y, YU H, et al. Early alterations in cortical morphology after neoadjuvant chemotherapy in breast cancer patients: a longitudinal magnetic resonance imaging study[J]. Hum Brain Mapp, 2022, 43(15): 4513-4528. DOI: 10.1002/hbm.25969.
[33]
ZHANG H W, LI P, LIU T H, et al. Focal white matter microstructural alteration after anthracycline-based systemic treatment in long-term breast cancer survivors: a structural magnetic resonance imaging study[J]. Brain Imaging Behav, 2022, 16(2): 843-854. DOI: 10.1007/s11682-021-00551-3.
[34]
PHILLIPS N S, RAO V, KMETZ L, et al. Changes in brain functional and effective connectivity after treatment for breast cancer and implications for intervention targets[J]. Brain Connect, 2022, 12(4): 385-397. DOI: 10.1089/brain.2021.0049.
[35]
HU Y X, YU F, ZHANG J Q, et al. Changes of resting-state brain functional activities in breast cancer patients after neoadjuvant chemotherapy: a short-term longitudinal study[J]. Chin J Magn Reson Imag, 2022, 13(2): 31-36. DOI: 10.12015/issn.1674-8034.2022.02.007.
[36]
YANG J, DENG Y C, LIU D H, et al. Brain network deficits in breast cancer patients after early neoadjuvant chemotherapy: a longitudinal MRI study[J]. J Neurosci Res, 2023, 101(7): 1138-1153. DOI: 10.1002/jnr.25178.
[37]
APPLE A C, SCHROEDER M P, RYALS A J, et al. Hippocampal functional connectivity is related to self-reported cognitive concerns in breast cancer patients undergoing adjuvant therapy[J/OL]. Neuroimage Clin, 2018, 20: 110-118 [2023-08-07]. https://pubmed.ncbi.nlm.nih.gov/30094161/. DOI: 10.1016/j.nicl.2018.07.010.
[38]
TANGLAY O, YOUNG I M, DADARIO N B, et al. Anatomy and white-matter connections of the precuneus[J]. Brain Imaging Behav, 2022, 16(2): 574-586. DOI: 10.1007/s11682-021-00529-1.
[39]
ASTAFIEV S V, STANLEY C M, SHULMAN G L, et al. Extrastriate body area in human occipital cortex responds to the performance of motor actions[J]. Nat Neurosci, 2004, 7(5): 542-548. DOI: 10.1038/nn1241.
[40]
LIN Y H, YOUNG I M, CONNER A K, et al. Anatomy and white matter connections of the inferior temporal gyrus[J/OL]. World Neurosurg, 2020, 143: e656-e666 [2023-08-07]. https://pubmed.ncbi.nlm.nih.gov/32798785/. DOI: 10.1016/j.wneu.2020.08.058.
[41]
CHEN B T, SETHI S K, JIN T H, et al. Assessing brain volume changes in older women with breast cancer receiving adjuvant chemotherapy: a brain magnetic resonance imaging pilot study[J/OL]. Breast Cancer Res, 2018, 20(1): 38 [2023-08-07]. https://pubmed.ncbi.nlm.nih.gov/29720224/. DOI: 10.1186/s13058-018-0965-3.
[42]
ZIUKELIS E T, MAK E, DOUNAVI M E, et al. Fractal dimension of the brain in neurodegenerative disease and dementia: a systematic review[J/OL]. Ageing Res Rev, 2022, 79: 101651 [2023-08-07]. https://pubmed.ncbi.nlm.nih.gov/35643264/. DOI: 10.1016/j.arr.2022.101651.
[43]
OTTO L D, RUSSART K L G, KULKARNI P, et al. Paclitaxel chemotherapy elicits widespread brain anisotropy changes in a comprehensive mouse model of breast cancer survivorship: evidence from in vivo diffusion weighted imaging[J/OL]. Front Oncol, 2022, 12: 798704 [2023-08-07]. https://pubmed.ncbi.nlm.nih.gov/35402248/. DOI: 10.3389/fonc.2022.798704.

PREV Apparent diffusion coefficient distinguishes histologic typing of lung cancer brain metastases and its correlation with the Ki-67 proliferation index
NEXT Resting MRI study on the effect of δ-catenin over expression on short-term brain cognitive function in breast cancer patients after chemotherapy
  



Tel & Fax: +8610-67113815    E-mail: editor@cjmri.cn