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Amide proton transfer weighted and diffusion-weighted imaging in evaluating rectal cancer tumor budding grade value
DU Yunxia  XU Wenxiang  HE Yuqi  SUN Yun  LI Feixiang  CAI Wei  HUANG Gang 

Cite this article as: DU Y X, XU W X, HE Y Q, et al. Amide proton transfer weighted and diffusion-weighted imaging in evaluating rectal cancer tumor budding grade value[J]. Chin J Magn Reson Imaging, 2025, 16(1): 42-47, 73. DOI:10.12015/issn.1674-8034.2025.01.007.


[Abstract] Objective To explore the value of amide proton transfer weighted (APTw) imaging with apparent diffusion coefficient (ADC) in the preoperative assessment of tumor budding (TB) grade in rectal cancer.Materials and Methods We retrospectively analyzed the clinical and imaging data of 121 patients with rectal cancer. Based on pathological tumor budding counts, the patients were categorized into intermediate-low-grade and high-grade groups. The APT and ADC values were compared between the two groups, and the correlation between APT and ADC values and TB grades was investigated. Intra-class correlation coefficients (ICC) were used to assess the consistency of data measured by the observer before and after evaluation. Binary logistic regression comprehensive input method was employed to analyze the association between variables and the grade of rectal cancer tumor budding. Receiver operating characteristic (ROC) curves were utilized to assess the statistical significance of parameters and their combined efficacy. The area under the curve (AUC) along with its 95% confidence interval, as well as corresponding thresholds, sensitivities, and specificities, were calculated. DeLong tests were conducted to compare the differences in AUC. Spearman correlation analysis was performed to investigate the relationship between each parameter and tumor budding.Results One hundred and twenty-one patients were enrolled, The distribution of TB grade was intermediate-low grade (n = 69) and high-grade (n = 52). The APT and ADC values measured by the two observers showed good consistency, with ICC values were 0.925, 0.877. The APT value for intermediate-low grade TB of rectal cancer was significantly lower (2.068% ± 0.588%) compared to high-grade TB (3.167% ± 0.592%) (P < 0.001). Additionally, the ADC value for intermediate-low grade rectal cancer TB [(1.064 ± 0.131) × 10-3 mm2/s] was higher than that of the high-grade TB group [(0.903 ± 0.138) × 10-3 mm2/s]. In multivariate analysis, APT value [OR: 15.079 (95% CI: 4.822 to 47.154)] and ADC value [OR: 0.004 (95% CI: 0.001 to 0.228)] were identified as independent risk factors for predicting TB grades. The areas under the curve (AUC) for APT, ADC, and their combined assessment of rectal cancer tumor budding grade were 0.916, 0.821, and 0.918, respectively. The DeLong test results showed statistically significant differences in AUCs between ADC and APT values, as well as their combined assessment of TB grade (P = 0.024, 0.004). The decision curve shows that the combination of the two has higher clinical value than using APT and ADC values alone. APT values exhibited a moderate positive correlation with TB grade (r = 0.713, P < 0.001), while ADC values demonstrated a moderate negative correlation with TB grade (r = -0.550, P < 0.001).Conclusions APT and ADC can effectively assess the TB grade of rectal cancer and have some clinical applications, and the combination of APT and ADC can significantly improve the diagnostic efficacy.
[Keywords] rectal cancer;tumor budding;magnetic resonance imaging;amide proton transfer imaging;apparent diffusion coefficient

DU Yunxia1   XU Wenxiang1   HE Yuqi1   SUN Yun1   LI Feixiang1   CAI Wei2   HUANG Gang3*  

1 The First Clinical Medical College of Gansu University of Chinese Medicine, Lanzhou 730000, China

2 Department of Pathology, Gansu Provincial Hospital, Lanzhou 730000, China

3 Department of Radiology, Gansu Provincial Hospital, Lanzhou 730000, China

Corresponding author: HUANG G, E-mail: huang_g2024@163.com

Conflicts of interest   None.

Received  2024-10-18
Accepted  2025-01-10
DOI: 10.12015/issn.1674-8034.2025.01.007
Cite this article as: DU Y X, XU W X, HE Y Q, et al. Amide proton transfer weighted and diffusion-weighted imaging in evaluating rectal cancer tumor budding grade value[J]. Chin J Magn Reson Imaging, 2025, 16(1): 42-47, 73. DOI:10.12015/issn.1674-8034.2025.01.007.

[1]
General Office of National Health Commission of the People's Republic of China, Oncology Branch of the Chinese Medical Association. The Standard for Diagnosis and Treatment of Chinese Colorectal Cancer(2023 Version)[J]. Med J Peking Union Med Coll Hosp, 2023, 14(4): 706-733. DOI: 10.12290/xhyxzz.2023-0315.
[2]
BRAY F, LAVERSANNE M, SUNG H, et al. Global cancer statistics 2022: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries[J]. CA Cancer J Clin, 2024, 74(3): 229-263. DOI: 10.3322/caac.21834.
[3]
YAO H W, LI X X, CUI L, et al. Annual report of Chinese colorectal cancer surgery database in 2022: a nationwide registry study[J]. Chin J Pract Surg, 2023, 43(1): 93-99. DOI: 10.19538/j.cjps.issn1005-2208.2023.01.13.
[4]
BENSON A B, VENOOK A P, AL-HAWARY M M, et al. Rectal cancer, version 2.2022, NCCN clinical practice guidelines in oncology[J]. J Natl Compr Canc Netw, 2022, 20(10): 1139-1167. DOI: 10.6004/jnccn.2022.0051.
[5]
FADEL M G, AHMED M, SHAW A, et al. Oncological outcomes of local excision versus radical surgery for early rectal cancer in the context of staging and surveillance: a systematic review and meta-analysis[J/OL]. Cancer Treat Rev, 2024, 128: 102753 [2024-03-04]. https://pubmed.ncbi.nlm.nih.gov/38761791/. DOI: 10.1016/j.ctrv.2024.102753.
[6]
LUGLI A, ZLOBEC I, BERGER M D, et al. Tumour budding in solid cancers[J]. Nat Rev Clin Oncol, 2021, 18(2): 101-115. DOI: 10.1038/s41571-020-0422-y.
[7]
VAN WYK H C, PARK J, ROXBURGH C, et al. The role of tumour budding in predicting survival in patients with primary operable colorectal cancer: a systematic review[J]. Cancer Treat Rev, 2015, 41(2): 151-159. DOI: 10.1016/j.ctrv.2014.12.007.
[8]
ROGERS A C, WINTER D C, HEENEY A, et al. Systematic review and meta-analysis of the impact of tumour budding in colorectal cancer[J]. Br J Cancer, 2016, 115(7): 831-840. DOI: 10.1038/bjc.2016.274.
[9]
LUGLI A, KIRSCH R, AJIOKA Y, et al. Recommendations for reporting tumor budding in colorectal cancer based on the International Tumor Budding Consensus Conference (ITBCC) 2016[J]. Mod Pathol, 2017, 30(9): 1299-1311. DOI: 10.1038/modpathol.2017.46.
[10]
TROTSYUK I, SPARSCHUH H, MÜLLER A J, et al. Tumor budding outperforms ypT and ypN classification in predicting outcome of rectal cancer after neoadjuvant chemoradiotherapy[J/OL]. BMC Cancer, 2019, 19(1): 1033 [2024-03-04]. https://pubmed.ncbi.nlm.nih.gov/31675950/. DOI: 10.1186/s12885-019-6261-5.
[11]
KIM S, HUH J W, LEE W Y, et al. Prognostic impact of lymphatic invasion, venous invasion, perineural invasion, and tumor budding in rectal cancer treated with neoadjuvant chemoradiotherapy followed by total mesorectal excision[J]. Dis Colon Rectum, 2023, 66(7): 905-913. DOI: 10.1097/DCR.0000000000002266.
[12]
JÄGER T, NEUREITER D, FALLAHA M, et al. The potential predictive value of tumor budding for neoadjuvant chemoradiotherapy response in locally advanced rectal cancer[J]. Strahlenther Onkol, 2018, 194(11): 991-1006. DOI: 10.1007/s00066-018-1340-0.
[13]
ZHOU J Y, PAYEN J F, WILSON D A, et al. Using the amide proton signals of intracellular proteins and peptides to detect pH effects in MRI[J]. Nat Med, 2003, 9(8): 1085-1090. DOI: 10.1038/nm907.
[14]
ZHOU J Y, ZAISS M, KNUTSSON L, et al. Review and consensus recommendations on clinical APT-weighted imaging approaches at 3T: Application to brain tumors[J]. Magn Reson Med, 2022, 88(2): 546-574. DOI: 10.1002/mrm.29241.
[15]
PADHANI A R, KOH D M, COLLINS D J. Whole-body diffusion-weighted MR imaging in cancer: current status and research directions[J]. Radiology, 2011, 261(3): 700-718. DOI: 10.1148/radiol.11110474.
[16]
CHEN W C, LI L, YAN Z X, et al. Three-dimension amide proton transfer MRI of rectal adenocarcinoma: correlation with pathologic prognostic factors and comparison with diffusion kurtosis imaging[J]. Eur Radiol, 2021, 31(5): 3286-3296. DOI: 10.1007/s00330-020-07397-1.
[17]
XIANG Y, ZHANG Q J, CHEN X, et al. Synthetic MRI and amide proton transfer-weighted MRI for differentiating between benign and malignant sinonasal lesions[J]. Eur Radiol, 2024, 34(10): 6820-6830. DOI: 10.1007/s00330-024-10696-6.
[18]
BULENS P, COUWENBERG A, INTVEN M, et al. Predicting the tumor response to chemoradiotherapy for rectal cancer: Model development and external validation using MRI radiomics[J]. Radiother Oncol, 2020, 142: 246-252. DOI: 10.1016/j.radonc.2019.07.033.
[19]
ZHAO X Y, XIE P Y, WANG M M, et al. Deep learning-based fully automated detection and segmentation of lymph nodes on multiparametric-MRI for rectal cancer: a multicentre study[J/OL]. EBioMedicine, 2020, 56: 102780 [2024-03-04]. https://pubmed.ncbi.nlm.nih.gov/32512507/. DOI: 10.1016/j.ebiom.2020.102780.
[20]
ZHANG P, DING W W, WANG A J, et al. Diagnostic application of amide proton transfer imaging combined with three-dimensional arterial spin labeling in patients with high-grade brain tumor[J]. Chin J Med Imag, 2022, 30(10): 981-985. DOI: 10.3969/j.issn.1005-5185.2022.10.002.
[21]
SCHÖN S, CABELLO J, LIESCHE-STARNECKER F, et al. Imaging glioma biology: spatial comparison of amino acid PET, amide proton transfer, and perfusion-weighted MRI in newly diagnosed gliomas[J]. Eur J Nucl Med Mol Imaging, 2020, 47(6): 1468-1475. DOI: 10.1007/s00259-019-04677-x.
[22]
ZHOU J Y, HEO H Y, KNUTSSON L, et al. APT-weighted MRI: Techniques, current neuro applications, and challenging issues[J]. J Magn Reson Imaging, 2019, 50(2): 347-364. DOI: 10.1002/jmri.26645.
[23]
DE SMEDT L, PALMANS S, ANDEL D, et al. Expression profiling of budding cells in colorectal cancer reveals an EMT-like phenotype and molecular subtype switching[J]. Br J Cancer, 2017, 116(1): 58-65. DOI: 10.1038/bjc.2016.382.
[24]
PAVLIČ A, BOŠTJANČIČ E, KAVALAR R, et al. Tumour budding and poorly differentiated clusters in colon cancer-different manifestations of partial epithelial-mesenchymal transition[J]. J Pathol, 2022, 258(3): 278-288. DOI: 10.1002/path.5998.
[25]
ZHENG S K, VAN DER BOM I M J, ZU Z L, et al. Chemical exchange saturation transfer effect in blood[J]. Magn Reson Med, 2014, 71(3): 1082-1092. DOI: 10.1002/mrm.24770.
[26]
ZHOU Z, SHEN F, LU H D, et al. The value of dynamic contrast-enhanced magnetic resonance imaging for preoperative evaluation of the tumor budding of rectal cancer[J]. Chin Comput Med Imag, 2022, 28(4): 379-384. DOI: 10.19627/j.cnki.cn31-1700/th.2022.04.002.
[27]
MOORES M, JOUNDI R A, SINGH N, et al. Magnetic resonance imaging assists with determining etiology after transient ischemic attack or minor stroke[J/OL]. J Am Heart Assoc, 2024, 13(7): e033817 [2024-03-04]. https://pubmed.ncbi.nlm.nih.gov/38533977/. DOI: 10.1161/JAHA.123.033817.
[28]
ZHANG G W, XU Z L, ZHENG J Y, et al. Prognostic value of multi b-value DWI in patients with locally advanced rectal cancer[J]. Eur Radiol, 2023, 33(3): 1928-1937. DOI: 10.1007/s00330-022-09159-7.
[29]
FENG F W, LIU Y Q, HU S, et al. The value of whole-volume ADC histogram analysis combined with ADC value in preoperatively prediction of tumor deposits in rectal cancer[J]. Chin J Magn Reson Imag, 2024, 15(4): 88-92. DOI: 10.12015/issn.1674-8034.2024.04.014.
[30]
CHEN F Y, ZHANG S T, MA X L, et al. Prediction of tumor budding in patients with rectal adenocarcinoma using b-value threshold map[J]. Eur Radiol, 2023, 33(2): 1353-1363. DOI: 10.1007/s00330-022-09087-6.
[31]
WU M H, JIANG T L, GUO M, et al. Amide proton transfer-weighted imaging and derived radiomics in the classification of adult-type diffuse gliomas[J]. Eur Radiol, 2024, 34(5): 2986-2996. DOI: 10.1007/s00330-023-10343-6.
[32]
ZHENG X, LU T Y, TANG Q, et al. The clinical value of applying diffusion-weighted imaging combined with T2-weighted imaging to assess diagnostic performance of muscularis propria invasion in mid-to-high rectal cancer[J/OL]. Abdom Radiol, 2024 [2024-12-27]. https://pubmed.ncbi.nlm.nih.gov/39207517/. DOI: 10.1007/s00261-024-04536-w.
[33]
CHEN W C, MAO L T, LI L, et al. Predicting treatment response of neoadjuvant chemoradiotherapy in locally advanced rectal cancer using amide proton transfer MRI combined with diffusion-weighted imaging[J/OL]. Front Oncol, 2021, 11: 698427 [2024-12-28]. https://pubmed.ncbi.nlm.nih.gov/34277445/. DOI: 10.3389/fonc.2021.698427.

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