Extramural venous invasion in gastric cancer: 9.4T magnetic resonance imaging assessment and circular RNA functional analysis

doi:10.3748/wjg.v31.i14.99897

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World Journal of Gastroenterology

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1007-9327

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World J Gastroenterol. Apr 14, 2025; 31(14): 99897
Published online Apr 14, 2025. doi: 10.3748/wjg.v31.i14.99897

Extramural venous invasion in gastric cancer: 9.4T magnetic resonance imaging assessment and circular RNA functional analysis

Cai-Zhen Feng, Xin-Yi Gou, Yi-Qun Liu, Yu-Wei Xin, Yin-Li Zhang, Hui-Min Zhao, Sheng-Cai Wei, Nan Hong, Yi Wang, Jin Cheng

Cai-Zhen Feng, Xin-Yi Gou, Sheng-Cai Wei, Nan Hong, Yi Wang, Jin Cheng, Department of Radiology, Peking University People’s Hospital, Beijing 100044, China

Yi-Qun Liu, Yu-Wei Xin, Department of Ultrasound, Peking University People’s Hospital, Beijing 100044, China

Yin-Li Zhang, Hui-Min Zhao, Department of Pathology, Peking University People’s Hospital, Beijing 100044, China

Co-first authors: Cai-Zhen Feng and Xin-Yi Gou.

Co-corresponding authors: Yi Wang and Jin Cheng.

Author contributions: Wang Y and Cheng J contributed to conceptualization; Xin YW, Zhang YL, Zhao HM, and Wei SC contributed to methodology and software; Feng CZ, Liu YQ and Gou XY contributed to Validation, formal analysis and investigation; Liu YQ, Zhang YL and Hong N contributed to resources; Feng CZ, Liu YQ and Gou XY contributed to data curation; Feng CZ and Gou XY contributed to writing - original draft; Feng CZ, Liu YQ, Gou XY and Cheng J contributed to writing - review and editing; Hong N contributed to supervision; Wang Y and Cheng J contributed to project administration and funding acquisition. All authors have read and approved the final manuscript. Feng CZ performed animal experiments and cell functional assays, participated in data interpretation, and contributed to manuscript drafting and revision. Gou XY conducted target gene screening and bioinformatics analysis, assisted in data curation, and co-authored the initial manuscript. Both Feng CZ and Gou XY made substantial and indispensable contributions to this study, thereby qualifying as co-first authors. Wang Y conceptualized and designed the research framework, supervised all experimental and analytical processes, secured funding, and led the critical revision and finalization of the manuscript. Cheng J spearheaded data analysis and mechanistic reinterpretation, optimized experimental design, participated in manuscript preparation, and co-acquired financial support. As co-corresponding authors, Wang Y and Cheng J played pivotal roles in project oversight, intellectual guidance, and ensuring the academic rigor of this work. The synergistic collaboration between Wang Y and Cheng J was essential for integrating multi-dimensional data, refining the manuscript’s focus on the relationship between extramural venous invasion and circular RNAs in gastric cancer, and advancing subsequent research phases.

Supported by The National Natural Science Foundation of China, No. 81901819; Peking University People’s Hospital Scientific Research Development Funds, No. RDX2024-08; and Beijing Natural Science Foundation, No. 7232187.

Institutional review board statement: The institutional review board of the Peking University People's Hospital approved this study (No. 2019PHB171-01), and the requirement for informed consent was waived.

Institutional animal care and use committee statement: All procedures involving animals were reviewed and approved by the Institutional Animal Care and Use Committee of the Peking University People's Hospital (IACUC protocol number: 2019PHE058).

Conflict-of-interest statement: All the authors report no relevant conflicts of interest for this article.

ARRIVE guidelines statement: The authors have read the ARRIVE guidelines, and the manuscript was prepared and revised according to the ARRIVE guidelines.

Data sharing statement: The data that support the findings of this study are available on request from the corresponding author at chengjinpkuph@outlook.com.

Corresponding author: Jin Cheng, MD, Associate Professor, Department of Radiology, Peking University People’s Hospital, No. 11 Xizhimen South Street, Xicheng District, Beijing 100044, China. chengjinpkuph@outlook.com

Received: August 2, 2024
Revised: February 19, 2025
Accepted: March 17, 2025
Published online: April 14, 2025
Processing time: 251 Days and 19.7 Hours

Abstract

BACKGROUND

Extramural venous invasion (EMVI) is a critical prognostic factor in gastric cancer (GC); however, its detection and underlying molecular mechanisms remain underexplored.

AIM

To investigate the relationship between EMVI and expression of the circular RNA hsa_circ_0097977 in orthotopic GC mouse models.

METHODS

A retrospective analysis was conducted in addition to a preclinical animal study, involving 13 GC patients and 24 orthotopic GC mouse models, respectively. EMVI was assessed using axial T2-weighted fat suppression sequences on a 9.4T magnetic resonance imaging (MRI) with histopathological confirmation as the gold standard for EMVI. The impact of hsa_circ_0097977 on EMVI and GC cell function was evaluated. Statistical analyses comprised consistency, area under the curve analysis, correlation, χ²/Fisher exact, and Mann-Whitney U/t-tests, with significance set at P < 0.05.

RESULTS

EMVI was accurately detected using 9.4T MRI in orthotopic mouse models with an area under the curve of 0.843 (sensitivity 78.6%, specificity 90.0%). MRI detected EMVI was the only imaging factor associated with distant metastasis (P = 0.04). Furthermore, knockdown of hsa_circ_0097977 was the only factor associated with EMVI (P = 0.043, 0.038) and led to reduced invasion and increased apoptosis in GC cells.

CONCLUSION

EMVI, a risk factor for distant metastasis in GC, is detectable by 9.4T MRI and regulated by hsa_circ_0097977, making it a potential therapeutic target.

Keywords: Gastric cancer; Circular RNA; Extramural venous invasion; Orthotopic mouse model; Magnetic resonance imaging; Pathology; Radiogenomics

Core Tip: This study demonstrates that extramural venous invasion (EMVI), a risk factor for distant metastasis in gastric cancer (GC), can be accurately detected using 9.4T magnetic resonance imaging in orthotopic GC mouse models, with histopathological confirmation. The expression of hsa_circ_0097977, a circular RNA, was found to regulate EMVI, and its knockdown reduced tumor cell invasion and promoted apoptosis, suggesting its potential as a therapeutic target in GC. These findings highlight the clinical relevance of EMVI detection and the role of hsa_circ_0097977 in GC progression.