References
Nougaret S, Horta M, Sala E, Lakhman Y, Thomassin-Naggara I, Kido A, Masselli G, Bharwani N, Sadowski E, Ertmer A, Otero-Garcia M, Kubik-Huch RA, Cunha TM, Rockall A, Forstner R (2019) Endometrial cancer MRI staging: updated guidelines of the European Society of Urogenital Radiology. Eur Radiol 29:792–805
Kubik-Huch RA, Weston M, Nougaret S, Leonhardt H, Thomassin-Naggara I, Horta M, Cunha TM, Maciel C, Rockall A, Forstner R (2018) European Society of Urogenital Radiology (ESUR) Guidelines: MR imaging of leiomyomas. Eur Radiol 28:3125–3137
Chapron C, Vannuccini S, Santulli P, Abrão MS, Carmona F, Fraser IS, Gordts S, Guo SW, Just PA, Noël JC, Pistofidis G, van den Bosch T, Petraglia F (2020) Diagnosing adenomyosis: an integrated clinical and imaging approach. Hum Reprod Update 26:392–411
Nougaret S, Sbarra M, Robbins J (2020) Imaging spectrum of benign uterine disease and treatment options. Radiol Clin N Am 58:239–256
Huang YT, Huang YL, Ng KK, Lin G (2019) Current status of magnetic resonance imaging in patients with malignant uterine neoplasms: a review. Korean J Radiol 20:18–33
Zhou J, Lal B, Wilson DA, Laterra J, van Zijl PC (2003) Amide proton transfer (APT) contrast for imaging of brain tumors. Magn Reson Med 50:1120–1126
Zhou J, Heo HY, Knutsson L, van Zijl PCM, Jiang S (2019) APT-weighted MRI: techniques, current neuro applications, and challenging issues. J Magn Reson Imaging 50:347–364
Jiang S, Eberhart CG, Lim M, Heo HY, Zhang Y, Blair L, Wen Z, Holdhoff M, Lin D, Huang P, Qin H, Quinones-Hinojosa A, Weingart JD, Barker PB, Pomper MG, Laterra J, van Zijl PCM, Blakeley JO, Zhou J (2019) Identifying recurrent malignant glioma after treatment using amide proton transfer-weighted MR imaging: a validation study with image-guided stereotactic biopsy. Clin Cancer Res 25:552–561
Jiang S, Eberhart CG, Zhang Y, Heo HY, Wen Z, Blair L, Qin H, Lim M, Quinones-Hinojosa A, Weingart JD, Barker PB, Pomper MG, Laterra J, van Zijl PCM, Blakeley JO, Zhou J (2017) Amide proton transfer-weighted magnetic resonance image-guided stereotactic biopsy in patients with newly diagnosed gliomas. Eur J Cancer (Oxford, England: 1990) 83:9–18
van Zijl PC, Yadav NN (2011) Chemical exchange saturation transfer (CEST): what is in a name and what isn’t? Magn Reson Med 65:927–948
Zhou J, Tryggestad E, Wen Z, Lal B, Zhou T, Grossman R, Wang S, Yan K, Fu DX, Ford E, Tyler B, Blakeley J, Laterra J, van Zijl PCM (2011) Differentiation between glioma and radiation necrosis using molecular magnetic resonance imaging of endogenous proteins and peptides. Nat Med 17:130–134
Kamimura K, Nakajo M, Yoneyama T et al (2018) Amide proton transfer imaging of tumors: theory, clinical applications, pitfalls, and future directions. Jpn J Radiol 37:109–116
Law BKH, King AD, Ai QY, Poon DMC, Chen W, Bhatia KS, Ahuja AT, Ma BB, Ka-Wai Yeung D, Fai Mo FK, Wang YX, Yuan J (2018) Head and neck tumors: amide proton transfer MRI. Radiology 288:782–790
Su C, Zhao L, Li S et al (2018) Amid proton transfer (APT) and magnetization transfer (MT) MRI contrasts provide complimentary assessment of brain tumors similarly to proton magnetic resonance spectroscopy imaging (MRSI). Eur Radiol 29:1203–1210
Zimmermann F, Korzowski A, Breitling J, Meissner JE, Schuenke P, Loi L, Zaiss M, Bickelhaupt S, Schott S, Schlemmer HP, Paech D, Ladd ME, Bachert P, Goerke S (2020) A novel normalization for amide proton transfer CEST MRI to correct for fat signal-induced artifacts: application to human breast cancer imaging. Magn Reson Med 83:920–934
Ohno Y, Kishida Y, Seki S, Yui M, Miyazaki M, Koyama H, Yoshikawa T (2018) Amide proton transfer-weighted imaging to differentiate malignant from benign pulmonary lesions: comparison with diffusion-weighted imaging and FDG-PET/CT. J Magn Reson Imaging 47:1013–1021
Takayama Y, Nishie A, Sugimoto M et al (2016) Amide proton transfer (APT) magnetic resonance imaging of prostate cancer: comparison with Gleason scores. Magma (New York, NY) 29:671–679
Nishie A, Asayama Y, Ishigami K, Ushijima Y, Takayama Y, Okamoto D, Fujita N, Tsurumaru D, Togao O, Sagiyama K, Manabe T, Oki E, Kubo Y, Hida T, Hirahashi-Fujiwara M, Keupp J, Honda H (2019) Amide proton transfer imaging to predict tumor response to neoadjuvant chemotherapy in locally advanced rectal cancer. J Gastroenterol Hepatol 34:140–146
Takayama Y, Nishie A, Togao O, Asayama Y, Ishigami K, Ushijima Y, Okamoto D, Fujita N, Sonoda K, Hida T, Ohishi Y, Keupp J, Honda H (2018) Amide proton transfer MR imaging of endometrioid endometrial adenocarcinoma: association with histologic grade. Radiology 286:909–917
He YL, Ding N, Qi YF, Li Y, Xiang Y, Qian TY, Liu H, Lin CY, Yuan L, Zhou HL, Jin ZY, Xue HD (2019) Visualising the boundary sharpness of uterine zonal structures using high-resolution T2-weighted images during the menstrual cycle. Clin Radiol 74:81.e19–81.e24
Zhou J, Zhu H, Lim M, Blair L, Quinones-Hinojosa A, Messina SA, Eberhart CG, Pomper MG, Laterra J, Barker PB, van Zijl PCM, Blakeley JO (2013) Three-dimensional amide proton transfer MR imaging of gliomas: initial experience and comparison with gadolinium enhancement. J Magn Reson Imaging 38:1119–1128
Zhao X, Wen Z, Huang F, Lu S, Wang X, Hu S, Zu D, Zhou J (2011) Saturation power dependence of amide proton transfer image contrasts in human brain tumors and strokes at 3 T. Magn Reson Med 66:1033–1041
Togao O, Hiwatashi A, Keupp J, Yamashita K, Kikuchi K, Yoshiura T, Yoneyama M, Kruiskamp MJ, Sagiyama K, Takahashi M, Honda H (2016) Amide proton transfer imaging of diffuse gliomas: effect of saturation pulse length in parallel transmission-based technique. PLoS ONE 11:e0155925
Eggers H, Brendel B, Duijndam A, Herigault G (2011) Dual-echo Dixon imaging with flexible choice of echo times. Magn Reson Med 65:96–107
Togao O, Keupp J, Hiwatashi A, Yamashita K, Kikuchi K, Yoneyama M, Honda H (2017) Amide proton transfer imaging of brain tumors using a self-corrected 3D fast spin-echo Dixon method: comparison with separate B0 correction. Magn Reson Med 77:2272–2279
Zhang S, Sun H, Li B, Wang X, Pan S, Guo Q (2019) Variation of amide proton transfer signal intensity and apparent diffusion coefficient values among phases of the menstrual cycle in the normal uterus: a preliminary study. Magn Reson Imaging 63:21–28
Jones CK, Schlosser MJ, van Zijl PC, Pomper MG, Golay X, Zhou J (2006) Amide proton transfer imaging of human brain tumors at 3T. Magn Reson Med 56:585–592
Jia G, Abaza R, Williams JD et al (2011) Amide proton transfer MR imaging of prostate cancer: a preliminary study. J Magn Reson Imaging 33:647–654
He YL, Li Y, Lin CY, Qi YF, Wang X, Zhou HL, Yang JJ, Xiang Y, Xue HD, Jin ZY (2019) Three-dimensional turbo-spin-echo amide proton transfer-weighted mri for cervical cancer: a preliminary study. J Magn Reson Imaging 50:1318–1325
Joo B, Han K, Choi YS, Lee SK, Ahn SS, Chang JH, Kang SG, Kim SH, Zhou J (2018) Amide proton transfer imaging for differentiation of benign and atypical meningiomas. Eur Radiol 28:331–339
Bazot M, Darai E (2018) Role of transvaginal sonography and magnetic resonance imaging in the diagnosis of uterine adenomyosis. Fertil Steril 109:389–397
Wen Z, Hu S, Huang F, Wang X, Guo L, Quan X, Wang S, Zhou J (2010) MR imaging of high-grade brain tumors using endogenous protein and peptide-based contrast. NeuroImage 51:616–622
Togao O, Hiwatashi A, Yamashita K, Kikuchi K, Keupp J, Yoshimoto K, Kuga D, Yoneyama M, Suzuki SO, Iwaki T, Takahashi M, Iihara K, Honda H (2017) Grading diffuse gliomas without intense contrast enhancement by amide proton transfer MR imaging: comparisons with diffusion- and perfusion-weighted imaging. Eur Radiol 27:578–588
Zhou J, Payen JF, Wilson DA, Traystman RJ, van Zijl PC (2003) Using the amide proton signals of intracellular proteins and peptides to detect pH effects in MRI. Nat Med 9:1085–1090
Acknowledgments
This work was supported by grants from the Natural Science Foundation of China (grant no. 81901829) and the Fundamental Research Funds for the Central Universities (grant no. 3332019032).
Author information
Authors and Affiliations
Contributions
1. Guarantor of the integrity of the entire study: Yuan Li, Cheng-Yu Lin, Yong-Lan He, Hua-Dan Xue, and Zheng-Yu Jin
2. Study concepts and design: Yong-Lan He, Hua-Dan Xue, Zheng-Yu Jin, and Yang Xiang
3. Literature research: Yuan Li, Yong-Lan He, and Cheng-Yu Lin
4. Clinical studies: Yuan Li, Jun-Jun Yang, Chen Bo, Cheng-Yu Lin, and Ya-Fei Qi
5. Experimental studies/data analysis: Yuan Li, Yong-Lan He, Cheng-Yu Lin, Ya-Fei Qi, Xiao-Qi Wang, and Hai-Long Zhou
6. Statistical analysis: Yong-Lan He, Cheng-Yu Lin, and Yuan Li
7. Manuscript preparation: Yuan Li, Yong-Lan He, and Xiao-Qi Wang
8. Manuscript editing: Yong-Lan He, Yuan Li, Xiao-Qi Wang, Jing Ren, Yang Xiang, Cheng-Yu Lin, and Hua-Dan Xue
Corresponding authors
Ethics declarations
Conflict of Interest
Author Xiao-Qi Wang is an employee of Philips Healthcare China. The other authors have no conflicts of interest to disclose. The authors not employed by Philips were in control of this study.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Keypoints
• Uterine three-dimensional turbo spin-echo APTw MR images revealed good quality in most cases.
• Endometrial adenocarcinoma showed significantly higher APT-weighted values than leiomyoma, adenomyosis, and normal myometrium.
• No significant differences were found among APT-weighted values of uterine benign lesions and normal myometrium.
Supplementary Information
ESM 1 (download DOCX )
(DOCX 15 kb)
Rights and permissions
About this article
Cite this article
Li, Y., Lin, CY., Qi, YF. et al. Non-invasive Differentiation of Endometrial Adenocarcinoma from Benign Lesions in the Uterus by Utilization of Amide Proton Transfer-Weighted MRI. Mol Imaging Biol 23, 446–455 (2021). https://doi.org/10.1007/s11307-020-01565-x
Received:
Revised:
Accepted:
Published:
Version of record:
Issue date:
DOI: https://doi.org/10.1007/s11307-020-01565-x