Diffusion volume (DV) measurement in endometrial and cervical cancer: A new MRI parameter in the evaluation of the tumor grading and the risk classification
Keywords Parole chiave: Mri, Dwi, Adc Maps, Diffusion Volume, Cervical Cancer, Endometrial Cancer, Adult, Aged, Article, Automation, Cancer Classification, Cancer Grading, Cancer Risk, Cancer Staging, Diffusion Weighted Imaging, Endometrium Cancer, Female, High Risk Population, Histopathology, Human, Kruskal Wallis Test, Major Clinical Study, Nuclear Magnetic Resonance Imaging, Priority Journal, Receiver Operating Characteristic, Uterine Cervix Cancer, Analysis Of Variance
, Diffusion Magnetic Resonance Imaging Methods
, Endometrial Neoplasms Pathology
, Image Interpretation, Computer-Assisted
, Middle Aged
, Neoplasm Grading
, Observer Variation
, Sensitivity And Specificity
, Tumor Burden
, Uterine Cervical Neoplasms Pathology
Affiliations Affiliazioni: *** IBB - CNR ***
IBB CNR, Napoli, Italy
Dipartimento di Scienze Biomediche Avanzate, Sezione di Radiologia, Università di Napoli “Federico II”, Napoli, Italy
IRCCS CROB, Rionero in Vulture, Italy
IRCCS SDN, Napoli, Italy
Dipartimento di Medicina e Chirurgia, Università degli Studi di Salerno, Salerno, Italy
References Riferimenti: [1] T. Koyama, K. Tamai, K. Togashi, Staging of carcinoma of the uterine cervix and endometrium, Eur. Radiol. 17 (8) (2007) 2009–2019.
[2] G. Rechichi, S. Galimberti, M. Signorelli, P. Perego, M.G. Valsecchi, S. Sironi, Myometrial invasion in endometrial cancer: diagnostic performance of diffusion weighted MR imaging at 1.5-T, Eur. Radiol. 20 (3) (2010) 754–762.
[3] A. Andreano, G. Rechichi, P. Rebora, S. Sironi, M.G. Valsecchi, S. Galimberti, MR 24 (6) (2014) 1327–1338.
[4] H.A. Rowley, P.E. Grant, T.P. Roberts, Diffusion MR imaging: theory and applications, Neuroimaging Clin. N. Am. 9 (2) (1999) 343–361.
[5] D.M. Koh, D.J. Collins, Diffusion-weighted MRI in the body: applications and challenges in oncology, AJR Am. J. Roentgenol. 188 (6) (2007) 1622–1635.
[6] S. Naganawa, C. Sato, H. Kumada, T. Ishigaki, S. Miura, O. Takizawa, Apparent diffusion coefficient in cervical cancer of the uterus: comparison with the normal uterine cervix, Eur. Radiol. 15 (1) (2005) 71–78.
[7] P.Z. McVeigh, A.M. Syed, M. Milosevic, A. Fyles, M.A. Haiderd,Diffusion-weighted MRI in cervical cancer, Eur. Radiol. 18 (5) (2008) 1058–1064.
[8] E. Sala, A. Rockall, D. Rangarajanc, R.A. Kubik-Huch, The role of dynamic contrast-enhanced and diffusion weighted magnetic resonance imaging in the female pelvis, Eur. J. Radiol. 76 (3) (2010) 367–385.
[9] S. Punwani, Diffusion weighted imaging of female pelvic cancers: concepts and clinical applications, Eur. J. Radiol. 78 (1) (2011) 21–29.
[10] G. Rechichi, S. Galimberti, M. Signorelli, C.T. Franzesi, P. Perego, M.G. Valsecchi, et al., Endometrial cancer: correlation of apparent diffusion coefficient with tumor grade, depth of myometrial invasion, and presence of lymph node metastases, AJR Am. J. Roentgenol. 197 (1) (2011) 256–262.
[11] S. Fujii, E. Matsusue, J. Kigawa, S. Sato, Y. Kanasaki, J. Nakanishi, et al., Diagnostic accuracy of the apparent diffusion coefficient in differentiating benign from malignant uterine endometrial cavity lesions: initial results, Eur. Radiol. 18 (2) (2008) 384–389.
[12] S.H. Shen, Y.Y. Chiou, J.H. Wang, M.S. Yen, R.C. Lee, C.R. Lai, et al., echo-planar imaging with parallel technique in assessment of endometrial cancer, AJR Am. J. Roentgenol. 190 (2) (2008)
[13] K. Tamai, T. Koyama, T. Saga, S. Umeoka, Y. Mikami, S. Fujii, et al., Diffusion weighted MR imaging of uterine endometrial cancer, J. Magn. Reson. Imaging 26 (3) (2007) 682–687.
[14] N. Bharwani, M.E. Miquel, A. Sahdev, P. Narayanan, G. Malietzis, R.H. Reznek, et al., Diffusion-weighted imaging in the assessment of tumour grade in endometrial cancer, Br. J. Radiol. 84 (1007) (2011) 997–1004.
[15] Y. Inada, M. Matsuki, G. Nakai, F. Tatsugami, M. Tanikake, I. Narabayashi, et al., Body diffusion weighted MR imaging of uterine endometrial cancer: is it helpful in the detection of cancer in non enhanced MR imaging? Eur. J. Radiol. 70 (1) (2009) 122–127.
[16] K. Cao, M. Gao, Y.S. Sun, Y.L. Li, Y. Sun, Y.N. Gao, et al., Apparent diffusion coefficient of diffusion weighted MRI in endometrial carcinoma-Relationship with local invasiveness, Eur. J. Radiol. 81 (8) (2012) 1926–1930.
[17] P. Beddy, A.C. O’Neil, A.K. Yamamoto, H.C. Addley, C. Reinhold, E. Sala, fiGO staging system for endometrial cancer: added benefits of MR imaging,Radiographics 32 (1) (2012) 241–254.
[18] K. Downey, S.F. Riches, V.A. Morgan, S.L. Giles, A.D. Attygalle, T.E. Ind, et al., Relationship between imaging biomarkers of stage I cervical cancer and poor-prognosis histologic features: quantitative histogram analysis of diffusion-weighted MR images, AJR Am. J. Roentgenol. 200 (2) (2013) 314–320.
[19] F. Kuang, J. Ren, Q. Zhong, F. Liyuan, Y. Huan, Z. Chen, The value of apparent diffusion coefficient in the assessment of cervical cancer, Eur. Radiol. 23 (4) (2013) 1050–1058.
[20] R. Bos, J.J. van Der Hoeven, E. van Der Wall, P. van Der Groep, P.J. van Diest, E.F.Comans, et al., Biologic correlates of (18) fluorodeoxyglucose uptake in human breast cancer measured by positron emission tomography, J. Clin. Oncol. 20 (2) (2002) 379–387.
[21] T. Higashi, N. Tamaki, T. Torizuka, Y. Nakamoto, H. Sakahara, T. Kimura, et al.,FDG uptake, GLUT-1, glucose transporter and cellularity in human pancreatic tumors, J. Nucl. Med. 39 (10) (1998) 1727–1735.
[22] K. Ito, T. Kato, T. Ohta, et al., fluorine-18 fluoro-2-deoxyglucose positron emission tomography in recurrent rectal cancer: relation to tumour size and cellularity, Eur. J. Nucl. Med. 23 (10) (1996) 1372–1377.
[23] R. Fonti, M. Larobina, S. Del Vecchio, S. De Luca, R. Fabbricini, L. Catalano, et al., Metabolic tumor volume assessed by 18F-FDG PET/CT for the prediction of outcome in patients with multiple myeloma, J. Nucl. Med. 53 (12) (2012) 1829–1835.
[24] N. Colombo, E. Preti, F. Landoni, S. Carinelli, A. Colombo, C. Marini, et al., Endometrial cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow up, Ann. Oncol. 22 (2011) 35–39, Suppl 7: vii.
[25] S.J. Freeman, A.M. Aly, M.Y. Kataoka, H.C. Addley, C. Reinhold, E. Sala, The revised fiGO staging system for uterine malignancies: implications for MR imaging, Radiographics 32 (6) (2012) 1805–1827.
[26] N. Colombo, S. Carinelli, A. Colombo, C. Marini, D. Rollo, C. Sessa, et al., Cervical cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up, Ann. Oncol. 23 (2012) 27–32, Suppl 7: vii.
[27] A. Berkowitz, S. Basu, S. Srinivas, S. Sankaran, S. Schuster, A. Alavi, Determination of whole-body metabolic burden as a quantitative measure of disease activity in lymphoma: a novel approach with fluorodeoxyglucose-PET, Nucl. Med. Commun. 29 (6) (2008) 521–526.
[28] H.H. Chung, J.W. Kim, K.H. Han, J.S. Eo, K.W. Kang, N.H. Park, et al., Prognostic value of metabolic tumor volume measured by FDG-PET/CT in patients with cervical cancer, Gynecol. Oncol. 120 (2) (2011) 270–274.
[29] G. Storto, E. Nicolai, M. Salvatore, [18F]FDG-PET-CT for early monitoring of tumor response: when and why, Q. J. Nucl. Med. Mol. Imaging 53 (2) (2009) 167–180.
[30] J.R. Olsen, J. Esthappan, T. DeWees, V.R. Narra, F. Dehdashti, B.A. Siegel, et al., Tumor volume and subvolume concordance between FDG-PET/CT and diffusion-weighted MRI for squamous cell carcinoma of the cervix, J. Magn. Reson. Imaging 37 (2) (2013) 431–434.
[31] H. Sun, J. Xin, S. Zhang, Q. Guo, Y. Lu, W. Zhai, et al., Anatomical and functional volume concordance between FDG PET, and T2 and diffusion-weighted MRI for cervical cancer: a hybrid PET/MR study, Eur. J. Nucl. Med. Mol. Imaging 41 (5) (2014) 898–905.
[32] M. Uhl, U. Saueressig, G. Koehler, U. Kontny, C. Niemeyer, W. Reichardt, et al., Evaluation of tumour necrosis during chemotherapy with diffusion-weighted MR imaging: preliminary results in osteosarcomas, Pediatr. Radiol. 36 (12) (2006) 1306–1311.
[33] M.Y. Choi, K.M. Lee, J.K. Chung, D.S. Lee, J.M. Jeong, J.G. Park, et al., Correlation between serum CEA level and metabolic volume as determined by FDG PET in postoperative patients with recurrent colorectal cancer, Ann. Nucl. Med. 19 (2) (2005) 123–129.
[34] E.H. Dibble, A.C. Alvarez, M.T. Truong, G. Mercier, E.F. Cook, R.M. Subramaniam, 18F-FDG metabolic tumor volume and total glycolytic activity of oral cavity and oropharyngeal squamous cell cancer: adding value to clinical staging, J. Nucl. Med. 53 (5) (2012) 709–715.
[35] P. Sridhar, G. Mercier, J. Tan, M.T. Truong, B. Daly, R.M. Subramaniam, FDG PET metabolic tumor volume segmentation and pathologic volume of primary human solid tumors, AJR Am. J. Roentgenol. 202 (5) (2014) 1114–1119.
[36] N. Withofs, C. Bernard, C. Van der Rest, P. Martinive, M. Hatt, S. Jodogne, et al., FDG PET/CT for rectal carcinoma radiotherapy treatment planning: comparison of functional volume delineation algorithms and clinical challenges, J. Appl. Clin. Med. Phys. 15 (5) (2014) 4696.
[37] S. Zhang, J. Xin, Q. Guo, J. Ma, Q. Ma, H. Sun, Comparison of tumor volume between PET and MRI in cervical cancer with hybrid PET/MR, Int. J. Gynecol. Cancer 24 (4) (2014) 744–750.
[38] D.M. Lambregts, G.L. Beets, M. Maas, L. Curvo-Semedo, A.G. Kessels, T. Thywissen, et al., Tumour ADC measurements in rectal cancer: effect of ROI methods on ADC values and interobserver variability, Eur. Radiol. 21 (12) (2011) 2567–2574.
Koyama, T., Tamai, K., Togashi, K., Staging of carcinoma of the uterine cervix and endometrium (2007) Eur. Radiol., 17 (8), pp. 2009-201
Rechichi, G., Galimberti, S., Signorelli, M., Perego, P., Valsecchi, M.G., Sironi, S., Myometrial invasion in endometrial cancer: Diagnostic performance of diffusione weighted MR imaging at 1.5-T (2010) Eur. Radiol., 20 (3), pp. 754-762
Andreano, A., Rechichi, G., Rebora, P., Sironi, S., Valsecchi, M.G., Galimberti, S., MR diffusion imaging for preoperative staging of myometrial invasion in patients with endometrial cancer: A systematic review and meta-analysis (2014) Eur. Radiol, 24 (6), pp. 1327-1338
Rowley, H.A., Grant, P.E., Roberts, T.P., Diffusion MR imaging: Theory and applications (1999) Neuroimaging Clin. N. Am., 9 (2), pp. 343-361
Koh, D.M., Collins, D.J., Diffusion-weighted MRI in the body: Applications and challenges in oncology (2007) AJR Am. J. Roentgenol., 188 (6), pp. 1622-1635
Naganawa, S., Sato, C., Kumada, H., Ishigaki, T., Miura, S., Takizawa, O., Apparent diffusion coefficient in cervical cancer of the uterus: Comparison with the normal uterine cervix (2005) Eur. Radiol., 15 (1), pp. 71-78
McVeigh, P.Z., Syed, A.M., Milosevic, M., Fyles, A., Haiderd, M.A., Diffusion-weighted MRI in cervical cancer (2008) Eur. Radiol., 18 (5), pp. 1058-1064
Sala, E., Rockall, A., Rangarajanc, D., Kubik-Huch, R.A., The role of dynamic contrast-enhanced and diffusion weighted magnetic resonance imaging in the female pelvis (2010) Eur. J. Radiol., 76 (3), pp. 367-385
Punwani, S., Diffusion weighted imaging of female pelvic cancers: Concepts and clinical applications (2011) Eur. J. Radiol., 78 (1), pp. 21-29
Fujii, S., Matsusue, E., Kigawa, J., Sato, S., Kanasaki, Y., Nakanishi, J., Diagnostic accuracy of the apparent diffusion coefficient in differentiating benign from malignant uterine endometrial cavity lesions: Initial results (2008) Eur. Radiol., 18 (2), pp. 384-389
Shen, S.H., Chiou, Y.Y., Wang, J.H., Yen, M.S., Lee, R.C., Lai, C.R., Diffusion-weighted single-shot echo-planar imaging with parallel technique in assessment of endometrial cancer (2008) AJR Am. J. Roentgenol., 190 (2), pp. 481-488
Tamai, K., Koyama, T., Saga, T., Umeoka, S., Mikami, Y., Fujii, S., Diffusion weighted MR imaging of uterine endometrial cancer (2007) J. Magn. Reson. Imaging, 26 (3), pp. 682-687
Bharwani, N., Miquel, M.E., Sahdev, A., Narayanan, P., Malietzis, G., Reznek, R.H., Diffusion-weighted imaging in the assessment of tumour grade in endometrial cancer (2011) Br. J. Radiol., 84 (1007), pp. 997-1004
Inada, Y., Matsuki, M., Nakai, G., Tatsugami, F., Tanikake, M., Narabayashi, I., Body diffusion weighted MR imaging of uterine endometrial cancer: Is it helpful in the detection of cancer in non enhanced MR imaging? (2009) Eur. J. Radiol., 70 (1), pp. 122-127
Cao, K., Gao, M., Sun, Y.S., Li, Y.L., Sun, Y., Gao, Y.N., Apparent diffusion coefficient of diffusion weighted MRI in endometrial carcinoma-Relationship with local invasiveness (2012) Eur. J. Radiol., 81 (8), pp. 1926-1930
Beddy, P., O'Neil, A.C., Yamamoto, A.K., Addley, H.C., Reinhold, C., Sala, E., FIGO staging system for endometrial cancer: Added benefits of MR imaging (2012) Radiographics, 32 (1), pp. 241-254
Downey, K., Riches, S.F., Morgan, V.A., Giles, S.L., Attygalle, A.D., Ind, T.E., Relationship between imaging biomarkers of stage i cervical cancer and poor-prognosis histologic features: Quantitative histogram analysis of diffusion-weighted MR images (2013) AJR Am. J. Roentgenol., 200 (2), pp. 314-320
Kuang, F., Ren, J., Zhong, Q., Liyuan, F., Huan, Y., Chen, Z., The value of apparent diffusion coefficient in the assessment of cervical cancer (2013) Eur. Radiol., 23 (4), pp. 1050-1058
Bos, R., Van Der Hoeven, J.J., Van Der Wall, E., Van Der Groep, P., Van Diest, P.J., Comans, E.F., Biologic correlates of (18) fluorodeoxyglucose uptake in human breast cancer measured by positron emission tomography (2002) J. Clin. Oncol., 20 (2), pp. 379-387
Higashi, T., Tamaki, N., Torizuka, T., Nakamoto, Y., Sakahara, H., Kimura, T., FDG uptake, GLUT-1, glucose transporter and cellularity in human pancreatic tumors (1998) J. Nucl. Med., 39 (10), pp. 1727-1735
Ito, K., Kato, T., Ohta, T., Fluorine-18 fluoro-2-deoxyglucose positron emission tomography in recurrent rectal cancer: Relation to tumour size and cellularity (1996) Eur. J. Nucl. Med., 23 (10), pp. 1372-1377
Fonti, R., Larobina, M., Del Vecchio, S., De Luca, S., Fabbricini, R., Catalano, L., Metabolic tumor volume assessed by 18F-FDG PET/CT for the prediction of outcome in patients with multiple myeloma (2012) J. Nucl. Med., 53 (12), pp. 1829-1835
Colombo, N., Preti, E., Landoni, F., Carinelli, S., Colombo, A., Marini, C., Endometrial cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow up (2011) Ann. Oncol., 22, pp. 35-39. , Suppl 7: vii
Freeman, S.J., Aly, A.M., Kataoka, M.Y., Addley, H.C., Reinhold, C., Sala, E., The revised FIGO staging system for uterine malignancies: Implications for MR imaging (2012) Radiographics, 32 (6), pp. 1805-1827
Colombo, N., Carinelli, S., Colombo, A., Marini, C., Rollo, D., Sessa, C., Cervical cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up (2012) Ann. Oncol., 23, pp. 27-32. , Suppl 7: vii
Berkowitz, A., Basu, S., Srinivas, S., Sankaran, S., Schuster, S., Alavi, A., Determination of whole-body metabolic burden as a quantitative measure of disease activity in lymphoma: A novel approach with fluorodeoxyglucose-PET (2008) Nucl. Med. Commun., 29 (6), pp. 521-526
Chung, H.H., Kim, J.W., Han, K.H., Eo, J.S., Kang, K.W., Park, N.H., Prognostic value of metabolic tumor volume measured by FDG-PET/CT in patients with cervical cancer (2011) Gynecol. Oncol., 120 (2), pp. 270-274
Storto, G., Nicolai, E., Salvatore, M., [18F]FDG-PET-CT for early monitoring of tumor response: When and why (2009) Q. J. Nucl. Med. Mol. Imaging, 53 (2), pp. 167-180
Olsen, J.R., Esthappan, J., DeWees, T., Narra, V.R., Dehdashti, F., Siegel, B.A., Tumor volume and subvolume concordance between FDG-PET/CT and diffusion-weighted MRI for squamous cell carcinoma of the cervix (2013) J. Magn. Reson. Imaging, 37 (2), pp. 431-434
Sun, H., Xin, J., Zhang, S., Guo, Q., Lu, Y., Zhai, W., Anatomical and functional volume concordance between FDG PET, and T2 and diffusion-weighted MRI for cervical cancer: A hybrid PET/MR study (2014) Eur. J. Nucl. Med. Mol. Imaging, 41 (5), pp. 898-905
Uhl, M., Saueressig, U., Koehler, G., Kontny, U., Niemeyer, C., Reichardt, W., Evaluation of tumour necrosis during chemotherapy with diffusion-weighted MR imaging: Preliminary results in osteosarcomas (2006) Pediatr. Radiol., 36 (12), pp. 1306-1311
Choi, M.Y., Lee, K.M., Chung, J.K., Lee, D.S., Jeong, J.M., Park, J.G., Correlation between serum CEA level and metabolic volume as determined by FDG PET in postoperative patients with recurrent colorectal cancer (2005) Ann. Nucl. Med., 19 (2), pp. 123-129
Dibble, E.H., Alvarez, A.C., Truong, M.T., Mercier, G., Cook, E.F., Subramaniam, R.M., 18F-FDG metabolic tumor volume and total glycolytic activity of oral cavity and oropharyngeal squamous cell cancer: Adding value to clinical staging (2012) J. Nucl. Med., 53 (5), pp. 709-715
Sridhar, P., Mercier, G., Tan, J., Truong, M.T., Daly, B., Subramaniam, R.M., FDG PET metabolic tumor volume segmentation and pathologic volume of primary human solid tumors (2014) AJR Am. J. Roentgenol., 202 (5), pp. 1114-1119
Withofs, N., Bernard, C., Van Der Rest, C., Martinive, P., Hatt, M., Jodogne, S., FDG PET/CT for rectal carcinoma radiotherapy treatment planning: Comparison of functional volume delineation algorithms and clinical challenges (2014) J. Appl. Clin. Med. Phys., 15 (5), p. 4696
Zhang, S., Xin, J., Guo, Q., Ma, J., Ma, Q., Sun, H., Comparison of tumor volume between PET and MRI in cervical cancer with hybrid PET/MR (2014) Int. J. Gynecol. Cancer, 24 (4), pp. 744-750
Lambregts, D.M., Beets, G.L., Maas, M., Curvo-Semedo, L., Kessels, A.G., Thywissen, T., Tumour ADC measurements in rectal cancer: Effect of ROI methods on ADC values and interobserver variability (2011) Eur. Radiol., 21 (12), pp. 2567-2574
Diffusion volume (DV) measurement in endometrial and cervical cancer: A new MRI parameter in the evaluation of the tumor grading and the risk classification
Purpose:
A new MRI parameter representative of active tumor burden is proposed: diffusion volume (DV), defined as the sum of all the voxels within a tumor with apparent diffusion coefficient (ADC) values within a specific range.
The aims of the study were: (a) to calculate DV on ADC maps in patients with cervical/endometrial cancer; (b) to correlate DV with histological grade (G) and risk classification; (c) to evaluate intra/inter-observer agreement of DV calculation.
Materials and methods:
Fifty-three patients with endometrial (n = 28) and cervical (n = 25) cancers under-went pelvic MRI with DWI sequences. Both endometrial and cervical tumors were classified on the basis of G (G1/G2/G3) and FIGO staging (low/medium/high-risk).
A semi-automated segmentation procedure was used to calculate the DV. A freehand closed ROI out-lined the whole visible tumor on the most representative slice of ADC maps defined as the slice with the maximum diameter of the solid neoplastic component. Successively, two thresholds were generated on the basis of the mean and standard deviation (SD) of the ADC values: lower threshold (LT = “mean minus three SD”) and higher threshold (HT = “mean plus one SD”). The closed ROI was expanded in 3D, including all the contiguous voxels with ADC values in the range LT-HT × 10–3 mm2/s.
A Kruskal–Wallis test was used to assess the differences in DV among G and risk groups. Intra-/inter-observer variability for DV measurement was analyzed according to the method of Bland and Altman and the intraclass-correlation–coefficient (ICC).
Results:
DV values were significantly different among G and risk groups in both endometrial (p < 0.05) and cervical cancers (p ≤ 0.01). For endometrial cancer, DV of G1 (mean ± sd: 2.81 ± 3.21 cc) neoplasms were significantly lower than G2 (9.44 ± 9.58 cc) and G3 (11.96 ± 8.0 cc) ones; moreover, DV of low risk cancers (5.23 ± 8.0 cc) were significantly lower than medium (7.28 ± 4.3 cc) and high risk (14.7 ± 9.9 cc) ones.
For cervical cancer, DV of G1 (0.31 ± 0.13 cc) neoplasms was significantly lower than G3 (40.68 ± 45.65 cc) ones; moreover, DV of low risk neoplasms (6.98 ± 8.08 cc) was significantly lower than medium (21.7 ± 17.13 cc) and high risk (62.9 ± 51.12 cc) ones and DV of medium risk neoplasms was significantly lower than high risk ones.
The intra-/inter-observer variability for DV measurement showed an excellent correlation for both cancers (ICC ≥ 0.86).
Conclusions:
DV is an accurate index for the assessment of G and risk classification of cervical/endometrial cancers with low intra-/inter-observer variability.
Diffusion volume (DV) measurement in endometrial and cervical cancer: A new MRI parameter in the evaluation of the tumor grading and the risk classification
Diffusion volume (DV) measurement in endometrial and cervical cancer: A new MRI parameter in the evaluation of the tumor grading and the risk classification
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