Assessing the Early Response of Advanced Cervical Cancer to Neoadjuvant Chemotherapy Using Intravoxel Incoherent Motion Diffusion-weighted Magnetic Resonance Imaging: A Pilot Study

Yan-Chun Wang, Dao-Yu Hu, Xue-Mei Hu, Ya-Qi Shen, Xiao-Yan Meng, Hao Tang, Zhen Li, Yan-Chun Wang, Dao-Yu Hu, Xue-Mei Hu, Ya-Qi Shen, Xiao-Yan Meng, Hao Tang, Zhen Li

Abstract

Background: Diffusion-weighted imaging (DWI) with the intravoxel incoherent motion (IVIM) model has shown promising results for providing both diffusion and perfusion information in cervical cancer; however, its use to predict and monitor the efficacy of neoadjuvant chemotherapy (NACT) in cervical cancer is relatively rare. The study aimed to evaluate the use of DWI with IVIM and monoexponential models to predict and monitor the efficacy of NACT in cervical cancer.

Methods: Forty-two patients with primary cervical cancer underwent magnetic resonance exams at 3 time points (pre-NACT, 3 weeks after the first NACT cycle, and 3 weeks after the second NACT cycle). The response to treatment was determined according to the response evaluation criteria in solid tumors 3 weeks after the second NACT treatment, and the subjects were classified as two groups: responders and nonresponders groups. The apparent diffusion coefficient (ADC), true diffusion coefficient (D), perfusion-related pseudo-diffusion coefficient (DFNx01), and perfusion fraction (f) values were determined. The differences in IVIM-derived variables and ADC between the different groups at the different time points were calculated using an independent samples t-test.

Results: The D and ADC values were all significantly higher for the responders than for the nonresponders at all 3 time points, but no significant differences were observed in the DFNx01 and f values. An analysis of the receiver operating characteristic (ROC) curves indicated that a D value threshold <0.93 × 10-3 mm 2 /s and an ADC threshold <1.11 × 10-3 mm 2 /s could differentiate responders from nonresponders at pre-NACT time point, yielding area under the curve (AUC) of which were 0.771 and 0.806, respectively. The ROC indicated that the AUCs of D and ADC at the 3 weeks after the first NACT cycle and 3 weeks after the second NACT cycle were 0.823, 0.763, and 0.787, 0.794, respectively. The AUC values of D and ADC at these 3 time points were not significantly different (P = 0.641, 0.512, and 0.547, respectively).

Conclusions: D and ADC values may be useful for predicting and monitoring the efficacy of NACT in cervical cancer. An IVIM model may be equal to monoexponential model in predicting and monitoring the efficacy of NACT in cervical cancer.

Figures

Figure 1
Figure 1
A 56-year-old woman with cervical squamous cell carcinoma (white arrow). Complete response after NACT. (a1-a6) Pre-NACT. (b1-b6) 3 weeks after the first NACT cycle. (c1-c6) 3 weeks after the second NACT cycle. (a1-c1) Sagittal T2-weighted images. (a2-c2) axial DWI with b = 800 s/mm2. (a3-c3) axial ADC maps. (a4-c4) D. (a5-c5) D*. (a6-c6) f values. Outlines indicate the tumor region. The following values were obtained for the 3 time points: ADC: 1.24 × 10−3 mm2/s, 1.40 × 10−3 mm2/s, and 1.42 × 10−3 mm2/s; D: 0.95 × 10−3 mm2/s, 1.13 × 10−3 mm2/s, and 1.29 × 10−3mm2/s; D*: 1.30 × 10−2mm2/s, 1.84 × 10−2mm2/s, and 1.23 × 10−2mm2/s; and f: 0.161, 0.185, and 0.186, respectively. The ADC and D values of the tumor clearly increased after NACT administration. The changes in the D* and f values were not significant. NACT: Neoadjuvant chemotherapy, DWI: Diffusion-weighted imaging, ADC: Apparent diffusion coefficient.
Figure 2
Figure 2
A 37-year-old woman with cervical squamous cell carcinoma (white arrow). Stable disease after NACT. (a1-a6) Pre-NACT. (b1-b6) 3 weeks after the first NACT. (c1-c6) 3 weeks after the second NACT. (a1-c1) Sagittal T2-weighted images. (a2-c2) axial DWI with b = 800 s/mm2. (a3-c3) axial ADC maps. (a4-c4) D. (a5-c5) D*.(a6-c6) f values. Outlines indicate the tumor area. The following values were obtained for the 3 time points: ADC: 0.98 × 10−3 mm2/s, 1.21 × 10−3 mm2/s, and 0.97 × 10−3 mm2/s; D: 0.78 × 10−3 mm2/s, 0.84 × 10−3 mm2/s, and 0.79 × 10−3 mm2/s; D*: 1.63 × 10−2 mm2/s, 1.35 × 10−2 mm2/s, and 1.15 × 10−2 mm2/s; and f: 0.135, 0.185, and 0.144, respectively. The ADC and D values of the tumor increased slightly after NACT administration. NACT: Neoadjuvant chemotherapy, DWI: Diffusion-weighted imaging, ADC: Apparent diffusion coefficient.
Figure 3
Figure 3
(a) ROC curves of the D and ADC values for differentiating responders from nonresponders at the pre-NACT time point. (b) ROC curves of the D and ADC values for differentiating responders from nonresponders 3 weeks after the first NACT cycle. (c) ROC curves of the D and ADC values for differentiating responders from nonresponders at 3 weeks after the second NACT cycle. NACT: Neoadjuvant chemotherapy, ADC: Apparent diffusion coefficient, ROC: Receiver operating characteristic.

References

    1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61:69–90. doi:10.3322/caac.20107.21296855.
    1. Sugiyama T, Nishida T, Kumagai S, Nishio S, Fujiyoshi K, Okura N, et al. Combination therapy with irinotecan and cisplatin as neoadjuvant chemotherapy in locally advanced cervical cancer. Br J Cancer. 1999;81:95–8. doi:10.1038/sj.bjc.6690656.10487618.
    1. McCormack M, Kadalayil L, Hackshaw A, Hall-Craggs MA, Symonds RP, Warwick V, et al. A phase II study of weekly neoadjuvant chemotherapy followed by radical chemoradiation for locally advanced cervical cancer. Br J Cancer. 2013;108:2464–9. doi:10.1038/bjc.2013.230.23695016.
    1. Edelmann DZ, Anteby SO. Neoadjuvant chemotherapy for locally advanced cervical cancer –Where does it stand?a review. Obstet Gynecol Surv. 1996;51:305–13. doi:10.1097/00006254-199605000-00022.8744415.
    1. Shoji T, Takatori E, Hatayama S, Omi H, Kagabu M, Honda T, et al. Phase II study of tri-weekly cisplatin and irinotecan as neoadjuvant chemotherapy for locally advanced cervical cancer. Oncol Lett. 2010;1:515–9. doi:10.3892/ol_00000091.22966335.
    1. Xiong Y, Liang LZ, Cao LP, Min Z, Liu JH. Clinical effects of irinotecan hydrochloride in combination with cisplatin as neoadjuvant chemotherapy in locally advanced cervical cancer. Gynecol Oncol. 2011;123:99–104. doi:10.1016/j.ygyno.2011.06.011.21741694.
    1. Kumar JV, Doval DC, Rao R, Rawal S. A retrospective study of patients with locally advanced cancer of the cervix treated with neoadjuvant chemotherapy followed by radical surgery. Int J Gynecol Cancer. 2009;19:417–22. doi:10.1111/IGC.0b013e3181a1c6df.19407570.
    1. Fu C, Bian D, Liu F, Feng X, Du W, Wang X. The value of diffusion-weighted magnetic resonance imaging in assessing the response of locally advanced cervical cancer to neoadjuvant chemotherapy. Int J Gynecol Cancer. 2012;22:1037–43. doi:10.1097/IGC.0b013e31825736d7.22683941.
    1. Himoto Y, Fujimoto K, Kido A, Matsumura N, Baba T, Daido S, et al. Assessment of the early predictive power of quantitative magnetic resonance imaging parameters during neoadjuvant chemotherapy for uterine cervical cancer. Int J Gynecol Cancer. 2014;24:751–7. doi:10.1097/IGC.0000000000000124.24685827.
    1. Rizzo S, Summers P, Raimondi S, Belmonte M, Maniglio M, Landoni F, et al. Diffusion-weighted MR imaging in assessing cervical tumour response to nonsurgical therapy. Radiol Med. 2011;116:766–80. doi:10.1007/s11547-011-0650-4.21424319.
    1. Chandarana H, Lee VS, Hecht E, Taouli B, Sigmund EE. Comparison of biexponential and monoexponential model of diffusion weighted imaging in evaluation of renal lesions: Preliminary experience. Invest Radiol. 2011;46:285–91. doi:10.1097/RLI.0b013e3181ffc485.21102345.
    1. Le Bihan D, Breton E, Lallemand D, Aubin ML, Vignaud J, Laval-Jeantet M. Separation of diffusion and perfusion in intravoxel incoherent motion MR imaging. Radiology. 1988;168:497–505. doi:10.1148/radiology.168.2.3393671.3393671.
    1. Lee EY, Yu X, Chu MM, Ngan HY, Siu SW, Soong IS, et al. Perfusion and diffusion characteristics of cervical cancer based on intraxovel incoherent motion MR imaging-a pilot study. Eur Radiol. 2014;24:1506–13. doi:10.1007/s00330-014-3160-7.24744198.
    1. Wu HH, Jia HR, Zhang Y, Liu L, Xu DB, Sun HR. Monitoring the progression of renal fibrosis by T2-weighted signal intensity and diffusion weighted magnetic resonance imaging in cisplatin induced rat models. Chin Med J. 2015;128:626–31. doi:10.4103/0366-6999.151660.25698194.
    1. Hu LB, Hong N, Zhu WZ. Quantitative measurement of cerebral perfusion with intravoxel incoherent motion in acute ischemia stroke: Initial clinical experience. Chin Med J. 2015;128:2565–9. doi:10.4103/0366-6999.166033.26415791.
    1. Eisenhauer EA, Therasse P, Bogaerts J, Schwartz LH, Sargent D, Ford R, et al. New response evaluation criteria in solid tumours: Revised RECIST guideline (version 1.1) Eur J Cancer. 2009;45:228–47. doi:10.1016/j.ejca.2008.10.026.19097774.
    1. Mayr NA, Taoka T, Yuh WT, Denning LM, Zhen WK, Paulino AC, et al. Method and timing of tumor volume measurement for outcome prediction in cervical cancer using magnetic resonance imaging. Int J Radiat Oncol Biol Phys. 2002;52:14–22. doi:10.1016/S0360-3016(01)01808-9.11777618.
    1. Harry VN, Semple SI, Gilbert FJ, Parkin DE. Diffusion-weighted magnetic resonance imaging in the early detection of response to chemoradiation in cervical cancer. Gynecol Oncol. 2008;111:213–20. doi:10.1016/j.ygyno.2008.07.048.18774597.
    1. Mayr NA, Yuh WT, Jajoura D, Wang JZ, Lo SS, Montebello JF, et al. Ultra-early predictive assay for treatment failure using functional magnetic resonance imaging and clinical prognostic parameters in cervical cancer. Cancer. 2010;116:903–12. doi:10.1002/cncr.24822.20052727.
    1. Padhani AR, Liu G, Koh DM, Chenevert TL, Thoeny HC, Takahara T, et al. Diffusion-weighted magnetic resonance imaging as a cancer biomarker: Consensus and recommendations. Neoplasia. 2009;11:102–25. doi:10.1593/neo.81328.19186405.
    1. Cohen AD, Schieke MC, Hohenwalter MD, Schmainda KM. The effect of low b-values on the intravoxel incoherent motion derived pseudodiffusion parameter in liver. Magn Reson Med. 2015;73:306–11. doi:10.1002/mrm.25109.24478175.
    1. Andreou A, Koh DM, Collins DJ, Blackledge M, Wallace T, Leach MO, et al. Measurement reproducibility of perfusion fraction and pseudodiffusion coefficient derived by intravoxel incoherent motion diffusion-weighted MR imaging in normal liver and metastases. Eur Radiol. 2013;23:428–34. doi:10.1007/s00330-012-2604-1.23052642.
    1. Koh DM, Collins DJ, Orton MR. Intravoxel incoherent motion in body diffusion-weighted MRI: Reality and challenges. AJR Am J Roentgenol. 2011;196:1351–61. doi:10.2214/AJR.10.5515.21606299.
    1. Koh DM, Blackledge M, Collins DJ, Padhani AR, Wallace T, Wilton B, et al. Reproducibility and changes in the apparent diffusion coefficients of solid tumours treated with combretastatin A4 phosphate and bevacizumab in a two-centre phase I clinical trial. Eur Radiol. 2009;19:2728–38. doi:10.1007/s00330-009-1469-4.19547986.

Source: PubMed

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