Narrative review of the utility of magnetic resonance imaging in radiotherapy for cervical cancer

Introduction

Cervical cancer is the fourth most diagnosed cancer and the fourth leading cause of cancer death in women worldwide (1). The standard curative treatment for locally advanced cervical cancer is concomitant chemoradiotherapy (CCRT), followed by brachytherapy (BT) (2). CCRT involves external beam radiotherapy (EBRT) with cisplatin as the chemotherapy agent (2). BT delivers boost of concentrated radiation doses through an applicator directly placed in the cervix and uterus (2). Magnetic resonance imaging (MRI) is considered the gold standard modality of volumetric imaging for image-guided adaptive BT (IGABT), as it enables accurate assessment of target volumes (TVs) and dose optimisation (3). Heterogeneity of disease based on tumour volume and parametrial disease, evaluated by MRI at the time of initial diagnosis and that of commencing BT is likely to influence target dosimetry in IGABT (4). The proposed advantages of MRI in IGABT are similarly relevant to EBRT.

EBRT planning is generally done through computed tomography (CT), as it is commonly available (5). Although less accessible, MRI provides superior soft tissue contrast to CT (6). It is therefore recommended that for contouring and treatment planning, MRI is acquired in the treatment position to delineate the volumes of a gross tumour and surrounding organs at risk (OAR), including the bladder, rectum and sigmoid (6). Based on the planning images, TV is defined for calculation of the radiation dose (5). However, the target and OARs are both deformable and mobile relative to each other (5). Substantial tumour regression may occur over time, further contributing to their position shift, within a fraction of treatment or between fractions (5). This poses a risk of geographical miss of the target, in which case OARs inadvertently captured in the treatment field are irradiated with higher than necessary dose (5). Predicting target motion through generating an internal TV (ITV) based on the bladder filling protocol can mitigate this risk. Intensity-modulated radiotherapy (IMRT) is one type that is often used to reduce normal tissue toxicity, as opposed to traditional conformal techniques (6,7). Furthermore, adaptive radiotherapy (ART) is utilised in clinical practice to account for the evolving anatomy during treatment (8).

ART involves modifying treatment plans under image guidance, CT and/or MRI, according to intrafraction and interfraction changes occurring throughout the treatment course (9). This may occur as ‘offline’ re-planning for TV changes or set-up issues, or as ‘online’ plan optimisation with the up-to-date anatomy on each fraction day (8). Accurate target contouring in MRI-guided ART (MRIgART) can ensure an adequate dose of radiation is delivered to sufficiently cover TV, while sparing OARs as much as practical (9). The aim of this review is to assess the evidence and gaps in the use of MRI in RT planning and ART for cervical cancer and discuss both the rationales for and challenges of its clinical implementation. We present this article in accordance with the Narrative Review reporting checklist (available at https://cco.amegroups.com/article/view/10.21037/cco-23-91/rc).

Methods

A literature search was conducted in July 2021 using the electronic databases Ovid Medline and PubMed. The main topics identified were MRI in the context of RT planning for cervical cancer, as well as changes and response to the treatment with or without ART. Subject headings and keywords are listed in Table 1. The Boolean operator AND was used to combine different keywords within each topic. Truncation (*) was used to search for words with the common prefix. OR was used to combine different topics into one search.

Full text papers in English language published between January 2011 and July 2021 were included for screening of titles and abstracts. Upon initial screening, papers exclusively discussing cancers of other organs or distant metastasis of cervical cancer were excluded. Papers about cervical cancer outside of the context of image-guided radiotherapy (RT) as a treatment were also excluded. Review papers were excluded. A detailed search strategy of Ovid Medline is presented in Table 2. Eight additional publications from references were later included. Full text was then assessed for relevance to yield the final studies for this review.

Results

The initial search yielded 85 articles, 60 from Ovid Medline and 25 from PubMed. After duplicates were removed, 66 were available for screening. Upon initial screening of title and abstracts, and application of inclusion and exclusion criteria, 32 were obtained. Full text assessment based on the same criteria with the addition of eight articles from references resulted in the final 37 studies for this review. The process of identifying the studies is outlined in Figure 1. Out of the 37 studies, four studies evaluated RT planning with target contouring and dose determination, eight evaluated intrafraction changes in TV and OARs, twelve evaluated interfraction changes TV and OARs, five evaluated advanced quantitative MRI (qMRI) as a measure of treatment response and prognosis, eight evaluated roles and rationales of ART, and three evaluated the limitations of ART, including duplicates. A more detailed summary of these studies is provided in Table 3.

Figure 1 Diagram of the review process.

Discussion

The role of MRI in EBRT planning

RT planning involves volumetric definition and delineation of the target and other OARs under image guidance. MRI is known to provide superior soft tissue visualisation, which is required for optimal target contouring (3). Therefore, in addition to the commonly used CT with the bladder filling protocol, MRI in the appropriate treatment position is recommended at treatment simulation and planning for EBRT (6).

The evidence of MRI use in EBRT planning was discussed to a limited extent in the included studies. One study demonstrated using both MRI and CT, acquired before the treatment and fused with planning CT of each fraction, to assess the range of target and organ motion and to generate internal margin (10). Another study completed cinematic MRI prior to EBRT, then weekly during EBRT, in 20 patients to track tumour and organ motion by selected anatomic points, and quantify margins around these points, suggesting the necessity of repeat adaptive planning (11). No studies evaluated overall dose escalation to TV in initial EBRT or BT planning at a significant level.

MRI changes during RT

Intrafraction changes and anatomical response

Image-guided strategies are used to assess organ motion within each fraction of the treatment. Organ motion is often complex and multi-dimensional, occurring in anteroposterior (AP), superoinferior and mediolateral directions (7,8,12). Individualised motion assessment and margin set-up are important, as the direction and extent to which the target and other organs shift in position can be influenced by patient characteristics, such as the cervix-uterus position, and bladder and rectal filling (5). Primary clinical TV (CTVp) typically includes the visible tumour, cervix, uterus, upper vagina and parametrium (5). The full range of motion of CTVp is measured when the bladder is full and empty, based on which an ITV is generated prior to dose calculation (9). Uterus displacement with bladder filling can be quantified, based on which patients are classified as having small or large target motion (10).

One study established a correlation between bladder inflow rate and the average length of intrafraction cervix-uterus displacement in EBRT (12). Primarily, displacement between pre-fraction and post-fraction cone-beam CT (CBCT) scans from 16 patients with large tip-of-uterus displacement (>2.5 cm) was measured (12). Movement was most significant in AP and craniocaudal (CC) directions, up to 5.8 mm posteriorly and up to 4.9 mm cranially (5th and 95th percentiles), within a mean time frame of 20.8 minutes (12). There were individual displacements that extended greater than 10 mm, again suggesting considerable inter-patient variation (12). In another study, intrafraction motion of 20 patients by selected anatomic points in cinematic MRI averaged over 5 weeks of EBRT showed the greatest movement at the uterine fundus, and progressively less at the isthmus and cervical os (11).

Bearing in mind MRI acquisition is a lengthy procedure, the change in position and volume of OARs can be magnified by the duration of treatment (34). Dosimetric impact of such change is variable for different OARs. In a prospective study of 43 patients undergoing EBRT, the bladder volume and displacement were measured in daily pre-fraction and post-fraction MRI, with a mean treatment time of 26.84 minutes (13). There was a significant average change in the bladder volume of 30 cm³ over the fraction, with a significant mean displacement in the bladder wall in AP and CC directions (13). With consistent bladder filling protocol for each fraction, a uniform bladder volume throughout the treatment duration may be achievable, thereby having overall less impact on dose distribution (13,34).

Given the variable cervix-uterus displacement and mobility of certain OARs, as well as their dosimetric consequences, accurate TV and OAR definition is critical. Although the majority of the studies were conducted using CT or CBCT-based contouring of TV and OARs, superior soft tissue contrast and reduced interobserver variability of MRI have substantiated its role toward better intrafraction motion assessment (10,12).

Interfraction changes and therapeutic response

Significant tumour regression and OAR volume changes occur throughout the treatment which has implications for dosimetry, target coverage and OAR toxicity. Interfraction MRI plays a defined role in the assessment of tumour regression and residual disease as a measure of treatment response. GTV regression throughout the course of EBRT has been discussed in a few studies. In a study of 27 patients undergoing weekly MRI during fractionated EBRT with concurrent chemotherapy (CCT), an overall regression of 33 to 6 cm³ in the median tumour volume occurred in all cases (16). Analysis of the weekly mean relative volume reduction indicated considerable inter-patient variability, which was attributed to complex biologic processes (16). In a different study of 81 patients undergoing a combination of EBRT and BT with or without CCT, three serial MRIs (pre-RT, mid-RT, post-RT) were performed to assess serial tumour volume regression and the regression rates at mid-RT (17). Overall, the mean tumour volume significantly decreased from 45 to 5 cm³ in the patients receiving RT alone and from 65 to 3 cm³ in those receiving CCRT (17). Furthermore, the mid-RT regression rate of ≥75% was associated with significantly higher 5-year local control rates in both treatment groups (17). Conversely, parametrial infiltration measured by signal intensity on MRI at diagnosis has been correlated with the rate of residual disease at the time of BT following EBRT (18).

The pattern and magnitude of the nodal position and volume changes are different from primary tumours (20). The presence of nodal disease has been associated with poor survival rates (20). On average 58% nodal regression is observed from pre-treatment to week four into IMRT (19). Failure to account for this trend may lead to geographical omission, and suboptimal dosimetry and control of disease, permitting possible regional recurrence in the remaining undertreated tissue (19).

OAR volume and geometry changes over the course of RT directly influence target coverage and the rate of OAR-related complications. In a study of 23 patients treated with 25 fractions of volumetric-modulated arc therapy (VMAT), large rectal filling, defined as displacing the cervix position anteriorly, was found to be the most frequently associated with the lack of target coverage in EBRT (10). Although internal margins for organ motion are evaluated at treatment planning and simulation, patients are likely to be in different stages of fullness on each fraction day of EBRT. This serves as the main rationale for daily re-imaging of bladder and rectal filling in clinical practice (10,35). A bladder filling protocol with each fraction also reduces the bowel volume in the treatment field, thereby reducing rectal doses received in EBRT (10). Late rectal complications are more frequently observed than the bladder, which has a relatively consistent volume and dose (35).

The mapping of the discussed interfraction changes in accordance with disease regression, the pattern of residual disease and OAR motion can be improved by the high soft tissue resolution of MRI. MRI-guided contouring of the dynamic TV for subsequent fractions of EBRT can optimise spatial dose distribution and target coverage. This is closely associated with the precision of target irradiation and minimisation of OAR toxicity, thereby improving overall clinical outcome.

Advanced quantitative imaging techniques

While T1- or T2-weighted imaging provides anatomical information in high soft tissue resolution, advanced qMRI techniques, such as diffuse-weighted imaging (DWI) or dynamic contrast-enhance MRI (DCE-MRI), have proven potential for predicting and monitoring clinical response (25,26). Studies have recently highlighted intravoxel incoherent motion (IVIM) imaging as an extension to DWI (26,27). IVIM-DWI generates dynamic parameters such as apparent diffusion coefficient (ADC), perfusion fraction (f), pure diffusion (D), and pseudo-diffusion (D*), which show early change during treatment and are surrogate markers of treatment response (25-28). Malignant tumours have lower ADC values at diagnosis (25,26). Significant increase in ADC values occurs throughout and beyond CCRT, as tumour regression leads to reduced tissue density and improved water motion (25-27). In the two studies assessing DWI-based parameters at four different time points (pre-CCRT, 2 and 4 weeks into CCRT, immediately post-CCRT), the average increase in ADC was 0.68 from pre-CCRT to post-CCRT in the total of 58 patients (25,27). In addition to change in ADC during the treatment, higher pre-treatment values of ADC and D have been associated with a worse outcome, determined by the presence of residual disease post-CCRT (25,28). DCE-MRI is also used to assess micro-perfusion and vascular permeability of tissues; however, it is more complex due to IV contrast involved (25). Inherent geometrical distortion of advanced qMRI can be corrected by deformable image registration to improve accuracy (29).

Rationales for MRIgART

The consistent aim of RT is to maintain target coverage while sparing OARs to reduce long-term gastrointestinal (GI) and haematological complications, and small planning TV margins are one such way (7,9,30). However, achieving small margins is not only difficult due to complex intrapelvic organ dynamics in cervical cancer, but it also risks target underdosing and local recurrence (30). MRIgART can mitigate these challenges with strategies that optimise RT treatment plans to the up-to-date soft tissue information provided by MRI.

There are two main streams of adaptive strategies: online automated adaptation and offline re-planning. The rationale for online ART is that the unique combination of target geometry and organ filling on each fraction day can be accounted for (8,31). The stepwise workflow of online ART is outlined in Figure 2. Achieving such a regimented and technical process within the limited treatment time, while patients remain on the treatment couch, may be challenging (5). Hence, offline re-planning is currently more commonly practised (33). In cervical cancer, dose-adapted re-plans has shown to be more effective in ensuring target coverage than anatomy-focused re-plans, with minimal to moderate impact on OAR doses (30). In one study of fifteen patients enrolled in 4-week IMRT, a hybrid of weekly online MRI and variable frequencies (none, single, or weekly) of offline re-planning were used in parallel (32). Geometric correction of online MRI was either done with reference to bony structures on CBCT, or on soft tissue matched to the image of planned dose distribution (32). The greatest efficacy in enhancing target coverage was seen when MRI-guided online re-planning with soft tissue matching and frequent offline re-planning were combined (32).

Figure 2 Workflow of online adaptive RT (5,9). MR, magnetic resonance; OAR, organs at risk; RT, radiotherapy.

Challenges of clinical implementation

Current barriers to the implementation of MRIgART are predominantly logistical, especially in lower-income countries (31,32). In EBRT, the scarcity of a magnetic resonance linear accelerator (MR-linac), and intensive resources for planning and timely delivery have restricted the use of MRIgART (31). In particular, online MRIgART not only requires an appropriate software, but also the skill sets of technicians and the adoption of such a regimented multidimensional workflow at a department or institution level (31). Moreover, financial implications for staff training and equipment cannot be overlooked (33). In summary, the favourable therapeutic outcome of MRIgART is a product of longer, more expensive, and more complex processes.

Limitations of this review

Some studies from this review have small sample sizes, although a few are in larger scales. Limited periods of data collection during the treatment, ranging from one to several fractions, and the lack of post-treatment follow-up for some of them are other potential limitations of the studies. There is currently limited literature available on MRIgART as this is an emerging technology, while most of the existing data pertain to MRI-guided BT (MRIgBT). Therefore, more research of clinical application and outcome of MRIgART is needed.

Conclusions

In RT for cervical cancer, MRI enables accurate target delineation, assessment of intrafraction organ motion, as well as interfraction volume and geometry changes. Advanced qMRI can further generate dynamic parameters to predict and monitor treatment response. MRIgART offers novel individualised strategies, which ensure that treatment plans are optimised to these changes, maintaining adequate target coverage, while minimising unnecessary OAR irradiation and toxicity. Ultimately, improved local control and overall outcome can be achieved, although more research is needed to evaluate its rationales against the logistical challenges.

Acknowledgments

Funding: None.

Footnote

Reporting Checklist: The authors have completed the Narrative Review reporting checklist. Available at https://cco.amegroups.com/article/view/10.21037/cco-23-91/rc

Peer Review File: Available at https://cco.amegroups.com/article/view/10.21037/cco-23-91/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://cco.amegroups.com/article/view/10.21037/cco-23-91/coif). The authors have no conflicts of interest to disclose.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

References

1. Sung H, Ferlay J, Siegel RL, et al. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA Cancer J Clin 2021;71:209-49. [Crossref] [PubMed]
2. Tan Mbbs Mrcp Frcr Md LT. Image-guided Adaptive Radiotherapy in Cervical Cancer. Semin Radiat Oncol 2019;29:284-98. [Crossref] [PubMed]
3. Mahantshetty U, Poetter R, Beriwal S, et al. IBS-GEC ESTRO-ABS recommendations for CT based contouring in image guided adaptive brachytherapy for cervical cancer. Radiother Oncol 2021;160:273-84. [Crossref] [PubMed]
4. Jastaniyah N, Yoshida K, Tanderup K, et al. A volumetric analysis of GTVD and CTVHR as defined by the GEC ESTRO recommendations in FIGO stage IIB and IIIB cervical cancer patients treated with IGABT in a prospective multicentric trial (EMBRACE). Radiother Oncol 2016;120:404-11. [Crossref] [PubMed]
5. White IM, Scurr E, Wetscherek A, et al. Realizing the potential of magnetic resonance image guided radiotherapy in gynaecological and rectal cancer. Br J Radiol 2019;92:20180670. [Crossref] [PubMed]
6. Lim K, Small W Jr, Portelance L, et al. Consensus guidelines for delineation of clinical target volume for intensity-modulated pelvic radiotherapy for the definitive treatment of cervix cancer. Int J Radiat Oncol Biol Phys 2011;79:348-55. [Crossref] [PubMed]
7. Kishigami Y, Nakamura M, Nakao M, et al. Three-dimensional assessment of interfractional cervical and uterine motions using daily magnetic resonance images to determine margins and timing of replanning. J Appl Clin Med Phys 2023;24:e14073. [Crossref] [PubMed]
8. Yen A, Zhong X, Lin MH, et al. Optimizing Online Adaptation Timing in the Treatment of Locally Advanced Cervical Cancer. Pract Radiat Oncol 2024;14:e159-64. [Crossref] [PubMed]
9. Shelley CE, Barraclough LH, Nelder CL, et al. Adaptive Radiotherapy in the Management of Cervical Cancer: Review of Strategies and Clinical Implementation. Clin Oncol (R Coll Radiol) 2021;33:579-90. [Crossref] [PubMed]
10. Jensen NBK, Assenholt MS, Fokdal LU, et al. Cone beam computed tomography-based monitoring and management of target and organ motion during external beam radiotherapy in cervical cancer. Phys Imaging Radiat Oncol 2018;9:14-20. [Crossref] [PubMed]
11. Chan P, Dinniwell R, Haider MA, et al. Inter- and intrafractional tumor and organ movement in patients with cervical cancer undergoing radiotherapy: a cinematic-MRI point-of-interest study. Int J Radiat Oncol Biol Phys 2008;70:1507-15. [Crossref] [PubMed]
12. Heijkoop ST, Langerak TR, Quint S, et al. Quantification of intra-fraction changes during radiotherapy of cervical cancer assessed with pre- and post-fraction Cone Beam CT scans. Radiother Oncol 2015;117:536-41. [Crossref] [PubMed]
13. Li X, Wang L, Cui Z, et al. Online MR evaluation of inter- and intra-fraction uterus motions and bladder volume changes during cervical cancer external beam radiotherapy. Radiat Oncol 2021;16:179. [Crossref] [PubMed]
14. Boldrini L, Chiloiro G, Pesce A, et al. Hybrid MRI guided radiotherapy in locally advanced cervical cancer: Case report of an innovative personalized therapeutic approach. Clin Transl Radiat Oncol 2019;20:27-9. [Crossref] [PubMed]
15. Peters NH, Patterson AJ, Horan G, et al. Assessment of ovarian movement on consecutive pelvic MRI examinations in patients with gynaecological malignancies: what is the planning organ-at-risk volume for radiotherapy? Br J Radiol 2012;85:1407-14. [Crossref] [PubMed]
16. Lim K, Chan P, Dinniwell R, et al. Cervical cancer regression measured using weekly magnetic resonance imaging during fractionated radiotherapy: radiobiologic modeling and correlation with tumor hypoxia. Int J Radiat Oncol Biol Phys 2008;70:126-33. [Crossref] [PubMed]
17. Nam H, Park W, Huh SJ, et al. The prognostic significance of tumor volume regression during radiotherapy and concurrent chemoradiotherapy for cervical cancer using MRI. Gynecol Oncol 2007;107:320-5. [Crossref] [PubMed]
18. Schmid MP, Fidarova E, Pötter R, et al. Magnetic resonance imaging for assessment of parametrial tumour spread and regression patterns in adaptive cervix cancer radiotherapy. Acta Oncol 2013;52:1384-90. [Crossref] [PubMed]
19. Schippers MG, Bol GH, de Leeuw AA, et al. Position shifts and volume changes of pelvic and para-aortic nodes during IMRT for patients with cervical cancer. Radiother Oncol 2014;111:442-5. [Crossref] [PubMed]
20. Russo L, Pasciuto T, Lupinelli M, et al. The value of MRI in quantification of parametrial invasion and association with prognosis in locally advanced cervical cancer: the "PLACE" study. Eur Radiol 2023; Epub ahead of print. [Crossref] [PubMed]
21. Serban M, Kirisits C, Pötter R, et al. Isodose surface volumes in cervix cancer brachytherapy: Change of practice from standard (Point A) to individualized image guided adaptive (EMBRACE I) brachytherapy. Radiother Oncol 2018;129:567-74. [Crossref] [PubMed]
22. Asher D, Padgett KR, Llorente RE, et al. Magnetic Resonance-guided External Beam Radiation and Brachytherapy for a Patient with Intact Cervical Cancer. Cureus 2018;10:e2577. [Crossref] [PubMed]
23. Pötter R, Georg P, Dimopoulos JC, et al. Clinical outcome of protocol based image (MRI) guided adaptive brachytherapy combined with 3D conformal radiotherapy with or without chemotherapy in patients with locally advanced cervical cancer. Radiother Oncol 2011;100:116-23. [Crossref] [PubMed]
24. Ma DJ, Zhu JM, Grigsby PW. Change in T2-fat saturation MRI correlates with outcome in cervical cancer patients. Int J Radiat Oncol Biol Phys 2011;81:e707-12. [Crossref] [PubMed]
25. Zhu L, Zhu L, Shi H, et al. Evaluating early response of cervical cancer under concurrent chemo-radiotherapy by intravoxel incoherent motion MR imaging. BMC Cancer 2016;16:79. [Crossref] [PubMed]
26. Zhu L, Wang H, Zhu L, et al. Predictive and prognostic value of intravoxel incoherent motion (IVIM) MR imaging in patients with advanced cervical cancers undergoing concurrent chemo-radiotherapy. Sci Rep 2017;7:11635. [Crossref] [PubMed]
27. Zhu L, Zhu L, Wang H, et al. Predicting and Early Monitoring Treatment Efficiency of Cervical Cancer Under Concurrent Chemoradiotherapy by Intravoxel Incoherent Motion Magnetic Resonance Imaging. J Comput Assist Tomogr 2017;41:422-9. [Crossref] [PubMed]
28. Zheng X, Guo W, Dong J, et al. Prediction of early response to concurrent chemoradiotherapy in cervical cancer: Value of multi-parameter MRI combined with clinical prognostic factors. Magn Reson Imaging 2020;72:159-66. [Crossref] [PubMed]
29. Haack S, Kallehauge JF, Jespersen SN, et al. Correction of diffusion-weighted magnetic resonance imaging for brachytherapy of locally advanced cervical cancer. Acta Oncol 2014;53:1073-8. [Crossref] [PubMed]
30. Lim K, Stewart J, Kelly V, et al. Dosimetrically triggered adaptive intensity modulated radiation therapy for cervical cancer. Int J Radiat Oncol Biol Phys 2014;90:147-54. [Crossref] [PubMed]
31. Bertholet J, Anastasi G, Noble D, et al. Patterns of practice for adaptive and real-time radiation therapy (POP-ART RT) part II: Offline and online plan adaption for interfractional changes. Radiother Oncol 2020;153:88-96. [Crossref] [PubMed]
32. Oh S, Stewart J, Moseley J, et al. Hybrid adaptive radiotherapy with on-line MRI in cervix cancer IMRT. Radiother Oncol 2014;110:323-8. [Crossref] [PubMed]
33. Lim K, van Dyk S, Khaw P, et al. Patterns of practice survey for brachytherapy for cervix cancer in Australia and New Zealand. J Med Imaging Radiat Oncol 2017;61:674-81. [Crossref] [PubMed]
34. Simha V, Patel FD, Sharma SC, et al. Evaluation of intrafraction motion of the organs at risk in image-based brachytherapy of cervical cancer. Brachytherapy 2014;13:562-7. [Crossref] [PubMed]
35. Morgia M, Cuartero J, Walsh L, et al. Tumor and normal tissue dosimetry changes during MR-guided pulsed-dose-rate (PDR) brachytherapy for cervical cancer. Radiother Oncol 2013;107:46-51. [Crossref] [PubMed]