Pelvic bone marrow sparing radiotherapy for cervical cancer: A systematic review and meta-analysis

Published:October 26, 2021DOI:https://doi.org/10.1016/j.radonc.2021.10.015

      Highlights

      • Pelvic (active) bone marrow (BM) sparing radiotherapy plans reduced pelvic (active) BM irradiation dose.
      • Pooled analysis found that pelvic BM-sparing radiotherapy decreased the incidence of G2+ and G3+ hematological toxicity (OR 0.31/0.42, P < 0.0001).
      • No significant differences in gastrointestinal and urological toxicity were observed between pelvic BM-sparing and non-sparing radiotherapy.
      • Pelvic active BM-sparing radiotherapy also decreased hematologic toxicity (OR 0.42/0.21, P < 0.01).
      • Clinical benefits of pelvic active BM-sparing radiotherapy over pelvic BM-sparing remains to be further investigated.

      Abstract

      Backgrounds

      Concurrent chemo-radiotherapy in patients with locally advanced cervical cancer has significant hematologic toxicities (HT), leading to treatment disruption and affecting patient prognosis. We performed the meta-analysis to assess the clinical benefit of pelvic (active) bone marrow (BM) sparing radiotherapy.

      Methods

      A systematic methodological search of six primary electronic databases was performed. This systematic review mainly assessed the differences in pelvic (active) BM dose-volume parameters (DVP), hematologic toxicity of pelvic (active) BM sparing versus non-sparing radiotherapy plans. The secondary objective was to explore optimal dose limitation regimens and evaluate other radiation-induced toxicities (gastrointestinal and urological toxicity (GT/UT)). Random-effects models were used for meta-analysis.

      Results

      Final 65 publications that met inclusion criteria were included in the meta-analysis and descriptive tables. Meta-analysis of mean pelvic BM-DVP differences showed that pelvic BM-V10,20,40,50 (Vx: volume of BM receiving ≥ X Gy) were reduced by −4.6% [95% CI: −6.6, −2.6], −10.9% [−13.2, −8.6], −7.3% [−9.5, −5.2] and −3.4% [−4.3, −2.4] in pelvic BM-sparing plans. Pelvic BM sparing radiotherapy decreased G2/3+ HT [odds ratio (OR) 0.31, (0.23, 0.41)/0.42, (0.28, 0.63)], without increasing GT [G2/3+: OR 0.76, (0.51, 1.14)/0.90, (0.47, 1.74)] and UT [G2/3+: OR 0.91, (0.57, 1.46)/0.54, (0.25, 1.17)]. Pelvic active BM sparing radiotherapy also reduced HT [G2/3+ HT: OR 0.42, (0.23, 0.77)/0.34, (0.16, 0.72)]. There were significant variations between publications in dose restriction regimens.

      Conclusion

      The pelvic BM protection radiotherapy can decrease BM dose and HT. Moreover, it does not increase GT and UT. The clinical benefit of pelvic active BM protection needs to be further validated in randomized controlled trials.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic and Personal
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Radiotherapy and Oncology
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

      1. Cohen PA, Jhingran A, Oaknin A, Denny L. Cervical cancer. Lancet 2019;393:169–82. https://doi.org/10.1016/S0140-6736(18)32470-X.

      2. Naga Ch P, Gurram L, Chopra S, Mahantshetty U. The management of locally advanced cervical cancer. Curr Opin Oncol 2018;30:323–29. https://doi.org/10.1097/CCO.0000000000000471

      3. Yu D, Bai Y, Feng Y, Wang L, et al. Which bone marrow sparing strategy and radiotherapy technology is most beneficial in bone marrow-sparing intensity modulated radiation therapy for patients with cervical cancer? Front Oncol 2020;10:554241. https://doi.org/10.3389/fonc.2020.554241.

        • Bao Z.
        • Wang D.
        • Chen S.
        • Chen M.
        • Jiang D.
        • Yang C.
        • et al.
        Optimal dose limitation strategy for bone marrow sparing in intensity-modulated radiotherapy of cervical cancer.
        Radiat Oncol. 2019; 14https://doi.org/10.1186/s13014-019-1324-y
      4. Wang SB, Liu JP, Lei KJ, Jia YM, et al. The volume of 99mTc sulfur colloid SPECT-defined active bone marrow can predict grade 3 or higher acute hematologic toxicity in locally advanced cervical cancer patients who receive chemo-radiotherapy. Cancer Med 2019;8:7219–226. https://doi.org/10.1002/cam4.2601.

        • Lewis S.
        • Chopra S.
        • Naga P.
        • Pant S.
        • Dandpani E.
        • Bharadwaj N.
        • et al.
        Acute hematological toxicity during post-operative bowel sparing image-guided intensity modulated radiation with concurrent cisplatin.
        Br J Radiol. 2018; 91: 20180005https://doi.org/10.1259/bjr.20180005
        • Li P.
        The role of active bone marrow dose limitation based on multimodal medical images in intensity-modulated radiotherapy for cervical cancer.
        Guangzhou Medical University, 2019
        • Franco P.
        • Arcadipane F.
        • Ragona R.
        • Mistrangelo M.
        • Cassoni P.
        • Racca P.
        • et al.
        Hematologic toxicity in anal cancer patients during combined chemo-radiation: a radiation oncologist perspective.
        Expert Rev Anticancer Ther. 2017; 17: 335-345
      5. Mell LK, Kochanski JD, Roeske JC, Haslam JJ, et al. Dosimetric predictors of acute hematologic toxicity in cervical cancer patients. Int J Radiat Oncol Biol Phys 2006;66:1356–365. https://doi.org/10.1016/j.ijrobp.2006.03.018.

        • Zhou Y.M.
        • Freese C.
        • Meier T.
        • Go D.
        • Khullar K.
        • Sudhoff M.
        • et al.
        The absolute volume of PET-defined, active bone marrow spared predicts for high grade hematologic toxicity in cervical cancer patients undergoing chemoradiation.
        Clin Transl Oncol. 2018; 20: 713-718
      6. Hozo SP, Djulbegovic B, Hozo I. Estimating the mean and variance from the median, range, and the size of a sample. BMC Med Res Methodol 2005;5:13. https://doi.org/10.1186/1471-2288-5-13.

        • Murakami N.
        • Okamoto H.
        • Kasamatsu T.
        • Kobayashi K.
        • et al.
        A dosimetric analysis of intensity-modulated radiation therapy with bone marrow sparing for cervical cancer.
        Anticancer Res. 2014; 34: 5091-5098
      7. Kumar T, Schernberg A, Busato F, Laurans M, et al. Correlation between pelvic bone marrow radiation dose and acute hematological toxicity in cervical cancer patients treated with concurrent chemoradiation. Cancer Manag Res 2019; 11:6285–297. https://doi.org/10.2147/CMAR.S195989.

        • Zhu H.
        • Zakeri K.
        • Vaida F.
        • Carmona R.
        • Dadachanji K.K.
        • Bair R.
        • et al.
        Longitudinal study of acute haematologic toxicity in cervical cancer patients treated with chemo-radiotherapy.
        J Med Imaging Radiat Oncol. 2015; 59: 386-393
        • Klopp A.H.
        • Moughan J.
        • Portelance L.
        • Miller B.E.
        • Salehpour M.R.
        • Hildebrandt E.
        • et al.
        Hematologic toxicity in RTOG 0418: A phase 2 study of postoperative IMRT for gynecologic cancer.
        Int J Radiat Oncol Biol Phys. 2013; 86: 83-90
      8. Mahantshetty U, Krishnatry R, Chaudhari S, Kanaujia A, et al. Comparison of 2 contouring methods of bone marrow on CT and correlation with concurrent cisplatin for cervical cancer. Int J Gynecol Cancer 2012;1427–434. https://doi.org/10.1097/IGC.0b013e3182664b46.

        • Rose B.S.
        • Aydogan B.
        • Liang Y.
        • Yeginer M.
        • Hasselle M.D.
        • Dandekar V.
        • et al.
        Normal tissue complication probability modeling of acute hematologic toxicity in cervical cancer patients treated with chemoradiotherapy.
        Int J Radiat Oncol Biol Phys. 2011; 79: 800-807
        • Albuquerque K.
        • Giangreco D.
        • Morrison C.
        • Siddiqui M.
        • Sinacore J.
        • Potkul R.
        • et al.
        Radiation-related predictors of hematologic toxicity after concurrent chemoradiation for cervical cancer and implications for bone marrow-sparing pelvic IMRT.
        Int J Radiat Oncol Biol Phys. 2011; 79: 1043-1047
      9. Huang J, Gu F, Ji T, Zhao J, et al. Pelvic bone marrow sparing intensity modulated radiotherapy reduces the incidence of the hematologic toxicity of patients with cervical cancer receiving concurrent chemo-radiotherapy: a single-center prospective randomized controlled trial. Radiat Oncol 2020;15:180. https://doi.org/10.1186/s13014-020-01606-3.

      10. Yan K, Ramirez E, Xie X, Gu X, et al. Predicting severe hematologic toxicity from extended-field chemoradiation of para-aortic nodal metastases from cervical cancer. Pract Radiat Oncol 2018;8:13–19. https://doi.org/10.1016/j.prro.2017.07.001.

        • Elicin O.
        • Callaway S.
        • Prior J.O.
        • Bourhis J.
        • Ozsahin M.
        • Herrera F.G.
        [18F] FDG-PET standard uptake value as a metabolic predictor of bone marrow response to radiation: impact on acute and late hematological toxicity in cervical cancer patients treated with chemoradiation therapy.
        Int J Radiat Oncol Biol Phys. 2014; 90: 1099-1107
        • Rose B.S.
        • Liang Y.
        • Lau S.K.
        • Jensen L.G.
        • Yashar C.M.
        • Hoh C.K.
        • et al.
        Correlation between radiation dose to 18F-FDG-PET defined active bone marrow subregions and acute hematologic toxicity in cervical cancer patients treated with chemoradiotherapy.
        Int J Radiat Oncol Biol Phys. 2012; 83: 1185-1191
        • Mell L.K.
        • Sirák I.
        • Wei L.
        • Tarnawski R.
        • Mahantshetty U.
        • Yashar C.M.
        • et al.
        Bone marrow-sparing intensity modulated radiation therapy with concurrent cisplatin for stage IB-IVA cervical cancer: an international multicenter phase II clinical trial (INTERTECC-2).
        Int J Radiat Oncol Biol Phys. 2017; 97: 536-545
        • Gupta N.
        • Prakash C.
        • Chakrabarty K.
        • Giri U.
        • et al.
        Potential advantages of bone marrow sparing IMRT in cancer cervix: a dosimetric evaluation.
        J Clin Diagn Res. 2019; 13: C1-C5https://doi.org/10.7860/JCDR/2019/39841.12745
      11. Singareddy R, Bajwa HK, Reddy MM. Dosimetric predictors of acute bone marrow toxicity in carcinoma cervix-experience from a tertiary cancer centre in India. Rep Pract Oncol Radiother 2021;26:259–65. https://doi.org/10.5603/RPOR.a2021.0039.

        • Xu X.M.
        • Yang J.
        • Liu Q.
        • Liu Y.
        • et al.
        Analysis of acute myelosuppression in intensity modulated radiotherapy for cervical cancer.
        Chin J Cancer Prev Treat. 2019; 26: 871-875
        • Qing H.
        • Chuanshu C.
        • Weijian Z.
        • Shaobin Z.
        • et al.
        Low-dose range of pelvic irradiation leads to acute hematological toxicity in early-stage cervical cancer with intermediate risk factors by postoperative intensity-modulated radiotherapy.
        Eur J Gynaecol Oncol. 2019; 40: 437-442
        • Khullar K.
        • Sudhoff M.
        • Elson J.
        • Herzog T.
        • Jackson A.
        • Billingsley C.
        • et al.
        A comparison of dosimetric parameters in PET-based active bone marrow volume and total bone volume in prediction of hematologic toxicity in cervical cancer patients treated with chemoradiation.
        J Radiat Oncol. 2017; 6: 161-165
      12. Bosque MÁS, Cervantes-Bonilla MÁ, Palacios-Saucedo GDC. Clinical and dosimetric factors associated with the development of hematologic toxicity in locally advanced cervical cancer treated with chemotherapy and 3D conformal radiotherapy. Rep Pract Oncol Radiother 2018;23:392–97. https://doi.org/ 10.1016/j.rpor.2018.07.011.

      13. Li Q, Jiang M, Chen J, Liu W, et al. Correlation between bone marrow dose volumes and acute hematological toxicity in postoperative gynecological cancer patients. Pak J Med Sci 2016;32:1547–552. https://doi.org/10.12669/pjms.326.11489.

        • Wang Y.
        • Jiang S.
        • Zhang S.
        • Zhao B.
        Dosimetric study of bone marrow sparing intensity modulated radiotherapy for patients with cervical cancer after hysterectomy.
        Chin J of Oncol Prev and Treat. 2018; 10: 38-41
        • Xiao F.
        • Li Y.
        • Wang H.
        • Chen J.
        • et al.
        Dosimetric study of protecting bone marrow by intensity-modulated radiotherapy for patients with cervical cancer after hysterectomy.
        China Oncol. 2013; 23: 200-206
        • Zhu L.
        • Su X.
        • Wu H.
        • Han S.
        • et al.
        Dosimetry of bone marrow irradiated by intensity modulated whole pelvis radiotherapy for cervical cancer.
        Chin J Radiol Med Prot. 2008; 28: 57-60https://doi.org/10.3969/j.issn.1674-5671.2018.01.08
        • Zhang Z.
        • Reyila M.
        • Hasiyeti W.
        • Gulimilamu A.
        • et al.
        Dose-volume restriction analysis based on≥gradeⅡmarrow suppression in radiotherapy for pelvic cancer.
        Chin J Radiat Oncol. 2019; 28: 905-908https://doi.org/10.3760/cma.j.issn.1004-4221.2019.12.006
        • Cui Y.
        • Wang X.
        Analysis of physical factors influencing adverse effects of intensity-modulated radiotherapy for cervical cancer.
        J Hebei Med Univ. 2017; 38: 1340-1344https://doi.org/10.3969/J.ISSN.1007-3205.2017.11.024
        • Feng J.
        • Lin J.
        • Liao S.
        • Luo H.
        • et al.
        The relationship between bone marrow suppression and dose volume of bone marrow irradiation for the postoperative cervical cancer patients received intensity modulated radiotherapy.
        Int J Radiat Med Nucl Med. 2020; 44: 143-150
        • Fang M.
        • Zhou Y.
        • Yang H.
        • Zheng J.
        • et al.
        Comparison of the effects of limited and unlimited pelvic bone marrow doses in postoperative intensity-modulated radiation therapy for cervical cancer.
        China Med Pharm. 2019; 9: 149-151
        • Luo C.
        • Lai L.
        • Huang J.
        • Xu S.
        • et al.
        Application of whole-pelvic intensity modulated radiotherapy to protect bone marrow in postoperative concurrent chemotherapy for cervical cancer.
        J Chin Res. 2018; 35: 347-349https://doi.org/10.3969/j.issn.1671-7171.2018.02.046
      14. Wei J, Li Q, Ning Z, Gu W. Effect of volumetric arc therapy with bone marrow protection on bone marrow irradiation in patients with cervical cancer after operation. Jiangsu Med J 2017;43:341–44. Doi: 10.19460/j.cnki.0253-3685.2017.05.012.

        • Gu K.
        • Hu Q.
        • Qu X.
        • Wang J.
        • et al.
        Intensiy modulated radiation therapy and bone marrow-sparing techniques for locally advanced cervical cancer: a dosimetric study.
        Acta Med Univ Sci Technol Huazhong. 2016; 45: 432-436
      15. Zhang F, Zheng M, Gao J. Bone marrow-sparing intensity-modulated radiotherapy for postoperative treatment of cervical cancer. Chinese-German Journal of Clinical Oncology 2011;10:349–53. http://dx.chinadoi.cn/10.1007 /s10330-011-0795-6.

        • Wu W.
        • Xu Y.
        • Guo L.
        • Lin Y.
        Analysis of correlation between radiation dose parameters of pelvic bone and acute bone marrow suppression in cervical cancer treated with intensity-modulated radiation therapy.
        Cancer Res Clinic. 2021; 33: 174-178
      16. Zhang B, Liu Z, Xu L, Wang J, et al. Relationship between the radiation dose of different anatomic bony sites and neutrophil toxicity in three-dimensional radiotherapy concurrent chemo-radiotherapy for cervical cancer. Chin J Radiat Oncol 2020;29:767–71. http://dx.chinadoi.cn/10. 3760/cma. j. cn113030-20200325-00135.

      17. Wang F, Cao H, Li Q, Liang Y, et al. Study the risk factors of acute hematological toxicity in intensity modulated radiotherapy for cervical cancer and its relationship with pelvic bone marrow receiving dose. J Guangxi Med Univ 2020;37:929–33. http://dx.chinadoi.cn/10.16190/j.cnki. 45-1211/r. 2020.05.027.

        • Xiao S.
        Study on the relationship between bone marrow dose volume parameters and acute myelosuppression and VMAT radiotherapy planning strategy in middle-aged and elderly patients with Cervical cancer treated with simultaneous radio-chemotherapy.
        North Sichuan Medical College. 2020; 66
        • Yang L.
        • Wang Q.
        • Chen X.
        • Shen L.
        • et al.
        The characteristics and influencing factors of bone marrow suppression during concurrent chemo-radiotherapy for patients with cervical carcinoma.
        Modern Oncol. 2019; 27: 4259-4263
        • Chen G.
        • Zuo Y.
        • Han X.
        • Yuan G.
        • et al.
        Relationship between the irradiation of iliac bone marrow and hematological toxicity after intensity-modulated radiotherapy for cervical cancer.
        China Continuing Med Educ. 2019; 11: 81-83
        • Fang M.
        • Gao Y.
        • Shi Y.
        • Li Z.
        • et al.
        Study on the related factors of postoperative Intensity-Modulated radiotherapy for Cervical Cancer in the treatment of myelosuppression.
        China Foreign Med Treat. 2019; 38: 7-10
        • Lu P.
        • Sun S.
        • Qiu H.
        • Wei Y.
        Association between pelvic dosimetric parameters and acute bone marrow suppression in cervical cancer patients receiving intensity modulated radiation therapy.
        J New Med. 2019; 29: 138-141
        • Gao L.
        • Yang S.
        • Liu M.
        Correlation between bone marrow-sparing intensity modulated radiation therapy and hematologic adverse reactions in patients with cervical cancer.
        Oncol Prog. 2017; 15: 1042-1044
        • Tang Y.
        • Yuan Y.
        Risk factors associated with hematologic toxicity in concurrent chemoradiotherapy and IMRT for cervical cancer.
        Cancer Res Prev Treat. 2016; 43: 277-281
        • Huang W.
        • Li Y.
        • Lu W.
        • Tan B.
        Identification of pelvic dose-volumetric parameters that predict acute bone marrow suppression in concurrent chemo-radiotherapy for cervical cancer.
        Chin J Radiol Med Prot. 2016; 36: 207-210
      18. Zhang Y. Factors predicting acute hematologic toxicity in cervical cancer treated with postoperative intensity-modulated radiotherapy and concurrent. Guangxi Medical University. 2015;55.

        • Gao L.
        Hematological toxicity analysis of intensity modulated radiation therapy for bone marrow protection after cervical cancer operation.
        J Pract Gynecol Endocrinol. 2018; 5: 11-14
      19. Huang R, Zeng X, Chen M. The value of bone marrow sparing intensity modulated radiotherapy in elderly cervical cancer after hysterectomy. Chin J Geriatric Care 2018;16:15–17. http://dx.chinadoi.cn/10. 3969/j.issn.1672- 2671.2018.02.005.

        • Wen L.
        • Huang W.
        • Wu W.
        • Cui H.
        • et al.
        Effect of bone marrow-sparing intensity-modulated radiotherapy on acute myelosuppression in patients with cervical cancer.
        Chin J Med Phys. 2018; 35: 399-403
      20. Liao B. Analysis of dosimetry and acute toxicity of bone marrow sparing intensity modulated radiotherapy in lymph-node positive cervical cancer. Guangzhou Medical University. 2018;53.

        • Ran J.
        • Zhang Y.
        • Xue X.
        • Shen J.
        • et al.
        Clinical study of bone marrow- sparing volumetric- modulated arc-radiation therapy for postoperative cervical cancer.
        Chin J General Pract. 2017; 15: 2021-2023
        • Zhang Q.
        • Wang H.
        Clinical study of bone marrow-sparing intensity-modulated radiation therapy for postoperative cervical cancer.
        Chin J Radiol Med Prot. 2015; 35: 441-444
      21. Shen N. Analysis of Dosimetry and Clinical Efficacy of Pelvic Bone Marrow-Sparing Intensity-Modulated Radiotherapy in Advanced Cervical Cancer. [D] HEBEI Medical University. 2015;49.

        • Du C.
        • Cai M.
        • Lin F.
        Clinical observation of hematologic toxicity in intensity modulated radiotherapy for cervical cancer to restrict dosimetry of bone marrow irradiated.
        Med J West China. 2013; 25: 1857-1858
      22. Luo J, Sun Y, Zhang L, Shi W. The dose and clinical study of MRI guided bone marrow protection intensity modulated radiotherapy in chemo-radiotherapy of cervical cancer. J Ningxia Med Univ 2020;42:1222–226. http://dx.chinadoi.cn/10.16050/j.cnki.issn1674-6309.2020.12.007.

      23. Liu J, Ren H, Zhou C, Zhou Y, et al. Correlation between pelvic active bone marrow and hematological toxicity in radiotherapy of cervical cancer. Chin J Radiol Health 2020;29:696–99. http://dx.chinadoi.cn/ 10.13491/j.issn.1004-714X.2020.06.030.

        • Huang G.
        • Deng K.
        • Chen W.
        • Lu Y.
        Study on the application effect of red bone marrow limited intensity modulated radiotherapy after radical cervical cancer resection.
        Chin J for Clinicians. 2019; 47: 586-588
        • Huang R.
        • Teng J.
        • Zeng X.
        • Chen M.
        Application of active bone marrow defined with single photon emission computed tomography to optimize the intensity modulated radiotherapy plan in cervical cancer after hysterectomy.
        Chin J Radiol Med Prot. 2018; 38: 419-423
        • Qin L.
        • Wei H.
        Analysis of hematologic toxicity related factors of intensity modulated radiotherapy combined with chemotherapy for cervical cancer.
        Chin Remedies Chin. 2020; 20https://doi.org/10.11655/zgywylc2020.01.043
        • Yuan J.
        The relationship between the receiving dose of ilium bone marrow and hematoxicity of postoperative in intensity modulating radiotherapy of cervical cancer.
        Guizhou Medical University, 2015
        • Sun S.
        Clinical study on acute toxicity of pelvic bone marrow-sparing intensity-modulated radiotherapy in cervical cancer after hysterectomy.
        Wenzhou Medical University, 2018
      24. Zhang D, Guo H, Zhang Q, Liu L. Dosimetric analysis of bone marrow-sparing pelvic intensity-modulated radiotherapy after surgery for cervical cancer. Chin J Radiat Oncol 2017;26:1303–307. http://dx.chinadoi.cn/ 10.3760/cma.j.issn.1004-4221.2017.11.013

        • Li P.
        • Zhang R.
        • Nie Z.
        • Long M.
        • Zhang G.
        • Fu Z.
        Comparison of nedaplatin- and cisplatin-based concurrent chemoradiotherapy in locally advanced cervical cancer patients: a propensity score analysis.
        Int J Gynecol Cancer. 2018; 28: 1029-1037https://doi.org/10.1097/IGC.0000000000001265
        • Sini C.
        • Fiorino C.
        • Perna L.
        • Noris Chiorda B.
        • Deantoni C.L.
        • Bianchi M.
        • et al.
        Dose-volume effects for pelvic bone marrow in predicting hematological toxicity in prostate cancer radiotherapy with pelvic node irradiation.
        Radiother Oncol. 2016; 118: 79-84https://doi.org/10.1016/j.radonc.2015.11.020
        • Wang J.
        • Tian Y.
        • Tang Y.
        • Wang X.
        • et al.
        A prospective phase II study of magnetic resonance imaging guided hematological bone marrow-sparing intensity-modulated radiotherapy with concurrent chemotherapy for rectal cancer.
        Radiol Med (Torino). 2016; 121: 308-314https://doi.org/10.1007/s11547-015-0605-2
        • McGuire S.M.
        • Menda Y.
        • Ponto L.L.B.
        • Gross B.
        • TenNapel M.
        • Smith B.J.
        • et al.
        Spatial mapping of functional pelvic bone marrow using FLT-PET.
        J Appl Clin Med Phys. 2014; 15: 129-136
        • Liang Y.
        • Bydder M.
        • Yashar C.M.
        • Rose B.S.
        • Cornell M.
        • Hoh C.K.
        • et al.
        Prospective study of functional bone marrow-sparing intensity modulated radiation therapy with concurrent chemotherapy for pelvic malignancies.
        Int J Radiat Oncol Biol Phys. 2013; 85: 406-414https://doi.org/10.1016/j.ijrobp.2012.04.044