Top

Journal of Neuro-Oncology

Published in:

01-12-2019 | Brain Tumor | Topic Review

Radiation chronotherapy—clinical impact of treatment time-of-day: a systematic review

Authors: Dorela D. Shuboni-Mulligan, Ghislain Breton, DeeDee Smart, Mark Gilbert, Terri S. Armstrong

Published in: Journal of Neuro-Oncology | Issue 3/2019

Abstract

Purpose

Many brain tumor patients suffer from radiation-induced toxicities. Chronotherapy is a treatment modality that utilizes circadian rhythms to optimize the effect on tumor while minimizing negative outcomes on healthy tissue. This review aims to systematically examine the literature on the application of a radiation chronotherapeutic for all cancers and determine the possible advantages of incorporating a circadian-based fixed time-of-day for radiotherapy into CNS cancers.

Methods

A systematic review of the literature was conducted in two electronic databases from inception to February 1, 2019. Primary research manuscripts were screened for those related to adult human subjects exposed to ionizing radiation using the chronotherapy technique.

Results

Nine manuscripts were included in the review from 79 eligible articles. Three were prospective randomized trails and 6 were retrospective reviews. This survey revealed that overall survival and tumor control do not have consistent effects with only 60% and 55.5% of paper which included the variables having some significance, respectively. Treatment symptoms were the primary endpoint for both the prospective trials and were examined in 3 of the retrospective reviews; effects were observed in sensitive tissue for all 5 studies including mucosal linings and skin basal layer.

Conclusions

Existing literature suggests that the application of radiation chronotherapy may reduce negative symptom outcome within highly proliferative tissues. Further examination of radiation chronotherapy in well-designed prospective trials and studies in brain tumor patients are merited.

Halberg F, Haus E, Cardoso SS, Scheving LE, Kühl JFW, Shiotsuka R et al (1973) Toward a chronotherapy of neoplasia: tolerance of treatment depends upon host rhythms. Experientia 29(8):909–934PubMed

Ballesta A, Innominato PF, Dallmann R, Rand DA, Levi FA (2017) Systems chronotherapeutics. Pharmacol Rev 69(2):161–199PubMedPubMedCentral

Ye Y, Xiang Y, Ozguc FM, Kim Y, Liu CJ, Park PK et al (2018) The genomic landscape and pharmacogenomic interactions of clock genes in cancer chronotherapy. Cell Syst 6(3):314–328PubMedPubMedCentral

Yoo SH, Yamazaki S, Lowrey PL, Shimomura K, Ko CH, Buhr ED et al (2004) PERIOD2: LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc Natl Acad Sci USA 101(15):5339–5346PubMed

Mure LS, Le HD, Benegiamo G, Chang MW, Rios L, Jillani N, et al (2018) Diurnal transcriptome atlas of a primate across major neural and peripheral tissues. Science 359(6381): eaao0318PubMedPubMedCentral

Mohawk JA, Green CB, Takahashi JS (2012) Central and peripheral circadian clocks in mammals. Annu Rev Neurosci 35:445–462PubMedPubMedCentral

Hurley JM, Loros JJ, Dunlap JC (2016) Circadian oscillators: Around the transcription–translation feedback loop and on to output. Trends Biochem Sci 41(10):834–846PubMedPubMedCentral

Rossetti S, Esposito J, Corlazzoli F, Gregorski A, Sacchi N (2012) Entrainment of breast (cancer) epithelial cells detects distinct circadian oscillation patterns for clock and hormone receptor genes. Cell Cycle 11(2):350–360PubMedPubMedCentral

Slat EA, Sponagel J, Marpegan L, Simon T, Kfoury N, Kim A et al (2017) Cell-intrinsic, Bmal1-dependent circadian regulation of temozolomide sensitivity in glioblastoma. J Biol Rhythms 32(2):121–129PubMedPubMedCentral

10.

Broadberry E, McConnell J, Williams J, Yang N, Zindy E, Leek A et al (2018) Disrupted circadian clocks and altered tissue mechanics in primary human breast tumours. Breast Cancer Res 20(1):125PubMedCentral

11.

You S, Wood PA, Xiong Y, Kobayashi M, Du-Quiton J, Hrushesky WJ (2005) Daily coordination of cancer growth and circadian clock gene expression. Breast Cancer Res Treat 91(1):47–60PubMed

12.

Zhanfeng N, Yanhui L, Zhou F, Shaocai H, Guangxing L, Hechun X (2015) Circadian genes Per1 and Per2 increase radiosensitivity of glioma in vivo. Oncotarget 6(12):9951PubMedPubMedCentral

13.

Levi F (2001) Circadian chronotherapy for human cancers. Lancet Oncol 2(5):307–315PubMed

14.

Ozturk N, Ozturk D, Kavakli IH, Okyar A (2017) Molecular aspects of circadian pharmacology and relevance for cancer chronotherapy. Int J Mol Sci 18(10):2168PubMedCentral

15.

Baskar R, Lee KA, Yeo R, Yeoh KW (2012) Cancer and radiation therapy: current advances and future directions. Int J Med Sci 9(3):193PubMedPubMedCentral

16.

Sancar A, Lindsey-Boltz LA, Kang TH, Reardon JT, Lee JH, Ozturk N (2010) Circadian clock control of the cellular response to DNA damage. FEBS Lett 584(12):2618–2625PubMedCentral

17.

Palombo P, Moreno-Villanueva M, Mangerich A (2015) Day and night variations in the repair of ionizing-radiation-induced DNA damage in mouse splenocytes. DNA Repair 28:37–47PubMed

18.

Ünsal-Kaçmaz K, Mullen TE, Kaufmann WK, Sancar A (2005) Coupling of human circadian and cell cycles by the timeless protein. Mol Cell Biol 25(8):3109–3116PubMedPubMedCentral

19.

Cotta-Ramusino C, McDonald ER, Hurov K, Sowa ME, Harper JW, Elledge SJ (2011) A DNA damage response screen identifies RHINO, a 9-1-1 and TopBP1 interacting protein required for ATR signaling. Science 332(6035):1313–1317PubMedPubMedCentral

20.

Kang TH, Leem SH (2014) Modulation of ATR-mediated DNA damage checkpoint response by cryptochrome 1. Nucleic Acids Res 42(7):4427–4434PubMedPubMedCentral

21.

Fu L, Pelicano H, Liu J, Huang P, Lee CC (2002) The circadian gene Period2 plays an important role in tumor suppression and DNA damage response in vivo. Cell 111(1):41–50PubMed

22.

Gery S, Komatsu N, Baldjyan L, Yu A, Koo D, Koeffler HP (2006) The circadian gene per1 plays an important role in cell growth and DNA damage control in human cancer cells. Mol Cell 22(3):375–382PubMed

23.

Corrà S, Salvadori R, Bee L, Barbieri V, Mognato M (2017) Analysis of DNA-damage response to ionizing radiation in serum-shock synchronized human fibroblasts. Cell Biol Toxicol 33(4):373–388PubMedPubMedCentral

24.

Xia HC, Niu ZF, Ma H, Cao SZ, Hao SC, Liu ZT, Wang F (2010) Deregulated expression of the Per1 and Per2 in human gliomas. Can J Neurol Sci 37(3):365–370PubMed

25.

Xia HC, Wang F, Li YH, Li ZK, Cao SZ, Li CY, Niu ZF (2012) The circadian gene expression of Per1 and Per2 and their influence on radiotherapeutic sensitivity of glioma in vitro. Future Neurol 7(3):341–348

26.

Bentzen SM (2006) Preventing or reducing late side effects of radiation therapy: radiobiology meets molecular pathology. Nat Rev Cancer 6(9):702PubMed

27.

Donahue B (1992) Short-and long-term complications of radiation therapy for pediatric brain tumors. Pediatr Neurosurg 18(4):207–217PubMed

28.

Prager I, Patties I, Himmelbach K, Kendzia E, Merz F, Müller K et al (2016) Dose-dependent short-and long-term effects of ionizing irradiation on neural stem cells in murine hippocampal tissue cultures: neuroprotective potential of resveratrol. Brain Behav 6(10):e00548PubMedCentral

29.

Stupp R, Mason WP, Van Den Bent MJ, Weller M, Fisher B, Taphoorn MJ et al (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352(10):987–996

30.

Armstrong TS, Vera-Bolanos E, Acquaye AA, Gilbert MR, Ladha H, Mendoza T (2016) The symptom burden of primary brain tumors: evidence for a core set of tumor-and treatment-related symptoms. Neuro-Oncology 18(2):252–260PubMed

31.

Armstrong TS, Vera E, Zhou R, Acquaye AA, Sullaway CM, Berger AM et al (2017) Association of genetic variants with fatigue in patients with malignant glioma. Neuro-Oncol Pract 5(2):122–128

32.

Comasco E, Nordquist N, Göktürk C, Åslund C, Hallman J, Oreland L, Nilsson KW (2010) The clock gene PER2 and sleep problems: association with alcohol consumption among Swedish adolescents. Upsala J Med Sci 115(1):41–48PubMed

33.

Lee KA, Gay C, Byun E, Lerdal A, Pullinger CR, Aouizerat BE (2015) Circadian regulation gene polymorphisms are associated with sleep disruption and duration, and circadian phase and rhythm in adults with HIV. Chronobiol Int 32(9):1278–1293PubMedPubMedCentral

34.

Gafarov V, Gromova E, Gagulin I, Panov D, Gafarova A, Krymov E (2019) Association of polymorphism RS934945 Gene PER2 with sleep disoders in the male population 25–44 years in Novosibirsk. Eur Neuropsychopharmacol 29:S923

35.

Toh KL, Jones CR, He Y, Eide EJ, Hinz WA, Virshup DM et al (2001) An hPer2 phosphorylation site mutation in familial advanced sleep phase syndrome. Science 291(5506):1040–1043PubMed

36.

Satoh K, Mishima K, Inoue Y, Ebisawa T, Shimizu T (2003) Two pedigrees of familial advanced sleep phase syndrome in Japan. Sleep 26(4):416–417PubMed

37.

Zheng B, Larkin DW, Albrecht U, Sun ZS, Sage M, Eichele G et al (1999) The mPer2 gene encodes a functional component of the mammalian circadian clock. Nature 400(6740):169PubMed

38.

Ikegami K, Iigo M, Yoshimura T (2013) Circadian clock gene Per2 is not necessary for the photoperiodic response in mice. PLoS ONE 8(3):e58482PubMedPubMedCentral

39.

Lee HJ, Kim L, Kang SG, Yoon HK, Choi JE, Park YM et al (2011) PER2 variation is associated with diurnal preference in a Korean young population. Behav Genet 41(2):273–277PubMed

40.

Bjarnason GA, MacKenzie RG, Nabid A, Hodson ID, El-Sayed S, Grimard L et al (2008) Comparison of toxicity associated with early morning versus late afternoon radiotherapy in patients with head-and-neck cancer: a prospective randomized trial of the National Cancer Institute of Canada Clinical Trials Group (HN3). Int J Radiat Oncol* Biol* Phys 73(1):166–172PubMed

41.

Shukla P, Gupta D, Bisht SS, Pant MC, Bhatt ML, Gupta R et al (2010) Circadian variation in radiation-induced intestinal mucositis in patients with cervical carcinoma. Cancer 116(8):2031–2035PubMed

42.

Goyal M, Shukla P, Gupta D, Bisht SS, Dhawan A, Gupta S, et al (2009) Oral mucositis in morning vs. evening irradiated patients: a randomised prospective study. Int J Radiat Biol 85(6):504–509PubMed

43.

Chan S, Zhang L, Rowbottom L, McDonald R, Bjarnason GA, Tsao M et al (2016) Effects of circadian rhythms and treatment times on the response of radiotherapy for painful bone metastases. Ann Palliat Med 6(1):14–25PubMed

44.

Noh JM, Choi DH, Park H, Huh SJ, Park W, Seol SW et al (2014) Comparison of acute skin reaction following morning versus late afternoon radiotherapy in patients with breast cancer who have undergone curative surgical resection. J Radiat Res 55(3):553–558PubMedPubMedCentral

45.

Hsu FM, Hou WH, Huang CY, Wang CC, Tsai CL, Tsai YC et al (2016) Differences in toxicity and outcome associated with circadian variations between patients undergoing daytime and evening radiotherapy for prostate adenocarcinoma. Chronobiol Int 33(2):210–219PubMed

46.

Badiyan SN, Ferraro DJ, Yaddanapudi S, Drzymala RE, Lee AY, Silver SA et al (2013) Impact of time of day on outcomes after stereotactic radiosurgery for non–small cell lung cancer brain metastases. Cancer 119(19):3563–3569PubMed

47.

Rahn DA III, Ray DK, Schlesinger DJ, Steiner L, Sheehan JP, O'Quigley JM, Rich T (2011) Gamma knife radiosurgery for brain metastasis of nonsmall cell lung cancer: is there a difference in outcome between morning and afternoon treatment? Cancer 117(2):414–420PubMed

48.

Chow E, Hoskin P, Mitera G, Zeng L, Lutz S, Roos D et al (2012) Update of the international consensus on palliative radiotherapy endpoints for future clinical trials in bone metastases. Int J Radiat Oncol* Biol* Phys 82(5):1730–1737PubMed

49.

Squire T, Buchanan G, Rangiah D, Davis I, Yip D, Chua YJ et al (2017) Does chronomodulated radiotherapy improve pathological response in locally advanced rectal cancer? Chronobiol Int 34(4):492–503PubMed

50.

Browman GP, Wong G, Hodson I et al (1993) Influence of cigarette smoking on the efficacy of radiation therapy in head and neck cancer. N Engl J Med 328:159–163PubMed

51.

Stone HB, Coleman CN, Anscher MS, McBride WH (2003) Effects of radiation on normal tissue: consequences and mechanisms. Lancet Oncol 4(9):529–536

52.

Harper E, Talbot CJ (2019) Is it time to change radiotherapy: the dawning of chronoradiotherapy? Clin Oncol 31(5):326–335

53.

Huang Y, Yu Q, Liu Y, Zhu Z, Wang L, Wang H, Li K (2017) Efficacy and safety of chronomodulated chemotherapy for patients with metastatic colorectal cancer: a systematic review and meta-analysis. Asia-Pac J Clin Oncol 13(2):e171–e178PubMed

54.

Lévi FA, Zidani R, Vannetzel JM, Perpoint B, Focan C, Faggiuolo R et al (1994) Chronomodulated versus fixed-infusion—rate delivery of ambulatory chemotherapy with oxaliplatin, fluorouracil, and folinic acid (Leucovorin) in patients with colorectal cancer metastases: a randomized multi-institutional trial. JNCI 86(21):1608–1617

55.

Eriguchi M, Levi F, Hisa T, Yanagie H, Nonaka Y, Takeda Y (2003) Chronotherapy for cancer. Biomed Pharmacoth 57:92–95

56.

Gerweck LE, Vijayappa S, Kurimasa A, Ogawa K, Chen DJ (2006) Tumor cell radiosensitivity is a major determinant of tumor response to radiation. Can Res 66(17):8352–8355

57.

Chang L, Li L, Li W, Jiang M, Jv Y, Wang L, Hou Y, Long Q, Yu S (2016) Research on radiotherapy at different times of the day for inoperable cervical cancer. Int J Clin Pharmacol Ther 54(11):856

58.

Johnson K, Chang-Claude J, Critchley AM, Kyriacou C, Lavers S, Rattay T, Seibold P, Webb A, West C, Symonds RP, Talbot CJ (2019) Genetic variants predict optimal timing of radiotherapy to reduce side-effects in breast cancer patients. Clin Oncol 31(1):9–16

59.

Ijiri K, Potten CS (1988) Circadian rhythms in the incidence of apoptotic cells and number of clonogenic cells in intestinal crypts after radiation using normal and reversed light conditions. Int J Radiat Biol 53(5):717–727

60.

Ijiri K, Potten CS (1990) The circadian rhythm for the number and sensitivity of radiation-induced apoptosis in the crypts of mouse small intestine. Int J Radiat Biol 58(1):165–175PubMed

61.

Bernabei PA, Balzi M, Saccardi R, Becciolini A, Ferrini PR (1992) Time-dependent sensitivity of rat CFU-GM to total body irradiation. Haematologica 77(1):21–24PubMed

62.

Robbins M, Greene-Schloesser D, Peiffer AM, Shaw E, Chan MD, Wheeler KT (2012) Radiation-induced brain injury: a review. Front Oncol 2:73PubMedPubMedCentral

63.

Hill RJ, Innominato PF, Lévi F, Ballesta A (2019) Optimizing drug infusion schedules towards personalized cancer chronotherapy. BioRes. https://doi.org/10.1101/688606 CrossRef

64.

Münch M, Kramer A (2019) Timing matters: new tools for personalized chronomedicine and circadian health. Acta Physiol 227:e13300

65.

Horne JA, Östberg O (1976) A self-assessment questionnaire to determine morningness-eveningness in human circadian rhythms. Int J Chronobiol 4:97–110PubMed

66.

Roenneberg T, Wirz-Justice A, Merrow M (2003) Life between clocks: daily temporal patterns of human chronotypes. J Biol Rhythms 18(1):80–90PubMed

67.

Duffy JF, Dijk DJ, Hall EF, Czeisler CA (1999) Relationship of endogenous circadian melatonin and temperature rhythms to self-reported preference for morning or evening activity in young and older people. J Investig Med 47(3):141–150PubMed

68.

Clodore M, Benoit O, Foret J (1986) Diurnal variation in subjective and objective measures of sleepiness: the effects of sleep reduction and circadian type. Chronobiol Int 3(4):255–263PubMed

69.

Chung MH, Chang FM, Yang CC, Kuo TB, Hsu N (2009) Sleep quality and morningness–eveningness of shift nurses. J Clin Nurs 18(2):279–284PubMed

70.

Vitale JA, Roveda E, Montaruli A, Galasso L, Weydahl A, Caumo A, Carandente F (2015) Chronotype influences activity circadian rhythm and sleep: differences in sleep quality between weekdays and weekend. Chronobiol Int 32(3):405–415PubMed

71.

Taillard J, Philip P, Bioulac B (1999) Morningness/eveningness and the need for sleep. J Sleep Res 8(4):291–295PubMed

72.

Parsons MJ, Moffitt TE, Gregory AM, Goldman-Mellor S, Nolan PM, Poulton R, Caspi A (2015) Social jetlag, obesity and metabolic disorder: investigation in a cohort study. Int J Obes 39(5):842

73.

Yong M, Fischer D, Germann C, Lang S, Vetter C, Oberlinner C (2016) Are chronotype, social jetlag and sleep duration associated with health measured by Work Ability Index? Chronobiol Int 33(6):721–729PubMed

74.

Gerbes AL, Arbogast B, Schick P, Messerschmidt O (1984) Acute radiation injury of mice and the influence of sudden time shift. Radiat Res 99(2):285–293PubMed

75.

Cui M, Xiao H, Luo D, Zhang X, Zhao S, Zheng Q et al (2016) Circadian rhythm shapes the gut microbiota affecting host radiosensitivity. Int J Mol Sci 17(11):1786PubMedCentral

76.

Chan S, Rowbottom L, McDonald R, Zhang L, Bjarnason GA, Tsao M, Danjoux C, Barnes E, Lam H, Popovic M, DeAngelis C (2016) Could time of whole brain radiotherapy delivery impact overall survival in patients with multiple brain metastases? Ann Palliat Med 5(4):267–279PubMed

77.

Bailey M, Silver R (2014) Sex differences in circadian timing systems: implications for disease. Front Neuroendocrinol 35(1):111–139PubMed

78.

Giacchetti S, Dugué PA, Innominato PF, Bjarnason GA, Focan C, Garufi C et al (2012) Sex moderates circadian chemotherapy effects on survival of patients with metastatic colorectal cancer: a meta-analysis. Ann Oncol 23(12):3110–3116PubMed

79.

Mostafaie N, Kállay E, Sauerzapf E, Bonner E, Kriwanek S, Cross HS et al (2009) Correlated downregulation of estrogen receptor beta and the circadian clock gene Per1 in human colorectal cancer. Mol Carcinog 48(7):642–647PubMed

80.

Dijk DJ, Duffy JF, Riel E, Shanahan TL, Czeisler CA (1999) Ageing and the circadian and homeostatic regulation of human sleep during forced desynchrony of rest, melatonin and temperature rhythms. J Physiol 516(2):611–627PubMedPubMedCentral

81.

Wise PM, Cohen IR, Weiland NG, London ED (1988) Aging alters the circadian rhythm of glucose utilization in the suprachiasmatic nucleus. Proc Natl Acad Sci USA 85(14):5305–5309PubMed

82.

Satinoff E, Li H, Tcheng TK, Liu CHEN, McArthur AJ, Medanic M, Gillette MU (1993) Do the suprachiasmatic nuclei oscillate in old rats as they do in young ones? Am J Physiol-Regul Integr Comp Physiol 265(5):R1216–R1222

83.

Aujard F, Herzog ED, Block GD (2001) Circadian rhythms in firing rate of individual suprachiasmatic nucleus neurons from adult and middle-aged mice. Neuroscience 106(2):255–261PubMed

84.

Davidson AJ, Sellix MT, Daniel J, Yamazaki S, Menaker M, Block GD (2006) Chronic jet-lag increases mortality in aged mice. Curr Biol 16(21):R914–R916PubMedPubMedCentral

Title: Radiation chronotherapy—clinical impact of treatment time-of-day: a systematic review
Authors: Dorela D. Shuboni-Mulligan
Ghislain Breton
DeeDee Smart
Mark Gilbert
Terri S. Armstrong
Publication date: 01-12-2019
Publisher: Springer US
Keywords: Brain Tumor
Radiotherapy
Published in: Journal of Neuro-Oncology / Issue 3/2019
Print ISSN: 0167-594X
Electronic ISSN: 1573-7373
DOI: https://doi.org/10.1007/s11060-019-03332-7

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Radiation chronotherapy—clinical impact of treatment time-of-day: a systematic review

Abstract

Purpose

Methods

Results

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 3/2019

Repeat stereotactic radiosurgery for the management of locally recurrent brain metastases

Surgical and radiosurgical treatment strategies for Cushing’s disease

Microscopic brain invasion in meningiomas previously classified as WHO grade I is not associated with patient outcome

EGFR gene amplification in monocentric and multicentric glioblastoma

Shortened ex vivo manufacturing time of EGFRvIII-specific chimeric antigen receptor (CAR) T cells reduces immune exhaustion and enhances antiglioma therapeutic function

Mortality patterns in long-term survivors of childhood or adolescent central nervous system tumour in Sweden