Skip to main content

Advertisement

Log in

Radiation-induced changes in normal-appearing gray matter in patients with nasopharyngeal carcinoma: a magnetic resonance imaging voxel-based morphometry study

  • Functional Neuroradiology
  • Published:
Neuroradiology Aims and scope Submit manuscript

Abstract

Introduction

Evidence is accumulating that temporal lobe radiation necrosis in patients with nasopharyngeal carcinoma (NPC) after radiotherapy (RT) could involve gray matter (GM). The purpose of the study was to assess the radiation-induced GM volume differences between NPC patients who had and had not received RT and the effect of time after RT on GM volume differences in those patients who had received RT.

Methods

We used magnetic resonance imaging voxel-based morphometry (VBM) to assess differences in GM volume between 30 NPC patients with normal-appearing whole-brain GM after RT and 15 control patients with newly diagnosed but not yet medically treated NPC. Correlation analyses were used to investigate the relationship between GM volume changes and time after RT.

Results

Patients who had received RT had GM volume decreases in the bilateral superior temporal gyrus, left middle temporal gyrus, right fusiform gyrus, right precentral gyrus, and right inferior parietal lobule (p < 0.001, uncorrected, cluster size >100 voxels). Moreover, the correlation analysis indicated that regional GM volume loss in the left superior temporal gyrus, left middle temporal gyrus, and right fusiform gyrus were negatively related to the mean dose to the ipsilateral temporal lobe, respectively.

Conclusion

These results indicate that GM volume deficits in bilateral temporal lobes in patients who had received RT might be radiation-induced. Our findings might provide new insight into the pathogenesis of radiation-induced structural damage in normal-appearing brain tissue. Yet this is an exploratory study, whose findings should therefore be taken with caution.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Chan AT (2010) Nasopharyngeal carcinoma. Ann Oncol 21(Suppl 7):i308–i312

    Google Scholar 

  2. Sun Y, Zhou GQ, Qi ZY, Zhang L, Huang SM, Liu LZ, Li L, Lin AH, Ma J (2013) Radiation-induced temporal lobe injury after intensity modulated radiotherapy in nasopharyngeal carcinoma patients: a dose-volume-outcome analysis. BMC Cancer 13:397

    Article  PubMed Central  PubMed  Google Scholar 

  3. Lee AW, Law SC, Ng SH, Chan DK, Poon YF, Foo W, Tung SY, Cheung FK, Ho JH (1992) Retrospective analysis of nasopharyngeal carcinoma treated during 1976–1985: late complications following megavoltage irradiation. Br J Radiol 65:918–928

    Article  CAS  PubMed  Google Scholar 

  4. Belka C, Budach W, Kortmann RD, Bamberg M (2001) Radiation induced CNS toxicity—molecular and cellular mechanisms. Br J Cancer 85:1233–1239

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  5. Sundgren PC (2009) MR spectroscopy in radiation injury. AJNR Am J Neuroradiol 30:1469–1476

    Article  CAS  PubMed  Google Scholar 

  6. Xiong WF, Qiu SJ, Wang HZ, Lv XF (2013) 1H-MR spectroscopy and diffusion tensor imaging of normal-appearing temporal white matter in patients with nasopharyngeal carcinoma after irradiation: initial experience. J Magn Reson Imaging 37:101–108

    Article  PubMed  Google Scholar 

  7. Wang HZ, Qiu SJ, Lv XF, Wang YY, Liang Y, Xiong WF (2012) Diffusion tensor imaging and 1H-MRS study on radiation-induced brain injury after nasopharyngeal carcinoma radiotherapy. Clin Radiol 67:340–345

    Google Scholar 

  8. Chan YL, Leung SF, King AD, Choi PH, Metreweli C (1999) Late radiation injury to the temporal lobes: morphologic evaluation at MR imaging. Radiology 213:800–807

    Article  CAS  PubMed  Google Scholar 

  9. Norris AM, Carrington BM, Slevin NJ (1997) Late radiation change in the CNS: MR imaging following gadolinium enhancement. Clin Radiol 52:356–362

    Article  CAS  PubMed  Google Scholar 

  10. Peterson K, Clark HB, Hall WA, Truwit CL (1995) Multifocal enhancing magnetic resonance imaging lesions following cranial irradiation. Ann Neurol 38:237–244

    Article  CAS  PubMed  Google Scholar 

  11. Chong VF, Fan YF, Mukherji SK (2000) Radiation-induced temporal lobe changes: CT and MR imaging characteristics. AJR Am J Roentgenol 175:431–436

    Article  CAS  PubMed  Google Scholar 

  12. Steen RG, Spence D, Wu S, Xiong X, Kun LE, Merchant TE (2001) Effect of therapeutic ionizing radiation on the human brain. Ann Neurol 50:787–795

    Article  CAS  PubMed  Google Scholar 

  13. Ashburner J, Friston KJ (2000) Voxel-based morphometry—the methods. Neuroimage 11:805–821

    Article  CAS  PubMed  Google Scholar 

  14. Agostini A, Benuzzi F, Filippini N, Bertani A, Scarcelli A, Farinelli V, Marchetta C, Calabrese C, Rizzello F, Gionchetti P, Ercolani M, Campieri M, Nichelli P (2013) New insights into the brain involvement in patients with Crohn’s disease: a voxel-based morphometry study. Neurogastroenterol Motil 25:147–182

    Article  CAS  PubMed  Google Scholar 

  15. Schmidt-Wilcke T, Leinisch E, Straube A, Kampfe N, Draganski B, Diener HC, Bogdahn U, May A (2005) Gray matter decrease in patients with chronic tension type headache. Neurology 65:1483–1486

    Article  CAS  PubMed  Google Scholar 

  16. McDonald BC, Conroy SK, Smith DJ, West JD, Saykin AJ (2013) Frontal gray matter reduction after breast cancer chemotherapy and association with executive symptoms: a replication and extension study. Brain Behav Immun 30(Suppl):S117–S125

    Article  PubMed Central  PubMed  Google Scholar 

  17. Qiu YW, Jiang GH, Su HH, Lv XF, Tian JZ, Li LM, Zhuo FZ (2013) The impulsivity behavior is correlated with prefrontal cortex gray matter volume reduction in heroin-dependent individuals. Neurosci Lett 538:43–48

    Article  CAS  PubMed  Google Scholar 

  18. Schecklmann M, Lehner A, Poeppl TB, Kreuzer PM, Rupprecht R, Rackl J, Burger J, Frank E, Hajak G, Langguth B, Landgrebe M (2013) Auditory cortex is implicated in tinnitus distress: a voxel-based morphometry study. Brain Struct Funct 218:1061–1070

    Article  CAS  PubMed  Google Scholar 

  19. Obermann M, Rodriguez-Raecke R, Naegel S, Holle D, Mueller D, Yoon MS, Theysohn N, Blex S, Diener HC, Katsarava Z (2013) Gray matter volume reduction reflects chronic pain in trigeminal neuralgia. Neuroimage 74:352–358

    Article  PubMed  Google Scholar 

  20. Lai SZ, Li WF, Chen L, Luo W, Chen YY, Liu LZ, Sun Y, Lin AH, Liu MZ, Ma J (2011) How does intensity-modulated radiotherapy versus conventional two-dimensional radiotherapy influence the treatment results in nasopharyngeal carcinoma patients? Int J Radiat Oncol Biol Phys 80:661–668

    Article  PubMed  Google Scholar 

  21. American Joint Committee on Cancer (AJCC) (2002) Pharynx (including base of tongue, soft palate and uvula). In: Greene FL, Page DL, Fleming ID (eds) AJCC cancer staging manual, 6th edn. Springer, New York, pp 157–164

    Chapter  Google Scholar 

  22. Ashburner J (2007) A fast diffeomorphic image registration algorithm. Neuroimage 38:95–113

    Article  PubMed  Google Scholar 

  23. Radua J, Canales-Rodriguez EJ, Pomarol-Clotet E, Salvador R (2013) Validity of modulation and optimal settings for advanced voxel-based morphometry. Neuroimage 86:80–91

    Google Scholar 

  24. Niedtfeld II, Schulze L, Krause-Utz A, Demirakca T, Bohus M, Schmahl C (2013) Voxel-based morphometry in women with borderline personality disorder with and without comorbid posttraumatic stress disorder. PLoS One 8:e65824

    Article  PubMed Central  PubMed  Google Scholar 

  25. Liao Y, Tang J, Liu T, Chen X, Hao W (2012) Differences between smokers and non-smokers in regional gray matter volumes: a voxel-based morphometry study. Addict Biol 17:977–980

    Article  PubMed  Google Scholar 

  26. Apkarian AV, Krauss BR, Fredrickson BE, Szeverenyi NM (2001) Imaging the pain of low back pain: functional magnetic resonance imaging in combination with monitoring subjective pain perception allows the study of clinical pain states. Neurosci Lett 299:57–60

    Article  CAS  PubMed  Google Scholar 

  27. Soussain C, Ricard D, Fike JR, Mazeron JJ, Psimaras D, Delattre JY (2009) CNS complications of radiotherapy and chemotherapy. Lancet 374:1639–1651

    Article  CAS  PubMed  Google Scholar 

  28. Mizumatsu S, Monje ML, Morhardt DR, Rola R, Palmer TD, Fike JR (2003) Extreme sensitivity of adult neurogenesis to low doses of X-irradiation. Cancer Res 63:4021–4027

    CAS  PubMed  Google Scholar 

  29. Monje ML, Vogel H, Masek M, Ligon KL, Fisher PG, Palmer TD (2007) Impaired human hippocampal neurogenesis after treatment for central nervous system malignancies. Ann Neurol 62:515–520

    Article  PubMed  Google Scholar 

  30. Gazdzinski LM, Cormier K, Lu FG, Lerch JP, Wong CS, Nieman BJ (2012) Radiation-induced alterations in mouse brain development characterized by magnetic resonance imaging. Int J Radiat Oncol Biol Phys 84:e631–e638

    Article  PubMed  Google Scholar 

  31. Aldridge K, Wang L, Harms MP, Moffitt AJ, Cole KK, Csernansky JG, Selemon LD (2012) A longitudinal analysis of regional brain volumes in macaques exposed to X-irradiation in early gestation. PLoS One 7:e43109

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. Tofilon PJ, Fike JR (2000) The radioresponse of the central nervous system: a dynamic process. Radiat Res 153:357–370

    Article  CAS  PubMed  Google Scholar 

  33. Panagiotakos G, Alshamy G, Chan B, Abrams R, Greenberg E, Saxena A, Bradbury M, Edgar M, Gutin P, Tabar V (2007) Long-term impact of radiation on the stem cell and oligodendrocyte precursors in the brain. PLoS One 2:e588

    Article  PubMed Central  PubMed  Google Scholar 

  34. Polito A, Reynolds R (2005) NG2-expressing cells as oligodendrocyte progenitors in the normal and demyelinated adult central nervous system. J Anat 207:707–716

    Article  PubMed Central  PubMed  Google Scholar 

  35. Dimou L, Simon C, Kirchhoff F, Takebayashi H, Gotz M (2008) Progeny of Olig2-expressing progenitors in the gray and white matter of the adult mouse cerebral cortex. J Neurosci 28:10434–10442

    Article  CAS  PubMed  Google Scholar 

  36. Hua K, Schindler MK, McQuail JA, Forbes ME, Riddle DR (2012) Regionally distinct responses of microglia and glial progenitor cells to whole brain irradiation in adult and aging rats. PLoS One 7:e52728

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  37. McDonald BC, Conroy SK, Ahles TA, West JD, Saykin AJ (2010) Gray matter reduction associated with systemic chemotherapy for breast cancer: a prospective MRI study. Breast Cancer Res Treat 123:819–828

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  38. de Ruiter MB, Reneman L, Boogerd W, Veltman DJ, Caan M, Douaud G, Lavini C, Linn SC, Boven E, van Dam FS, Schagen SB (2012) Late effects of high-dose adjuvant chemotherapy on white and gray matter in breast cancer survivors: converging results from multimodal magnetic resonance imaging. Hum Brain Mapp 33:2971–2983

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the National Nature Science Foundation of China (no. 81071207, 81271622, and 81071890), the Training Programme Foundation for the Talents by Sun Yat-sen University Cancer Center, the Program for New Century Excellent Talents in University in China, the Program for New Century Excellent Talents in University (NCET-12-0562), the Sun Yat-Sen University Clinical Research 5010 Program (201310), the Guangdong Provincial Natural Science Foundation of China (no. S2013020012726), and Science and Technology Planning Project of Guangdong Province, China (no. 2011B061300090).

Conflict of interest

We declare that we have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Li Li.

Additional information

Xiao-Fei Lv, Xiao-Li Zheng, and Wei-Dong Zhang contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lv, XF., Zheng, XL., Zhang, WD. et al. Radiation-induced changes in normal-appearing gray matter in patients with nasopharyngeal carcinoma: a magnetic resonance imaging voxel-based morphometry study. Neuroradiology 56, 423–430 (2014). https://doi.org/10.1007/s00234-014-1338-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00234-014-1338-y

Keywords

Navigation