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DWI-based MR thermometry: could it discriminate Alzheimer’s disease from mild cognitive impairment and healthy subjects?

  • Diagnostic Neuroradiology
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Abstract

Purpose

The aim of this study is to compare lateral ventricular cerebrospinal fluid (CSF) temperature of the patients with Alzheimer’s disease (AD), mild cognitive impairment (MCI), and healthy subjects (HS) using diffusion-weighted imaging (DWI)-based magnetic resonance (MR) thermometry.

Methods

Seventy-two patients (37 AD, 19 MCI, 16 HS) who underwent 3-T MR examination from September 2018 to August 2019 were included in this study. Smoking habits, education level, disease duration, and comorbidity status were recorded. Patients were assessed using Mini-Mental State Examination (MMSE) and the Clinical Dementia Rating (CDR) score. Brain temperatures were measured using DWI-based MR thermometry. Group comparisons of brain temperature were performed using the Pearson chi-square, Mann–Whitney, and Kruskal–Wallis tests. Further analysis was performed using the post hoc Bonferroni test. Receiver operating characteristic (ROC) analysis was also used.

Results

A CDR score of 0.5, 1, and 2 was 2 (5.4%), 14 (37.8%), and 21 (56.8%) in AD, respectively. The median MMSE score had significant differences among groups and also in pairwise comparisons. The median CSF temperature (°C) values showed statistically significant difference among groups (HS: 38.5 °C, MCI: 38.17 °C, AD: 38.0 °C). The post hoc Mann–Whitney U test indicated a significant difference between AD patients and HS (p = 0.009). There were no significant CSF temperature differences in other pairwise comparisons.

Conclusion

Lower CSF temperatures were observed in AD patients than in HS, probably due to decreased brain metabolism in AD. DWI-based MR thermometry as a noninvasive imaging method enabling the measurement of CSF temperatures may contribute to the diagnosis of AD.

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References

  1. Buchman AS, Bennett DA (2011) Loss of motor function in preclinical Alzheimer’s disease. Expert Rev Neurother 11(5):665–676

    Article  PubMed  PubMed Central  Google Scholar 

  2. Masters C, Bateman R, Blennow K, Rowe C, Sperling R, Cummings J (2015) Alzheimer’s disease. Nat Rev Disease Primers 1:15056

    Article  PubMed  Google Scholar 

  3. Amieva H, Le Goff M, Millet X, Orgogozo JM, Pérès K, Barberger-Gateau P, Jacqmin-Gadda H, Dartigues JF (2008) Prodromal Alzheimer’s disease: successive emergence of the clinical symptoms. Ann Neurol: Off J Am Neurol Assoc Child Neurol Soc 64(5):492–498

    Article  Google Scholar 

  4. Black DW, Grant JE, DSM-5® guidebook: the essential companion to the diagnostic and statistical manual of mental disorders. Am Psychiatr Pub2014.

  5. Petersen RC, Smith GE, Waring SC, Ivnik RJ, Tangalos EG, Kokmen E (1999) Mild cognitive impairment: clinical characterization and outcome. Arch Neurol 56(3):303–308

    Article  CAS  PubMed  Google Scholar 

  6. Gauthier S, Reisberg B, Zaudig M, Petersen RC, Ritchie K, Broich K, Belleville S, Brodaty H, Bennett D, Chertkow H (2006) Mild cognitive impairment. Lancet 367(9518):1262–1270

    Article  PubMed  Google Scholar 

  7. Busse A, Hensel A, Gühne U, Angermeyer M, Riedel-Heller S (2006) Mild cognitive impairment: long-term course of four clinical subtypes. Neurology 67(12):2176–2185

    Article  CAS  PubMed  Google Scholar 

  8. Dickerson BC, Sperling RA (2005) Neuroimaging biomarkers for clinical trials of disease-modifying therapies in Alzheimer’s disease. NeuroRx 2(2):348–360

    Article  PubMed  PubMed Central  Google Scholar 

  9. Frisoni GB, Fox NC, Jack CR, Scheltens P, Thompson PM (2010) The clinical use of structural MRI in Alzheimer disease. Nat Rev Neurol 6(2):67–77

    Article  PubMed  PubMed Central  Google Scholar 

  10. Whitten TA, Martz LJ, Guico A, Gervais N, Dickson CT (2009) Heat synch: inter-and independence of body-temperature fluctuations and brain-state alternations in urethane-anesthetized rats. J Neurophysiol 102(3):1647–1656

    Article  PubMed  Google Scholar 

  11. Gerard R, Hill A, Zotterman Y (1927) The effect of frequency of stimulation on the heat production of nerve. J Physiol 63(2):130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Sakai K, Yamada K, Sugimoto N (2012) Calculation methods for ventricular diffusion-weighted imaging thermometry: phantom and volunteer studies. NMR Biomed 25(2):340–346

    Article  PubMed  Google Scholar 

  13. Salcman M, Moriyama E, Elsner HJ, Rossman H, Gettleman RA, Neuberth G, Corradino G (1989) Cerebral blood flow and the thermal properties of the brain: a preliminary analysis. J Neurosurg 70(4):592–598

    Article  CAS  PubMed  Google Scholar 

  14. Bracko O, Cruz Hernández JC, Park L, Nishimura N, Schaffer CB (2021) Causes and consequences of baseline cerebral blood flow reductions in Alzheimer’s disease. J Cereb Blood Flow Metab 41(7):1501–1516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Yin F, Sancheti H, Patil I, Cadenas E (2016) Energy metabolism and inflammation in brain aging and Alzheimer’s disease. Free Radical Biol Med 100:108–122

    Article  CAS  Google Scholar 

  16. Cunnane S, Nugent S, Roy M, Courchesne-Loyer A, Croteau E, Tremblay S, Castellano A, Pifferi F, Bocti C, Paquet N (2011) Brain fuel metabolism, aging, and Alzheimer’s disease. Nutrition 27(1):3–20

    Article  CAS  PubMed  Google Scholar 

  17. Blass JP, Sheu RKF, Gibson GE (2000) Inherent abnormalities in energy metabolism in Alzheimer disease: interaction with cerebrovascular compromise. Ann N Y Acad Sci 903(1):204–221

    Article  CAS  PubMed  Google Scholar 

  18. Kozak L, Bango M, Szabo M, Rudas G, Vidnyanszky Z, Nagy Z (2010) Using diffusion MRI for measuring the temperature of cerebrospinal fluid within the lateral ventricles. Acta Paediatr 99(2):237–243

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Yamada K, Sakai K, Akazawa K, Yuen S, Sugimoto N, Sasajima H, Mineura K, Nishimura T (2010) Moyamoya patients exhibit higher brain temperatures than normal controls. NeuroReport 21(13):851–855

    Article  PubMed  Google Scholar 

  20. Sakai K, Yamada K, Mori S, Sugimoto N, Nishimura T (2011) Age-dependent brain temperature decline assessed by diffusion-weighted imaging thermometry. NMR Biomed 24(9):1063–1067

    Article  PubMed  Google Scholar 

  21. Sparacia G, Sakai K (2021) Temperature measurement by diffusion-weighted imaging. Magn Reson Imaging Clin N Am 29(2):253–261

    Article  PubMed  Google Scholar 

  22. Le Bihan D, Breton E, Lallemand D, Grenier P, Cabanis E, Laval-Jeantet M (1986) MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 161(2):401–407

    Article  PubMed  Google Scholar 

  23. Einstein A (1956) Investigations on the theory of the Brownian movement. Courier Corporation

  24. Sakai K, Yamada K, Sugimoto N (2013) Automated temperature calculation method for DWI-thermometry: volunteer study. Medical Imaging 2013: Image Process IntSoc Optics Photon 866922

  25. Nagy Z, Kozak L, Bango M, Szabo M, Gabor R, Vidnyanszki Z (2009) Measuring the cerebrospinal fluid temperature using diffusion MRI. Proc Int Soc Mag Reson Med 2700

  26. Le Bihan D, Delannoy J, Levin RL (1989) Temperature mapping with MR imaging of molecular diffusion: application to hyperthermia. Radiology 171(3):853–857

    Article  PubMed  Google Scholar 

  27. Sakai K, Nakai R (2013) Temperature controllable phantom for reliable MR-thermometry: construction of flow water system and initial consideration. Trans Japan Soc Med Biol Eng 51(Supplement) R-95-R-95

  28. II′ yasov KA, Prof JH (1998) Single‐shot diffusion‐weighted RARE sequence: application for temperature monitoring during hyperthermia session. J MagnReson Imaging 8(6) 1296-1305

  29. Morvan D, Leroy-Willig A, Malgouyres A, Cuenod CA, Jehenson P, Syrota A (1993) Simultaneous temperature and regional blood volume measurements in human muscle using an MRI fast diffusion technique. Magn Reson Med 29(3):371–377

    Article  CAS  PubMed  Google Scholar 

  30. Tofts PS, Jackson JS, Tozer DJ, Cercignani M, Keir G, MacManus DG, Ridgway GR, Ridha BH, Schmierer K, Siddique D (2008) Imaging cadavers: cold FLAIR and noninvasive brain thermometry using CSF diffusion. Magn Reson Med: An Off J Int Soc Magn Reson Med 59(1):190–195

    Article  Google Scholar 

  31. Rieke V, (2011) MR thermometry. Interv Magn Reson Imaging 271–288.

  32. Quesson B, de Zwart JA, Moonen CT (2000) Magnetic resonance temperature imaging for guidance of thermotherapy. J Magn Reson Imaging: An Off J Int Soc Magn Reson Med 12(4):525–533

    Article  CAS  Google Scholar 

  33. Odéen H, Parker DL (2019) Magnetic resonance thermometry and its biological applications – physical principles and practical considerations. Prog Nucl Magn Reson Spectrosc 110:34–61

    Article  PubMed  PubMed Central  Google Scholar 

  34. A.P. Association, Diagnostic and statistical manual of mental disorders (DSM-5®), American Psychiatric Pub 2013.

  35. Morris JC (1997) Clinical dementia rating: a reliable and valid diagnostic and staging measure for dementia of the Alzheimer type. Int Psychogeriatr 9(S1):173–176

    Article  PubMed  Google Scholar 

  36. Mitchell AJ (2009) A meta-analysis of the accuracy of the mini-mental state examination in the detection of dementia and mild cognitive impairment. J Psychiatr Res 43(4):411–431

    Article  PubMed  Google Scholar 

  37. Güngen C, Ertan T, Eker E, Yaşar R, Engin F (2002) Standardize mini mental test’in Türk toplumunda hafif demans tan› s› nda geçerlik ve güvenilirliği. Turk Psikiyatri Derg 13(4):273–281

    PubMed  Google Scholar 

  38. Yildiz GB, Özçelik EU, Kolukisa M, IŞIK AT, Gürsoy E, Kocaman G, Celebi A (2016) Validity and reliability studies of modified mini mental state examination (MMSE-I) for Turkish illiterate patients with diagnosis of alzheimer disease. Turkish J Psychiatry 27(1):41–46

    Google Scholar 

  39. Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”: a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12(3):189–198

    Article  CAS  PubMed  Google Scholar 

  40. Mills R (1973) Self-diffusion in normal and heavy water in the range 1–45. deg. J Phys Chem 77(5):685–688

    Article  CAS  Google Scholar 

  41. Cummings JL, Cole G (2002) Alzheimer disease. JAMA 287(18):2335–2338

    Article  CAS  PubMed  Google Scholar 

  42. Scheltens P, Blennow K, Breteler M, de Strooper B, Frisoni G, Salloway S, Van der Flier W (2016) Alzheim Dis Lancet (Lond Engl) 388:505–517

    Article  CAS  Google Scholar 

  43. Rossini PM, DiIorio R, Vecchio F, Anfossi M, Babiloni C, Bozzali M, Bruni AC, Cappa SF, Escudero J, Fraga FJ (2020) Early diagnosis of Alzheimer’s disease: the role of biomarkers including advanced EEG signal analysis. Report from the IFCN-sponsored panel of experts. Clin Neurophysiol 131(6):1287–1310

    Article  CAS  PubMed  Google Scholar 

  44. Vandal M, White PJ, Tournissac M, Tremblay C, St-Amour I, Drouin-Ouellet J, Bousquet M, Traversy M-T, Planel E, Marette A (2016) Impaired thermoregulation and beneficial effects of thermoneutrality in the 3× Tg-AD model of Alzheimer’s disease. Neurobiol Aging 43:47–57

    Article  CAS  PubMed  Google Scholar 

  45. Del Sole A, Clerici F, Chiti A, Lecchi M, Mariani C, Maggiore L, Mosconi L, Lucignani G (2008) Individual cerebral metabolic deficits in Alzheimer’s disease and amnestic mild cognitive impairment: an FDG PET study. Eur J Nucl Med Mol Imaging 35(7):1357–1366

    Article  PubMed  Google Scholar 

  46. Fouquet M, Desgranges B, Landeau B, Duchesnay E, Mézenge F, de La Sayette V, Viader F, Baron J-C, Eustache F, Chételat G (2009) Longitudinal brain metabolic changes from amnestic mild cognitive impairment to Alzheimer’s disease. Brain 132(8):2058–2067. https://doi.org/10.1093/brain/awp132

  47. Dai W, Lopez OL, Carmichael OT, Becker JT, Kuller LH, Gach HM (2009) Mild cognitive impairment and alzheimer disease: patterns of altered cerebral blood flow at MR imaging. Radiology 250(3):856–866

    Article  PubMed  PubMed Central  Google Scholar 

  48. Sparacia G, Sakai K, Yamada K, Giordano G, Coppola R, Midiri M, Grimaldi LM (2017) Assessment of brain core temperature using MR DWI-thermometry in Alzheimer disease patients compared to healthy subjects. Jpn J Radiol 35(4):168–171

    Article  PubMed  Google Scholar 

  49. Sumida K, Sato N, Ota M, Sakai K, Nippashi Y, Sone D, Yokoyama K, Ito K, Maikusa N, Imabayashi E (2015) Intraventricular cerebrospinal fluid temperature analysis using MR diffusion-weighted imaging thermometry in Parkinson’s disease patients, multiple system atrophy patients, and healthy subjects. Brain Behav 5(6):e00340

    Article  PubMed  PubMed Central  Google Scholar 

  50. Chen H-L, Yamada K, Sakai K, Lu C-H, Chen M-H, Lin W-C (2020) Alteration of brain temperature and systemic inflammation in Parkinson’s disease. Neurol Sci 41(5):1267–1276

    Article  PubMed  PubMed Central  Google Scholar 

  51. Sai A, Shimono T, Sakai K, Takeda A, Shimada H, Tsukamoto T, Maeda H, Sakamoto S, Miki Y (2014) Diffusion-weighted imaging thermometry in multiple sclerosis. J Magn Reson Imaging 40(3):649–654

    Article  PubMed  Google Scholar 

  52. Ota M, Sato N, Sakai K, Okazaki M, Maikusa N, Hattori K, Hori H, Teraishi T, Shimoji K, Yamada K (2014) Altered coupling of regional cerebral blood flow and brain temperature in schizophrenia compared with bipolar disorder and healthy subjects. J Cereb Blood Flow Metab 34(12):1868–1872

    Article  PubMed  PubMed Central  Google Scholar 

  53. Powers WJ, Videen TO, Markham J, Black KJ, Golchin N, Perlmutter JS (2008) Cerebral mitochondrial metabolism in early Parkinson’s disease. J Cereb Blood Flow Metab 28(10):1754–1760

    Article  CAS  PubMed  Google Scholar 

  54. Herholz K, Westwood S, Haense C, Dunn G (2011) Evaluation of a calibrated 18F-FDG PET score as a biomarker for progression in Alzheimer disease and mild cognitive impairment. J Nucl Med 52(8):1218–1226

    Article  PubMed  Google Scholar 

  55. Chen Y, Wolk D, Reddin J, Korczykowski M, Martinez P, Musiek E, Newberg A, Julin P, Arnold S, Greenberg J (2011) Voxel-level comparison of arterial spin-labeled perfusion MRI and FDG-PET in Alzheimer disease. Neurology 77(22):1977–1985

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Zhu M, Ackerman JJ, Sukstanskii AL, Yablonskiy DA (2006) How the body controls brain temperature: the temperature shielding effect of cerebral blood flow. J Appl Physiol 101(5):1481–1488

    Article  PubMed  Google Scholar 

  57. Zhu M, Ackerman JJ, Yablonskiy DA (2009) Body and brain temperature coupling: the critical role of cerebral blood flow. J Comp Physiol B 179(6):701–710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Kety SS, Schmidt CF (1948) The nitrous oxide method for the quantitative determination of cerebral blood flow in man: theory, procedure and normal values. J Clin Investig 27(4):476–483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Kety SS (1956) Human cerebral blood flow and oxygen consumption as related to aging. J Chronic Dis 3(5):478–486

    Article  CAS  PubMed  Google Scholar 

  60. Lebrun-Grandié P, Baron J-C, Soussaline F, Loch’h C, Sastre J, Bousser M-G (1983) Coupling between regional blood flow and oxygen utilization in the normal human brain: a study with positron tomography and oxygen 15. Arch Neurol 40(4):230–236

    Article  PubMed  Google Scholar 

  61. Hasan KM, Moeller FG, Narayana PA (2014) DTI-based segmentation and quantification of human brain lateral ventricular CSF volumetry and mean diffusivity: validation, age, gender effects and biophysical implications. Magn Reson Imaging 32(5):405–412

    Article  PubMed  PubMed Central  Google Scholar 

  62. Kuriyama N, Yamada K, Sakai K, Tokuda T, Akazawa K, Tomii Y, Tamura A, Kondo M, Watanabe I, Ozaki E (2015) Ventricular temperatures in idiopathic normal pressure hydrocephalus (iNPH) measured with DWI-based MR thermometry. Magn Reson Med Sci 2014–0076

  63. Tazoe J, Yamada K, Sakai K, Akazawa K (2012) Brain core temperature of mild head trauma patients as assessed by DWI. Proc Int Soc Magn Reson Med (ISMRM)

  64. Sakai K, Sakamoto R, Okada T, Sugimoto N, Togashi K (2012) DWI based thermometry: the effects of b-values, resolutions, signal-to-noise ratio, and magnet strength. Ann Int Conf IEEE Eng Med Biol Soc IEEE 2012:2291–2293

    Google Scholar 

  65. Reitz C, Brayne C, Mayeux R (2011) Epidemiology of Alzheimer disease. Nat Rev Neurol 7(3):137–152

    Article  PubMed  PubMed Central  Google Scholar 

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The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

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Authors and Affiliations

  1. Department of Radiology, Faculty of Medicine, School of Medicine, Gazi University, 06500, Besevler, Ankara, Turkey

    Berrak Barutcu Asfuroğlu, Nesrin Erdoğan Kaydu, Ali Yusuf Öner & E. Turgut Tali

  2. Department of Neurology, Faculty of Medicine, School of Medicine, Gazi University, Ankara, Turkey

    Tuğberk Andaç Topkan & Yahya Karaman

  3. Department of Radiology, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Kyoto, Japan

    Koji Sakai & Kei Yamada

  4. Department of Radiology, School of Medicine, Lokman Hekim University, Ankara, Turkey

    E. Turgut Tali

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  1. Berrak Barutcu Asfuroğlu
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  2. Tuğberk Andaç Topkan
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  3. Nesrin Erdoğan Kaydu
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  4. Koji Sakai
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Contributions

Berrak Barutcu Asfuroğlu and E. Turgut Tali contributed to the study conception and design. Material preparation and data collection and analysis were performed by all authors. The first draft of the manuscript was written by Berrak Barutcu Asfuroğlu, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Berrak Barutcu Asfuroğlu.

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Ethics approval

All procedures performed in this study involving human participants were in accordance with the ethical standards of the national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. Local ethics committee approved this study in 10.09.2018 with 591 decision number.

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Asfuroğlu, B.B., Topkan, T.A., Kaydu, N.E. et al. DWI-based MR thermometry: could it discriminate Alzheimer’s disease from mild cognitive impairment and healthy subjects?. Neuroradiology 64, 1979–1987 (2022). https://doi.org/10.1007/s00234-022-02969-y

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