• 1. Gujar SK, Maheshwari S, Björkman-Burtscher I, et al. Magnetic resonance spectroscopy. J Neuroophthalmol 2005; 25: 217226.

  • 2. Byrd SE, Tomita T, Palka PS, et al. Magnetic resonance spectroscopy (MRS) in the evaluation of pediatric brain tumors, part I: introduction to MRS. J Natl Med Assoc 1996; 88: 649654.

    • Search Google Scholar
    • Export Citation
  • 3. Barker PB, Bizzi A, De Stefano N, et al. Introduction to MR spectroscopy in vivo. In: Barker PB, Bizzi A, De Stefano N, et al. Clinical MR spectroscopy: techniques and applications. New York: Cambridge University Press, 2010;118.

    • Search Google Scholar
    • Export Citation
  • 4. Soares DP, Law M. Magnetic resonance spectroscopy of the brain: review of metabolites and clinical applications. Clin Radiol 2009; 64: 1221.

    • Search Google Scholar
    • Export Citation
  • 5. Rudkin TM, Arnold DL. Proton magnetic resonance spectroscopy for the diagnosis and management of cerebral disorders. Arch Neurol 1999; 56: 919926.

    • Search Google Scholar
    • Export Citation
  • 6. Bonavita S, Di Salle F, Tedeschi G. Proton MRS in neurological disorders. Eur J Radiol 1999; 30: 125131.

  • 7. Urenjak J, Williams SR, Gadian DG, et al. Proton nuclear magnetic resonance spectroscopy unambiguously identifies different neural cell types. J Neurosci 1993; 13: 981989.

    • Search Google Scholar
    • Export Citation
  • 8. Chernov MF, Kasuya H, Nakaya K, et al. 1H-MRS of intracranial meningiomas: what it can add to known clinical and MRI predictors of the histopathological and biological characteristics of the tumor? Clin Neurol Neurosurg 2011; 113: 202212.

    • Search Google Scholar
    • Export Citation
  • 9. Lai PH, Li KT, Hsu SS, et al. Pyogenic brain abscess: findings from in vivo 1.5-T and 11.7-T in vitro proton MR spectroscopy. AJNR Am J Neuroradiol 2005; 26: 279288.

    • Search Google Scholar
    • Export Citation
  • 10. Lai PH, Hsu SS, Ding SW, et al. Proton magnetic resonance spectroscopy and diffusion-weighted imaging in intracranial cystic mass lesions. Surg Neurol 2007; 68: S25S36.

    • Search Google Scholar
    • Export Citation
  • 11. Yue Q, Isobe T, Shibata Y, et al. New observations concerning the interpretation of magnetic resonance spectroscopy of meningioma. Eur Radiol 2008; 18: 29012911.

    • Search Google Scholar
    • Export Citation
  • 12. MacKay S, Meyerhoff DJ, Constans JM, et al. Regional gray and white matter metabolite differences in subjects with AD, with subcortical ischemic vascular dementia, and elderly controls with 1H magnetic resonance spectroscopic imaging. Arch Neurol 1996; 53: 167174.

    • Search Google Scholar
    • Export Citation
  • 13. Broom KA, Anthony DC, Lowe JP, et al. MRI and MRS alterations in the preclinical phase of murine prion disease: association with neuropathological and behavioural changes. Neurobiol Dis 2007; 26: 707717.

    • Search Google Scholar
    • Export Citation
  • 14. Chernov MF, Nakaya K, Kasuya H, et al. Metabolic alterations in the peritumoral brain in cases of meningiomas: 1H-MRS study. J Neurol Sci 2009; 284: 168174.

    • Search Google Scholar
    • Export Citation
  • 15. Kadota T, Horinouchi T, Kuroda C. Development and aging of the cerebrum: assessment with proton MR spectroscopy. AJNR Am J Neuroradiol 2001; 22: 128135.

    • Search Google Scholar
    • Export Citation
  • 16. Angelie E, Bonmartin A, Boudraa A, et al. Regional differences and metabolic changes in normal aging of the human brain: proton MR spectroscopic imaging study. AJNR Am J Neuroradiol 2001; 22: 119127.

    • Search Google Scholar
    • Export Citation
  • 17. Baker EH, Basso G, Barker PB, et al. Regional apparent metabolite concentrations in young adult brain measured by 1H MR spectroscopy at 3 Tesla. J Magn Reson Imaging 2008; 27: 489499.

    • Search Google Scholar
    • Export Citation
  • 18. Degaonkar MN, Pomper MG, Barker PB. Quantitative proton magnetic resonance spectroscopic imaging: regional variations in the corpus callosum and cortical gray matter. J Magn Reson Imaging 2005; 22: 175179.

    • Search Google Scholar
    • Export Citation
  • 19. Michaelis T, Merboldt KD, Bruhn H, et al. Absolute concentrations of metabolites in the adult human brain in vivo: quantification of localized proton MR spectra. Radiology 1993; 187: 219227.

    • Search Google Scholar
    • Export Citation
  • 20. Raininko R, Mattsson P. Metabolite concentrations in supraventricular white matter from teenage to early old age: a short echo time 1H magnetic resonance spectroscopy (MRS) study. Acta Radiol 2010; 51: 309315.

    • Search Google Scholar
    • Export Citation
  • 21. Barker PB, Breiter SN, Soher BJ, et al. Quantitative proton spectroscopy of canine brain: in vivo and in vitro correlations. Magn Reson Med 1994; 32: 157163.

    • Search Google Scholar
    • Export Citation
  • 22. Barker PB, Blackband SJ, Chatham JC, et al. Quantitative proton spectroscopy and histology of a canine brain tumor model. Magn Reson Med 1993; 30: 458464.

    • Search Google Scholar
    • Export Citation
  • 23. Martin-Vaquero P, da Costa RC, Echandi RL, et al. Magnetic resonance spectroscopy of the canine brain at 3.0 T and 7.0 T. Res Vet Sci 2012; 93: 427429.

    • Search Google Scholar
    • Export Citation
  • 24. Stiles J, Jernigan TL. The basics of brain development. Neuropsychol Rev 2010; 20: 327348.

  • 25. Gross B, Garcia-Tapia D, Riedesel E, et al. Normal canine brain maturation at magnetic resonance imaging 2010; 51: 361373

  • 26. Insua D, Suárez ML, Santamarina G, et al. Dogs with canine counterpart of Alzheimer's disease lose noradrenergic neurons. Neurobiol Aging 2010; 31: 625635.

    • Search Google Scholar
    • Export Citation
  • 27. Mouton PR, Pakkenberg B, Gundersen HJ, et al. Absolute number and size of pigmented locus coeruleus neurons in young and aged individuals. J Chem Neuroanat 1994; 7: 185190.

    • Search Google Scholar
    • Export Citation
  • 28. Shimada A, Kuwamura M, Awakura T, et al. An immunohistochemical and ultrastructural study on age-related astrocytic gliosis in the central nervous system of dogs. J Vet Med Sci 1992; 54: 2936.

    • Search Google Scholar
    • Export Citation
  • 29. Nichols NR. Glial responses to steroids as markers of brain aging. J Neurobiol 1999; 40: 585601.

  • 30. Chambers JK, Uchida K, Nakayama H. White matter myelin loss in the brains of aged dogs. Exp Gerontol 2012; 47: 263269.

  • 31. Pannese E. Morphological changes in nerve cells during normal aging. Brain Struct Funct 2011; 216: 8589.

  • 32. Westman E, Wahlund LO, Foy C, et al. Magnetic resonance imaging and magnetic resonance spectroscopy for detection of early Alzheimer's disease. J Alzheimers Dis 2011; 26: 307319.

    • Search Google Scholar
    • Export Citation
  • 33. Mayer D, Zahr NM, Sullivan EV, et al. In vivo metabolite differences between the basal ganglia and cerebellum of the rat brain detected with proton MRS at 3T. Psychiatry Res 2007; 154: 267273.

    • Search Google Scholar
    • Export Citation
  • 34. Zahr NM, Mayer D, Rohlfing T, et al. In vivo glutamate measured with magnetic resonance spectroscopy: behavioral correlates in aging. Neurobiol Aging 2013; 34: 12651276.

    • Search Google Scholar
    • Export Citation
  • 35. Gruber S, Pinker K, Riederer F, et al. Metabolic changes in the normal ageing brain: consistent findings from short and long echo time proton spectroscopy. Eur J Radiol 2008; 68: 320327.

    • Search Google Scholar
    • Export Citation
  • 36. Lee SH, Kim SY, Woo DC, et al. Differential neurochemical responses of the canine striatum with pentobarbital or ketamine anesthesia: a 3T proton MRS study. J Vet Med Sci 2010; 72: 583587.

    • Search Google Scholar
    • Export Citation
  • 37. Makaryus R, Lee H, Yu M, et al. The metabolomic profile during isoflurane anesthesia differs from propofol anesthesia in the live rodent brain. J Cereb Blood Flow Metab 2011; 31: 14321442.

    • Search Google Scholar
    • Export Citation
  • 38. Zhang H, Wang W, Gao W, et al. Effect of propofol on the levels of neurotransmitters in normal human brain: a magnetic resonance spectroscopy study. Neurosci Lett 2009; 467: 247251.

    • Search Google Scholar
    • Export Citation
  • 39. Stoop MP, Coulier L, Rosenling T, et al. Quantitative proteomics and metabolomics analysis of normal human cerebrospinal fluid samples. Mol Cell Proteomics 2010; 9: 20632075.

    • Search Google Scholar
    • Export Citation
  • 40. Nagae-Poetscher LM, McMahon M, Braverman N, et al. Metabolites in ventricular cerebrospinal fluid detected by proton magnetic resonance spectroscopic imaging. J Magn Reson Imaging 2004; 20: 496500.

    • Search Google Scholar
    • Export Citation
  • 41. McPhail MJ, Taylor-Robinson SD. The role of magnetic resonance imaging and spectroscopy in hepatic encephalopathy. Metab Brain Dis 2010; 25: 6572.

    • Search Google Scholar
    • Export Citation
  • 42. Rothuizen J. Important clinical syndromes associated with liver disease. Vet Clin North Am Small Anim Pract 2009; 39: 419437.

  • 43. Grover VP, Dresner MA, Forton DM, et al. Current and future applications of magnetic resonance imaging and spectroscopy of the brain in hepatic encephalopathy. World J Gastroenterol 2006; 12: 29692978.

    • Search Google Scholar
    • Export Citation
  • 44. Costa MO, Lacerda MT, Garcia Otaduy MC, et al. Proton magnetic resonance spectroscopy: normal findings in the cerebellar hemisphere in childhood. Pediatr Radiol 2002; 32: 787792.

    • Search Google Scholar
    • Export Citation
  • 45. Majós C, Julià-Sapé M, Alonso J, et al. Brain tumor classification by proton MR spectroscopy: comparison of diagnostic accuracy at short and long TE. AJNR Am J Neuroradiol 2004; 25: 16961704.

    • Search Google Scholar
    • Export Citation

Advertisement

Regional variations and age-related changes detected with magnetic resonance spectroscopy in the brain of healthy dogs

Kaori Ono DVM1, Masato Kitagawa DVM, PhD2, Daisuke Ito DVM, PhD3, Natsumi Tanaka DVM4,5, and Toshihiro Watari DVM, PhD6
View More View Less
  • 1 Laboratory of Comprehensive Veterinary Clinical Studies, College of Bioresource Sciences, Nihon University, 1866 Kameino, Fujisawa, Kanagawa 252-0880, Japan.
  • | 2 Laboratory of Comprehensive Veterinary Clinical Studies, College of Bioresource Sciences, Nihon University, 1866 Kameino, Fujisawa, Kanagawa 252-0880, Japan.
  • | 3 Laboratory of Comprehensive Veterinary Clinical Studies, College of Bioresource Sciences, Nihon University, 1866 Kameino, Fujisawa, Kanagawa 252-0880, Japan.
  • | 4 Laboratory of Comprehensive Veterinary Clinical Studies, College of Bioresource Sciences, Nihon University, 1866 Kameino, Fujisawa, Kanagawa 252-0880, Japan.
  • | 5 Grace Animal Hospital, 5-4-9 Ogikubo, Suginami, Tokyo 167-0051, Japan
  • | 6 Laboratory of Comprehensive Veterinary Clinical Studies, College of Bioresource Sciences, Nihon University, 1866 Kameino, Fujisawa, Kanagawa 252-0880, Japan.

Abstract

Objective—To investigate age-related and regional differences in estimated metabolite concentrations in the brain of healthy dogs by means of magnetic resonance spectroscopy (MRS).

Animals—15 healthy Beagles.

Procedures—Dogs were grouped according to age as young (n = 5; all dogs were 2 months old), adult (5; mean age, 4.5 years), or geriatric (5; all dogs were 12 years old). Imaging was performed by use of a 1.5-T MRI system with T1- and T2-weighted spin-echo and fluid-attenuated inversion recovery sequences. Signal intensity measurements for N-acetyl aspartate, creatine, choline, and lactate-alanine (the spectroscopic peaks associated with alanine and lactate could not be reliably differentiated) were determined with MRS, and areas under the spectroscopic peaks (representing concentration estimates) were calculated. Ratios of these metabolite values were compared among age groups and among brain regions with regression analysis.

Results—The choline-to-creatine ratio was significantly higher in young dogs, compared with other age groups. The N-acetyl aspartate-to-choline ratio was significantly lower in young dogs and geriatric dogs than in adult dogs. When all age groups were considered, the choline-to-creatine ratio was significantly higher and N-acetyl aspartate-to-choline ratio was significantly lower in the frontal lobe than in all other regions. The N-acetyl aspartate-to-creatine ratio was significantly lower in the cerebellum than in other regions.

Conclusions and Clinical Relevance—Metabolite ratios varied significantly among age groups and brain regions in healthy dogs. Future studies should evaluate absolute concentration differences in a larger number of dogs and assess clinical applications in dogs with neurologic diseases.

Contributor Notes

Address correspondence to Dr. Kitagawa (kitagawa@brs.nihon-u.ac.jp).