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Comparative Clinical Pathology

, Volume 28, Issue 4, pp 1137–1142 | Cite as

Aging of bovine spinal cord: an alteration of myelinated nerve fibers in the white matter

  • S. OhfujiEmail author
Original Article
  • 9 Downloads

Abstract

To gain more knowledge of age-related changes in the spinal cord of the bovine species, the structure of 15 clinically normal aged cattle (Holstein-Friesian cows 8–13 years of age) was histopathologically examined. In 12 (80%) of the 15 animals, the common histopathological features identified were alteration of a small number of myelinated nerve fibers in the white matter, with less than 4 nerve fibers affected per cross-sectional area of the spinal cord. Alteration of nerve fibers was characterized by dilation of myelin sheaths with loss of axons or macrophage infiltration, resembling features of Wallerian axonal degeneration. The occurrence of this nerve fiber alteration had a predilection for the lateral and ventral white matter funiculi. In eight cattle, so-called axonal spheroids were rarely present in the white matter. There was little evidence of glial reaction against nerve fiber alteration. Gray horn neurons were unremarkable. Lipofuscin granules were recognized in neurons, glial cells, and neuropil of the medulla oblongata examined in six cows. The changes observed in the spinal cord white matter of the present cows were similar to those described previously in aged human beings and domestic and laboratory animals, and thus were likely to have been a phenomenon which was closely related to aging. The strict clinical significance of the histopathological changes in the spinal cord white matter remains undetermined.

Keywords

Aging Bovine Myelinated nerve fiber alteration Spinal cord 

Notes

Compliance with ethical standards

Conflict of interest

The author declares that he has no competing interests.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

References

  1. Adalbert R, Coleman MP (2013) Review: axon pathology in age-related neurodegenerative disorders. Neuropathol Appl Neurobiol 39:90–108CrossRefGoogle Scholar
  2. Biasibetti E, Bisanzio D, Mioletti S, Amedeo S, Iuliano A, Bianco P, Capucchio MT (2016) Spontaneous age-related changes of peripheral nerves in cattle: morphological and biochemical studies. Anat Histol Embrol 45:100–108CrossRefGoogle Scholar
  3. Borras D, Ferrer I, Pumarola M (1999) Age-related changes in the brain of the dog. Vet Pathol 36:202–211CrossRefGoogle Scholar
  4. Buchman AS, Leurgans SE, VanderHorst VGJM et al (2018) Spinal motor neurons and motor function in older adults. J Neurol 266:174–182.  https://doi.org/10.1007/s00415-018-9118-y CrossRefGoogle Scholar
  5. Cummings BJ, Head E, Afagh AJ, Milgram NW, Cotman CW (1996a) β-amyloid accumulation correlates with cognitive dysfunction in the aged canine. Neurobiol Learn Mem 66:11–23CrossRefGoogle Scholar
  6. Cummings BJ, Satou T, Head E et al (1996b) Diffuse plaques contain C-terminal Aβ42 and not Aβ40: evidence from cats and dogs. Neurobiol Aging 14:653–659Google Scholar
  7. Double KL, Dedov VN, Fedorow H, Kettle E, Halliday GM, Garner B, Brunk UT (2008) The comparative biology of neuromelanin and lipofuscin in the human brain. Cell & Mol Life Sci 65:1669–1682CrossRefGoogle Scholar
  8. Ferrer I, Pumarola M, Rivera R, Zújar MJ, Cruz-Sánchez F, Vidal A (1993) Primary central white matter degeneration in old dogs. Acta Neuropathol 86:172–175CrossRefGoogle Scholar
  9. Fujisawa K (1967) A unique type of axonal alteration (so-called axonal dystrophy) as seen in Goll’s nucleus of 277 cases of controls. Acta Neuropathol 8:255–275CrossRefGoogle Scholar
  10. Gavier-Widen D, Wells GAH, Simmons MM, Wilesmith JWW, Ryan J (2001) Histological observations on the brains of symptomless 7-year-old cattle. J Comp Pathol 124:52–59CrossRefGoogle Scholar
  11. Geertsen SS, Willerslev-Olsen M, Lorentzen J, Nielsen JB (2017) Development and aging of human spinal cord circuitries. J Neurophysiol 118:1133–1140CrossRefGoogle Scholar
  12. Goyal VL (1982) Lipofuscin pigment accumulation in human brain during aging. Exp Gerontol 17:481–487CrossRefGoogle Scholar
  13. Hanshaw DM, Finnie JW, Manavis J, Kessell AE (2015) Axonal spheroid accumulation in the brainstem and spinal cord of a young Angus cow with ataxia. Aust Vet J 93:283–286CrossRefGoogle Scholar
  14. Hubbard BM, Andersson JM (1985) Age-related variations in the neuron content of the cerebral cortex in senile dementia of Alzheimer type. Neuropathol Appl Neurobiol 11:369–382CrossRefGoogle Scholar
  15. Ishihara T, Gondo T, Takahashi M, Uchino F, Ikeda SI, Allsop D, Imai K (1991) Immunohistochemical and immunoelectron microscopical characterization of cereberovascular and senile plaque amyloid in aged dogs’ brains. Brain Res 548:196–205CrossRefGoogle Scholar
  16. Itabashi HH, Andrews JM, Tomiyasu U, Erlich SS, Sathyavagiswaran L (2007) Forensic neuropathology. Academic Press, San DiegoGoogle Scholar
  17. Jahns H, Callanan J, McElroy MC et al (2006) Age-related and non-age-related changes in 100 surveyed horse brains. Vet Pathol 43:740–750CrossRefGoogle Scholar
  18. Jeffrey M (1992) A neuropathological survey of brains submitted under the bovine spongiform encephalopathy orders in Scotland. Vet Rec 131:332–337CrossRefGoogle Scholar
  19. Jolly RD, Douglas BV, Davey PM et al (1995) Lipofuscin in bovine muscle and brain: a model for studying age pigment. Gerontol 41(Suppl 2):183–195Google Scholar
  20. Jubb KVF, Huxtable CR (1993) The nervous system. In: Jubb KVF, Kennedy PC, Palmer N (eds) Pathology of domestic animals, vol 1, 4th edn. Academic Press, San Diego, pp 267–439CrossRefGoogle Scholar
  21. Jyothi HJ, Vidyadhara DJ, Mahadevan A, Philip M, Parmar SK, Manohari SG, Shankar SK, Raju TR, Alladi PA (2015) Aging causes morphological alterations in astrocytes and microglia in human substantia nigra pars compacta. Neurobiol Aging 36:3321–3333CrossRefGoogle Scholar
  22. Kessell AE, Finnie JW, Blumbergs PC et al (2012) Neuroaxonal dystrophy in Australian merino lambs. J Comp Pathol 142:62–72CrossRefGoogle Scholar
  23. Konno T, Yoshida K, Mizuno T, Kawarai T, Tada M, Nozaki H, Ikeda SI, Nishizawa M, Onodera O, Wszolek ZK, Ikeuchi T (2017) Clinical and genetic characterization of adult-onset leukoencephalopathy with axonal spheroids and pigmented glia associated with CSF1R mutation. Eur J Neurol 24:37–45CrossRefGoogle Scholar
  24. de Lahunta A (1983) Veterinary neuroanatomy and clinical neurology, 2nd edn. W. B. Saunders, PhiladelphiaGoogle Scholar
  25. Lexell J (1997) Evidence for nervous system degeneration with advancing age. J Nutr 127:1011S–1013SCrossRefGoogle Scholar
  26. Liu H, Yang Y, Xia Y, Zhu W, Leak RK, Wei Z, Wang J, Hu X (2017) Aging of cerebral white matter. Ageing Res Rev 34:64–76CrossRefGoogle Scholar
  27. Lowe J, Mirra SS, Hyman BT et al (2008) Ageing and dementia. In: Love S, Louis DN, Ellison DW (eds) Greenfield’s neuropathology, 8th edn. Tayler & Francis, Boca Raton, pp 1031–1152Google Scholar
  28. Mani RB, Lohr JB, Jeste DV (1986) Hippocampal pyramidal cells and aging in the human: a quantitative study of neuronal loss in sectors CA1 to CA4. Exp Neurol 94:29–40CrossRefGoogle Scholar
  29. Mann DM, Yates PO, Stamp JE (1978) The relationship between lipofuscin pigment and ageing in the human nervous system. J Neurol Sci 37(1–2):83–93CrossRefGoogle Scholar
  30. Marner L, Nyengaard JR, Tang Y, Pakkenberg B (2003) Marked loss of myelinated nerve fibers in the human brain with age. J Comp Neurol 462:144–152CrossRefGoogle Scholar
  31. Mufson EJ, Stein DG (1980) Degeneration in the spinal cord of old rats. Exp Neurol 70:179–186CrossRefGoogle Scholar
  32. Nielsen K, Peters A (2000) The effects of aging on the frequency of nerve fibers in rhesus monkey striate cortex. Neurobiol Aging 21:621–628CrossRefGoogle Scholar
  33. Ojo JO, Rezaie P, Gabbott PL et al (2015) Impact of age-related neuroglial cell responses on hippocampal deterioration. Front Aging Neurosci 7:57CrossRefGoogle Scholar
  34. Okazaki T, Kanchiku T, Nishida N et al (2018) Age-related changes of the spinal cord: a biomechanical study. Exp Therap Med 15:2824–2829Google Scholar
  35. Paltsyn AA, Komissarova SV (2015) Age-related changes of the brain. Patol Fiziol Eksp Ter 59:108–116Google Scholar
  36. Peters A (2002) The effects of normal aging on myelin and nerve fibers: a review. J Neurocytol 31:581–593CrossRefGoogle Scholar
  37. Peters (2007) The effects of normal aging on nerve fibers and neuroglia in the central nervous system. In: Riddle DR (ed) Brain aging: models, methods, and mechanisms. Taylor & Francis, Boca Raton, pp 97–126CrossRefGoogle Scholar
  38. Peters A (2009) The effects of normal aging on myelinated nerve fibers in monkey central nervous system. Front Neuroanat 3:11CrossRefGoogle Scholar
  39. Rahimi J, Kovacs GG (2014) Prevalence of mixed pathologies in the aging brain. Alzheimers Res Ther 6:82CrossRefGoogle Scholar
  40. Rotshenker S (2011) Wallerian degeneration: the innate-immune response to traumatic nerve injury. J Neuroinflammation 8:109CrossRefGoogle Scholar
  41. Ryu J, Horkayne-Szakaly I, Xu L, Pletnikova O, Leri F, Eberhart C, Troncoso JC, Koliatsos VE (2014) The problem of axonal injury in the brains of veterans with histories of blast exposure. Acta Neuropathol Comm 2:153CrossRefGoogle Scholar
  42. Shimada A, Kuwamura M, Awakura T et al (1992) An immunohistochemical and ultrastructural study on age-related astrocytic gliosis in the central nervous system of dogs. J Vet Med Sci 54:29–36CrossRefGoogle Scholar
  43. Stahon KE, Bastian C, Griffith S, Kidd GJ, Brunet S, Baltan S (2016) Age-related changes in axonal and mitochondrial ultrastructure and function in white matter. J Neurosci 36:9990–10001CrossRefGoogle Scholar
  44. Summers BA, Cummings BJ, de Lahunta A (1995) Neuropathology of aging. In: Veterinary neuropathology. Mosby-Year Book, Saint Louis, pp 49–67Google Scholar
  45. Suzuki Y, Ohta K, Suu S (1979) Correlative studies of axonal spheroids and lafora-like bodies in aged dogs. Acta Neuropathol 111:213–219Google Scholar
  46. Wang Y, Hashizume Y, Yoshida M, Inagaki T, Kameyama T (1999) Pathological changes of the spinal cord in centenarians. Pathol Int 49:118–124CrossRefGoogle Scholar
  47. Whiteford R, Getty R (1966) Distribution of lipofuscin in the canine and porcine brain as related to aging. J Gerontol 21:31–44CrossRefGoogle Scholar
  48. Wider C, Wszolek ZK (2014) Hereditary diffuse leukoencephalopathy with axonal spheroids: more than just a rare disease. Neurol 82:102–103CrossRefGoogle Scholar
  49. Yamanami S, Ishihara T, Takahashi M et al (1992) Comparative study of intraneuronal polyglucosan bodies from patients with Lafora disease and aged dogs. Acta Pathol Jpn 42:787–791Google Scholar
  50. Yanai T, Masegi T, Kawada M, Ishikawa K, Fukuda K, Yamazoe K, Iwasaki T, Ueda K, Goto N (1994) Spontaneous vascular mineralization in the brain of cows. J Comp Pathol 111:213–219CrossRefGoogle Scholar
  51. Yoshino T, Uchida K, Tateyama S, Yamaguchi R, Nakayama H, Goto N (1996) A retrospective study of canine senile plaques and cerebral amyloid angiopathy. Vet Pathol 33:230–234CrossRefGoogle Scholar
  52. Youssef SA, Capuccino MT, Rofina JE et al (2016) Pathology of aging brain in domestic and laboratory animals, and animal models of human neurodegenerative diseases. Vet Pathol 53:327–348CrossRefGoogle Scholar

Copyright information

© Springer-Verlag London Ltd., part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Histopathology, Diagnostic Animal Pathology OfficeSapporoJapan

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