Hypoglycaemia causes degeneration of large myelinated nerve fibres in the vagus nerve of insulin-treated diabetic BB/Wor rats

Acta Neuropathologica

Volumn 109, Issue 2, 2005, Pages 198-206

  Jamali, Reza ^a   Mohseni, Simin ^a  

^a LINKÖPING UNIVERSITY   (Sweden)

Author keywords

BB Wor rat; Diabetes mellitus; Hypoglycaemia; Neuropathy; Vagus nerve

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIABETES MELLITUS; DIABETIC NEUROPATHY; FEMALE; HYPERGLYCEMIA; HYPOGLYCEMIA; MYELINATED NERVE; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; RAT; RAT STRAIN; RECURRENT LARYNGEAL NERVE; VAGUS NERVE;

ANIMALS; AXONS; DIABETIC NEUROPATHIES; DISEASE MODELS, ANIMAL; FEMALE; HYPOGLYCEMIA; INSULIN; INSULIN INFUSION SYSTEMS; MICROSCOPY, ELECTRON, TRANSMISSION; NERVE DEGENERATION; NERVE FIBERS, MYELINATED; RATS; RATS, INBRED BB; VAGUS NERVE;

EID: 16344364388     PISSN: 00016322     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00401-004-0932-1     Document Type: Article

References (62)

1. Altschuler SM, Bao XM, Bieger D, Hopkins DA, Miselis RR (1989) Viscerotopic representation of the upper alimentary tract in the rat: Sensory ganglia and nuclei of the solitary and spinal trigeminal tracts. J Comp Neurol 283:248-268 1:STN:280:BiaB1M3is10%3D
2. Bolinder J, Sjöberg S, Persson A, Ahrén B, Sundkvist G (2002) Autonomic neuropathy is associated with impaired pancreatic polypeptide and neuropeptide Y responses to insulin-induced hypoglycaemia in Type 1 diabetic patients. Diabetologia 45:1043-1044 1:CAS:528:DC%2BD38XltlOnt7s%3D
3. Bott S, Bott U, Berger M, Mühlhauser I (1997) Intensified insulin therapy and the risk of severe hypoglycaemia. Diabetologia 40:926-932 10.1007/s001250050769
4. Bottini P, Boschetti E, Pampanelli S, Ciofetta M, Del Sindaco P, Scionti L, Brunetti P, Bolli GB (1997) Contribution of autonomic neuropathy to reduced plasma adrenaline responses to hyperglycaemia in IDDM. Diabetes 46:814-823 1:CAS:528:DyaK2sXjtVGntLs%3D
5. Chiarelli F, Verrotti A, Catino M, Sabatino G, Pinelli L (1999) Hypoglycaemia in children with type 1 diabetes mellitus. Acta Paediatr 427:31-34
6. Cryer PE (1999) Symptoms of hypoglycaemia, thresholds for their occurrence, and hypoglycaemia unawareness. Endocrinol Metab Clin North Am 28:495-500 1:STN:280:DyaK1MvjtVOitg%3D%3D
7. Dahlqvist Å. Carlsöö B. Hellström S. (1982) Fibre components of the recurrent laryngeal nerve of the rat: A study by light and electron microscopy. Anat Rec 204:365-370 1:STN:280:BiyD1MfksV0%3D
8. Dahlqvist Å. Carlsöö B. Hellström S Domeij S, Kourtopoulos H (1986) Fibre composition of the recurrent laryngeal nerve after experimental vagotomy and sympathectomy. A qualitative study by light and electron microscopy. Acta Anat 125:114-120 1:STN:280:BimC2MvnvV0%3D
9. Dahlqvist Å. Hellström S, Carlsöö B, Perquignot JM (1987) Paraganglia of the rat recurrent laryngeal nerve after long-term hypoxia: A morphometric and biochemical study. J Neurocytol 16:289-297 1:STN:280:BiiB1c3kslU%3D
10. Dahlqvist Å. Pequignot JM, Hellström S (1991) Laryngeal nerve paraganglia of the rat are morphologically and biochemically unchanged by long-term hypercapnia. Neurosci Lett 134:25-28 1:STN:280:By2B2s%2FhtV0%3D
11. Diabetes Control and Complications Trial Research Group (1993) The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med 329:977-986 10.1056/NEJM199309303291401
12. Diani AR, Grogan DM, Yates ME, Risinger DL, Gerritsen GC (1979) Radiologic changes and autonomic neuropathology in the digestive tract of the ketonuric diabetic Chinese hamster. Diabetologia 17:33-40 1:STN:280:CSaB3sjjs1w%3D
13. Dovas A, Lucchi ML, Bortolami R, Grandis A, Palladino AR, Banelli E, Caretta M, Magni F, Paolocci N (1998) Collaterals of recurrent laryngeal nerve fibres innervate the thymus: A fluorescent tracer and HRP investigation of efferent vagal neurons in the rat brainstem. Brain Res 809:141-148 10.1016/S0006-8993(98)00705-7
14. Duchen LW, Anjorin A, Watkins PJ, Mackay JD (1980) Pathology of autonomic neuropathy in diabetes mellitus. Ann Intern Med 92:301-303 1:STN:280:Bi%2BC38fjvVI%3D
15. Evans DHL, Murray JG (1954) Histological and functional studies on the fibre composition of the vagus nerve of the rabbit. J Anat 88:320-337
16. Fox EA, Powley TL (1985) Longitudinal columnar organization within the dorsal motor nucleus represents separate branches of the abdominal vagus. Brain Res 341:269-282 10.1016/0006-8993(85)91066-2
17. Gabella G, Pease HL (1973) Number of axons in the abdominal vagus of the rat. Brain Res 58:465-469 10.1016/0006-8993(73)90015-2
18. Gaster B, Hirsch IB (1998) The effects of improved glycaemic control on complications in type 2 diabetes. Arch Intern Med 158:134-140 10.1001/ archinte.158.2.134
19. Gerich JE, Mokan M, Veneman T, Korytkowski M, Mitrakou A (1991) Hypoglycaemia unawareness. Endocr Rev 12:356-371. 1:STN:280:By2C3cvgvFw%3D
20. Greene EC (1963) Anatomy of the rat. Hafner, New York
21. Guy RJC, Dawson JL, Garrett JR, Laws JW, Thomas PK, Sharma AK, Watkins PJ (1984) Diabetic gastroparesis from autonomic neuropathy: Surgical considerations and changes in vagus nerve morphology. J Neurol Neurosurg Psychiatry 47:686-691 1:STN:280:BiuB28nptVQ%3D
22. Haak T (1999) New developments in the treatment of type 1 diabetes mellitus. Exp Clin Endocrinol Diabetes 107 Suppl 3:S108-113
23. Hinrichsen CFL, Ryan AT (1981) Localization of laryngeal motoneurons in the rat: Morphologic evidence for dual innervation? Exp Neurol 74:341-355 10.1016/0014-4886(81)90174-6
24. Hisa Y, Lyon MJ, Malmgren LT (1985) Central projection of the sensory component of the rat recurrent laryngeal nerve. Neurosci Lett 55:185-190 10.1016/0304-3940(85)90017-5
25. Hoeldtke RD, Boden G (1994) Epinephrine secretion, hypoglycaemia unawareness and diabetic autonomic neuropathy. Ann Intern Med 120:512-517 1:STN:280:ByuC2cvpvVA%3D
26. Jacob HJ, Pettersson A, Wilson D, Mao Y, Lernmark A, Lander ES (1992) Genetic dissection of autoimmune type I diabetes in the BB rat. Nat Genet 2:56-60 10.1038/ng0992-56
27. Jamali R, Ludvigsson J, Mohseni S (2002) Continuous monitoring of the subcutaneous glucose level in freely moving normal and diabetic rats and in humans with type 1 diabetes. Diabetes Technol Ther 4:305-312 10.1089/ 152091502760098447
28. Kalia M, Mesulam M-M (1980) Brain stem projections of sensory and motor components of the vagus complex in the cat. I. The cervical vagus and nodose ganglia. J Comp Neurol 193:435-465 1:STN:280:Bi6D2s%2FitFM%3D
29. Kalia M, Mesulam M-M (1980) Brain stem projections of sensory and motor components of the vagus complex in the cat. II. Laryngeal, tracheobronchial, cardiac and gastrointestinal bronchus. J Comp Neurol 193:467-508 1:STN:280:Bi6D2s%2FitFw%3D
30. Karnes J, Robb R, O'Brien PC, Lambert EH, Dyck PJ (1977) Computerized image recognition for morphometry of nerve attribute of shape of sampled transverse sections of myelinated fibres which best estimates their average diameter. J Neurol Sci 34:43-51 10.1016/0022-510X(77)90090-9
31. Kohno T, Mori S, Mito M (1987) Cells of origin innervating the liver and their axonal projections with synaptic terminals into the liver parenchyma in rats. Hokkaido Igaku Zasshi 62:933-946 1:STN:280:BieC28fjsFw%3D
32. Kristensson K, Nordborg C, Olsson Y, Sourander P (1971) Changes in the vagus nerve in diabetes mellitus. Acta Pathol Microbiol Scand 79:684-685 1:STN:280:CS2D2M%2Fps10%3D
33. Lu K-S, Chien C-L, Chau Y-P (1992) Effects of 5-hydroxydopamine and 6-hydroxydopamine on the ultrastructure of type I cells in paraganglia of the rat recurrent nerve. Arch Histol Cytol 55:57-65 1:CAS:528:DyaK3sXitFShsrs%3D
34. Malik T, Trence DL (2003) Treating diabetes using oral agents. Prim Care 30:527-541 14692199
35. Mandelbaum JA, Felten DL, Westfall SG, Newlin GE, Peterson RG (1983) Neuropathic changes associated with insulin treatment of diabetic rats: Electron microscopic and morphometric analysis. Brain Res Bull 10:377-384 1:CAS:528:DyaL3sXktlensbk%3D
36. Marca MC, Loste A, Unzueta A, Perez M (2000) Blood glycated hemoglobin evaluation in sick dogs. Can J Vet Res 64:141-144 1:CAS:528:DC%2BD3cXjsFaru7w%3D
37. Mohseni S (2000) Hypoglycaemic neuropathy in diabetic BB/Wor rats treated with insulin implants affects ventral root axons but not dorsal root axons. Acta Neuropathol 100:415-420 10.1007/s004010000204
38. Mohseni S (2001) Hypoglycaemic neuropathy. Acta Neuropathol 102:413-421 1:CAS:528:DC%2BD3MXotFSiur4%3D
39. Mohseni S, Hildebrand C (1998) Neuropathy in diabetic BB/Wor rats treated with insulin implants. Acta Neuropathol 96:144-150 10.1007/ s004010050874
40. Mohseni S, Hildebrand C (1998) Hypoglycaemic neuropathy in BB/Wor rats treated with insulin implants: Electron microscopic observations. Acta Neuropathol 96:151-156 10.1007/s004010050875
41. Mohseni S, Lillesaar C, Theodorsson E, Hildebrand C (2000) Hypoglycaemic neuropathy: Occurrence of axon terminals in plantar skin and plantar muscle of diabetic BB/Wor rats treated with insulin implants. Acta Neuropathol 99:257-262 1:CAS:528:DC%2BD3cXms1CqsQ%3D%3D
42. Nordfeldt S, Ludvigsson J (1999) Adverse events in intensively treated children and adolescents with type I diabetes. Acta Paediatr 88:1184-1193 1:STN:280:DC%2BD3c%2Flslektw%3D%3D
43. Norgren R, Smith GP (1988) Central distribution of subdiaphragmatic vagal branches in the rat. J Comp Neurol 273:207-223 1:STN:280:BieA3s7ks10%3D
44. Patrickson JW, Smith TE, Zhou S-S (1991) Motor neurons of the laryngeal nerves. Anat Rec 230:551-556 1:STN:280:By2D38npt1E%3D
45. Patrickson JW, Smith TE, Zhou S-S (1991) Afferent projections of the superior and recurrent laryngeal nerves. Brain Res 539:169-174 10.1016/ 0006-8993(91)90702-W
46. Perkins BA, Bril V (2003) Diabetic neuropathy: A review emphasizing diagnostic methods. Clin Neurophysiol 114:1167-1175 12842711
47. Powley TL, Fox EA, Berthoud HR (1987) Retrograde tracer technique for assessment of selective and total subdiaphragmatic vagotomies. Am J Physiol 253:361-370
48. Prechtl JC, Powley TL (1987) A light and electron microscopic examination of the vagal hepatic branch of the rat. Anat Embryol 176:115-126 1:STN:280:BiiB28flsFc%3D
49. Prechtl JC, Powley TL (1990) The fibre composition of the abdominal vagus of the rat. Anat Embryol 181:101-115 10.1007/BF00198950
50. Qi BQ, Merei J, Farmer P, Hasthorpe S, Myers NA, Beasley SW, Hutson JM (1997) The vagus and recurrent laryngeal nerves in the rodent experimental model of esophageal atresia. J Pediat Surg 32:1580-1586 10.1016/S0022-3468(97)90457-7
51. Robertson DM, Sima AAF (1980) Diabetic neuropathy in the mutant mouse [C57BL/ks(db/db)]: A morphometric study. Diabetes 29:60-67 1:CAS:528:DyaL3cXitFeisbg%3D
52. Romeo HE, Diaz MC, Ceppi J, Zaninovich AA, Cardinali DP (1988) Effect of inferior laryngeal nerve section on thyroid function in rats. Endocrinology 122:2527-2532 1:CAS:528:DyaL1cXktFOnu70%3D
53. Scheen AJ (2003) Treatment of type 2 diabetes. Acta Clin Belg 58:318-324 14748101
54. Schmidt RE, Plurad SB, Modert CW (1983) Experimental autonomic neuropathy. Characterization in streptozotocin-diabetic Sprague-Dawley rats. Lab Invest 49:538-552 1:STN:280:BiuD3sjnsFQ%3D
55. Sharma AK, Thomas PK (1974) Peripheral nerve structure and function in experimental diabetes. J Neurol Sci 23:1-15 10.1016/0022-510X(74)90136-1
56. Sharma AK, Duguid IGM, Blanchard DS, Thomas PK (1985) The effect of insulin treatment on myelinated nerve fibre maturation and integrity and on body growth in streptozotocin-diabetic rats. J Neurol Sci 67:285-297 10.1016/0022-510X(85)90153-4
57. Smith D, Amiel SA (2002) Hypoglycaemia unawareness and the brain. Diabetologia 45:949-958 10.1007/s00125-002-0877-7
58. Stathakis P, Fernando DA, Lord RSA (1994) The course of the right recurrent laryngeal nerve within the vagus nerve of the rat. Acta Anat 149:70-73 1:STN:280:ByuB2c%2FpsFQ%3D
59. Tay SS, Wong WC (1994) Short- and long-term effects of streptozotocin-induced diabetes on the dorsal motor nucleus of the vagus nerve in the rat. Acta Anat (Basel) 150:274-281
60. Westfall SG, Felten DL, Mandelbaum JA, Moore SA, Peterson RG (1983) Degenerative neuropathy in insulin-treated diabetic rats. J Neurol Sci 61:93-107 10.1016/0022-510X(83)90057-6
61. Yagihashi S, Sima AAF (1986) Diabetic autonomic neuropathy in BB rat. Ultrastructural and morphometric changes in parasympathetic nerves. Diabetes 35:733-743 1:STN:280:BimB2cfjvVI%3D
62. Zhang W-X, Chakrabarti S, Greene DA, Sima AF (1990) Diabetic autonomic neuropathy in BB rats and effect of ARI treatment on heart-rate variability and vagus nerve structure. Diabetes 39:613-618 1:CAS:528:DyaK3cXktFOksbc%3D