Microvasculitis and ischemia in diabetic lumbosacral radiculoplexus neuropathy
Abstract
Objective: To determine whether microscopic vasculitis explains the clinical and pathologic features of diabetic lumbosacral radiculoplexus neuropathy (DLSRPN).
Background: DLSRPN is usually attributed to metabolic derangement or ischemic injury, but microscopic vasculitis as the sole cause needs consideration.
Methods: We prospectively studied the clinical, laboratory, and EMG features as well as the pathology of distal cutaneous nerve biopsy specimens of patients with DLSRPN.
Results: Study of DLSRPN nerve biopsy specimens (n = 33) compared with those from healthy controls (n = 14) and those with diabetic polyneuropathy (n = 21) provided strong evidence for ischemic injury (axonal degeneration, multifocal fiber loss, focal perineurial necrosis and thickening, injury neuroma, neovascularization, and swollen fibers with accumulated organelles), which we attribute to microscopic vasculitis (epineurial vascular and perivascular inflammation, vessel wall necrosis, and evidence of previous bleeding). Segmental demyelination was significantly associated with multifocal fiber loss.
Conclusions: 1) This severe, debilitating neuropathy begins with symptoms unilaterally and focally in the leg, thigh, or buttock and spreads to involve the other regions of the same and then opposite side and is due to multifocal involvement of lumbosacral roots, plexus, and peripheral nerve (i.e., diabetic lumbosacral radiculoplexus neuropathy). 2) Motor, sensory, and autonomic fibers are all involved. 3) Ischemic injury explains the clinical features and pathologic abnormalities of nerve. 4) The proximate cause of the ischemic injury appears to be microscopic vasculitis. 5) The segmental demyelination is probably secondary to ischemic axonal dystrophy, thus providing a unifying hypothesis for both axonal degeneration and segmental demyelination.
Get full access to this article
View all available purchase options and get full access to this article.
References
1.
Pirart J. Diabetes mellitus and its degenerative complications: a prospective study of 4,400 patients observed between 1947 and 1973. Part 1. Diabetes Care 1978;1:168–188.
2.
Dyck PJ, Kratz KM, Karnes JL, et al. The prevalence by staged severity of various types of diabetic neuropathy, retinopathy, and nephropathy in a population-based cohort: the Rochester Diabetic Neuropathy Study. Neurology 1993;43:817–824.
3.
Bruns L. Ueber neuritsche Lahmungen beim diabetes mellitus. Berlin Klin Wochenschr 1890;27:509.
4.
Leyden E. Beitrag zur Klinik des diabetes mellitus. Wien Med Wochenschr 1893;43:926.
5.
Garland HT, Tavernor D. Diabetic myelopathy. Br Med J 1953;2:1405–1408.
6.
Garland H. Diabetic amyotrophy. Br Med J 1955;2:1287–1290.
7.
Garland H. Diabetic amyotrophy. Br J Clin Pract 1961;15:9–13.
8.
Skanse B, Gydell K. A rare type of femoral-sciatic neuropathy in diabetes mellitus. Acta Med Scand 1956;155:463–468.
9.
Calverley JR, Mulder DW. Femoral neuropathy. Neurology 1960;10:963–967.
10.
Chokroverty S, Reyes MG, Rubino FA. Bruns-Garland syndrome of diabetic amyotrophy. Trans Am Neurol Assoc 1977;102:1–4.
11.
Barohn RJ, Sahenk Z, Warmolts JR, Mendell JR. The Bruns-Garland syndrome (diabetic amyotrophy) revisited 100 years later. Arch Neurol 1991;48:1130–1135.
12.
Bastron JA, Thomas JE. Diabetic polyradiculopathy: clinical and electromyographic findings in 105 patients. Mayo Clin Proc 1981;56:725–732.
13.
Raff MC, Asbury AK. Ischemic mononeuropathy and mononeuropathy multiplex in diabetes mellitus. N Engl J Med 1968;279:17–22.
14.
Raff MC, Sangalang V, Asbury AK. Ischemic mononeuropathy multiplex associated with diabetes mellitus. Arch Neurol 1968;18:487–499.
15.
Williams IR, Mayer RF. Subacute proximal diabetic neuropathy. Neurology 1976;26:108–116.
16.
Asbury AK. Proximal diabetic neuropathy. Ann Neurol 1977;2:179–180.
17.
Bradley WG, Chad D, Verghese JP. Painful lumbosacral plexopathy with elevated erythrocyte sedimentation rate: a treatable inflammatory syndrome. Ann Neurol 1984;15:457–464.
18.
Taylor BV, Dyck PJ. Classification of the diabetic neuropathies. In: Dyck PJ, Thomas PK, eds. Diabetic neuropathy. 2nd ed.Philadelphia:W.B. Saunders, 1999:407–414.
19.
Chokroverty S, Reyes MG, Rubino FA, Tonaki H. The syndrome of diabetic amyotrophy. Ann Neurol 1977;2:181–199.
20.
Chokroverty S. Proximal nerve dysfunction in diabetic proximal amyotrophy. Arch Neurol 1982;39:403–407.
21.
Chokroverty S, Sander HW. AAEM case report #13: diabetic amyotrophy. Muscle Nerve 1996;19:939–945.
22.
Said G, Goulen-Goeau C, Lacroix C, Moulonguet A. Nerve biopsy findings in different patterns of proximal diabetic neuropathy. Ann Neurol 1994;35:559–569.
23.
Said G, Elgrably F, Lacroix C, et al. Painful proximal diabetic neuropathy: inflammatory nerve lesions and spontaneous favorable outcome. Ann Neurol 1997;41:762–770.
24.
Llewelyn JG, Thomas PK, King RHM. Epineurial microvasculitis in proximal diabetic neuropathy. J Neurol 1998;245:159–165.
25.
Krendel DA, Costigan DA, Hopkins LC. Successful treatment of neuropathies in patients with diabetes mellitus. Arch Neurol 1995;52:1053–1061.
26.
Pascoe MK, Low PA, Windebank AJ, Litchy WJ. Subacute diabetic proximal neuropathy. Mayo Clin Proc 1997;72:1123–1132.
27.
Dyck PJ, Sherman WR, Hallcher LM, et al. Human diabetic endoneurial sorbitol, fructose, and myoinositol related to sural nerve morphometry. Ann Neurol 1980;8:590–596.
28.
Dyck PJ, Kratz KM, Lehman KA, et al. The Rochester Diabetic Neuropathy Study: design, criteria for types of neuropathy, selection bias, and reproducibility of neuropathic tests. Neurology 1991;41:799–807.
29.
Dyck PJ, Zimmerman IR, O’Brien PC, et al. Introduction of automated systems to evaluate touch-pressure, vibration, and thermal cutaneous sensation in man. Ann Neurol 1978;4:502–510.
30.
Dyck PJ, Zimmerman IR, Gillen DA, Johnson DM, Karnes JL, O’Brien PC. Cool, warm, and heat-pain detection thresholds: testing methods and inferences about anatomic distribution of receptors. Neurology 1993;43:1500–1508.
31.
Dyck PJ, Litchy WJ, Lehman KA, Hokanson JL, Low PA, O’Brien PC. Variables influencing neuropathic endpoints: the Rochester Diabetic Neuropathy Study of Healthy Subjects (RDNS-HS). Neurology 1995;45:1115–1121.
32.
Low PA. Composite autonomic scoring scale for laboratory quantification of generalized autonomic failure. Mayo Clin Proc 1993;68:748–752.
33.
Dyck PJ, Giannini C, Lais A. Pathologic alterations of nerves. In: Dyck PJ, Thomas PK, Low PA, Griffin JW, Poduslo JF, eds. Peripheral neuropathy. 3rd ed.Philadelphia:W.B. Saunders, 1993:514–595.
34.
Gregersan G. Diabetic amyotrophy: a well defined syndrome? Acta Med Scand 1969;185:303–310.
35.
Dyck PJ, Conn DL, Okazaki H. Necrotizing angiopathic neuropathy: three-dimensional morphology of fiber degeneration related to sites of occluded vessels. Mayo Clin Proc 1972;47:461–475.
36.
Nukada H, Dyck PJ. Microsphere embolization of nerve capillaries and fiber degeneration. Am J Pathol 1984;115:275–287.
37.
Nukada H, Dyck PJ. Acute ischemia causes axonal stasis, swelling, attenuation, and secondary demyelination. Ann Neurol 1987;22:311–318.
38.
Korthals JK, Wisniewski HM. Peripheral nerve ischemia. Part 1. Experimental model. J Neurol Sci 1975;24:65–76.
39.
Korthals JK, Gieron MA, Wisniewski HM. Nerve regeneration patterns after acute ischemic injury. Neurology 1989;39:932–937.
40.
Benstead TJ, Dyck PJ, Sangalang V. Inner perineurial cell vulnerability in ischemia. Brain Res 1989;489:177–181.
41.
Parry GJ, Brown MJ. Arachidonate-induced experimental nerve infarction. J Neurol Sci 1981;50:123–133.
42.
Younger DS, Rosoklija G, Hays AP, Trojaborg W, Latov N. Diabetic peripheral neuropathy: a clinicopathologic and immunohistochemical analysis of sural nerve biopsies. Muscle Nerve 1996;19:722–727.
43.
Cotran RS, Kumar V, Robbins SL. Robbins pathologic basis of disease. 5th ed.Philadelphia:W.B. Saunders, 1994:496.
44.
Dyck PJ, Johnson WJ, Lambert EH, O’Brien PC. Segmental demyelination secondary to axonal degeneration in uremic neuropathy. Mayo Clin Proc 1971;46:400–431.
45.
Dyck PJ, Lais AC. Evidence for segmental demyelination secondary to degeneration in Friedreich’s ataxia. In: Kakulas BA, ed. Clinical studies in myology. Amsterdam: Excerpta Medica, 1973:73.
46.
Dyck PJ, Lais AC, Karnes JL, et al. Permanent axotomy, a model of axonal atrophy and secondary segmental demyelination and remyelination. Ann Neurol 1981;9:575–583.
Information & Authors
Information
Published In
Copyright
© 1999.
Publication History
Received: September 29, 1998
Accepted: August 18, 1999
Published online: December 1, 1999
Published in print: December 1, 1999
Authors
Metrics & Citations
Metrics
Citations
Download Citations
If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Select your manager software from the list below and click Download.
Cited By
- Bruns Garland Syndrome as the first presentation of type 2 diabetes: two case reports and a practical approach to diagnosis, Journal of Medical Case Reports, 18, 1, (2024).https://doi.org/10.1186/s13256-023-04327-9
- Vasculitic neuropathy-related disability, pain, quality of life, and autonomic symptoms: a survey of 312 patients, Rheumatology, (2024).https://doi.org/10.1093/rheumatology/keae038
- Neuropatie nei diabetici, EMC - Neurologia, 24, 2, (1-11), (2024).https://doi.org/10.1016/S1634-7072(24)48980-0
- Focal inflammatory neuropathies, Focal Neuropathies, (273-290), (2024).https://doi.org/10.1016/B978-0-323-90108-6.00009-0
- Vasculitic Neuropathies, Current Treatment Options in Neurology, 26, 3, (67-77), (2024).https://doi.org/10.1007/s11940-024-00782-x
- Diabetic Neuropathies, CONTINUUM: Lifelong Learning in Neurology, 29, 5, (1401-1417), (2023).https://doi.org/10.1212/CON.0000000000001291
- Neurologic Complications of Endocrine Disorders, CONTINUUM: Lifelong Learning in Neurology, 29, 3, (887-902), (2023).https://doi.org/10.1212/CON.0000000000001262
- Current perspectives on the diagnosis, assessment, and management of vasculitic neuropathy, Expert Review of Neurotherapeutics, 22, 11-12, (941-952), (2023).https://doi.org/10.1080/14737175.2022.2166831
- Understanding the role of hyperglycemia and the molecular mechanism associated with diabetic neuropathy and possible therapeutic strategies, Biochemical Pharmacology, 215, (115723), (2023).https://doi.org/10.1016/j.bcp.2023.115723
- Critical illness–associated weakness and related motor disorders, Motor System Disorders, Part I: Normal Physiology and Function and Neuromuscular Disorders, (707-777), (2023).https://doi.org/10.1016/B978-0-323-98818-6.00031-5
- See more
Loading...
View Options
Get Access
Login options
Check if you have access through your login credentials or your institution to get full access on this article.
Personal login Institutional LoginPurchase Options
Purchase this article to access the full text.