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Fine structural evaluation of altered Schmidt-Lanterman incisures in human sural nerve biopsies

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Summary

Fine structural alterations of Schmidt-Lanterman incisures (SLI) were investigated in a series of 242 unselected sural nerve biopsies that had been examined for diagnostic purposes. The series included cases with Friedreich's ataxia, HSAN I, HMSN I-III, HMSN VI, tomaculous neuropathy, metachromatic leukodystrophy, ceroidlipofuscinosis, dysproteinemic neuropathies, and myotonic dystrophy, in addition to several neuropathies less-specifically classified as either of a predominantly demyelinating, axonal, or neuronal type. The following classification of SLI alterations is proposed: (A) abnormal inclusions: (B) changes in shape and dimension; and (C) modes of disintegration. Abnormal inclusions comprised membranous whorls, uniform and pleomorphous lysosome-like bodies, and accumulation of granular substances at the site of the major dense line, or granular deposits at the site of the intraperiod line of the myelin sheath. Variations of incisural shape and dimension included folding, dilatation, and pocket formation (compartmentalization). Disintegration at incisures comprised a fine, vesicular and a gross, vacuolar type. Various combinations of these changes were observed. The most frequent change consisted of membranous whorls, detected in SLI of 89 biopsies. They were most prominent in chloroquine neuropathy where they occurred in SLI as well as in the adaxonal and abaxonal cytoplasm of Schwann cells. Compartmentalization of the myelin sheath at incisures associated with formation of myelin loops was a frequent feature in myotonic dystrophy. It is concluded, that changes of incisural ultrastructure are sensitive indicators of human neuropathies offering clues to the type of the underlying pathomechanism.

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References

  1. Allt G, Ghabriel MN, Sikri K (1988) Lysophosphatidyl choline-induced demyelination. A freeze fracture study. Acta Neuropathol (Berl) 75:456–464

    Google Scholar 

  2. Bischoff AJ (1979) The peripheral nerves. In: Johannessen JV (ed) Electron microscopy in human medicine. McGraw-Hill, New York, pp 136–236

    Google Scholar 

  3. Cajal SR (1928) Degeneration and Regeneration of the nervous system. Vol 1. Oxford University Press, London, pp 67–74

    Google Scholar 

  4. Celio MR (1976) The Schmidt-Lanterman incisures of the myelin sheath of Mauthner axons: places of longitudinal growth of myelin. Brain Res 108:221–235

    Google Scholar 

  5. Cros D, Harnden P, Pouget J, Pellissier JF, Gestaut JL, Serratrice G (1988) Peripheral neuropathy in myotonic dystrophy: a nerve biopsy study. Ann Neurol 23:470–476

    Google Scholar 

  6. Dayan AD, Graveson GS, Robinson PK, Woodhouse MA (1968) Globular neuropathy: a disorder of axons and Schwann cells. J Neurol Neurosurg Psychiatry 31:552–560

    Google Scholar 

  7. Dyck PJ, Karnes J, Lais A, Lofgren EP, Stevens JC (1984) Pathologic alterations of the peripheral nervous system in humans. In: Dyck PJ, Thomas PK, Lambert EH, Bunge R (eds) Peripheral neuropathy, 2nd edn. WB Saunders, Philadelphia, pp 760–780

    Google Scholar 

  8. Ericsson JE, Biberfeld P (1967) Studies on aldehyde fixation. Fixation rates and their relation to fine structure and some histochemical reactions in liver. Lab Invest 17:281–298

    Google Scholar 

  9. Ghabriel MN, Allt G (1979) The role of Schmidt-Lanterman incisures in Wallerian degeneration. I. A quantitative teased fiber study. Acta Neuropathol (Berl) 48:83–93

    Google Scholar 

  10. Ghabriel MN, Allt G (1979) The role of Schmidt-Lanterman incisures in Wallerian degeneration. II. An electron microscopic study. Acta Neuropathol (Berl) 48:95–103

    Google Scholar 

  11. Ghabriel MN, Allt G (1981) Incisures of Schmidt-Lanterman. Prog Neurobiol 17:25–58

    Google Scholar 

  12. Hall SM, Williams PL (1970) Studies on the “incisures” of Schmidt and Lanterman. J Cell Sci 6:767–791

    Google Scholar 

  13. Hiscoe HB (1947) Distribution of nodes and incisures in normal and regenerated nerve fibres. Anat Rec 99:447

    Google Scholar 

  14. Ho ST, Yu HS (1989) Ultrastructural changes of the peripheral nerve induced by vibration: an experimental study. Br J Ind Med 46:157–164

    Google Scholar 

  15. Hruban Z (1984) Pulmonary and generalized lysosomal storage induced by amphiphilic drugs. Environ Health Perspect 55:53–76

    Google Scholar 

  16. Jacobs JM, Scadding JW (1990) Morphological changes in IGM paraproteinaemic neuropathy. Acta Neuropathol 80:77–84

    Google Scholar 

  17. Lanterman AJ (1877) deÜber den feineren Bau der markhaltigen Nervenfasern. Arch Mikrosk Anat Entwicklungsmech 13:1–8

    Google Scholar 

  18. Lazar L, Maros T (1962) Beitrag zur funktionellen Bedeutung der Schmidt-Lantermanschen Einkerbungen. Rev Sci Med 7:51–54

    Google Scholar 

  19. Lüllmann H, Lüllmann-Rauch R, Wassermann O (1978) Lipidosis induced by amphiphilic cationic drugs. Biochem Pharmacol 27:1103–1108

    Google Scholar 

  20. Meier C, Moll C (1982) Hereditary neuropathy with liability to pressure palsies. Report of two families and review of the literature. J Neurol 228:73–95

    Google Scholar 

  21. Mugnaini E, Osen KK, Schnapp B, Friedrich VL (1977) Distribution of Schwann cell cytoplasm and plasmalemmal vesicles (caveolae) in peripheral myelin sheaths. An electron microscopic study with thin sections and freeze fracturing. J Neurocytol 6:647–668

    Google Scholar 

  22. Nardelli E, Steck AJ, Barkas T, Schluep M, Jerusalem F (1988) Motor neuron syndrome and monoclonal IgM with antibody activity against gangliosides GM1 and GD1b. Ann Neurol 23:524–528

    Google Scholar 

  23. Onishi A, Yoshiyuki M, Masato I, Tsutomu F, Hirokazu F, Yoshigoro K (1989) Autosomal recessive motor and sensory neuropathy with excessive myelin outfolding. Muscle Nerve 12:568–575

    Google Scholar 

  24. Pages M, Pages AM (1984) Lésios du nerf périphérigue dans le neuromyopathie à la chloroquine. Ann Pathol 4:289–295

    Google Scholar 

  25. Ranvier ML (1878) Leçons sur l'Histologie du Système Nerveux. Savy, Paris

    Google Scholar 

  26. Rebai T, Mhiri C, Heine P, Charfi H, Meyrignac C, Gherardi R (1989) Focal myelin thickenings in a peripheral neuropathy associated with IgM monoclonal gammopathy. Acta Neuropathol 79:226–232

    Google Scholar 

  27. Robertson JD (1958) The ultrastructure of Schmidt-Lanterman clefts and related shearing defects of the myelin sheath. J Biophys Biochem Cytol 4:39–46

    Google Scholar 

  28. Robertson JD (1962) The unit membrane of cells and mechanism of myelin formation. In: Korey SR, Pope A, Robins E (eds) Ultrustructure and metabolism of the nervous system, Williams & Wilkins, Baltimore, pp 94–158

    Google Scholar 

  29. Saida K, Saida T, Brown M, Silberberg DH, Asbury AK (1978) Antiserum-mediated demyelination in vivo. A sequential study using intraneural injection of experimental allergic neuritis serum. Lab Invest 39:449–462

    Google Scholar 

  30. Saida T, Saida K, Brown MJ, Silberberg DH (1979) Peripheral nerve demyelination induced by intraneural injection of experimental allergic encephalomyelitis serum. J Neuropathol Exp Neurol 38:498–518

    Google Scholar 

  31. Santoro M, Thomas FP, Fink ME, Lange DJ, Uncini A, Wadia NH, Latov N, Hays AP (1990) IgM deposits at nodes of Ranvier in a patient with amyotrophic lateral sclerosis, anti-GM1 antibodies, and multifocal conduction block. Ann Neurol 28:373–377

    Google Scholar 

  32. Schmidt HD (1874) On the construction of the dark or double bordered nerve fibre. Non Microsc J (Lond) 11:200–222

    Google Scholar 

  33. Schröder JM (1974) Two-dimensional reconstruction of Schwann cell changes following remyelination of regenerated nerve fibres. In: Hausmanova-Petrusewicz I, Jedrzejowska H (eds) Proceedings of the symposium on structure and function of normal and diseased muscle and peripheral nerve. Polish Medical Editors, Warsaw, pp 299–304

    Google Scholar 

  34. Schröder JM (1981) Pathomorphologie des peripheren Nerven. In: Neundörfer B (ed) Polyneuritiden und Polyneuropathien, Edition Medizin. VCH, Weinheim, pp 11–104

    Google Scholar 

  35. Schröder JM (1988) Muskel- und Nervenbiopsien. In: Schliack H, Hopf HC (eds) Diagnostik in der Neurologie. Georg Thieme Verlag, Stuttgart New York, pp 147–188

    Google Scholar 

  36. Thomas PK (1974) Nerve injury. In: Bellairs R, Gray EF (eds) Essays on the nervous system. Clarendon Press, Oxford, pp 44–70

    Google Scholar 

  37. Thomas PK, Ochoa J (1984) Microscopic anatomy of peripheral nerve fibers. In: Dyck PJ, Thomas PK, Lambert EH, Bunge R (eds) Peripheral neuropathy, vol 1. WB Saunders, Philadelphia London Toronto, pp 39–96

    Google Scholar 

  38. Trapp BD, Andrews B, Wong A, O'Connell M, Griffin JW (1989) Co-localization of the myelin-associated glycoprotein and the microfilament components F-actin and spectrin in Schwann cells of myelinated nerve fibers. J Neurocytol 18:47–60

    Google Scholar 

  39. Vital C, Vallat JM (1987) Ultrustructural study of the human diseased peripheral nerve. Elsevier, New York Amsterdam London, pp 27–85

    Google Scholar 

  40. Vital A, Vital C, Riviere JP, Brechenmacher C, Marot J (1987) Variability of morphological features in early infantile polyneuropathy with defective myelination. Acta Neuropathol (Berl) 73:295–300

    Google Scholar 

  41. Vuorinen VS, Röyttä M (1990) Taxol-induced neuropathy after nerve crush: long-term effects on Schwann and endoneurial cells. Acta Neuropathol 79:653–662

    Google Scholar 

  42. Vuorinen VS, Röyttä M (1990) Taxol-induced neuropathy after nerve crush: long-term effects on regenerating axons. Acta Neuropathol 79:663–671

    Google Scholar 

  43. Vuorinen VS, Röyttä M, Raine CS (1988) The acute effects of taxol upon regenerating axons after nerve crush. Acta Neuropathol (Berl) 76:26–34

    Google Scholar 

  44. Vuorinen VS, Röyttä M, Raine CS (1988) The acute response of Schwann cells to taxol after nerve crush. Acta Neuropathol (Berl) 76:17–25

    Google Scholar 

  45. Webster H deF (1964) The relationship between Schmidt-Lanterman incisures and myelin segmentation during Wallerian degeneration. Ann NY Acad Sci 122:29–38

    Google Scholar 

  46. Westland K, Pollard JD (1987) Proteinase-induced demyelination. An electrophysiological and histological study. J Neurol Sci 82:41–53

    Google Scholar 

  47. Young JZ (1944) Surface tension and the degeneration of nerve fibers. Nature 154:521–522

    Google Scholar 

Download references

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  1. Institut für Neuropathologie der Rheinisch-Westfälischen Technischen Hochschule Aachen, Pauwelsstrasse 30, W-5100, Aachen, Federal Republic of Germany

    J. M. Schröder & F. Himmelmann

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  1. J. M. Schröder
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Schröder, J.M., Himmelmann, F. Fine structural evaluation of altered Schmidt-Lanterman incisures in human sural nerve biopsies. Acta Neuropathol 83, 120–133 (1992). https://doi.org/10.1007/BF00308471

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  • DOI: https://doi.org/10.1007/BF00308471

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