Serum antibodies to GM1 and GM3-gangliosides in systemic lupus erythematosus with chronic inflammatory demyelinating polyradiculoneuropathy Sindern E, Stark E, Haas J, Steck AJ. Serum antibodies to GMI and GM3-gangliosides in systemic lupus erythematosus with chronic inflammatory demyelinating polyradiculoneuropathy. Acta Neurol S c a d 1991: 83: 399-402.
Acute symmetric dernyelinating polyneuropathy of the Guillain-Barre type is known in systemic lupus erythematosus (SLE).Chronic idiopathic demyelinating polyneuropathy (CIDP) has been reported rarely with SLE. A case is reported of CIDP accompaning SLE with autoantibodies against GM 1-and GM3-gangliosides.There was no historical evidence to suggest SLE, and CIDP was the first manifestation of SLE.The 38-year-old patient had elevated CSF-protein, slow nerve conduction velocities, sural nerve biopsy revealed mixed axon loss with demyelination and CIDP white matter lesions were observed in magnetic resonance imaging. the GMI-and GM3- autoantibodies may play a role in the pathogenesis of CIDP in SLE. The Guillain-Barrt syndrome (GBS) and the chronic type of idiopathic demyelinating polyradiculoneuropathy (CIDP) have similar clinical features. In GBS the clinical deficit reaches its maximum within 4 weeks. The minimal duration of progression for CIDP is 6 months (1). A common pathogenetic mechanism has been proposed for both. A humoral factor has been inferred, because serum from patients with both diseases may cause demyelination (2,3). Some patients with CIDP and GBS benefit from plasmapheresis (4).This indicates that circulating factors play a role in the pathogenesis of these diseases. Ilyas et al. ( 5 ) recently demonstrated antibodies to gangliosides in GBS. The occurrence of GBS and CIDP in association with autoimmune diseases has been reported (6). We report of a patient with autoantibodies against gangliosides, in whom CIDP was the first clinical manifestation of systemic lupus erythematosus (SLE). Material and methods
A 38-year-old man was admitted after a sevenmonth history of fatigue and malaise with a weight loss of 12 kg and fluctuating dysesthesia in hand and feet. Neurologic examination revealed a moderate proximal and distal weakness of all limbs. Pin prick
E. Sindern', E. Stark', J. Haas', A. J. Steck2 Department of ' Neurology and clinical Neurophysiology, Medical School of Hannover, Germany, Neurology, Centre Hospitalier Universitaire Vaudois, Lausanne, Switzerland
Key words: systemic lupus erythematosus; chronic inflammatory demyelinating polyradikuloneuropathy; antibodies to GM1 and GM3gangliosides
Eckhart Sindern, Department of Neurology and Clinical Neurophysiology, Medical School Hannover, Konstanty Gutschow Str. 8, 3000 Hannover 6 1, Germany Accepted for publication November 28, 1990
and touch sens tion was reduced with sock and glove distribution. Vibration and position sense were highly impaired in hands and feet. Deep tendon reflexes were absent. Ataxia of the limbs and trunk with a postural and intention tremor as well as a tremor of the head was prominent. Speech was dysarthric. Except from facial myokymia, cranial nerves were normal. A fixed malar rash was prominent. He had a pityriasis versicolor. Further general physical examination was normal. Serum routine studies, porphyrin-screening and cryoglobulins were negative. Antibodies against adeno-, entero-, cytomegalo-, herpes simplex-, varicella zoster-, polio-, HIV 1 or 2-virus, toxoplasma gondii and borrelia burgdorferi were not found. Serum IgM was raised to 6 g/1 with no evidence of monoclonal gammopathy. Haptoglobin, CRP, CH50 and C3 showed normal values. Complementfactor C4 was reduced to 0.19 g/l. Latex test was negative. Westergren erythrocyte sedimentation rate was 40/82. Antinuclear antibodies were positive up to 1 : 480 with a homogen pattern, anti ds-DNA 39 IE/ml, anti-Sm positive and anti-RNP negative. Examination of the cerebrospinal fluid revealed 3.3 cells/ul, mainly monocytes. The total protein was elevated to 490 mg/dl. IgG-index was normal. Identical oligoclonal IgG fractions were determined by isoelectric focussing in polyacrylamide gels. Median
399
Sindern et al.
and tibial distal motor latency were prolonged (43.4 msec and 63.6 msec); and nerve conduction velocities were slow (14m/sec and 16 m/sec), Fwave latency to m. adductor polticis brevis was abnormal (113 msec). Sural and median sensory potentials were absent. EMG revealed positive sharp waves in m. tibialis anterior. Motor unit potentials were polyphasic. MR-images of the head and the spinal cord revealed at T2-sequencies white matter lesions in the right parietal area, the brainstem and thoracal spinal cord. Steroid therapy was started with prednisone 100 mg/d for 2 weeks, with reduction 50 mg/d and 30 mg/d alternating. Strength and hypesthesia had improved, but 6 month later there was a relapsing deterioration. The patient was additionally treated with azathioprine 150mg/d and a moderate improvement was observed. Eight mont later the neurologic status deteriorated again, and there was a amelioration with cyclophosphamide 1000 mg monthly. No relapses were observed in the following 6 months. Now central nervous system symptoms like dysarthria, ataxia of the trunk, intention tremor of the limbs as well as tremor of the head are the prominent clinical features.
15 14
n
13 E
=
0
x -5 c
12
11 10
c
9 $ 8 .8 7
-
Q
0
6
5 4
3 2 1 n
Antibody assays and results
Serum was assayed for circulating antibodies to gangliosides G M l , asialo GM1, GDla, GDlb, GM2 and GM3 (Fidia Research Laboratories Abano Terme Italy) by an enzyme-linked immunosorbent assay method essentially as published (7). Minor modifications include assay at 4°C and coating of plates with 1 ug of gangliosides. A titer of up to 20 is within the range of normal control sera and encompasses two standard deviation above the mean. We found a titer of anti-GM1 antibodies of over 160, representing a significant elevation. Further examination of the pattern of serum anti-gangliosides antibody activity, revealed a predominant component to GM1, asialo GM1 and GM3 (Fig. 1). Discussion
The initial prominent manifestation of this patient was a symmetrical motor and sensory polyneuropathy with sensory ataxia and absent tendon reflexes. The patient fulfilled the criteria for diagnosis of CIDP (8). Other causes of neuropathy were absent. Clinical examination suggested further additional involvement of the central nervous system. Magnetic resonance imaging (MRI) revealed subcortical, brainstem and spinal cord white matter lesions. The observation of MRI “lesions” in CIDP is uncom400
Fig. I . Binding of the patient’s serum at a 1 : 10 dilution to different purified gangliosides as measured by ELISA, showing a significant reactivity to GM 1, asialo GM 1 and GM3 gangliosides.
mon (9). However, patients with CIDP associated with CNS disorder indistinguishable from multiple sclerosis (MS) showed MRI “lesions” typical of MS (10, 11). In our patient the condition developed into a definite SLE (12), in whom focal white matter lesions similair to those in MS were reported (13). The course has been relapsing-remitting (Fig. 2). Immunosuppressive therapy led to an improvement of peripheral neurological symptoms, but the central nervous system symptoms accelerated. The occurrence of CIDP in association with autoimmune diseases such as acute glomerulonephritis, Hashimotos thyreoiditis, multiple sclerosis and myasthenia gravis has been episodically reported. Korn-Lubetzki and Abramsky reported that 5 / 8 (63%) patients with CIDP and 5/58 (9%) patients with GB S had associated autoimmune diseases (6). Eight further definite or probable cases of SLE with CIDP have been reported (14). Including our case, 5 patients had a relapsing course, while the illness was monophasic with prolonged progression in the other 4. Eight CSF specimens demonstrated high protein content (122 to 535 mg/dl) without cells, in one patient the CSF was
CIDP, SLE & GM1-, GMIautoantibodies
remission relapse remission clinical course: relapse prednisone therapy : - prednisone azathioprine
relapse remission prednisone cyclophospharnide
t , , , , t , , , , , , , t , , , # ? , I
normal. The pathologic-morphologic basis of this syndrome does not seem uniform. In histologic studies of affected nerves in 3 patients, the primary pathology involved the myelin sheath with preservation of the axis cylinder, in 3 others, including our case, primary loss of axons respectively mixed axon loss with demyelination was found. A common mechanism may be the development of autoantibodies that either cross-react with or are directed against axon or myelin constituents. Humoral factors may play a major role in the pathogenesis of inflammatory demyelinating neuropathy. In some patients with GBS and CIDP plasma exchange has an ameliorating effect on neurologic dysfunction and nerve conduction velocity (4, 15). In animal models injected serum from patients with acute demyelinating neuropathy may cause demyelination (2, 3). Several autoantibodies to peripheral nerve structures have been found in inflammatory neuropathies. Koski et al. observed significantly high titers of anti-peripheral nerve myelin antibodies in sera from 11/12 patients with GBS and 3/4 with CIDP (16). Recently Koski et al. found that these antibodies bind a neutral glycolipid of peripheral myelin (17). Antibodies against gangliosides have been detected in relative high levels in 20% of GBS patients (5). Endo et al. detected antibodies against ganglioside GM 1 and asialo GM1 in 19/31 patients with SLE (18). The present case demonstrates very high titers of antibodies to GM1- and GM3-gangliosides in a patient with CIDP in SLE. These antibodies may represent an autoimmune response that may contribute to the neuropathology associated with these inflammatory diseases.
References 1 . DYCKPJ, LAISAC, OHTAM, BASTRON JA, OKAZAKIH, 2.
3.
4.
5.
6.
GROOVERRV. Chronic inflammatory polyradikuloneuropathy. Mayo Clinic Proceedings 1975: 50: 621-637. Low PA, SCHMELZER J, DYCKPJ, KELLYJJ Jr. Endoneurial effects of sera from patients with acute inflammatory polyradikuloneuropathy: electrophysiologic studies on normal and demyelinated rat nerves. Neurology 1982: 32: 720-724. HARRISON BM, HANSENLA, POLLARD JD, M c LEODJG. Demyelination induced by serum from patients with Guillain-Barrt syndrome. AM Neurol 1984: 15: 163-170. DYCK PJ, DAUBEJ, OBRIEN P, PINEDAA, Low PA, WINDEBANK AJ, SWANSON C. Plasma exchange in chronic inflammatory demyelinating polyradikuloneuropathy. N Engl J Med 1986: 14: 461-465. ILYASAA, WILLISON HJ, QUARLES RH, JUNGALAWA FB, CORNBLATH DR, TRAPPED, GRIFFINJW, M c KHANN GM. Serum antibodies to gangliosides in Guillain-Barrt syndrome. Ann Neurol 1988: 23: 440-447. KORN-LUBETZKI I, ABRAMSKY0. Acute and chronic demyelinating inflammatory polyradiculoneuropathy. Association with autoimmune diseases and lymphocyte response to human neuritogenic protein. Arch Neurol 1986: 43:
604-608. 7. BOLLENSEN E, SCHIPPERHI, STECKAJ. Motor neuropathy with activity of monoclonal IgM antibody to G D l a ganglioside. J Neurol 1989: 236: 353-355. 8. DYCKPJ, ARNASON GBW. Chronic inflammatory demyeli-
nating polyradiculoneuropathy. In: DYCKPJ, THOMAS PK, LAMBERTEH, BUNGE R (Eds.). Peripheral neuropathy. Philadelphia: WB Saunders, 1975: 1012-1019. 9. FEASBYTE, HAHNAF, KOOPMAN WJ, LEE DH. Central lesions in chronic inflammatory demyelinating polyneuropathy: an MRI study. Neurology 1990: 40: 476-478. 10. THOMAS PK, WALKERRWH, RUDGEP etal. Chronic demyelinating peripheral neuropathy associated with multifocal central nervous system demyelination. Brain 1987: 110: 53-76.
11. MENDELL JR, KOLKINS , KISSELJT, WEIS KL, CHAKARES DW, RAMMOHAN KW. Evidence for central nervous system demyelination in chronic inflammatory demyelinating polyradiculoneuropathy. Neurology 1987: 37: 1291-1294.
401
Sindern et al. 12. TANEM, COHENAS, FRIESJ F etal. The 1982 revised criteria for the classification of systemic lupus erythematodes. Arthritis Rheum 1982: 25: 1271-1277. 13. MCCUNEWJ, MCGUIRE A, AISENA, GEBARSKI S. Identification of brain lesions in neuropsychiatric systemic lupus erythematosus by magnetic resonance scanning. Arthritis Rheum 1988: 31: 159-166. 14. RECHTHAND E, CORNBLATH DR, STERNBJ, MEYERHOFF JO. Chronic demyelinating polyneuropathy in systemic lupus erythematodes. Neurology 1984: 34: 1375-1457. 15. The Guillain-Barrt Syndrome Study Group. Plasmapheresis and acute Guillain-Barrt syndrome. Neurology (NY) 1985: 35: 1096-1 104.
16. KOSKICL, HUMPHREY R, SHINML. Anti-peripheral myelin antibody in patients with demyelinating neuropathy: Quantitative and kinetic determination of serum antibody by complement component 1 fixation. Proc Natl Acad Sci USA 1985: 82: 905-909. 17. KOSKICL, CHOUDKH, JUNGALAWA FB. Anti-peripheral nerve myelin antibodies in Guillain-Barrt syndrome bind a neutral glycolipid of peripheral myelin and cross-react with Forssman antigen. J Clin Invest 1989: 84: 280-287. 18. ENDOT, S c o r r DD, STEWART SS, KUNDUSK, MARCUS DM. Antibodies to glycosphingolipids in patients with multiple sclerosis and SLE. J Immunol 1984: 132: 1793-1797.
Acute symmetric dernyelinating polyneuropathy of the Guillain-Barre type is known in systemic lupus erythematosus (SLE).Chronic idiopathic demyelinating polyneuropathy (CIDP) has been reported rarely with SLE. A case is reported of CIDP accompaning SLE with autoantibodies against GM 1-and GM3-gangliosides.There was no historical evidence to suggest SLE, and CIDP was the first manifestation of SLE.The 38-year-old patient had elevated CSF-protein, slow nerve conduction velocities, sural nerve biopsy revealed mixed axon loss with demyelination and CIDP white matter lesions were observed in magnetic resonance imaging. the GMI-and GM3- autoantibodies may play a role in the pathogenesis of CIDP in SLE. The Guillain-Barrt syndrome (GBS) and the chronic type of idiopathic demyelinating polyradiculoneuropathy (CIDP) have similar clinical features. In GBS the clinical deficit reaches its maximum within 4 weeks. The minimal duration of progression for CIDP is 6 months (1). A common pathogenetic mechanism has been proposed for both. A humoral factor has been inferred, because serum from patients with both diseases may cause demyelination (2,3). Some patients with CIDP and GBS benefit from plasmapheresis (4).This indicates that circulating factors play a role in the pathogenesis of these diseases. Ilyas et al. ( 5 ) recently demonstrated antibodies to gangliosides in GBS. The occurrence of GBS and CIDP in association with autoimmune diseases has been reported (6). We report of a patient with autoantibodies against gangliosides, in whom CIDP was the first clinical manifestation of systemic lupus erythematosus (SLE). Material and methods
A 38-year-old man was admitted after a sevenmonth history of fatigue and malaise with a weight loss of 12 kg and fluctuating dysesthesia in hand and feet. Neurologic examination revealed a moderate proximal and distal weakness of all limbs. Pin prick
E. Sindern', E. Stark', J. Haas', A. J. Steck2 Department of ' Neurology and clinical Neurophysiology, Medical School of Hannover, Germany, Neurology, Centre Hospitalier Universitaire Vaudois, Lausanne, Switzerland
Key words: systemic lupus erythematosus; chronic inflammatory demyelinating polyradikuloneuropathy; antibodies to GM1 and GM3gangliosides
Eckhart Sindern, Department of Neurology and Clinical Neurophysiology, Medical School Hannover, Konstanty Gutschow Str. 8, 3000 Hannover 6 1, Germany Accepted for publication November 28, 1990
and touch sens tion was reduced with sock and glove distribution. Vibration and position sense were highly impaired in hands and feet. Deep tendon reflexes were absent. Ataxia of the limbs and trunk with a postural and intention tremor as well as a tremor of the head was prominent. Speech was dysarthric. Except from facial myokymia, cranial nerves were normal. A fixed malar rash was prominent. He had a pityriasis versicolor. Further general physical examination was normal. Serum routine studies, porphyrin-screening and cryoglobulins were negative. Antibodies against adeno-, entero-, cytomegalo-, herpes simplex-, varicella zoster-, polio-, HIV 1 or 2-virus, toxoplasma gondii and borrelia burgdorferi were not found. Serum IgM was raised to 6 g/1 with no evidence of monoclonal gammopathy. Haptoglobin, CRP, CH50 and C3 showed normal values. Complementfactor C4 was reduced to 0.19 g/l. Latex test was negative. Westergren erythrocyte sedimentation rate was 40/82. Antinuclear antibodies were positive up to 1 : 480 with a homogen pattern, anti ds-DNA 39 IE/ml, anti-Sm positive and anti-RNP negative. Examination of the cerebrospinal fluid revealed 3.3 cells/ul, mainly monocytes. The total protein was elevated to 490 mg/dl. IgG-index was normal. Identical oligoclonal IgG fractions were determined by isoelectric focussing in polyacrylamide gels. Median
399
Sindern et al.
and tibial distal motor latency were prolonged (43.4 msec and 63.6 msec); and nerve conduction velocities were slow (14m/sec and 16 m/sec), Fwave latency to m. adductor polticis brevis was abnormal (113 msec). Sural and median sensory potentials were absent. EMG revealed positive sharp waves in m. tibialis anterior. Motor unit potentials were polyphasic. MR-images of the head and the spinal cord revealed at T2-sequencies white matter lesions in the right parietal area, the brainstem and thoracal spinal cord. Steroid therapy was started with prednisone 100 mg/d for 2 weeks, with reduction 50 mg/d and 30 mg/d alternating. Strength and hypesthesia had improved, but 6 month later there was a relapsing deterioration. The patient was additionally treated with azathioprine 150mg/d and a moderate improvement was observed. Eight mont later the neurologic status deteriorated again, and there was a amelioration with cyclophosphamide 1000 mg monthly. No relapses were observed in the following 6 months. Now central nervous system symptoms like dysarthria, ataxia of the trunk, intention tremor of the limbs as well as tremor of the head are the prominent clinical features.
15 14
n
13 E
=
0
x -5 c
12
11 10
c
9 $ 8 .8 7
-
Q
0
6
5 4
3 2 1 n
Antibody assays and results
Serum was assayed for circulating antibodies to gangliosides G M l , asialo GM1, GDla, GDlb, GM2 and GM3 (Fidia Research Laboratories Abano Terme Italy) by an enzyme-linked immunosorbent assay method essentially as published (7). Minor modifications include assay at 4°C and coating of plates with 1 ug of gangliosides. A titer of up to 20 is within the range of normal control sera and encompasses two standard deviation above the mean. We found a titer of anti-GM1 antibodies of over 160, representing a significant elevation. Further examination of the pattern of serum anti-gangliosides antibody activity, revealed a predominant component to GM1, asialo GM1 and GM3 (Fig. 1). Discussion
The initial prominent manifestation of this patient was a symmetrical motor and sensory polyneuropathy with sensory ataxia and absent tendon reflexes. The patient fulfilled the criteria for diagnosis of CIDP (8). Other causes of neuropathy were absent. Clinical examination suggested further additional involvement of the central nervous system. Magnetic resonance imaging (MRI) revealed subcortical, brainstem and spinal cord white matter lesions. The observation of MRI “lesions” in CIDP is uncom400
Fig. I . Binding of the patient’s serum at a 1 : 10 dilution to different purified gangliosides as measured by ELISA, showing a significant reactivity to GM 1, asialo GM 1 and GM3 gangliosides.
mon (9). However, patients with CIDP associated with CNS disorder indistinguishable from multiple sclerosis (MS) showed MRI “lesions” typical of MS (10, 11). In our patient the condition developed into a definite SLE (12), in whom focal white matter lesions similair to those in MS were reported (13). The course has been relapsing-remitting (Fig. 2). Immunosuppressive therapy led to an improvement of peripheral neurological symptoms, but the central nervous system symptoms accelerated. The occurrence of CIDP in association with autoimmune diseases such as acute glomerulonephritis, Hashimotos thyreoiditis, multiple sclerosis and myasthenia gravis has been episodically reported. Korn-Lubetzki and Abramsky reported that 5 / 8 (63%) patients with CIDP and 5/58 (9%) patients with GB S had associated autoimmune diseases (6). Eight further definite or probable cases of SLE with CIDP have been reported (14). Including our case, 5 patients had a relapsing course, while the illness was monophasic with prolonged progression in the other 4. Eight CSF specimens demonstrated high protein content (122 to 535 mg/dl) without cells, in one patient the CSF was
CIDP, SLE & GM1-, GMIautoantibodies
remission relapse remission clinical course: relapse prednisone therapy : - prednisone azathioprine
relapse remission prednisone cyclophospharnide
t , , , , t , , , , , , , t , , , # ? , I
normal. The pathologic-morphologic basis of this syndrome does not seem uniform. In histologic studies of affected nerves in 3 patients, the primary pathology involved the myelin sheath with preservation of the axis cylinder, in 3 others, including our case, primary loss of axons respectively mixed axon loss with demyelination was found. A common mechanism may be the development of autoantibodies that either cross-react with or are directed against axon or myelin constituents. Humoral factors may play a major role in the pathogenesis of inflammatory demyelinating neuropathy. In some patients with GBS and CIDP plasma exchange has an ameliorating effect on neurologic dysfunction and nerve conduction velocity (4, 15). In animal models injected serum from patients with acute demyelinating neuropathy may cause demyelination (2, 3). Several autoantibodies to peripheral nerve structures have been found in inflammatory neuropathies. Koski et al. observed significantly high titers of anti-peripheral nerve myelin antibodies in sera from 11/12 patients with GBS and 3/4 with CIDP (16). Recently Koski et al. found that these antibodies bind a neutral glycolipid of peripheral myelin (17). Antibodies against gangliosides have been detected in relative high levels in 20% of GBS patients (5). Endo et al. detected antibodies against ganglioside GM 1 and asialo GM1 in 19/31 patients with SLE (18). The present case demonstrates very high titers of antibodies to GM1- and GM3-gangliosides in a patient with CIDP in SLE. These antibodies may represent an autoimmune response that may contribute to the neuropathology associated with these inflammatory diseases.
References 1 . DYCKPJ, LAISAC, OHTAM, BASTRON JA, OKAZAKIH, 2.
3.
4.
5.
6.
GROOVERRV. Chronic inflammatory polyradikuloneuropathy. Mayo Clinic Proceedings 1975: 50: 621-637. Low PA, SCHMELZER J, DYCKPJ, KELLYJJ Jr. Endoneurial effects of sera from patients with acute inflammatory polyradikuloneuropathy: electrophysiologic studies on normal and demyelinated rat nerves. Neurology 1982: 32: 720-724. HARRISON BM, HANSENLA, POLLARD JD, M c LEODJG. Demyelination induced by serum from patients with Guillain-Barrt syndrome. AM Neurol 1984: 15: 163-170. DYCK PJ, DAUBEJ, OBRIEN P, PINEDAA, Low PA, WINDEBANK AJ, SWANSON C. Plasma exchange in chronic inflammatory demyelinating polyradikuloneuropathy. N Engl J Med 1986: 14: 461-465. ILYASAA, WILLISON HJ, QUARLES RH, JUNGALAWA FB, CORNBLATH DR, TRAPPED, GRIFFINJW, M c KHANN GM. Serum antibodies to gangliosides in Guillain-Barrt syndrome. Ann Neurol 1988: 23: 440-447. KORN-LUBETZKI I, ABRAMSKY0. Acute and chronic demyelinating inflammatory polyradiculoneuropathy. Association with autoimmune diseases and lymphocyte response to human neuritogenic protein. Arch Neurol 1986: 43:
604-608. 7. BOLLENSEN E, SCHIPPERHI, STECKAJ. Motor neuropathy with activity of monoclonal IgM antibody to G D l a ganglioside. J Neurol 1989: 236: 353-355. 8. DYCKPJ, ARNASON GBW. Chronic inflammatory demyeli-
nating polyradiculoneuropathy. In: DYCKPJ, THOMAS PK, LAMBERTEH, BUNGE R (Eds.). Peripheral neuropathy. Philadelphia: WB Saunders, 1975: 1012-1019. 9. FEASBYTE, HAHNAF, KOOPMAN WJ, LEE DH. Central lesions in chronic inflammatory demyelinating polyneuropathy: an MRI study. Neurology 1990: 40: 476-478. 10. THOMAS PK, WALKERRWH, RUDGEP etal. Chronic demyelinating peripheral neuropathy associated with multifocal central nervous system demyelination. Brain 1987: 110: 53-76.
11. MENDELL JR, KOLKINS , KISSELJT, WEIS KL, CHAKARES DW, RAMMOHAN KW. Evidence for central nervous system demyelination in chronic inflammatory demyelinating polyradiculoneuropathy. Neurology 1987: 37: 1291-1294.
401
Sindern et al. 12. TANEM, COHENAS, FRIESJ F etal. The 1982 revised criteria for the classification of systemic lupus erythematodes. Arthritis Rheum 1982: 25: 1271-1277. 13. MCCUNEWJ, MCGUIRE A, AISENA, GEBARSKI S. Identification of brain lesions in neuropsychiatric systemic lupus erythematosus by magnetic resonance scanning. Arthritis Rheum 1988: 31: 159-166. 14. RECHTHAND E, CORNBLATH DR, STERNBJ, MEYERHOFF JO. Chronic demyelinating polyneuropathy in systemic lupus erythematodes. Neurology 1984: 34: 1375-1457. 15. The Guillain-Barrt Syndrome Study Group. Plasmapheresis and acute Guillain-Barrt syndrome. Neurology (NY) 1985: 35: 1096-1 104.
16. KOSKICL, HUMPHREY R, SHINML. Anti-peripheral myelin antibody in patients with demyelinating neuropathy: Quantitative and kinetic determination of serum antibody by complement component 1 fixation. Proc Natl Acad Sci USA 1985: 82: 905-909. 17. KOSKICL, CHOUDKH, JUNGALAWA FB. Anti-peripheral nerve myelin antibodies in Guillain-Barrt syndrome bind a neutral glycolipid of peripheral myelin and cross-react with Forssman antigen. J Clin Invest 1989: 84: 280-287. 18. ENDOT, S c o r r DD, STEWART SS, KUNDUSK, MARCUS DM. Antibodies to glycosphingolipids in patients with multiple sclerosis and SLE. J Immunol 1984: 132: 1793-1797.
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