SJOGREN'S SYNDROME: A STUDY OF ITS NEUROLOGICAL COMPLICATIONS
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1 British Journal of Rheumatology 988;27: SJOGREN'S SYNDROME: A STUDY OF ITS NEUROLOGICAL COMPLICATIONS BY A. BINDER, M. L. SNAITH AND D. ISENBERG The Bloomsbury Rheumatology Department, University College and Middlesex Hospitals, London. SUMMARY A detailed retrospective study of 05 patients with Sj6gren's syndrome (50 primary and 55 secondary cases), showed that had vasculitis and 8 had neurological abnormalities which after full investigation were not attributable to other causes. Most of the neurological symptoms were mild and when found in patients with secondary Sjogren's syndrome were more characteristic of the underlying autoimmune rheumatic disease. We found no significant association between the frequency of either vasculitis or any autoantibodies and the presence of neurological disease, but did confirm a significant association between vasculitis and the presence of antibodies to extractable nuclear antigens. We therefore question whether severe and relapsing neurological disease is common in patients with SjSgren's syndrome KEY WORDS: Sjogren's syndrome, CNS disease. THERE have been many sporadic reports of neurological lesions which have developed in patients with Sjogren's syndrome (SS) occurring as a primary disorder or when complicating rheumatoid arthritis (), systemic lupus erythematosus () or other autoimmune rheumatic disease (ARD) [-8]. Kaltreider and Talal [9] noted a mild peripheral neuropathy in 0 patients with SS, four also having trigeminal neuralgia. As nine of these 0 patients had cutaneous vasculitis, they questioned its pathogenetic significance. Steinberg et al. [0], Peyronnard et al. [] and Pavlidis et al. [2] also reported evidence of vasculitis in a few patients with SS who had serious neurological lesions. The Baltimore group has recently emphasized the frequency and severity of neurological abnormalities in their patients with SS, with involvement of the central nervous system (CNS) [-8] and peripheral nervous system (PNS) [, 4, 6-8], sometimes with prominent neuropsychiatric features [9]. Some patients showed a relapsing course with a cumulative neurological deficit which was indistinguishable from multiple sclerosis [20]. As so many of their patients with neurological lesions also had vasculitis [-2], they felt the vasculitis was causative, with the anti-ro (SSA) antibody showing increased frequency [22] in the subset of patients most at risk for the neurological disease. Our impressions in the Bloomsbury Rheumatol- Submitted 26 August; accepted December 987. Correspondence to: Dr. Allan Binder, The Bloomsbury Rheumatology Department, Arthur Stanley House, Tottenham Street, London WP9PG. 275 ogy Department, London did not seem to support the data from Baltimore in terms of the frequency or severity of neurological abnormalities in SS. We therefore undertook a retrospective review of the case records of the primary and secondary patients with SS seen in the rheumatology department over the previous 4 years. PATIENTS AND METHOD All patients seen in the rheumatology department were entered into a diagnostic index and those seen between 982 and 985 with features of Sjogren's syndrome were chosen for more detailed consideration in the present study. For primary SS, patients had to be symptomatic for the sicca complex of xerostomia, xerophthalmia or recurrent parotitis. Furthermore, they also had to have at least two of the following:. a positive Schirmer's test (less than 5 mm of filter paper moistening in 5 min), 2. keratoconjunctivitis sicca on Rose-Bengal testing [2] or,. a positive (grade or 4) labial (minor salivary gland biopsy [24]. Those patients who in addition met the recognized criteria for another ARD such as [25], [26], mixed connective tissue disease (MCTD) [27], scleroderma [28] or polymyositis [29] were termed secondary SS. As so many of the latter patients had, this group (-SS) was distinguished from the other ARD (ARD- SS). For entry into the study, patients also required adequate documentation over a minimum period of year. Of 0 patients' records, Downloaded from at Pennsylvania State University on May 0, 206
2 276 BRITISH JOURNAL OF RHEUMATOLOGY VOL. XXVII NO. 4 six failed to satisfy the entrance criteria and 25 had insufficient data or inadequate duration of follow-up and were excluded. One hundred and five patients were included in the study50 with primary SS, 0 with -SS and 25 with ARD-SS. The ARD-SS group included 8 patients with, four with MCTD, two with polymyositis and one with scleroderma. Six patients had died by the time the survey was performed, two from acute myocardial infarction, two from Hodgkin's disease and one each from T-cell lymphoma and amyloid induced renal disease. The case records of the patients included in the study were reviewed for evidence of vasculitis and in particular, confirmation of this on biopsy or by a dermatological opinion. Similarly, neurological lesions were also sought with any neurological investigations and opinions. The results of immunological tests were also noted, namely the rheumatoid factor (RF), antinuclear antibody (ANA) titre and the presence of antibodies to extractable nuclear antigen (ENA). Where the anti-ro (SSA) and anti-la (SSB) had been identified, this was also noted. Contingency table analysis with Yates' correction (chi squared) was used for statistical evaluation. RESULTS Of the 05 patients in the study, only six were male and six (all secondary SS cases) were black. The median (and range) of sicca symptoms was 7 years in the primary (-2) and -SS (-22) groups and.5 years (-2) in the ARD-SS group. Eighty-nine patients had undergone labial biopsy and in only three cases had this failed to confirm the diagnosis. A rash considered by the rheumatologist to be vasculitic in nature was noted in patients during the period of follow-up with primary SS (26%), four with -SS (5%) and 4 with ARD-SS (56%). In 2 patients the macular or maculopapular rash was biopsied and confirmed cutaneous vasculitis. Nine other patients had lesions largely confined to the fingers and toes which were not amenable to biopsy. In these and four other cases with a purpuric rash over the shins, a dermatological opinion was sought and the rash was considered to be vasculitic. Two other patients had livedo reticularis, two macular eruptions and one patient had leg ulcers which were also accepted as being vasculitic. One other patient developed proteinuria, renal failure, hyperglobulinaemia (IgM) and hyperviscosity syndrome soon after the onset of sicca symptoms and diplopia. A renal biopsy unexpectedly showed evidence of vasculitis. Unexplained neurological symptoms were documented in 8 patients (Table I), being referred to a neurologist for detailed investigation and follow-up. Only the six patients with carpal tunnel syndrome () and one with trigeminal neuralgia which resolved rapidly on carbamazepine were not assessed by the neurologist, although five of the six lesions were confirmed by EMG studies. The details of the 8 patients are summarized in Table II. In five patients, transient cerebral events were documented. Two patients had EEG-proven TABLE I NEUROLOGICAL ABNORMALITIES IN SJOGREN'S PATIENTS WITH NO OTHER OBVIOUS CAUSE Cerebral Widespread dysfunction Transient dysfunction Cerebral haemorrhage Brain stem Diplopia (intcmuclcar ophthalmoplcgia) Spinal cord Dysaesthesiae and neurogeme bladder Peripheral nervous system Symmetrical sensory neuropathy Carpal tunnel syndrome Trigeminal neuralgia Atypical facial pain Ptosis Ulnar neuropathy (n = 7)' -SS (" = 5)* ARD-SS Scleroderma (n = )* Downloaded from at Pennsylvania State University on May 0, 206 * Some patients showed more than one abnormality.
3 Patient 79CF 2 62CF 50IF 4 42CF 5 0WIF 6 5CF 7 26CF 8 7ICF 9 76CF 0 74CF 82CF 2 54CF 58CF 4 68CM 5 27CF 6 40WIF 7 2WIF 8 6CF SjOgrcn's type Scleroderma Vasculitic features Digital nodules Lower limb purpura Renal vasculitis Lower limb purpura Macular Papular and digital ulcers TABLE II SUMMARY OF THE8 SJOGREN'S PATIENTS wrra NEUROLOGICAL LESIONS Central nervous system lesions 5 grand mal seizures Vertigo lasting 6 months Transient unconsciousness Diplopia (internuclcar ophthalmoplegia) Depersonalization Mood change Diplopia Dysacsthesiae Bladder dysfunction Cerebral haemorrhage grand mal seizures Digital ulcers Transient ischaemic attacks over months Peripheral nervous system lesions Trigeminal neuralgia Atypical facial pain Ptosis Proptosis Ulnar neuropathy RF Antibody profile ANA ENA SSA SSB SSA SSB neg SSA SSB Other tests Hyperglobulinaemia EMG normal CT scan and EMG normal, EEG abnormal EMG neuropathic CT scan normal Hyperviscosily Hyperglobulinaemia Hyperglobulinaemia Cryoglobulinaemia EEGdiffuse abnormality CT scan normal CT scan proven CT scan and EEG normal CT scan normal, lesions Outcome of neurological lesions with steroids in 2 years with steroids with steroid injection after 6 episodes with steroid injection with steroid injection Improved with steroids and plasmapheresis in 6 months with steroids Relapsing course Residual hcmiplcgia ; transposed ulnar nerve C, Caucasian; I, Indian; WI, West Indian; F, female; M, male;, carpal tunnel syndrome; RF, rheumatoid factor; ANA, antinuclear antibody; ENA, extractable nuclear antigen. m at Pennsylvania State University on May 0, 206 CD Z m?o f*i 'y rn C?O D \^ Q^^ (j r o 2 L O sioila in ^* LJ tn z in D JO oo m
4 278 BRITISH JOURNAL OF RHEUMATOLOGY VOL. XXVII NO. 4 gtand mal epileptic seizures which resolved on therapy and did not recur when therapy was withdrawn 6 months after the last fit. CT brain scans revealed no abnormalities. Transient ischaemic attacks, vertigo and repeated episodes of transient loss of consciousness affected three other patients, but again no cause was discovered after repeated neurological investigation. In all these cases, the symptoms disappeared without residual disability, although the vertigo lasted for 8 months before resolution. One patient with severe (case 5), showed a relapsing course with episodes of cerebral, spinal and peripheral nervous system dysfunction. The major features during the periods of active disease were mood alterations, feeling of depersonalization, dysaesthesiae and transient areflexia. Ptosis, diplopia and bladder dysfunction showed only partial recovery between the acute episodes. One other patient (case 6) suffered an intracerebral haemorrhage, confirmed on CT brain scan, which resulted in a residual hemiplegia. Four patients developed a mild symmetrical sensory neuropathy, in two cases associated with hyperglobulinaemia and in one patient a purpuric rash on the lower limbs. The neuropathy resolved in all of these patients, although three required systemic corticosteroids and symptoms often persisted for prolonged periods (up to 2 years). A carpal tunnel syndrome () developed in seven cases, three having. Trigeminal neuralgia, atypical facial pain, diplopia and ulnar neuropathy also occurred. Only seven of the 8 patients (9%) with neurological lesions had evidence of vasculitis, compared with 24 of the 87 (28%) without neurological disease, the difference not reaching significance. The RF was measured in 0 patients and ANA in 02 cases with a titre equal to or greater than /40 being considered positive. A positive RF was found in 50% of patients with and 48% without neurological disease, the difference not being significant. The ANA was positive in 6 % with and 5% without neurological lesions (not significant). Antibodies to EN A were also documented in 89 cases, being found in 28% with and 2% without neurological symptoms, the difference as with RF and ANA again failing to reach significance. The only association which reached significance was the presence of vasculitis and a positive ENA. With vasculitis, 6 of 0 patients (5%) were ENA positive, compared with nine of 6 (5%) without vasculitis, the difference being significant (x 2 =.5, p < 0.00). The SSA antibody was found in six patients in each group and SSB in nine patients with and five without vasculitis. DISCUSSION While neurological abnormalities not attributable to other causes were found in 7% of our Sjogren's patients which was similar to the Baltimore group [, 6], the abnormalities were usually mild and self-limited. Furthermore, many of the lesions developed in patients with secondary SS and were recognized complications of the underlying ARE). Both the patient with relapsing disease and the patient with a cerebral haemorrhage suffered from severe and only mild SS and their neurological lesions were more typical of the [0, ]. Four of the seven cases with carpal tunnel syndrome occurred secondary to (three cases) or scleroderma and this commonly occurs in these conditions even in the absence of SS. While vasculitis was more common in patients with neurological lesions, this difference was not significant when compared to those without the neurological features. Furthermore, five of the seven patients with vasculitis and neurological disease had an underlying ARD which could also have been the cause of their vasculitis. We have confirmed an association between vasculitis and an antibody to ENA, but unlike Alexander et al. [22] the antibody to SSB was more often found than the antibody to SSA. Whilst there may be problems with retrospective assessments, our patients with SS have been carefully documented over several years, many having attended a special clinic for follow-up and it is unlikely that significant vasculitis or neurological lesions went unnoticed. Furthermore, where abnormalities did develop they were refered to the relevant specialists for an opinion and detailed investigation. Many of the lesions reported from Baltimore were severe and recurrent, leading to serious disability [-20]. One difference in the patient populations in Baltimore and London was a higher incidence of black patients in Baltimore. Furthermore, the generally recognized interest in the neurological complications of SS in Baltimore may also have biased this feature in their SS population. We therefore question the frequency of serious and progressive neurological lesions in SS. In patients with secondary SS we found it impossible to ascertain whether the lesion was due to the SS or the underlying ARD. Downloaded from at Pennsylvania State University on May 0, 206
5 BINDER ETAL.: NEUROLOGICAL COMPLICATIONS IN SJOGREN'S SYNDROME 279 REFERENCES. Sheldon JH. Sjogren's syndrome associated with pigmentation and scleroderma of the legs. Proc R Soc Med 99;2: Weber FP. Sjogren's syndrome, especially its non-ocular features. Br J Ophthalmol 945; 29: Coverdale H. Some unusual cases of Sjogren's syndrome. BrJ Ophthalmol 948,2: Heaton JM. Sjogren's syndrome and systemic lupus erythematosus. Br Med J 959;: Whitehouse AC, Buckley CE, Nagayu H, McCarter J. Macroglobulinemia and vasculitis in Sjogren's syndrome. Experimental observations relating to pathogenesis. Am J Med 967;4: Massey EW. Sjogren's syndrome and mononeuritis multiplex. Ann Intern Med 980;92: Hull RG, Morgan SH, Harding AE, Hughes GR. Sjogren's syndrome presenting as severe sensory neuropathy including involvement of the trigmeninal nerve. BrJ Rheumatol 984;2: De La Monte SM, Hutchins GM, Gupta PK. Aseptic meningitis, trimethoprim and Sjogren's syndrome. JAMA 985;25: Kaltreider HB, Talal N. The neuropathy of Sjogren's syndrome. Trigeminal nerve involvement. Ann Intern Med 969;70: Steinberg AD, Green WT, Talal N. Thrombotic thrombocytopenic purpura complicating Sjogren's syndrome. JAMA 97;2: Peyronnard JM, Charron L, Beaudet F, Couture F Vasculitic neuropathy in rheumatoid arthritis and Sjogren's syndrome. Neurology (NY) 982;2:8SM5. 2. Pavlidis NA, Karsh J, Moutsopoulos HM. The clinical picture of primary Sjogren's syndrome. A retrospective study. J Rheumatol 982;9: Alexander GE, Provost TT, Stevens MB, Alexander EL. Sjogren's syndrome. Central nervous system manifestations. Neurology (NY) 98;: Alexander EL, Provost TT, Stevens MB, Alexander GE. Neurological complications of primary Sjogren's syndrome. Medicine 982; 6: Alexander EL, Alexander GE. Recurrent aseptic meningoencephalitis in primary SjogTen's syndrome. Neurology (NY) 98; : Molina R, Provost TT, Alexander EL. Peripheral inflammatory vascular disease in Sjogren's syndrome. Association with nervous system complications. Arthritis Rheum 985;28: Molina R, Provost TT, Alexander EL. Two types of inflammatory vascular disease in Sjogren's syndrome. Differential association with seroreactivity to rheumatoid factor and antibodies to Ro(SSA) and with hypocomplementemia. Arthritis Rheum 985;28: Molina R, Provost TT, Arnett FC, et al. Sjogren's syndrome in men. Clinical, serologic and immunogenetic features.,4m / Me<U986;80: Malinow KL, Molina R, Gordon B, Seines OA, Provost TT, Alexander EL. Neuropsychiatric dysfunction in primary Sjfigren's syndrome. Ann Intern Med 985;0: Alexander EL, Malinow KL, Lejewski JE, Jerdan MS, Provost TT, Alexander GE. Sjogren's syndrome with central nervous system disease mimicking multiple sclerosis. Ann Intern Med 986;04: Alexander EL, Provost TT. Cutaneous manifestations of primary Sjogren's syndrome. A reflection of vasculitis and association with anti-ro(ssa) antibodies. J Invest Dermatol 98;80: Alexander EL, Arnett FC, Provost TT, Stevens MB. Sjogren's syndrome: association of anti-ro(ssa) antibodies with vasculitis, hematologic abnormalities and serologic hyperreactivity. Ann Intern Med 98;98: Holm S. Keratoconjunctivitis sicca and the sicca syndrome. Ada Ophthalmol (Suppl) 949;: Chisholm DM, Mason DK. Labial salivary gland biopsy in Sjogren's disease. J Clin Pathol 968;2: Ropes MW, Bennett GA, Cobb S, Jacox R, Jessar. 958 revision of diagnostic criteria for rheumatoid arthritis. Bull Rheum Dis 958;9: Tan EM, Cohen AS, Fries JF, et al. The 982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 982;25: Sharp GC, Irvin WS, Tan EM, Gould RG, Holman HR. Mixed connective tissue diseasean apparently distinct rheumatic disease syndrome associated with a specific antibody to an extractable nuclear antigen (ENA). Am J Med 972;52: Subcommittee for scleroderma criteria of the American Rheumatism Association Diagnostic and Therapeutic Criteria Committee. Preliminary criteria for the classification of systemic sclerosis (scleroderma). Arthritis Rheum 980;2: Bohan A, Peters JB. Polymyositis and dermatomyositis. N Engl J Med 980;292:44-7. Downloaded from at Pennsylvania State University on May 0, 206
6 280 BRITISH JOURNAL OF RHEUMATOLOGY VOL. XXVII NO Johnson RT, Richardson EP. The neurological. Ellis SG, Verity MA. Central nervous system manifestations of systemic lupus ery- involvement in systemic lupus erythematosus. A clinico-pathological study of thematosus: a review of neuropathological 24 cases and review of the literature. findings in 57 cases, Arthritis Medicine 968;47:7-64. Rheum 979;8:22-2. NOTICES INTERNATIONAL MEETING ON LUPUS NEPHRITIS Date: Thursday, 20 October 988. Venue: University and Middlesex School of Medicine, Middlesex Hospital. Speakers to include: Stewart Cameron, Dan Eilat, Philip Hodemaeker, Graham Hughes, Alfred Steinberg, David Turner, Mark Walport, Gwyn Williams. Further information: Dr. D. Isenberg or Dr. M. Snaith, Bloomsbury Rheumatology Unit, Arthur Stanley House, Tottenham Street, London WP 9PG. Tel.: (0) FOURTH INTERNATIONAL CONFERENCE OF THE INFLAMMATION RESEARCH ASSOCIATION Dates: 2-27 October 988. Venue: Pocono Hershey Resort, White Haven, PA, USA. Symposium topics include: Cytokines; Autoimmunity; Arachidonic acid in the inflammatory process; Comparative roles of leukotrienes and PAF in non-rheumatic diseases; Drugs for arthritis. Further information: Inflammation Research Association Conference, Marcia L. Bliven, Registrar, Pfizer Central Research, Eastern Point Road, Groton, CT 0640, USA. Telex: ITT. Tele-fax: INTERNATIONAL CONFERENCE ON BEHCETS DISEASE Dates: 4-5 September 989. Venue: Mayo Clinic, Rochester, Minnesota, USA. Further information: Mr. W. Nietz, Continuing Education, Mayo Clinic, Rochester, Minnesota 55905, USA. Tel.: (507) SECOND INTERNATIONAL CONFERENCE ON SYSTEMIC LUPUS ERYTHEMATOSUS Dates: 26-0 November 989. Venue: Singapore. Meeting will combine clinical and scientific plenary sessions, seminars and free papers. Further information: Dr. P. Feng, c/o Department of Medicine IV, Tang Tock Seng Hospital, Moulmein Road, Singapore 0. Tel.: (65) Telex: RS 9675 TTSH. Downloaded from at Pennsylvania State University on May 0, 206
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