Acute Motor-dominant Polyneuropathy as Guillain-Barré Syndrome and Multiple Mononeuropathies in a Patient with Sjögren s Syndrome
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1 CASE REPORT Acute Motor-dominant Polyneuropathy as Guillain-Barré Syndrome and Multiple Mononeuropathies in a Patient with Sjögren s Syndrome Kenichiro Tanaka 1, Hiroyuki Nakayasu 1, Yutaka Suto 1, Shotaro Takahashi 1, Yoshihiro Konishi 2, Hirotake Nishimura 3,RinoUeno 4, Susumu Kusunoki 4 and Kenji Nakashima 5 Abstract A patient with xerostomia and xerophthalmia due to Sjögren s syndrome presented with acute motordominant polyneuropathy and multiple mononeuropathy with antiganglioside antibodies. Nerve conduction studies and a sural nerve biopsy revealed the neuropathy as a mixture of segmental demyelination and axonal degeneration. Positive results were obtained for several antiganglioside antibodies. Corticosteroid treatment proved effective. The neuropathy was considered to represent a mixture of polyneuropathy as Guillain-Barré syndrome and multiple mononeuropathy via Sjögren s syndrome. We speculate that Guillain-Barré syndrome occurred in the patient and Guillain-Barré syndrome itself activated multiple mononeuropathy via Sjögren s syndrome. Key words: Sjögren s syndrome, Guillain-Barré syndrome, antiganglioside antibody () () Introduction Sjögren s syndrome (SS) is an autoimmune disorder and occasionally manifests with neurological complications. Approximately 10-25% of patients with SS experience neurological complications (1), most frequently as peripheral neuropathy. Peripheral neuropathy occurs in 10-20% of patients with SS (2). Peripheral neuropathy associated with SS appears in various forms, such as sensory neuropathy (sensory ataxic neuropathy, painful sensory neuropathy without sensory ataxia), multiple mononeuropathy, cranial neuropathy (multiple cranial neuropathy, trigeminal neuropathy), autonomic neuropathy, and radiculoneuropathy (3, 4). In multiple mononeuropathy, both large and small myelinated fibers are markedly depleted with prominent active axonal degeneration in the sural nerves, and perivascular cellular invasion is frequently observed, indicating the occurrence of vasculitis. Regarding other autoimmune neuropathies, recent studies have demonstrated that antiganglioside antibodies play an important role in the pathogenesis of autoimmune peripheral neuropathies such as Guillain-Barré syndrome (GBS) (5). We herein report a case of SS showing acute motordominant demyelinating and axonal neuropathy with several antiganglioside antibodies (GD1a IgG, GD1b IgG, GT1b IgG), as GBS. Case Report A 57-year-old Japanese man who had been well and on no medications noticed weakness in the lower extremities and right facial palsy. These symptoms progressed and he also felt weakness in the upper extremities after two days. Department of Neurology, Tottori Prefectural Central Hospital, Japan, Department of Clinical Research, Tottori Medical Center, Japan, Department of Pathology, Faculty of Medicine, Kawasaki University, Japan, Department of Neurology, Kinki University Faculty of Medicine, Japan and Division of Neurology, Department of Brain and Neurosciences, Faculty of Medicine, Tottori University, Japan Received for publication November 22, 2015; Accepted for publication January 29, 2016 Correspondence to Dr. Kenichiro Tanaka, tanakaken@pref.tottori.jp 2717
2 Table 1. Nerve Conduction Study. Day 2 Day 21 Day 43 Normal range Left median DL (ms) ~4.0 CMAP (mv) ~18.0 MCV (m/s) ~63.0 SNAP ( V) ND ~60.0 SCV (m/s) ND ~70.0 F-waves Lat (ms) ND ~27.5 F-waves Vel (m/s) ND ~68.0 F-waves Occur (%) 0% 81% 38% >60% Right median DL (ms) ~4.0 CMAP (mv) ~18.0 MCV (m/s) ~63.0 SNAP ( V) ~60.0 SCV (m/s) ~70.0 F-waves Lat (ms) ~27.5 F-waves Vel (m/s) ~68.0 F-waves Occur (%) 25% 50% 63% >60% Left tibial DL (ms) ~6.0 CMAP (mv) ~25.0 MCV (m/s) ~52.0 F-waves Lat (ms) ND ND ND 42.5~50.0 F-waves Vel (m/s) ND ND ND 45.0~57.0 F-waves Occur (%) 0% 0% 0% 100% Right tibial DL (ms) ~6.0 CMAP (mv) ~25.0 MCV (m/s) ~52.0 F-waves Lat (ms) ND ~50.0 F-waves Vel (m/s) ND ~57.0 F-waves Occur (%) 0% 19% 25% 100% Left sural SNAP ( V) ND 1.7 ND (biopsy) 5.0~30.0 SCV (m/s) ND 38.7 ND (biopsy) 45.0~60.0 Right sural SNAP ( V) ~30.0 SCV (m/s) ~60.0 DL: distal latency, CMAP: compound muscle action potential, MCV: muscle nerve conduction velocity, SNAP: Sensory nerve action potential, SCV: sensory nerve conduction velocity, Lat: latency, Vel: velocity, Occur: occurrence He presented to the emergency room with quadriplegia and facial palsy and was admitted to our hospital (Tottori Prefectural Central Hospital). He had experienced diarrhea starting 6 days previously. On neurological examination, his consciousness was alert. He had right peripheral facial nerve palsy, distal-dominant quadriparesis with hyperreflexia, and constipation. We evaluated the quadriparesis using Manual Muscle testing, which revealed the following results: deltoid, 5/5; biceps, 5/5; triceps, 5/5; wrist extensor, 4/3; wrist flexor, 4/3; iliopsoas, 5/ 5; quadriceps, 5/5; hamstrings, 5/4-; tibialis anterior, 3+/5; and gastrocnemius, 3+/4. His grip strength was 1 kg/0 kg. Sensory disturbance was not clear, and other neurological functions were normal. Electrophysiological studies showed delayed motor conduction velocities with a very low amplitude for compound muscle action potential (CMAP) and elongated distal latency. F-waves were almost undetectable. Sensory conduction velocities were also delayed and a low amplitude for sensory nerve action potential (SNAP) was observed (Table 1). His neuropathy was classified as acute inflammatory demyelination polyneuropathy (AIDP) according to Ho s criteria (6). The initial cerebrospinal fluid analysis showed the following findings: protein, 35 mg/dl; no white blood cells; and immunoglobulin (Ig) G index, Serum studies showed positive results for several antiganglioside antibodies (Table 2). The complete blood cell count, the erythrocyte sedimentation rate, and levels of C-reactive protein, electrolytes, hepatic and renal function, and vitamins were normal. Sinus rhythm was seen on electrocardiography and the vital capacity was normal. Magnetic resonance imaging (MRI) of the brain and spinal cord showed normal images. According to these findings, we diagnosed the patient with GBS and administered intravenous Ig (IVIG) at 0.4 g/ kg/day for 5 days. Hyperreflexia gradually turned into hyporeflexia and deep sensation disturbance appeared thereafter, however, the progression of quadriplegia stopped on day 5. Nerve conduction studies on day 21 showed a partial improvement of distal latencies, amplitude, and nerve conduction velocities. However, his right peripheral facial nerve palsy continued to worsen. Dysphagia and trachyphonia by left-dominant bilateral recurrent nerve paralysis subsequently occurred. Although IVIG was again administered from day 20 to day 24, cranial nerve paralysis was not improved. The patient was unable to take meals orally, thus he was fed via a tube. We again examined the patient in detail to reconsider the diagnosis. Results for autoimmune antibodies are shown in 2718
3 Table 2. Autoimmune Antibodies. Anti-nuclear antibody SS-A antibody SS-B antibody Anti-DNA antibody TPO antibody Tg antibody TSAb Microsome test Thyroid test CCP antibody c-anca p-anca RNP antibody SCL70 antibody APL antibody ACE AQP4 antibody U/mL 2.4 U/mL (-) 38.1 IU/mL IU/mL 129% U/mL 1.7 IU/mL 0.7 IU/mL 0.5 U/mL <0.5 U/mL 10 U/mL 3.9 IU/L (-) Anti-ganglioside antibodies (IgG) GD1a antibody GD1b antibody GT1b antibody GM1, GM2, GM3, GD3, GQ1b Gal-C, GalNAc-GD1a antibody (+++) (+) (+) All (-) SS-A: Sjögren syndrome A, SS-B: Sjögren syndrome B, TPO: anti-thyroid peroxidase, Tg: thyroglobulin, TSAb: thyroid-stimulating antibody, CCP: cyclic citrullinated peptide, c-anca: cytosolic anti-neutrophilic cytoplasmic antibody, p-anca: perinuclear anti-neutrophilic cytoplasmic antibody, RNP: ribonuclear protein, SCL70: anti-topoisomerase, APL: antiphospholipid, ACE: angiotensin-converting enzyme, AQP4: aquaporin 4 A B 200 m 50 m Figure 1. A salivary gland biopsied from the lip shows periductal lymphocytic infiltration with more than 1 focus per 4 mm 2. Sialadenitis fulfilled the diagnostic criteria of primary SS (A: 100 ; B: 400 ). Table 2. Negative results were seen for herpes simplex virus (HSV), varicella zoster virus (VZV), Epstein-Barr virus (EBV), and cytomegalovirus (CMV). Negative results were also obtained for Campylobacter jejuni in a fecal culture. Schirmer s test yielded positive results (right: impossible to estimate with peripheral facial nerve palsy; left: 1 mm/5 minutes) and a salivary gland biopsy showed sialadenitis (Fig. 1: >1 focus/4 mm 2 ). As the patient had felt xerostomia and xerophthalmia before peripheral neuropathy, we diagnosed him with SS. The diagnostic criteria for primary SS were fulfilled (7). In addition, asymptomatic chronic thyroiditis was identified. A histopathological examination of a sural nerve biopsy showed no clear lymphocytic infiltration, and variable severity of myelinated fiber loss in each bundle was observed in axial sections (Fig. 2). A teased fiber analysis also showed segmental demyelination and axonal degen- 2719
4 A B 100 m C 20 m 40 m Figure 2. A sural nerve biopsy (axial section) shows no clear lymphocytic infiltration and variable severity of myelinated fiber loss in each bundle in axial sections (A, B: toluidine blue-stained 1 μm section; C: Hematoxylin and Eosin staining section) (A: 40 ; B: 200 ; C: 100 ). A B 50 m 50 m Figure 3. A teased fiber analysis shows segmental demyelination (A) and axonal degeneration (B) (fixed in glutaraldehyde and osmium tetroxide, lying in a pool of glycerin) (normal: segmental demyelination: axonal degeneration=63.7%: 20.8%: 15.4%) (A, B: 200 ). eration (normal : segmental demyelination : axonal degeneration = 63.7% : 20.8% : 15.4%) (Fig. 3). We considered the neuropathy to be related to SS and subsequently initiated methylprednisolone pulse therapy (1 g/day) from days 33 to 35 and from days 40 to 42. A relatively early improvement was seen, and he regained the ability to walk with assistance and ingest food orally. Furthermore, hyporeflexia, deep sensation disturbance, xerostomia and xerophthalmia gradually improved. An electrophysiological study also showed an improvement in the neuropathy (Table 1). We then administered oral prednisolone (60 mg/day), which was maintained for almost a month during rehabilitation. SS-A antibody, anti-thyroid peroxidase antibody, anti-thyroglobulin antibody, and antiganglioside antibodies became negative after these treatments. He was subsequently transferred to a rehabilitation unit at Tottori Medi- 2720
5 cal Center on day 62, and oral prednisolone was gradually tapered while rehabilitation continued. His symptoms improved slowly, and he was treated with low-dose prednisolone (10 mg/day) over half a year without relapse. The patient can now eat a regular diet by himself and walk using a walker. Furthermore, he no longer exhibits xerostomia or xerophthalmia. Discussion We encountered a case of acute motor-dominant motor and sensory neuropathy related to antiganglioside antibody in the presence of SS. The neurological examination showed distal-dominant tetraparesis with sensory disturbance and cranial nerve palsy, and the laterality of muscle weakness indicated that the neuropathy represented a mixture of polyneuropathy and multiple mononeuropathy. Regarding the electrophysiological study, the first study showed delayed nerve conduction velocity, prolonged terminal latencies, and very low CMAP, indicating segmental demyelination and axonal degeneration. The very low detection of F-waves might have indicated radiculoneuropathy. The pathology of the sural nerve indicated a mixture of segmental demyelination and axonal degeneration, with segmental demyelination more dominant than axonal degeneration in the teased fiber analysis. We could not find any direct findings of vasculitis in the sural nerve, however, the variable severity in each nerve bundle suggested the presence of vasculitis (8). The neuropathy showed the following specific characteristics. The phases of progression of quadriplegia and cranial neuropathy were not parallel. From the very early stage, nerve conduction studies showed severe conduction delay and lowamplitude CMAP. Deep tendon reflexes were also partly exaggerated in the early stage. We considered the presence of antiganglioside antibodies and SS to be very important factors in the consideration of his pathophysiology. First, we evaluated the pathophysiology from the presence of antiganglioside antibody. Each antiganglioside antibody is reportedly related to different clinical features. Regarding the antiganglioside antibodies detected in our patient, anti-gd1a antibody is considered to be related to axonal degeneration, facial palsy, and hyperreflexia (9, 10). Anti-GD1b antibody is related to segmental demyelination, although anti-gt1b antibody has not been reported in relation to specific clinical features (10, 11). In our case, the patient showed both axonal degeneration and segmental demyelination as confirmed from the nerve biopsy, along with hyperreflexia and cranial neuropathy. These results indicated that the clinical features were closely related to the presence of antiganglioside antibodies. Diarrhea as an antecedent infection also suggested a relationship between neuropathy and antiganglioside antibodies. However, this case was atypical for GBS in that the patient had clear laterality of quadriparesis, and the effect of IVIG was limited to quadriparesis. Thus, we cannot explain the pathophysiology as typical GBS. Next, we evaluated the pathophysiology from the perspective of SS. If the neuropathy is a neurological manifestation of SS, then the pattern of motor neuropathy tends to be multiple mononeuropathy, cranial neuropathy, or radiculoneuropathy. Both multiple mononeuropathy and cranial neuropathy via SS are effectively treated using corticosteroid therapy, and not IVIG (4). On the contrary, radiculoneuropathy can be effectively treated with IVIG, but not with corticosteroid (4). The neuropathy in this case was successfully treated using corticosteroid, indicating that the neuropathy in this case was related to multiple mononeuropathy and cranial neuropathy. In addition, the biopsied nerve showed variable severity in each bundle on axial sections. This pathological finding also suggested multiple mononeuropathy via SS because it occurred through a mechanism of vasculitis. However, the teased fiber analysis showing the dominance of segmental demyelination, rather than axonal degeneration, was an inconsistent finding. Furthermore, electrophysiological studies indicated conduction delay, suggesting demyelination. Thus the neuropathy in this case cannot be explained as a typical neurological manifestation of SS. According to the above findings, we reached the conclusion that the neuropathy in this case represented a mixture of polyneuropathy as GBS and multiple mononeuropathy via SS. We speculate that GBS occurred by diarrhea and GBS itself activated multiple mononeuropathy via SS. As a result, both neuropathies were coincidental. We consider that polyneuropathy as GBS was partially treated by IVIG, and multiple mononeuropathy via SS was successfully treated with corticosteroid. Regarding GBS, we considered the patient s neuropathy to be either acute motor axonal neuropathy (AMAN) or AIDP. His neuropathy was classified as AIDP according to Ho s criteria, but he also exhibited axonal degeneration. A high level of IgG antibodies to GD1a supported the suspicion of AMAN. In addition, the electrophysiological criteria do not necessarily reflect whether the neuropathy was AMAN or AIDP (12). Although the first electrophysiological study and pathological findings indicated his neuropathy to be AIDP, it was possible that the patient already had subclinical SS-related neuropathy and it influenced the results of the electrophysiological study and pathological findings because he had suffered from xerostomia and xerophthalmia before developing GBS. In that situation, we can consider that his neuropathy was AMAN. However, it was difficult to classify his neuropathy into AMAN or AIDP because his neuropathy was not pure GBS, but a mixture of polyneuropathy as GBS and SS-related neuropathy. It was possible that SS-related neuropathy influenced both axonal degeneration and segmental demyelination. Therefore, we could not classify his neuropathy into either AMAN or AIDP. The delayed progression of cranial neuropathy can be explained from SS-related multiple mononeuropathy activated via GBS. However, the delayed progression of cranial neuropathy, especially facial nerve palsy, was previously reported in GBS, thus it may be explained from only GBS. On the other hand, the background 2721
6 of SS causes several immunological dysfunctions, thus the patient might have had both autoimmune antibodies related to the thyroid as asymptomatic chronic thyroiditis and antiganglioside antibodies as in GBS. It is possible that GBS and SS were related to one another. A similar case was previously reported by Awad et al. (13), who reported the case of a 26-year-old man with AMAN via anti-gm1 antibody with SS. The patient did not show xerostomia or xerophthalmia, but displayed positive results for SS-A antibody and sialadenitis on a salivary gland biopsy, and was thus diagnosed with SS. Some differences from our case were evident. First, no sensory disturbance was present. Second, no xerosis of the eyes or mouth was present. Finally, treatment with IVIG proved effective. Our report is the first report of a patient who had acute peripheral neuropathy with more than one antiganglioside antibody with SS. We hope similar cases are reported to clarify the pathogenesis of such cases. Acute peripheral neuropathy can show many etiologies. Therefore, if we encounter a patient with atypical GBS, other immunological diseases must be considered, including SS. SS is associated with various symptoms, however, its diagnosis is occasionally delayed, particularly among patients with no symptoms other than xerostomia (14). If xerostomia and xerophthalmia are present, then the possible existence of SS should not be overlooked. The authors state that they have no Conflict of Interest (COI). Acknowledgement We wish to thank all the staff who engaged in the treatment of this patient and supported the writing of this paper. References 1. Delalamde S, de Seze J, Fauchais AL, et al. Neurologic manifestations in primary Sjögren syndrome: a study of 82 patients. Medicine 83: , Alexander EL. Central nervous system (CNS) manifestations of primary Sjögren syndrome: an over view. Scand J Rheumatol Suppl 61: , Kaplane JG, Rosenberg R, Reinitz E, et al. Invited review: peripheral neuropathy in Sjögren s syndrome. Muscle Nerve 13: , Mori K, Iijima M, Koike H, et al. The wide spectrum of clinical manifestations in Sjögren s syndrome-associated neuropathy. Brain 128: , Kusunoki S, Kaida K, Ueda M. Antibodies against gangliosides and ganglioside complexes in Guillain-Barré syndrome: new aspects of research. Biochemi Biophys Acta 1780: , Ho TW, Mishu B, Li CY, et al. Guillain-Barré syndrome in northern China: relationship to Campylobacter jejuni infection and antiglycolipid antibodies. Brain 118: , Vitali C, Bombardieri S, Moutsopoulos HM, et al. Preliminary criteria for the classification of Sjögren s syndrome. Arthritis Rheum 36: , Chalk CH, Dyck PJ, Conn DL. Vasculitic neuropathy. In: Peripheral Neuropathy. 3rd ed. WB Saunders, Philadelphia, 1993: Neuwirth C, Mojon D, Weber M. GD1a-associated pure motor Guillain-Barré syndrome with hyperreflexia and bilateral papillitis. J Clin Neuromuscular Dis 11: , Kim JK, Bae JS, Kim DS, et al. Prevalence of anti-ganglioside antibodies and their clinical correlates with Guillain-Barré syndrome in Korea: a nationwide multicenter study. J Clin Neurol 10: , Miyazaki T, Kusunoki S, Kaida K, et al. Guillain-Barré syndrome associcated with IgG monospecific to ganglioside GD1b. Neurology 56: , Kuwabara S, Yuki N. Axonal Guillain-Barré syndrome : concepts and controversies. Lancet Neurol 12: , Awad A, Mathew S, Katirji B. Acute motor axonal neuropathy in association with Sjögren syndrome. Muscle Nerve 42: , Delalande S, de Seze J, Fauchais AL, et al. Neurologic manifestations in primary Sjögren syndrome: a study of 82 patients. Medicine 83: , The Internal Medicine is an Open Access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License. To view the details of this license, please visit ( by-nc-nd/4.0/) The Japanese Society of Internal Medicine
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