OBSERVATION. Akira Yoshioka, MD; Yoko Yamaya, MD; Shinji Saiki, MD; Genjiro Hirose, MD; Kohei Shimazaki, MD; Masaaki Nakamura, MD; Yukio Ando, MD
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1 OBSERVATION A Case of Familial Amyloid Polyneuropathy Homozygous for the Transthyretin Val30Met Gene With Motor-Dominant Sensorimotor Polyneuropathy and Unusual Sural Nerve Pathological Findings Akira Yoshioka, MD; Yoko Yamaya, MD; Shinji Saiki, MD; Genjiro Hirose, MD; Kohei Shimazaki, MD; Masaaki Nakamura, MD; Yukio Ando, MD Objective: To report a case of familial amyloid polyneuropathy homozygous for the amyloidogenic transthyretin (ATTR) Val30Met gene with motor-dominant sensorimotor polyneuropathy and unusual sural nerve pathological findings. Methods: Mass spectrometry analysis and polymerase chain reaction restricting fragment length polymorphism were performed. A right sural nerve biopsy specimen was obtained for histological investigation. Setting: Academic medical center. Results: A 56-year-old Japanese man living in a local town (Nakajima, Japan) in Ishikawa Prefecture, a nonendemic area of type I familial amyloidotic polyneuropathy, had vitreous amyloidosis, motor-dominant sensorimotor polyneuropathy, erectile dysfunction, and urinary incontinence. He had neither orthostatic hypotension nor indolent diarrhea. Restriction enzyme analysis with EcoT22 I of amplified DNA and mass spectrometry analysis revealed homozygosity for ATTR Val30Met. Of 8 family members, 5 were evaluated and found to be heterozygous for ATTR Val30Met; a family history found no relative with the similar neurologic disorders. The sural nerve biopsy specimen showed focal edema and an amyloid deposit in the subperineural tissue, associated with moderate loss of myelinated and unmyelinated fibers. Conclusions: In addition to the findings characteristic of homozygosity for ATTR Val30Met such as vitreous amyloidosis and relatively less autonomic involvements, this case had the unique findings of motor-dominant sensorimotor polyneuropathy and unusual sural nerve biopsy specimen results. Arch Neurol. 2001;58: From the Department of Neurology, Kanazawa Medical University, Uchinada (Drs Yoshioka, Yamaya, Saiki, and Hirose); Department of Internal Medicine, Hamano Hospital, Nanao City (Dr Shimazaki); and the Department of Laboratory Medicine, Kumamoto University School of Medicine, Kumamoto (Drs Nakamura and Ando), Japan. FAMILIAL amyloidotic polyneuropathy (FAP) type I is an autosomal-dominant disorder characterized by extracellular amyloid deposit in systemic organs and by polyneuropathy involving sensory, motor, and autonomic nerves. 1 The cause of FAP type I has been shown to be a single amino acid substitution of methionine for valine at position 30 of the amyloidogenic transthyretin (ATTR) Val30Met gene. 2 Although many patients with ATTR Val30Met FAP type I are heterozygous, 13 patients homozygous for ATTR Val30Met (including 3 asymptomatic carriers) from Sweden, Turkey, and Japan have been previously identified. 3-9 Characteristics of patients homozygous for ATTR Val30Met FAP have been reported to have late-onset, ocular manifestation (vitreous amyloidosis), 4 decreased focal depth, and less autonomic involvement. 6-8 We report a case of homozygous ATTR Val30Met FAP with motor-dominant sensorimotor polyneuropathy and unusual sural nerve biopsy specimen findings. REPORT OF A CASE A 56-year-old Japanese man living in Nakajima, Ishikawa Prefecture, believed to be a nonendemic area of FAP in Japan, was admitted to our service on February 14, 2000, for generalized muscle atrophy. His deceased parents were second cousins who had lived in the same town. Both parents died of cerebral infarction his father at the age of 87 years and his mother at the age of 82 years. A family history disclosed no relatives with similar neurologic disorders. We did not find any kinship with residents of Ogawa Village, Nagano Prefecture, and Arao City, Kumamoto Prefecture, 2 endemic foci of FAP type I in Japan. 10,
2 METHODS MASS SPECTROMETRY To screen a mutant TTR in serum, a mass spectrometer (Bruker Reflex; Bruker Franzen Analytik GmbH, Bremen, Germany) was used. Fifty microliters of test serum was mixed with 20 µl of an anti-ttr polyclonal antibody (Dako, Glostrup, Denmark) and assayed as described previously. 12 In the proband s serum sample, peaks of dalton that corresponded to ATTR Val30Met were predominantly observed and no normal TTR peaks were detected (data not shown). DNA ANALYSIS For screening ATTR Val30Met, polymerase chain reaction restricting fragment length polymorphism (PCR-RFLP) was performed: PCR-RFLP showed a normal band of 195 base pair (bp) in a normal subject (Figure 1A, lane 1), an extra band of 115 and 80 bp associated with ATTR Val30Met mutation in the proband (Figure 1A, lane 2), and both bands in a heterozygous patient with FAP ATTR Val30Met (Figure 1A, lane 3). These results suggest that the proband was a homozygote with FAP ATTR Val30Met. The PCR-RFLP analysis for 8 family members revealed 5 heterozygotic ATTR Val30Met gene carriers (Figure 1B-C). SURAL NERVE FINDINGS Congo red staining and polarized light analysis of excised sural nerve showed amyloid deposit in the perineural and endoneural tissues (data not shown). After the specimen was embedded in epoxy resin and stained with toluidine blue, it showed focal edema and amyloid deposits in the subperineural tissue (Figure 2A-B). There was a moderate loss of myelinated fibers (3773 fibers per square millimeter) and unmyelinated fibers (14800 fibers per square millimeter). Myelinated fibers with thin myelin sheaths, indicative of remyelinated fibers, were noted. Numbers of both large- and small-diameter myelinated fibers decreased (Figure 2C). The 2-peak pattern of myelinated fibers was well preserved. Electron microscopic findings showed amyloid fibrils intermixed with collagen fibers in the subperineural tissue (Figure 2D). Our patient had been well until 1989, when he noticed blurred vision. In 1991, a right vitrectomy was performed. Amyloid was recovered from the vitreous material. At that time, the patient did not have any muscle atrophy or sensory disturbances. He noticed erectile dysfunction and dysuria in He first noticed muscle atrophy of his upper and lower extremities in July 1999 and was referred to the hematology group at our hospital, where a biopsy specimen of his lip disclosed an amyloid deposit, although a biopsy specimen of his bone marrow revealed no increase in plasma cells. The patient did not report orthostatic dizziness or diarrhea. On admission, his blood pressure was 110/76 mm Hg in the sitting and standing positions, his pulse rate was 68/min and regular, his body weight was 41 kg, and his height was 161 cm. Neurologically, his mental status was alert and well oriented to time, place, and person. Cranial nerves were well preserved, except for the right eye, which showed a sluggish light reflex and lens opacity. Significant symmetrical muscle atrophy and weakness of the upper and lower extremities were noted with distal predominance and marked fasciculation. Deep tendon reflexes were hypoactive in the upper extremities and areflexic in the lower extremities. The plantar response was flexor bilaterally. Pain and vibratory sensations were slightly decreased below the ankles, but position sense was well preserved. Findings from examination of the cerebral spinal fluid showed no abnormalities. Motor conduction velocity was markedly decreased at the right ulnar nerve (22.4 m/s), the right peroneal nerve (15.5 m/s), the left peroneal nerve (20.8 m/s), the right posterior tibial nerve (34.7 m/s), and the left posterior tibial nerve (34.6 m/s). Motor conduction was not evoked at the right median nerve. No significant conduction block was noted. Conversely, sensory conduction velocity was well preserved at the left median nerve (48.8 m/s) and the left ulnar nerve (50.4 m/s). Sensory conduction was not evoked at the right median and ulnar nerves. The F- wave conduction velocity was decreased at the right ulnar nerve (32.4 m/s) and the left peroneal nerve (29.8 m/s), but it was preserved at the left posterior tibial nerve (41.3 m/s). F waves were not evoked at the median nerves bilaterally, the left ulnar nerve, the right peroneal nerve, and the right posterior tibial nerve. An echocardiogram showed no cardiomegaly and a computed tomographic scan of the abdomen revealed no organomegaly. The patient s muscle atrophy progressed and his body weight was 36.6 kg in October COMMENT We found a family in which the proband is homozygous for ATTR Val30Met and 5 of the 8 family members are heterozygous for ATTR Val30Met. The patient s parents, now deceased, were second cousins living in Nakajima, Ishikawa Prefecture, which is a nonendemic area of FAP type I in Japan. No kinship was found in the families from endemic areas such as Ogawa Village and Arao City, where the large foci of FAP ATTR Val30Met exist. Previously, Yoshinaga et al 7 described 3 patients with FAP homozygosity for ATTR Val30Met living in Kanazawa City, Ishikawa Prefecture, about 70 km south of Nakajima. We could not find any common ancestors between the family in that article and the family of our patient. Further study is needed to determine whether Nakajima might be another endemic area of FAP type I in Japan. The patient showed his first clinical symptom, vitreous amyloidosis, when he was 45 years old. This age of onset is younger than the average previously reported in homozygous cases of ATTR Val30Met (mean age±sd, 57.3±5.4 years; age range, years). 13 The patient noticed erectile dysfunction and dysuria at the 1915
3 M M A B I II (+) (+) (++) ( ) ( ) III 4 5 (+) (+) 7 8 (+) ( ) C (++) (+) (+) ( ) ( ) TTR-Met30 Homozygote TTR-Met30 Heterozygote TTR-Met30 Negative Figure 1. A, Polymerase chain reaction restricting fragment length polymorphism (PCR-RFLP) showed a normal band of 195 base pairs (bp) in a normal subject (lane 1), an extra band of 115 and 80 bp associated with amyloidogenic transthyretin (ATTR) Val30Met gene mutation in the proband (lane 2), and both bands in a patient with heterozygote familial amyloid polyneuropathy ATTR Val30Met (lane 3). M indicates DNA size marker. B, Polymerase chain reaction restricting fragment length polymorphism analysis for 8 family members revealed 5 heterozygotic ATTR Val30Met gene carriers. M indicates DNA size marker; lane 1, normal control; lanes 2-9, family members evaluated; and lane 10, a patient heterozygous for ATTR Val30Met from a different pedigree. C, Pedigree of family. The arrow indicates the proband; circle, females; squares, males; daggers, dead; 6, 3, 2, 9, 4, 5, 7, and 8, all represent persons who were tested and these numbers correspond to the lane numbers in Figure 1B. age of 54 years and had motor-dominant sensorimotor polyneuropathy at the age of 55 years. In addition to the clinical symptoms characteristic of homozygosity for ATTR Val30Met such as vitreous amyloidosis and less autonomic involvements (without orthostatic hypotension and diarrhea), the patient showed motor-dominant sensorimotor polyneuropathy with distally predominant muscle atrophy and marked fasciculation. Pain and temperature sensations were mildly involved, but vibratory sensation was spared. Nerve conduction velocity studies showed a predominant motor involvement. Patients with FAP type I usually have symptoms of sensory and autonomic neuropathy in their early courses and motor neuropathy later. 10 Motordominant polyneuropathy in early-stage FAP type I has apparently been reported in only 3 patients. 14,15 A case of primary amyloidosis with early motor-dominant neuropathy that mimicked lower motor neuron disease has been reported. 16 Muscle weakness is noted in the patients with amyloid myopathy, which is a wellrecognized, but rare, manifestation of amyloidosis. 17 However, it is the primary amyloidosis that most often has involvement of skeletal muscle. 17 The present case disclosed unusual sural nerve biopsy specimen findings: focal edema and amyloid deposits in the subperineural tissue, associated with moderate loss of myelinated and unmyelinated fibers. The morphometric analysis revealed a relatively preserved 2-peak pattern of myelinated fibers. The previous studies of sural nerve biopsy specimens from patients with FAP type I revealed the deposit of amyloid substances within nerve fasciculus, selective loss of small myelinated and unmyelinated fibers, and predominant axonal degeneration. 18,19 We could not see pathological findings of subperineural edema in the sural nerves of patients with FAP type I whose cases were previously reported. However, Hanyu et al 20 evaluated 3 autopsy cases of FAP type I and found endoneural edema with segmental demyelination in the brachial plexus and sciatic nerves, but not in the sural nerves or spinal roots. These researchers suggested that the proximal nerve lesions induced by endoneural edema resulting from amyloid deposits on the vessels might secondarily damage distal nerves such as sural nerves. Regarding the sural nerves of patients with homozygous ATTR Val30Met, Yoshinaga et al 13 reported 1 case showing a marked loss of 1916
4 A B 2000 Total No.: 3773 Fibers/mm2 No. of Myelinated Fibers 1000 C Diameter, µm D Figure 2. Biopsy findings of sural nerve (A and B). After the specimen was embedded in epoxy resin and stained with toluidine blue, it showed focal edema and amyloid deposit in the subperineural tissue as well as a moderate loss of myelinated fibers (3773 fibers per square millimeter) and unmyelinated fibers (14800 fibers per square millimeter). Myelinated fibers with thin myelin sheaths, indicative of remyelinated fibers were noted. C, Morphometric analysis of the sural nerve showed a loss of both large- and small-diameter myelinated fibers. The 2-peak pattern of myelinated fibers was preserved. D, Electron microscopic findings showed amyloid fibrils intermixed with collagen fibers in the subperineural tissue. myelinated and unmyelinated fibers, but they did not find edema or an amyloid deposit in the subperineural tissue. Patients homozygous for the ATTR Val30Met gene do not appear to suffer from more severe illness. 6-8 Even asymptomatic homozygous ATTR Val30Met gene carriers have been described. 7,8 However, most of the neurologic symptoms of FAP are due to infiltrated deposits of amyloid fibrils in the tissues. Characterization of the various amyloidogenic TTR mutations has set the stage for an effort to clarify the mechanisms underlying fibril formation. Amyloid fibrillogenesis has been considered a multifactorial process. 21 The factors influence fibril formation in FAP, consist of the intrinsic conformation of the TTR fibril protein, its concentration, the structual effects of TTR mutation, microenvironments of the lysosome, proteolytic processing, amyloid cofactors and tissuespecific determinants. 21 Therefore, the clinical phenotypic heterogeneity of TTR mutations can be explained by these complicated multifactorial mechanisms. Accepted for publication March 30, Corresponding author: Akira Yoshioka, MD, Department of Neurology, Kanazawa Medical University, 1-1 Daigaku, Uchinada, Kahoku, Ishikawa , Japan ( a-yos@kanazawa-med.ac.jp). REFERENCES 1. Andrade C. A peculiar form of peripheral neuropathy: familial atypical generalized amyloidosis with special involvement of the peripheral nerves. Brain. 1952; 75: Tawara S, Nakazato M, Kangawa K, Matsuo H, Araki S. Identification of amyloid prealbumin variant in familial amyloidotic polyneuropathy (Japanese type). Biochem Biophys Res Commun. 1983;116: Holmgren G, Haettner E, Nordenson I, Sandgren O, Steen L, Lundgren E. Homozygosity for the transthyretin-met 30 -gene in two Swedish siblings with familial amyloidotic polyneuropathy. Clin Genet. 1988;34: Sandgren O, Holmgren G, Lundgren E. Vitreous amyloidosis associated with homozygosity for the transthyretin methionine-30 gene. Arch Ophthalmol. 1990; 108: Skare J, Yazici H, Erken E, et al. Homozygosity for the Met 30 transthyretin gene in a Turkish kindred with familial amyloidotic polyneuropathy. Hum Genet. 1990; 86: Holmgren G, Bergström S, Drugge U, et al. Homozygosity for the transthyretin- Met 30 -gene in seven individuals with familial amyloidosis with polyneuropathy detected by restriction enzyme analysis of amplified genomic DNA sequences. Clin Genet. 1992;41: Yoshinaga T, Nakazato M, Ikeda S, Ohnishi A. Homozygosity for the transthyretin- Met 30 gene in three Japanese siblings with type I familial amyloidotic polyneuropathy. Neurology. 1992;42:
5 8. Ikeda S, Nakano T, Yanagisawa N, Nakazato M, Tsukagoshi H. Asymptomatic homozygous gene carrier in a family with type I familial amyloid polyneuropathy. Eur Neurol. 1992;32: Holmgren G, Lundgren E, Kangawa K, et al. Diagnostic radioimmunoassay and DNA-analysis in Swedish and Japanese patients with familial amyloidotic polyneuropathy: homozygosity for the TTR-Met 30 gene. Acta Neurol Scand. 1993; 87: Araki S, Mawatari S, Ohta M, et al. Polyneuritic amyloidosis in a Japanese family. Arch Neurol. 1968;18: Kito S, Itoga E, Kamiya K, et al. Studies on familial amyloid polyneuropathy in Ogawa Village, Japan. Eur Neurol. 1980;19: Ando Y, Ohlsson PI, Suhr O, et al. A new simple and rapid screening method for variant transthyretin-related amyloidosis. Biochem Biophys Res Commun. 1996; 228: Yoshinaga T, Nakazato M, Ikeda S, Ohnishi A. Three siblings homozygous for the transthyretin-met 30 gene in familial amyloidotic polyneuropathy: evaluation of their clinical pictures with reference to those of other 10 cases reported. Clin Neurol. 1994;34: Kincaido JC, Wallace MR, Benson MB. Late-onset familial amyloidotic polyneuropathy in an American family of English origin. Neurology. 1989;39: Ando Y, Ueyama H, Watanabe S, et al. Early involvement of motor nerve dysfunction in atypical cases with familial amyloidotic polyneuropathy (FAP) type I. Muscle Nerve. 1993;16: Quattrini A, Nemni R, Sferrazza B, et al. Amyloid neuropathy simulating lower motor neuron disease. Neurology. 1998;51: Gertz M, Kyle RA. Myopathy in primary systemic amyloidosis. J Neurol Neurosurg Psychiatry. 1996;60: Dyck PJ, Lambert EH. Dissociated sensation in amyloidosis: compound action potential, quantitative histologic and teased-fiber, and electron microscopic studies of sural nerve biopsies. Arch Neurol. 1969;20: Said G, Ropert A, Faux N. Length-dependent degeneration of fibers in Portuguese amyloid polyneuropathy: a clinicopathological study. Neurology. 1984; 34: Hanyu N, Ikeda S, Nakadai A, Yanagisawa N, Powell HC. Peripheral nerve pathological findings in familial amyloid polyneuropathy: a correlative study of proximal sciatic nerve and sural nerve lesions. Ann Neurol. 1989;25: Herbert J. Familial amyloidotic polyneuropathy. In: Rosenberg RN, Prusiner SB, DiMauro S, Barchi RL eds. The Molecular and Genetic Basis of Neurological Disease. Boston, Mass: Butterworth-Heinemann; 1997:
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