Peripheral Nerve Amyloidosis in Sural Nerve Biopsies. A Clinicopathologic Analysis of 13 Cases
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1 Peripheral Nerve Amyloidosis in Sural Nerve Biopsies A Clinicopathologic Analysis of 13 Cases Bijal Rajani, MB, BS; Vakesh Rajani, MB, BS; Richard A. Prayson, MD Objective. Amyloidosis is a well-recognized but uncommon cause of peripheral neuropathy. Our objectives were to determine the overall prevalence of peripheral nerve amyloidosis in sural nerve biopsies and to evaluate the clinical and pathologic features of these lesions. Methods. All available histologic and ultrastructural materials on biopsy tissue from 13 cases of peripheral nerve amyloidosis were examined. Muscle biopsies performed at the same time as the nerve biopsy were reviewed when available. Clinical data were collected on all patients. Results. The prevalence of amyloidosis in sural nerve biopsies at our institution was 13 (1.2%) of 1098 cases over a 15.8-year period. These patients ranged in age from 41 to 82 years (median, 61 years) at initial presentation and included 10 men and 3 women. Presenting neuropathy symptoms were sensory in 6 of the 13 patients, motor in 2 cases, and mixed in 5 cases. Cardiac, renal, or gastrointestinal involvement was present in 7 of 13 cases. Two patients had myeloma and 7 had systemic autonomic symptoms. Two patients had probable familial amyloid polyneuropathy, and 1 patient demonstrated an alanine 60 point mutation. Amyloid, identified as amorphous eosinophilic extracellular deposits demonstrating apple green birefringence on Congo red stain or recognized by its characteristic fibrillar ultrastructure by electron microscopy, was identified in the endoneurium in 12 nerves, perineurium in 2 nerves, and epineurium in 9 nerves. Chronic inflammation was identified in 5 nerves. Axonal loss was recorded as mild ( 25%) in 1 nerve, moderate (25% to 75%) in 8 nerves, and severe ( 75%) in 4 nerves. Axonal degeneration predominated over demyelination in 8 of 10 cases that could be evaluated. Concomitant muscle biopsies contained amyloid deposits in 8 of 9 cases. Conclusions. Amyloidosis is a rare (1.2% in our series) cause of peripheral neuropathy with a distinct microscopic and ultrastructural appearance. Just over half the patients in our study had visceral organ involvement and systemic autonomic symptoms. The peripheral neuropathy was associated with axonal degeneration and a moderate to severe axonal loss in the majority of cases. Amyloid deposition was present in 8 out of 9 muscle biopsies performed at the same time. (Arch Pathol Lab Med. 2000;124: ) Amyloidosis is associated with the deposition of a variety of proteins in the extracellular space within tissues. These fibrillary proteins share a beta-pleated sheet configuration, which accounts for the characteristic staining pattern of amyloid with a variety of stains, including Congo red. Peripheral nerve involvement by amyloid is well recognized and may be associated with deposition of light chain immunoglobulin-derived amyloid, familial amyloid polyneuropathy (most commonly associated with variant plasma transthyretin), or dialysis-associated amyloidosis ( 2 -microglobulin) leading to carpal tunnel syndrome. 1,2 Much of the research in recent years has focused on familial amyloid polyneuropathy and the various genetic mutations associated with this group of disorders. 3,4 This paper reports on the clinical presentations and patho- Accepted for publication May 27, From the Departments of Anatomic Pathology (Drs B. Rajani and Prayson) and Internal Medicine (Dr V. Rajani), The Cleveland Clinic Foundation, Cleveland, Ohio. Presented in part at the XXII International Congress of the International Academy of Pathology and 13th World Congress of Academic and Environmental Pathology, Nice, France, October Reprints: Richard A. Prayson, MD, Department of Anatomic Pathology (L25), Cleveland Clinic Foundation, 9500 Euclid Ave, Cleveland, OH logic features of a group of 13 patients with peripheral nerve amyloidosis diagnosed by sural nerve biopsy during a 15.8-year period at one institution. MATERIALS AND METHODS The surgical pathology files at the Cleveland Clinic Foundation, Cleveland, Ohio, were searched retrospectively from January 1981 through September 1996 for cases of amyloid deposition in sural nerve biopsies. Of the 1098 sural nerve biopsies examined during this period, 13 cases of peripheral nerve amyloidosis were diagnosed. All available histologic materials, including electron micrographs from the 13 cases, were examined and the diagnosis was confirmed in all cases. Peripheral nerve sections in all cases were stained with hematoxylin-eosin, Luxol fast blue, Masson s trichrome, and Congo red stains. In addition, 1- m-thick toluidine blue stained sections were also examined. Electron micrographs were available for review in all cases. The presence of amyloid was confirmed by either Congo red staining or ultrastructural evaluation. The distribution of amyloid (endoneurial, perineurial, or epineurial), the presence of inflammation, and the presence of axonal degeneration or demyelination were recorded for each case. A semiquantitative assessment of myelinated axon loss was also made; 114 Arch Pathol Lab Med Vol 124, January 2000 Peripheral Nerve Amyloidosis in Sural Nerve Biopsies Rajani et al
2 losses were graded as less than 25% of axons lost (mild), 25% to 75% of axons lost (moderate), and greater than 75% of axons lost (severe). In 9 cases, concomitant muscle biopsies were performed, and histologic materials from these cases were also reviewed. Routine evaluation of each of these muscle biopsies included stains with hematoxylin-eosin, adenosine triphosphatase at ph 4.6 and 9.8, nicotinamide-adenine dinucleotide (reduced form), cytochrome C oxidase, and Gomori s trichrome. Either a sulfonated Alcian blue stain or Congo red stain was used in the initial evaluation for amyloidosis. Electron micrographs were available for review in 3 muscle biopsies. The presence and distribution of amyloid and the nature of muscle pathology were noted in each case. Clinical information was obtained from medical records or consulting physicians in all cases. Information tabulated included the age and gender of the patient; peripheral nerve symptomatology; and presence of concomitant systemic autonomic symptoms, such as orthostatic hypotension, alternating constipation and diarrhea, gastric retention and distention, sexual impotence, urinary hesitancy, dry skin, abnormal pupillary reflexes, and other organ involvement. History of carpal tunnel syndrome, evidence of myeloma, and evidence of family history of amyloidosis was also documented when noted. RESULTS Clinical Findings The prevalence of amyloid deposition in sural nerve biopsies at our institution was 13 (1.2%) out of The cohort included 10 men and 3 women, ranging in age from 41 to 82 years (median, 61 years). Eleven of the 13 patients initially presented with sensory nerve symptoms, motor peripheral nerve symptoms, or both. These symptoms included (either alone or in various combinations) paresthesias, dysesthesias, hyperesthesias, weakness, clumsiness, and foot drop. Initial peripheral nerve symptoms were classified as sensory in 6 patients, motor in 2 patients, or mixed in 5 patients. The symptoms involved the lower extremity in 4 cases, upper extremity in 2 cases, and both upper and lower extremities in 7 cases. Symptoms were bilateral in 6 patients and unilateral in 1 patient; in 5 patients it was unclear as to whether symptoms were unilateral or bilateral. Seven of the 13 patients developed systemic autonomic symptoms, including orthostatic hypotension in 6 patients, alternating constipation/diarrhea in 5 patients, sexual impotence in 5 patients, urinary hesitancy in 3 patients, and gastric retention/distention in 3 patients. Each of the 7 patients had at least 2 of the symptoms listed. Two patients were known to have carpal tunnel syndrome. Other organ involvement by amyloidosis, excluding skeletal muscle involvement, was documented in 7 patients as follows: cardiac (n 6), gastrointestinal (n 2), and renal (n 1). Two patients had been diagnosed with multiple myeloma, and 1 patient had a history of malignant melanoma. Two patients were known to have a hereditary familial form of amyloidosis; one of these patients had a documented transthyretin (Ala 60) abnormality. Histopathology Amyloid deposits in the sural nerve biopsies were identified in a perivascular or interstitial location in the endoneurium in 12 cases, in the epineurium in 9 cases, and in the perineurium in 2 cases (Figures 1 and 2). Amyloid was identified either histologically as amorphous eosinophilic extracellular deposits demonstrating apple green birefringence on a Congo red stain or by electron microscopy, in which the characteristic fibrillar ultrastructural appearance was recognized (Figure 3). Chronic inflammation, consisting primarily of lymphocytes, was present in 5 of 13 cases. Loss of myelinated axons was documented as being mild in 1 case, moderate in 8 cases, and severe in 4 cases (Figure 4). Evidence of axonal degeneration was noted in 10 of 10 cases that could be evaluated (Figure 5). Active demyelination was noted in 6 of 10 cases that could be evaluated. In 8 out of 10 cases, axonal degeneration appeared to be the predominant pattern of injury. In the remaining 3 cases, the material was felt to be insufficient to assess the degree of axonal degeneration or demyelination accurately. Varying degrees of unmyelinated axonal loss were observed in most nerves as well. Concomitant muscle biopsies were performed and examined in 9 patients. Muscle sites from which biopsies were taken included the gastrocnemius (n 6), quadriceps femoralis (n 1), rectus femoris (n 1), and lower extremity (not further specified) (n 1). The presence of amyloid confirmed histologically by either Congo red or sulfonated Alcian blue stains or by electron microscopy was seen in 8 muscles. Amyloid was distributed in a perivascular or interstitial location within the endomysium in 7 muscles and in the epimysium in 4 muscles (Figure 6). All 9 muscles demonstrated evidence of neurogenic atrophy characterized by the presence of angular atrophic esterase-positive muscle fibers or fiber-type grouping. Central core fibers and cytoplasmic bodies were observed in one muscle. COMMENT The hereditary amyloidoses are characterized by peripheral nerve involvement in the majority of cases. In contrast, other forms of amyloidosis present less commonly as a peripheral neuropathy. Clinically, peripheral neuropathy occurs in approximately 15% to 35% of light chain type amyloidosis (AL) and overall is the presenting symptom in fewer than 10% of cases. 1,5 The majority of the literature on peripheral nerve amyloidosis has focused attention on reviews and studies of the familial forms of polyneuropathy. 1,3,4,6 14 Familial amyloid polyneuropathy (FAP) was first described by Andrade 15 in a group of Portuguese patients in Since then, numerous cases of hereditary polyneuropathy associated with amyloidosis have been reported from several countries. Three groups of proteins have been reported to be associated with FAP. The usual protein deposited as amyloid in FAP is a variant form of transthyretin. Other less commonly described proteins include mutant apolipoprotein A-1 and gelsolin. The hereditary polyneuropathies are classified according to the point mutation that is present. The most common mutation involves methionine 30 (Met 30) in the transthyretin gene. The peripheral neuropathy associated with patients with FAP typically begins as a sensory neuropathy in the lower extremities. 4 Carpal tunnel syndrome does develop in some patients. The clinical manifestations are variable among the different types of FAP and even among patients with the same genetic abnormality. Amyloid deposition can occur in other organs, such as the heart, and involvement of the autonomic nervous system can give rise to symptoms such as gastric and bladder dysfunction, alter- Arch Pathol Lab Med Vol 124, January 2000 Peripheral Nerve Amyloidosis in Sural Nerve Biopsies Rajani et al 115
3 Figure 1. Patient 8. Endoneurial perivascular deposition of amyloid (Congo red, original magnification 400). Figure 2. Patient 5. Endoneurial interstitial deposition of amyloid (hematoxylin-eosin, original magnification 400). nating diarrhea and constipation, orthostatic hypotension, and sexual impotence. In light chain associated amyloid peripheral neuropathy, symptoms usually commence in the lower extremity with painful dysesthesias and loss of light touch and temperature perception. 1,5 Autonomic dysfunction and other organ involvement can also occur, as in FAP. Upper limb and motor involvement typically occur later in the course of the disease. 2 Yamada and colleagues 16 described clinical features in 20 autopsy cases of systemic amyloidosis. Eight patients had clinical manifestations of polyneuropathy. The average age at onset of symptoms was 59 years for patients with nonhereditary amyloid polyneuropathy (6 cases) and 24 years for FAP patients (2 cases). The 2 patients with FAP and 3 of the 6 patients with nonhereditary neuropathy presented with predominantly neurological symptoms, including ascending and progressive sensory disturbances in the lower extremity. Dissociated sensory loss (ie, selective impairment of pain and sensation) was noted in 2 cases of FAP, while all modes of sensation were affected in nonhereditary cases. Motor disturbances developed later. Autonomic dysfunction was seen in 5 of 8 cases and was more prominent in FAP than in nonhereditary cases. In our series, 11 of 13 patients with peripheral nerve amyloidosis first presented with peripheral nerve symptoms (including the 2 patients with FAP). One patient initially presented with autonomic symptoms (progressive erectile dysfunction), and a second patient presented with peripheral edema secondary to proteinuria and renal involvement. Both these patients subsequently developed peripheral nerve symptoms. The initial peripheral nerve symptoms reported by the 13 patients in our study were sensory in 6 cases, motor in 2 cases, and mixed in 5 cases. It is difficult to determine whether sensory dysfunction preceded motor disturbances in the 5 patients with mixed sensory and motor symptoms at initial clinical presentation. Similar to the findings of Yamada et al, 16 autonomic 116 Arch Pathol Lab Med Vol 124, January 2000 Peripheral Nerve Amyloidosis in Sural Nerve Biopsies Rajani et al
4 Figure 3. Patient 7. Characteristic fibrillar ultrastructure of amyloid (original magnification ). Figure 5. Patient 4. Axonal degeneration seen by electron microscopy (original magnification 4600). Figure 4. Patient 13. Severe loss of both large and small myelinated axons (toluidine blue, original magnification 200). dysfunction developed in more than 50% (7/13) of our cases. The 2 patients with FAP did not develop carpal tunnel syndrome or amyloid deposition in other organs such as the heart, kidney, or gastrointestinal tract. The 1 FAP patient in our series in whom the point mutation was known (alanine [Ala] 60), presented with sensory and motor symptoms in the upper and lower extremities at 75 years of age. Familial amyloid polyneuropathy Ala 60 (Irish/Appalachian) is described to have a late clinical onset (usually in the sixth or seventh decade), and both motor involvement and large fiber sensory loss are more prominent than in the more common Met The literature on the microscopic distribution of amyloid and peripheral nerve pathology in amyloid-associated polyneuropathy cases is sparse and predominantly focuses on FAP cases, in which amyloid deposits are described as occurring mainly in the endoneurium. 6,7,9,12 Thomas and King 17 described 4 cases of amyloid neuropathy, 3 of which were sporadic and 1 which had a family history of a similar disorder. Light microscopic examination of all 4 nerves (3 sural nerve biopsies and 1 radial nerve biopsy) revealed the presence of amyloid deposits, which were most evident around endoneurial blood vessels but which were also observed free in the endoneurium and epineurial connective tissues. In our series, the amyloid deposits were seen in the endoneurium (12 cases) more often than in the epineurium (9 cases) or perineurium (2 cases). Axonal degeneration is described as the predominant peripheral nerve pathology in sural nerve biopsies from patients with peripheral nerve amyloidosis with a preferential early loss of small myelinated and unmyelinated axons. 14,17,18 Ii and colleagues 19 described clinical and pathologic features in transthyretin and light chain cases of amyloid polyneuropathy and could not demonstrate significant differences between the 2 groups of patients. The percentage of fibers judged to be undergoing axonal degeneration and regeneration (in both groups of patients) was increased beyond that found in controls, whereas the percentage of fibers showing demyelination and remyelination was not significantly increased beyond that found in controls. 19 Others have noted that some demyelination can occur, although not to the same degree as the axonal degeneration. 18 Sobue et al 7 described 2 cases of FAP in which segmental demyelination was more prominent in the proximal portions of nerves, but axonal degeneration was more conspicuous in the distal portions. 7 In the current study, evidence of axonal degeneration was present in 10 of 10 cases that could be evaluated, and evidence of occasional axonal demyelination was evident in 6 of 10 cases, with axonal degeneration predominating over demyelination in the majority of cases. The mechanism underlying amyloid neuropathy is unclear. One hypothesized cause of nerve fiber loss is ischemia related to the preferential perivascular deposition of amyloid. 9,20 The selective loss of unmyelinated and small Arch Pathol Lab Med Vol 124, January 2000 Peripheral Nerve Amyloidosis in Sural Nerve Biopsies Rajani et al 117
5 Figure 6. Patient 8. Muscle biopsy demonstrating endomysial amyloid deposition highlighted using a Congo red stain. On polarization, the presence of amyloid was confirmed by demonstrating apple green birefringence (original magnification 400). myelinated fibers in amyloid-associated peripheral neuropathy argues against the ischemia theory, as one would expect preferential large fiber loss first in this scenario. Others have attributed the neuropathy to direct mechanical compression of nerve fibers by amyloid deposits. 14,17,21,22 Dyck and Lambert s report documenting that segmental demyelination of fibers occurred in relation to amyloid masses lends credence to this hypothesis. 14 It has been suggested that localized compression of Schwann cells in the endoneurium related to the close apposition of amyloid fibrils to the Schwann cell basal lamina could lead to demyelination and Schwann cell death. 18 If this was the predominant peripheral nerve mechanism of injury in amyloidosis, one would expect to see primarily a demyelinative neuropathy picture with Schwann cell loss, rather than the predominant axonal degeneration that has been observed. It is also possible, however, that direct compression of axons may induce axonal damage independent of Schwann cell dysfunction. In all but one of the cases in which a muscle biopsy was performed at the same time as the sural nerve biopsy, amyloid was also identified in the muscle biopsy specimen. This finding suggests that in most of these patients, the amyloid is probably not confined to a single organ system. Not surprisingly, changes consistent with neurogenic atrophy attributable to the disease in the peripheral nerve is the most commonly observed pathology in the muscle. Although rare and untreatable in most cases, the diagnosis of amyloidosis can be important. The prognosis in multiple myeloma patients is worse with systemic amyloid deposition. In patients with FAP, genetic counseling becomes an important aspect of patient management, and although proven effective treatment is not available, some recent approaches, such as liver transplantation, have shown promise in management of hereditary forms of amyloid polyneuropathy. 23 Special thanks go to Denise Egleton for her help in the preparation of this article. References 1. Reilly MM, Staunton M. Peripheral nerve amyloidosis. Brain Pathol. 1996; 6: Haan J, Peters WG. Amyloid and peripheral nervous system disease. Clin Neurol Neurosurg. 1994;96: Reilly MM, King RHM. Familial amyloid polyneuropathy. Brain Pathol. 1993;3: Benson MD. Familial amyloidotic polyneuropathy. Trends Neurosci. 1989; 12: Glenner GG, Murphy MA. Amyloidosis of the nervous system. J Neurol Sci. 1989;94: Toyooka K, Fujimura H, Ueno S, et al. Familial amyloid polyneuropathy associated with transthyretin Gly 42 mutation: a quantitative light and electron microscope study of the peripheral nervous system. Acta Neuropathol. 1995;90: Sobue G, Nakao N, Murakami K, et al. Type I familial amyloid polyneuropathy: a pathological study of the peripheral nervous system. Brain. 1990;113: Kiuru S. Familial amyloidosis of the Finnish type (FAF): a clinical study of 30 patients. Acta Neurol Scand. 1992;86: 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: Tanimura A, Takanori C, Shinohara Y, et al. Familial amyloidosis: a histopathological study. Acta Pathol Jpn. 1984;34: Staunton H, Dervan P, Kale R, Linke RP, Kelly P. Hereditary amyloid polyneuropathy in North West Ireland. Brain. 1987;110: Coimbra A, Andrade C. Familial amyloid polyneuropathy: an electron microscope study of the peripheral nerve in five cases, I: interstitial changes. Brain. 1971;94: Hofer PA, Andersson R. Postmortem findings in primary familial amyloidosis with polyneuropathy. Acta Pathol Microbiol Scand. 1975;83: 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: Andrade C. A peculiar form of peripheral neuropathy: familial atypical generalized amyloidosis with special involvement of the peripheral nerves. Brain. 1952;75: Yamada M, Hatakeyama S, Tsukagoshi H. Peripheral and autonomic nerve lesions in systemic amyloidosis: three pathological types of amyloid polyneuropathy. Acta Pathol Jpn. 1984;34: Thomas PK, King RHM. Peripheral nerve changes in amyloid neuropathy. Brain. 1974;97: Thomas PK, Landon DN, King RHM. Diseases of the peripheral nerves. In: Graham DI, Lantos PL, eds. Greenfield s Neuropathology. Vol 2. London, England: Arnold Publishers; 1997: Ii K, Kyle RA, Dyck PJ. Immunohistochemical characterization of amyloid proteins in sural nerves and clinical associations in amyloid neuropathy. Am J Pathol. 1992;141: Kernohan JW, Woltman HW. Amyloid neuritis. Arch Neurol Psychiatry. 1942;47: Horder JM, Treip CS. Primary amyloidosis with involvement of the peripheral nervous system. Neuropathol Appl Neurobiol. 1977;3: Said G, Ropert A, Faux N. Length dependent degeneration of fibers in Portuguese amyloid polyneuropathy: a clinicopathological study. Neurology. 1984;34: Coelho T. Familial amyloid polyneuropathy: new developments in genetics and treatment. Curr Opin Neurol. 1996;9: Arch Pathol Lab Med Vol 124, January 2000 Peripheral Nerve Amyloidosis in Sural Nerve Biopsies Rajani et al
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