Amyotrophic lateral sclerosis causes small fiber pathology
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1 SHORT COMMUNICATION Amyotrophic lateral sclerosis causes small fiber pathology E. Dalla Bella a,b, R. Lombardi b, C. Porretta-Serapiglia b, C. Ciano a,c, C. Gellera a,d, V. Pensato a,d, D. Cazzato b and G. Lauria a,b a Motor Neuron Diseases Centre, IRCCS Foundation Carlo Besta Neurological Institute, Milan, Italy; b Third Neurology Unit, IRCCS Foundation Carlo Besta Neurological Institute, Milan, Italy; c Clinical Neurophysiology Unit, IRCCS Foundation Carlo Besta Neurological Institute, Milan, Italy; and d Genetics of Neurodegenerative and Metabolic Diseases Unit, IRCCS Foundation Carlo Besta Neurological Institute, Milan, Italy EUROPEAN JOURNAL OF NEUROLOGY Keywords: amyotrophic lateral disease, intraepidermal nerve fiber density, motor neuron disease, neuropathic pain, skin biopsy, small fiber neuropathy Received 3 August 2015 Accepted 4 November 2015 European Journal of Neurology 2016, 23: doi: /ene Background and purpose: Our aim was to address the correlation between small fiber loss and amyotrophic lateral sclerosis (ALS) for disease onset, phenotype, genotype, duration, severity and sensory findings. Methods: Consecutive patients referred for suspected ALS were screened. Exclusion criteria were possible ALS and previous diagnosis or known risk factors for small fiber neuropathies. A sural nerve conduction study (NCS) was bilaterally recorded. The ALS functional rating scale revised was administered and loss of functions were calculated using the Milano Torino staging (MITOS) system. Sensory symptoms and signs were recorded. Genetic analysis was performed by the next-generation sequencing approach. Skin biopsy was performed at the distal leg and intraepidermal nerve fiber (IENF) density was quantified in three non-consecutive sections following published guidelines. Findings were referred to age- and sex-adjusted normative values. Results: Fifty-seven patients including six with facial onset sensory and motor neuronopathy (FOSMN) were enrolled. Eight (15.7%) pure ALS patients and five (83%) FOSMN patients complained of sensory disturbances with different distributions. Sural NCS was normal in all except two patients. IENF density was reduced in 75.4% of pure ALS and 50% of FOSMN patients, without correlation with any disease features. IENF density was similarly reduced in bulbar (78.5%), flail limb (87.5%), pyramidal (100%), and spinal (68.2%) onset, as well as in genetic (83.3%) and sporadic (82%) ALS. There was no correlation with genotype, disease duration and severity. Conclusions: Intraepidermal nerve fiber loss is a feature of most ALS patients. It does not correlate with onset, phenotype, course and severity of the disease, and cannot be considered a clinical or prognostic biomarker. Introduction Amyotrophic lateral sclerosis (ALS) is caused by the degeneration of upper and lower motor neurons leading to diffuse muscle waste and weakness, and eventually death. Besides clinical examination, in accordance with the El Escorial revised criteria, ALS diagnosis is supported by a nerve conduction study (NCS), needle Correspondence: G. Lauria, MD, Third Neurology Unit, IRCCS Foundation Carlo Besta Neurological Institute, Milan, Italy (tel.: ; fax: ; glauria@istituto-besta.it). electromyography and motor evoked potentials. A sensory NCS is expected to be normal; when impaired, it can challenge the diagnosis and prompt further work-up to rule out potentially treatable conditions such as peripheral neuropathy. Nevertheless, some studies have reported sensory NCS abnormalities, most commonly subclinical, in up to 23% of patients with an eventually confirmed diagnosis of ALS [1,2]. More recently, skin biopsy studies in two small ALS cohorts showed small nerve fiber loss in a much larger proportion of patients, but providing different results. The first study [3] showed subclinical 416
2 SFN IN ALS 417 decrease of intraepidermal nerve fiber (IENF) density in about 80% of patients, whereas the second [4] suggested that IENF loss could cluster spinal from normally innervated bulbar ALS patients. Our aim was to address to what extent ALS patients are affected by small fiber neuropathy, if there is any correlation with disease onset, symptoms, duration, phenotype, severity and sensory NCS findings, and if skin biopsy can serve as a biomarker to classify patients and to provide prognostic information. Patients and methods All consecutive patients referred to our Motor Neuron Diseases Center for suspected ALS were screened. Exclusion criteria were a diagnosis of possible ALS, a previous diagnosis of peripheral neuropathy associated or not to systemic illnesses (e.g. diabetes, immune-mediated neuropathy), any known cause of small fiber neuropathy [5], known bleeding disorders, and anticoagulant treatment. All patients underwent a wide panel of laboratory tests to exclude known causes of neuropathy and malignancies, including blood cell count, liver and renal function, thyroid hormones, B and C hepatitis, serum electrophoresis, vitamin B 12, folate, fasting glycemia and glycated hemoglobin. Neurophysiological examination included bilateral sural sensory nerve action potential amplitude and conduction velocity recording. The ALS functional rating scale revised (ALSFRS-R) was administered and functional impairment was calculated using the Milano Torino staging (MITOS) system [6]. Sensory symptoms and signs were recorded. All patients underwent genetic analysis by the nextgeneration sequencing approach using the TruSeq Custom Amplicon Illumina method and Studio Design software (Illumina Inc., San Diego, CA, USA) for a large panel of ALS-related genes. Sequencing was performed using the NGS MiSeq Illumina sequencer (Illumina). All enrolled patients underwent 3-mm punch skin biopsy at the distal site of the leg, 10 cm above the external malleolus within the territory of the sural nerve. The procedure was performed with a disposable device in a sterile technique, after topical anesthesia with spray ice. No suture was used. Biopsies were processed following available guidelines [7] and IENF density was quantified on three randomly selected and non-consecutive 50-lm-thick sections immunoassayed with polyclonal anti-protein gene product 9.5 antibody (1:1000; Biogenesis, Poole, Dorset, UK) using the free-floating protocol. The linear density of IENFs (IENF/mm) was calculated following available guidelines [7] and values were compared with the published age- and sex-adjusted normative reference values [8]. Analyses were done with an Axiophot2 microscope (Zeiss, Germany) with a CCD camera (Visitron Systems, Tuchheim, Oberkochen, Germany) and SPOTTM advanced software (Windows Version 4.5; Diagnostic Instruments Inc, Sterling Heights, MI, USA). Standard protocol approvals, registrations and patient consents The local ethics committee approved the study and each subject was enrolled after giving written informed consent. Statistical analysis Data were presented using descriptive statistics, and comparison between groups was performed using parametric or non-parametric statistics where appropriate. Analyses were carried out using Stata 9 software (College Station, TX, USA). Results Ninety-six patients were screened and 39 of them were excluded because of anti-myelin-associated glycoprotein neuropathy (one), type 2 diabetes (five), active C hepatitis (two), vitamin B 12 deficiency (three), folate deficiency (one), hypothyroidism (two), monoclonal gammopathy (one), recent alcohol abuse (one), celiac disease (one), severe hypoxemia (two), anticoagulant treatment (one), possible/suspected ALS (three), other diagnosis (nine), consent not given (seven). Fifty-seven patients meeting the El Escorial revised criteria for probable, laboratory-supported probable or definite ALS were eventually enrolled (27 women, 30 men; mean age ). Amongst them, six patients met the diagnosis of facial onset sensory and motor neuronopathy (FOSMN) according to published criteria [9]. Table 1 details demographics and clinical characteristics of all patients. Eight of 51 (15.7%) pure ALS patients complained of mild sensory disturbances with a different distribution and no correlation to any feature of the disease. All six FOSMN patients were men (mean age years) and presented with progressive bulbar symptoms associated with bilaterally absent corneal reflex and blink reflex. Five of them reported sensory disturbances at the face and hands as first symptoms, and two had been formerly diagnosed with burning mouth syndrome. Patient 25 was previously
3 418 E. DALLA BELLA ET AL. Table 1 Demographic, genetic, clinical, neurophysiological and skin biopsy findings No. Sex Age ALS phenotype FTD Genotype Months from onset ALSFRS-R score MITOS system Sensory symptoms Right sural SNAP amplitude (lv)/ conduction velocity (m/s) IENF Density Cutoff 1 F 57 Bulbar Unknown / M 58 Bulbar + Unknown / M 48 Bulbar + C9orf / F 66 Bulbar Unknown / M 74 Bulbar + Unknown / F 79 Bulbar Unknown / M 66 Bulbar Unknown Left cheek 6.1/ burning; BMS 8 F 60 Bulbar + C9orf / M 60 Bulbar + Unknown / F 68 Bulbar SOD / (p.ser108leufs a 15) 11 F 67 Bulbar Unknown / M 79 Bulbar + Unknown / F 72 Bulbar C9orf72 b / F 64 Bulbar + Unknown / M 57 Flail arm Unknown / M 68 Flail arm Unknown / M 66 Flail arm Unknown / M 45 Flail arm VCP / (p.arg155cys) 19 M 57 Flail leg Unknown / M 77 Flail leg Unknown / F 59 Flail leg Unknown / M 68 Flail leg SQSTM1 (Lys238Glu) / M 53 FOSMN SOD1 (p.asp90ala)hz Perioral and hands 10.2/ M 76 FOSMN Unknown Lips and hands 15/ ; BMS 25 M 58 FOSMN Unknown c / M 72 FOSMN Unknown Lips 11.8/ ; BMS 27 M 65 FOSMN Unknown Right cheek 10.2/ and hands 28 M 62 FOSMN Unknown d Left cheek 17/ F 65 Pyramidal Unknown / M 58 Pyramidal Unknown / F 43 Pyramidal Unknown / F 41 Pyramidal Unknown / M 51 Pyramidal Unknown / M 67 Pyramidal Unknown / F 35 Spinal SOD / (p.gly93aps) 36 F 52 Spinal Unknown Paroxysmal 11.2/ shock lower limbs 37 F 57 Spinal Unknown / (continued)
4 SFN IN ALS 419 Table 1 (Continued) No. Sex Age ALS phenotype FTD Genotype Months from onset ALSFRS-R score MITOS system Sensory symptoms Right sural SNAP amplitude (lv)/ conduction velocity (m/s) IENF Density Cutoff 38 F 46 Spinal Unknown / F 61 Spinal Unknown a Numbness 8.5/ left hands 40 F 63 Spinal Unknown Diffuse 11.2/ F 72 Spinal Unknown Lower limbs 18/ parasthesia 42 F 57 Spinal + C9orf / M 81 Spinal Unknown / F 75 Spinal Unknown / F 59 Spinal SOD Lower 10/ (p.asn65ser) limb pain 46 F 53 Spinal Unknown / F 64 Spinal Unknown / F 64 Spinal Unknown / M 73 Spinal + C9orf / F 72 Spinal Unknown / M 40 Spinal Unknown / M 71 Spinal + Unknown / M 65 Spinal Unknown / M 39 Spinal + C9orf / M 42 Spinal Unknown Transient feet 4.6/ M 75 Spinal + Unknown / F 48 Spinal SOD1 (p.asp90ala) Lower limb pain 13/ BMS, burning mouth syndrome; FOSMN, facial onset sensory and motor neuronopathy; FTD, frontotemporal dementia; SNAP, sensory nerve action potential. Severity of disease is measured by the amyotrophic lateral sclerosis functional rating score revised (ALSFRS-R) and the Milano Torino staging (MITOS) system. Intraepidermal nerve fiber (IENF) density is compared with the corresponding age- and sex-adjusted cut-off value (5th centile); bold values are abnormal. a First-degree cousin with ALS; b expansion at lower cut-off (28 repeats; pathological value 30); c parents first-degree cousins; d brother died with classic ALS. reported to harbor heterozygous D90A-SOD1 mutation [10], whereas patient 28 s older brother died with ALS. Sensory NCS was bilaterally normal in all except patient 18 who showed reduced sural conduction velocity and patient 55 who showed decreased sural sensory nerve action potential amplitude. The latter patient underwent also sural nerve biopsy which, like the skin biopsy, did not show significant changes. The other 13 patients showed normal IENF density compared to age- and sex-normative reference values. Conversely, IENF density was reduced in 75.4% of patients (40 of 51 pure ALS and three of six FOSMN) (Table 1). However, IENF loss did not cluster with any feature of the disease. Indeed, IENF density was reduced in 11 of 14 (78.5%) bulbar, seven of eight (87.5%) flail limb, six of six (100%) pyramidal and 15 of 22 (68.2%) spinal onset patients. Similarly, 10 of 12 (83.3%) genetic and 41 of 50 (82%) sporadic ALS patients had reduced IENF density. Three patients (numbers 12, 44, 46) underwent 6-month follow-up skin biopsy that revealed unchanged IENF density. Finally, no correlation was found between IENF density and disease duration and severity as measured by ALSFRS-R or the MITOS system for loss of function. Discussion Our study confirmed that IENF loss is a feature of ALS, being present in at least three-quarters of patients irrespective of the disease duration. It suggests that skin innervation is probably impaired from the very beginning of the disease in a large proportion of patients. Moreover, in three patients with normal IENF density, follow-up biopsy at 6 months showed unchanged values, demonstrating that small fibers are not impaired in a subgroup of ALS patients. The rea-
5 420 E. DALLA BELLA ET AL. son for such variability is unknown. Indeed, the loss of IENF was not associated to sensory symptoms, which occurred in a small percentage of patients, and not even all those complaining of sensory disturbances had reduced IENF density. Furthermore, IENF density did not cluster with any other feature of the disease including type of onset, genotype, disability and loss of function. This observation widens what was previously reported in a smaller cohort of ALS patients who underwent skin biopsy at an average of 34 months after disease onset [3]. Our case series includes patients diagnosed with FOSMN, a condition recently recognized and characterized by predominantly bulbar and upper limb progressive amyotrophy associated with large sensory nerve fiber dysfunction mainly involving the trigeminal territory [11]. Despite possible peculiar pathogenic mechanisms and, more frequently, longer course [9], FOSMN can be considered a variant of the ALS phenotype. Indeed, its presentation is very similar to bulbar ALS from which, in clinical practice, it can be distinguished by the lack of corneal reflex. Immunotherapy does not change its course and death occurs due to swallowing and respiratory insufficiency. Finally, our recent report of a heterozygous D90A-SOD1 mutation found in one patient [10] and the diagnosis of classic ALS in the sibling of patient 28 (Table 1) further suggest a link between the two conditions [12]. Despite more prominent sensory disturbances, only three of five FOSMN patients showed reduced IENF density, a percentage not very different from that of ALS patients in our case series. The recently reported clustering of spared IENF density in ALS patients with bulbar onset [4] was not confirmed. Whilst such difference cannot be explained because the two subgroups did not differ as to mean age, disease duration and severity, it is emphasized that the percentage of bulbar ALS patients with reduced IENF was similar to that of the other subgroups (e.g. spinal and pyramidal). Our findings suggest that the neurodegenerative process underlying ALS affects also small nerve fibers or probably the small-size dorsal root ganglion, although to a much lesser extent than motor axons and neurons. The lack of correlation with ALS features does not currently make IENF density a clinical or prognostic biomarker. However, it suggests that, as in Parkinson disease [13], molecular mechanisms through which diseasecausative dysfunctions lead to cell dysfunction are shared between different cell types, although at different degrees of severity and therefore clinical outcome. Further studies at molecular level are warranted to clarify the involvement of the somatosensory system in motor neurodegenerative diseases, including ALS. Acknowledgements The study was financed by internal funds (IRCCS Foundation Carlo Besta Neurological Institute, Ricerca Corrente, Italian Ministry of Health) and the Fondazione Italiana di ricerca per la SLA Sclerosi Laterale Amiotrofica. Disclosure of conflicts of interest The authors report no disclosures. References 1. Dyck PJ, Stevens JC, Mulder DW, Espinosa RE. Frequency of nerve fiber degeneration of peripheral motor and sensory neurons in amyotrophic lateral sclerosis. Morphometry of deep and superficial peroneal nerves. Neurology 1975; 25: Pugdahl K, Fuglsang-Frederiksen A, de Carvalho M, et al. Generalised sensory system abnormalities in amyotrophic lateral sclerosis: a European multicentre study. J Neurol Neurosurg Psychiatry 2007; 78: Weis J, Katona I, Muller-Newen G, et al. Small-fiber neuropathy in patients with ALS. Neurology 2011; 76: Truini A, Biasiotta A, Onesti E, et al. Small-fibre neuropathy related to bulbar and spinal-onset in patients with ALS. J Neurol 2015; 262: Lauria G, Merkies IS, Faber CG. Small fibre neuropathy. Curr Opin Neurol 2012; 25: Tramacere I, Dalla Bella E, Chio A, et al. The MITOS system predicts long-term survival in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry 2015; 86: Lauria G, Hsieh ST, Johansson O, et al. European Federation of Neurological Societies/Peripheral Nerve Society Guideline on the use of skin biopsy in the diagnosis of small fiber neuropathy. J Peripher Nerv Syst 2010; 15: Lauria G, Bakkers M, Schmitz C, et al. Intraepidermal nerve fiber density at the distal leg: a worldwide normative reference study. J Peripher Nerv Syst 2010; 15: Vucic S, Stein TD, Hedley-Whyte ET, et al. FOSMN syndrome: novel insight into disease pathophysiology. Neurology 2012; 79: Dalla Bella E, Rigamonti A, Mantero V, et al. Heterozygous D90A-SOD1 mutation in a patient with facial onset sensory motor neuronopathy (FOSMN) syndrome: a bridge to amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry 2014; 85: Vucic S, Tian D, Chong PS, Cudkowicz ME, Hedley- Whyte ET, Cros D. Facial onset sensory and motor neuronopathy (FOSMN syndrome): a novel syndrome in neurology. Brain 2006; 129: Vucic S. Facial onset sensory motor neuronopathy (FOSMN) syndrome: an unusual amyotrophic lateral sclerosis phenotype? J Neurol Neurosurg Psychiatry 2014; 85: Nolano M, Provitera V, Estraneo A, et al. Sensory deficit in Parkinson s disease: evidence of a cutaneous denervation. Brain 2008; 131:
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