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Skin innervation across amyotrophic lateral sclerosis clinical stages: new prognostic biomarkers

肌萎缩侧索硬化 医学 皮肤活检 去神经支配 神经纤维 感觉系统 人口 活检 周围神经病变 病理 内科学 疾病 解剖 糖尿病 内分泌学 认知心理学 环境卫生 心理学
作者
Maria Nolano,Vincenzo Provitera,Giuseppe Caporaso,Ines Fasolino,Ilaria Borreca,Annamaria Stancanelli,Valentina Virginia Iuzzolino,Gianmaria Senerchia,Floriana Vitale,Stefano Tozza,Lucia Ruggiero,Rosa Iodice,Sérgio Ferrari,Lucio Santoro,Fiore Manganelli,Raffaele Dubbioso
出处
期刊:Brain [Oxford University Press]
卷期号:147 (5): 1740-1750 被引量:12
标识
DOI:10.1093/brain/awad426
摘要

Abstract Over recent decades, peripheral sensory abnormalities, including the evidence of cutaneous denervation, have been reported among the non-motor manifestations in amyotrophic lateral sclerosis (ALS). However, a correlation between cutaneous innervation and clinical features has not been found. The aims of this study were to assess sensory involvement by applying a morpho-functional approach to a large population of ALS patients stratified according to King’s stages and correlate these findings with the severity and prognosis of the disease. We recruited 149 ALS patients and 41 healthy controls. Patients undertook clinical questionnaires for small fibre neuropathy symptoms (Small Fiber Neuropathy Symptoms Inventory Questionnaire) and underwent nerve conductions studies (NCS) and 3-mm punch skin biopsies from leg, thigh and fingertip. We assessed intraepidermal nerve fibre (IENF) and Meissner corpuscle (MC) density by applying an indirect immunofluorescence technique. Moreover, a subset of 65 ALS patients underwent a longitudinal study with repeat biopsies from the thigh at 6- and 12-month follow-ups. Serum NfL levels were measured in 40 patients. Sensory symptoms and sensory NCS abnormalities were present in 32.2% and 24% of patients, respectively, and increased across clinical stages. Analogously, we observed a progressive reduction in amplitude of the sensory and motor ulnar nerve potential from stage 1 to stage 4. Skin biopsy showed a significant loss of IENFs and MCs in ALS compared with healthy controls (all P < 0.001). Across the clinical stages, we found a progressive reduction in MCs (P = 0.004) and an increase in IENFs (all P < 0.027). The increase in IENFs was confirmed by the longitudinal study. Interestingly, the MC density inversely correlated with NfL level (r = −0.424, P = 0.012), and survival analysis revealed that low MC density, higher NfL levels and increasing IENF density over time were associated with a poorer prognosis (all P < 0.024). To summarize, in patients with ALS, peripheral sensory involvement worsens in parallel with motor disability. Furthermore, the correlation between skin innervation and disease activity may suggest the use of skin innervation as a putative prognostic biomarker.
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