Cutaneous nerve biomarkers in transthyretin familial amyloid polyneuropathy

Ann Neurol. 2017 Jul;82(1):44-56. doi: 10.1002/ana.24972. Epub 2017 Jun 20.

Abstract

Objective: To determine the utility of skin biopsies as a biomarker of disease severity in subjects with amyloid neuropathy.

Methods: Five groups of patients were studied: (1) transthyretin (TTR) familial amyloidotic polyneuropathy (FAP; n = 20), (2) TTR mutation carriers without peripheral neuropathy (TTR-noPN; n = 10), (3) healthy controls (n = 20), (4) diabetic neuropathy disease controls (n = 20), and (5) patients with light-chain (AL) amyloid (n = 2). All subjects underwent neurological examination and 3mm skin biopsies. Sections were stained with anti-PGP9.5, anti-TTR, and Congo red. Intraepidermal (IENFD), sweat gland (SGNFD), and pilomotor nerve fiber densities (PMNFD) were measured. Correlations between the amount of amyloid present (amyloid burden), fiber subtype, and Neuropathy Impairment Score in the Lower Limbs (NIS-LL) were evaluated.

Results: IENFD, SGNFD, and PMNFD were all significantly reduced in TTR-FAP patients versus healthy controls, whereas TTR-noPN subjects had intermediate reductions. Lower nerve fiber densities were associated with NIS-LL (p < 0.001). Congo red staining revealed brilliant red amyloid deposits confirmed by apple-green birefringence within dermal collagen, sweat glands, and arrector pili that engulfed axons. The diagnostic sensitivity and specificity to detect amyloid in skin were 70% and 100%. Both AL amyloidosis and 2 of 10 TTR-noPN subjects were Congo red-positive. Amyloid burden correlated with IENFD (r = -0.63), SGNFD (r = -0.67), PMNFD (r = -0.50), and NIS-LL (r = -0.57). Wild-type TTR staining was less prominent in TTR-FAP patients.

Interpretation: Cutaneous amyloid was detected in 70% of TTR-FAP and 20% of TTR-noPN subjects. Amyloid burden correlated strongly with reductions in IENFD, SGNFD, PMNFD, and NIS-LL. Skin is an attractive tissue to establish an amyloid diagnosis, and amyloid burden has potential as a biomarker to detect treatment effect in TTR-FAP drug trials. Ann Neurol 2017;82:44-56.

MeSH terms

  • Adolescent
  • Adult
  • Aged
  • Aged, 80 and over
  • Amyloid / metabolism*
  • Amyloid Neuropathies, Familial / genetics
  • Amyloid Neuropathies, Familial / metabolism*
  • Amyloid Neuropathies, Familial / pathology*
  • Biomarkers / metabolism
  • Case-Control Studies
  • Diabetic Neuropathies / metabolism
  • Diabetic Neuropathies / pathology
  • Female
  • Heterozygote
  • Humans
  • Male
  • Middle Aged
  • Mutation / genetics
  • Nerve Fibers / pathology*
  • Prealbumin / genetics
  • Severity of Illness Index
  • Skin / metabolism*
  • Skin / pathology*
  • Sweat Glands / metabolism*
  • Young Adult

Substances

  • Amyloid
  • Biomarkers
  • Prealbumin

Supplementary concepts

  • Amyloidosis, Hereditary, Transthyretin-Related