Epidermal Nerve Fiber and Schwann cell densities in the distal leg of Nine-banded Armadillos with Experimental Leprosy neuropathy
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1 Epidermal Nerve Fiber and Schwann cell densities in the distal leg of Nine-banded Armadillos with Experimental Leprosy neuropathy Gigi J Ebenezer 1 Richard Truman 2 David Scollard 2 Michael Polydefkis 1 Ramanuj Lahiri 2 Justin C McArthur 1 1 Department of Neurology, Johns Hopkins University, Baltimore, MD, USA 2 DHHS/HSB/BPHC/National Hansen's Disease Program, Baton Rouge, LA, USA
2 Skin innervation Unmyelinated (C) and Myelinated (A-fibers) fibers and specialized mechano receptors C- fibers end as free nerve endings Epidermis : Small caliber unmyelinated C fibers light touch, pain and temperature sensations Undetectable by electrophysiological tests Invasive nature of nerve biopsies Difficulty to discern differences between autonomic & somatic unmyelinated fibers Lauria G & Lombardi R. Small Fiber Neuropathy: Is Skin Biopsy the Holy Grail? Curr Diab Rep (2012) 12: Ebenezer et al., J Neuropathol Exp Neurol. 2007; 66: Review. 3mm skin punches- to diagnose distal sensory neuropathies Autonomic function using sweat gland innervation
3 Different components of skin structures can be evaluated Dermis All photographs taken at cutaneous nerve laboratory, JHU
4 ARMADILLOS Nine banded armadillos are naturally susceptible to M.leprae Experimental neuropathy: Develop extensive involvement of their peripheral nerves when infected with M.leprae Recapitulates leprosy neuritis in humans M.leprae in Armadillos PN
5 Sharma R, Lahiri R, Scollard DM. et al., The armadillo: a model for the neuropathy of leprosy and potentially other neurodegenerative diseases. Dis Model Mech. 2013;6: Review. Progressive nerve conduction deficit in compound motor action potential (CMAP; mv; y-axis) complete conduction block in late infection. The upper lines : stimulation at the ankle lower ones to the knee.
6 Nearly all of the animals that developed a conduction deficit exhibited signs of clinical neuropathy in their foot pads M.leprae infected Armadillo feet Lepromatous leprosy feet The earliest clinical sign is loss of sensation
7 Collaboration between JHU and HRSA/National Hansen's disease programme, USA Neurophysiology * National Hansen's disease programme, Baton Rouge Skin biopsy *Cutaneous nerve lab, Neurology
8 Objective Assess nerve conduction velocity in M.leprae infected animals vs. control animals Investigate epidermal nerve fiber density and Schwann cell density in M.leprae infected vs. control animals
9 Methodology 11 naïve and 9 M.leprae-infected armadillos Caldwell Sierra II portable electrophysiology unit Surface stimulation of the posterior tibial nerve: Distally at the ankle Proximally at the knee Motor nerve conduction velocity (MNCV) Compound muscle action potential recorded (CMAP)
10 Methodology-Skin punches 3mm skin punches Naïve : ears, upper and lower abdomen, distal leg M.leprae infected animals: distal leg 50µm sections: Free floating techniques Protein gene product 9.5 / neuronal marker Epidermal nerve fibers quantified in 4 serial sections/biopsy Established nerve counting rules. Double stained immuno staining-confocal microscopy Statistical analysis Lauria et al., Eur J Neurol 2005;12: Distal leg Bx
11 Dermal Schwann cells (cells/mm 3 ) Morphometry P75 (low-affinity and pan-neurotrophin receptor) Stereology technique Optical Fractionator Thick sections Continuously aligned unbiased counting frames 3 serial sections Growth Associated Protein-43 (GAP-43) Nerve regeneration marker Ebenezer et al., Brain. 2011;134: MBF
12 Results Neurophysiology The mean distance between the two stimulation points was 4.47 ± 0.32 cm. MNCV (Mean+ SD): naïve animals was ± 7.99 m/s; M.leprae: 54.5 ± 15.4 m/s Using a standard threshold of 49 m/s, 3 infected armadillos showed abnormal MNCV in both limbs and 2 animals in at least one limb. Depressed CMAP amplitude (<0.9mV) in five infected armadillos
13 Epidermal nerve fibers in Naïve Armadillos Fewer ENF in distal leg Human: Length dependent innervation SFN: Progressive decrease of ENF density in distal limb Intraepidermal nerve fiber density at the distal leg: a worldwide normative reference study. Lauria et al., J Peripher Nerv Syst. 2010; 3:202-7.
14 ENF density/mm Armadillos Naive Naive M.leprae Inf. M.leprae infected Epidermis M.leprae infected armadillos ENF density trended lower (no. of ENF/mm) (Mean + SD; Naive: ; M.leprae: ; p=0.2) 5 th percentile: 21/mm M.leprae: 13/mm- 1 animal Quantification ENF is feasible
15 Schwann cells in dermal cutaneous nerves-armadillos Schwann cells ensheath axons and co-localize
16 Schwann cells in dermis no.of cells/mm 3 Remak Schwann cell nucleus Naive M.leprae Inf. M.leprae infected armadillos Schwann cells trended towards an increasing density Mean + SD; Naive: ; M.leprae: ; p=0.1 Dermal Schwann cells harbor and provide a fertile milieu
17 GAP43 +ve regenerating fibers in nerve bundles co-localize with PGP9.5 +ve axons Regenerating fibers are + in M.leprae infected armadillos
18 CONCLUSIONS Infected armadillos showed NCV abnormalities compared to naïve animals Similar to human, Naïve Armadillos exhibit length dependent, progressively decreasing epidermal nerve fiber innervation ENF density trended lower among M.leprae infected animals degeneration of small sensory fibers Increasing proliferation of Schwann cells in M.leprae infected Armadillos: Small fiber neuropathy in Human-degeneration of Schwann cells M.leprae -housing and modify Remak Schwann cells of small sensory fibers in skin Corroborates another study Reprogramming adult Schwann cells to stem cell-like cells by leprosy bacilli promotes dissemination of infection. Rambukkana et al., Cell. 2013;152:51-67.
19 Summary Quantifying ENF density and Schwann cells is feasible in nine-banded armadillos An important tool for investigating experimental neuropathy and early sensory neuropathy in leprosy: Diagnostic tool: Somatic and autonomic nerve function ( sweat gland innervation) Pain markers Progression of disease Drug trials
20 Acknowledgement DHHS/HRSA/HSB/Nation al Hansen's Disease Program, Baton Rouge, LA, USA Maria Pena Greg McCormick Roena Stevenson Heidi Zhang Gaya Balamayooran Rahul Sharma Cutaneous Nerve Laboratory, Department of Neurology, Johns Hopkins University, Baltimore Michael Polydefkis (Director) Ying Liu Peter Hauer ( administrator) Ryan O Donnell Jennifer Billiet Yanning Shou Baohan Pan India SIH-R&LC Late Prof. C.K. JOB Prof. Sunder Rao Ebenezer Daniel NIH, ALM, NIAID, HRSA
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